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Infraorder astacidea Latreille, 1802 P.O. : The freshwater crayﬁsh
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CHAPTER 67
INFRAORDER ASTACIDEA LATREILLE, 1802 P.P.:

THE FRESHWATER CRAYFISH1 )
BY
FRANCESCA GHERARDI, CATHERINE SOUTY-GROSSET, GÜNTER

VOGT, JAVIER DIÉGUEZ-URIBEONDO AND KEITH A. CRANDALL
Contents. – Introduction – Overview – Diagnosis. External morphology – General habitus –

Cephalothorax – Pleon – Appendages. Internal morphology – Musculature – Circulatory system –
Immune system – Respiratory system – Excretory system – Digestive system – Reproductive system
– Endocrine system – Nervous system – Sense organs. Reproduction and development – Sexual
maturation – Sex determination and sex ratios – Intersexes, parthenogenesis, and hybridization –
Embryonic development. Ecology – Crayfish in their habitat – Feeding habits – Crayfish in the food
web. Behavior – Habitat selection – Choosing the time to be active – Avoidance of predators –
Burrowing – Food acquisition – Movement – Reproduction – Agonistic behavior. Parasites and
diseases – Aphanomyces astaci (crayfish plague) – Thelohania contejeani (porcelain disease) –
Psorospermium haeckeli – Viral diseases – Epibionts – Other parasites and diseases. Conservation
– Conservation status in different countries – Methods and policies. Economic importance.
Phylogeny and biogeography – Present distribution and areas of endemicity – Phylogeny and
historical processes. Systematics. Acknowledgements. Appendix. Bibliography.
INTRODUCTION
[F. G HERARDI ]
It is a matter of common information that a number of our streams and rivulets harbour small
animals, rarely more than three or four inches long, which are very similar to little lobsters,
except that they are usually of a dull, greenish or brownish colour, generally diversified with pale
yellow on the under side of the body, and sometimes with red on the limbs. – T. H. Huxley, 1880.
1 ) Manuscript concluded June 2009.
© Koninklijke Brill NV, Leiden, 2010 Crustacea 9A (67): 269-423

270 F. GHERARDI ET AL.
Overview
Modern crayfish are an incredibly diverse group of organisms with over 600 described
species worldwide (Crandall & Buhay, 2008; see also section Phylogeny and Biogeogra-
phy) organized into two superfamilies, Astacoidea and Parastacoidea. Astacoidea consists
of the Jurassic Cricoidoscelosidae and two extant families, both restricted to the North-
ern Hemisphere: Astacidae and Cambaridae (cf. Hobbs, 1989; Crandall & Buhay, 2008).
Parastacoidea is composed of a single family, Parastacidae, and is distributed throughout
Madagascar, southern South America, and Australasia (Crandall & Buhay, 2008). Crayfish
are naturally absent from the Antarctic continent, continental Africa, the Indian subcon-
tinent, and much of Asia. In recent times, however, their original distribution has been
altered due to the massive human-mediated introduction of species outside their native
range and the subsequent spread of some of the introduced crayfish across the introduced
area (Gherardi & Holdich, 1999; Lodge et al., 2000).
Crayfish form a monophyletic group (Crandall et al., 2000; Scholtz, 2001; see Phy-
logeny, below). Their sister group seems to be the clawed lobsters, Nephropoidea Dana,
1852, as first suggested by Crandall et al. (2000) and recently supported by Porter et al.
(2005) [but see the suggestion of Thalassinidea Latreille, 1831 as sister group by Scholtz
& Richter, 1995]. Astacoidea, Parastacoidea, and Nephropoidea thus make up the infra-
order Astacidea Latreille, 1802; in this chapter we treat the two freshwater superfamilies
from that taxon. Fossil crayfish and their burrows (Hasiotis & Mitchell, 1993) support the
hypothesis that crayfish are an extremely old group of organisms with the last common
ancestor existing at least in the Triassic period with a Pangaean origin. The separation
of Astacoidea and Parastacoidea seems to be originated around 185 mya, with the break-
up of Pangaea into the northern supercontinent Laurasia and the southern supercontinent
Gondwana (Crandall et al., 2000; section Phylogeny and Biogeography).
Although crayfish taxonomy is reasonably well resolved at the highest levels, the
designation of the levels below remains still contentious (Starobogatov, 1995). Such an
open debate is in great part due to the conservatism of some morphological characters in
many species, the high intraspecific diversity in others, e.g., Orconectes luteus (Creaser,
1933), the recorded convergence with habitat diversity, e.g., in the case of cave species,
and the various cryptic species that require an appropriate bioinformatic approach coupled
with a set of molecular tools (AFLPs, microsatellites, and PCR primers for various gene
regions) (Fetzner & Crandall, 2002) and/or refined morphometrical studies (Bertocchi et
al., 2008) to be identified.
Two centers of crayfish diversity have been described, the first in the southern Ap-
palachian Mountains of the southeastern United States (Northern Hemisphere center) and
the second in southeastern Australia (Southern Hemisphere center) (Crandall & Buhay,
2008); hot spots of diversity have been also identified for single families or genera, e.g.,
Fratini et al. (2005). Yet, crayfish diversity is in serious decline due to growing habitat
loss and degradation often acting in synergy with the detrimental effects of invasions by
alien species, over-harvesting, and chemical pollution (section Conservation). Over 50%
of the U.S. species, for example, are imperiled to some degree (Taylor et al., 1996): 20
INFRAORDER ASTACIDEA: FRESHWATER CRAYFISH 271
species are known from less than five localities (with 15 known only from a single local-
ity) and over 210 are considered endangered or threatened. In the 1960-70s, North Ameri-
can species were introduced into Europe for aquaculture and stocking purposes (Gherardi
& Holdich, 1999); now they are displacing the European species, being also the vector
of the parasite Aphanomyces astaci Schikora lethal to the indigenous crayfish. Similarly,
charismatic species, such as Astacopsis gouldi Clark, 1936 in Tasmania (Horwitz, 1994)
and Astacoides madagascarensis (H. Milne Edwards & Audouin, 1839) in Madagascar
(Jones et al., 2005) are threatened by the combined impact of over-harvesting and habitat
fragmentation.
The augmented menaces to their diversity have contributed to the recent upsurge of
interest by the scientific community in crayfish conservation (cf. Souty-Grosset et al.,
2006). Indeed, the keystone role played by crayfish in their freshwater systems is widely
recognized (section Ecology). Crayfish diversity is also a surrogate for the diversity in
other organisms of freshwater communities, their presence reflecting the health of the
entire ecosystem. Unfortunately, appropriate measures to protect crayfish and particularly
many of those recognized to be at risk of extinction have not been taken yet by many
national governments (cf. the U.S. Endangered Species List) with a few exceptions (cf. the
E.U. Habitats Directive).
Indeed, the bulk of crayfish diversity is a reflection of the multitude of their morpho-
logical, physiological, behavioral, and ecological adaptations. They come in a variety of
sizes, from Gramastacus insolitus Riek, 1972, endemic to southwest Victoria and south-
east South Australia, with a maximum total length of 40 mm (Zeidler & Adams, 1990), to
the Tasmanian giant lobster, Astacopsis gouldi, the world’s largest freshwater invertebrate
that reaches lengths over 40 cm and weights over 5 kg (Horwitz, 1994). They also come in
a variety of colors, from red, blue, orange, green, brown, to even pigment-less. There are
crayfish with spots, stripes, and patterns of various sorts (Crandall, 2006).
The grand morphological variety that crayfish show within the constraints posed by the
typical decapod body plan is strictly related to their ecological diversity, coupled with the
extreme isolation to which many species have been subject for ages (at least 15 of over 600
described species are known from a single location and most species have a very narrow
distribution range; Crandall, 2006). Crayfish fall into eco-categories. Primary burrowers
are those crayfish that spend their entire life cycle in burrows, burrowing down to the
water table; they are not restricted to fresh waters but some are essentially terrestrial.
[One of the most impressive primary burrowers is Fallicambarus devastator Hobbs &
Whiteman, 1987, even able to construct over 60 000 chimneys per ha in southern Texas
(Hobbs & Whiteman, 1991).] As an adaptation to their terrestrial life-style, species of the
Australian genus Engaeus Erichson, 1846 exhibit a relatively complex social behavior,
with parents and juveniles sharing a communal burrow (Riek, 1972). Crayfish also may
inhabit fast flowing streams (lotic water species), ponds, lakes, or other slow waters (lentic
water species); lotic and lentic species include secondary burrowers, i.e., crayfish that
require connectivity of their burrows with water. Finally, there are stygobitic species,
i.e., obligate cave-dwellers, such as Orconectes incomptus Hobbs & Barr, 1972 from
northern Tennessee, U.S.A. (Hobbs & Barr, 1972) and Procambarus cavernicola Mejía-
Ortíz, Hartnoll & Viccon-Pale, 2003 from Oaxaca, Mexico (Mejia-Ortiz et al., 2003).
Each eco-category has some distinctive morphological adaptations for the habitat occupied
(fig. 67.1). Thus, primary burrowers typically have a vaulted carapace to accommodate
larger gill surface area and robust pincers for digging and burrow protection. Lotic water
species typically have large pleons for swimming and are highly intolerant of low oxygen
content in the water. Cave species typically have the suite of cave-adapted morphologies
including loss of pigmentation, loss of eyes, elongated antennae, and elongated limbs.
Crayfish are omnivorous and nocturnal. They are voracious eaters and can be extremely
destructive when introduced to non-native habitats. A few crayfish are particularly inva-
sive, e.g., Orconectes rusticus (Girard, 1852), and/or were distributed by the aquaculture
trade, e.g., Procambarus clarkii Girard, 1852. These introduced species wreak havoc on
natural ecosystems to which they are not native, but the vast majority of crayfish is ex-
tremely narrowly distributed and hence are endangered due mainly to the destruction of
the freshwater ecosystems in general.
The majority of crayfish species have separate sexes, but some are hermaphroditic
and some even reproduce parthenogenetically, such as the enigmatic marbled crayfish
(Marmorkrebs) (Scholtz et al., 2003; section Reproduction and Development). Young
stages are not planktonic but emerge from the egg resembling miniature adults. They
remain attached to their mother’s pleon by transient structures (Vogt & Tolley, 2004)
and then freely crawl onto her body for a period ranging between one or few weeks in
most species and three-four months or more in Procambarus clarkii (cf. Huner, 1994) and
Paranephrops zealandicus (White, 1847) (cf. Whitmore & Huryn, 1999).
Some crayfish species, such as Procambarus clarkii, show many characteristics proper
of r-selected species, with the only exception of the extended maternal care (Aquiloni &
Gherardi, 2008d): they are relatively short-lived, highly fecund (500+ eggs), fast growing,
and reach maturity within a year or less. Other crayfish may live beyond 15 years, are
relatively low fecund, and take two years or longer to reach maturity with a relatively
larger size, thus behaving as typical K-selected species. A distinction between extreme r-
and extreme K-selected species might reflect the invasive potential of the former, and the
vulnerability to threats of the latter, with a long gradient in between.
From the human side, crayfish are a much sought-after food item all over the world, but
rarely provide a subsistence diet today (exceptions in Jones et al., 2006), being most often
served as a gourmet food (Holdich, 2002). Some species are commercially harvested from
wild stocks and others are a significant aquaculture commodity in countries such as U.S.A.,
China, and Australia (section Economic value). A second important aspect for which
crayfish serve to humans is their cultural value: because of their diversity, coupled with
a relative ease of collection, their conspicuousness in the ecological community, and their
charismatic role for some cultures (Swahn, 2004), crayfish are used as a model organism
of study in a variety of research fields (Crandall, 2006) (fig. 67.2). Indeed, crayfish have
been of interest to man since the times of Aristotle (cf. “On the parts of animals” written
around 350 BC). Thomas H. Huxley, “Darwin’s bulldog”, produced an introductory text
to the study of zoology based solely on the crayfish (1880). More recently, George Wald,
Fig. 67.1. Comparison of the four distinct morphotypes of freshwater crayfish: from top to bottom,
(1) primary burrower – an undescribed species of Procambarus from Arkansas, U.S.A.; (2) slow
water generalist – Orconectes virilis (Hagen, 1870) collected from the Muskegon River in Muskegon,
Michigan, U.S.A.; (3) stream specialist – Orconectes harrisonii (Faxon, 1884) known only from
streams of St. Genevieve and Washington Counties, Missouri, U.S.A.; and (4) a cave species –
Cambarus hamulatus (Cope, 1881) collected from Bluff River Cave, Jackson County, Alabama,
U.S.A. [Photos by Keith A. Crandall.]
Fig. 67.2. Frequency distribution (in %) per scientific field of the articles with crayfish as the main
subjects published per year in peer-reviewed journals (after Web of Science). Fields are: ECO,
ecology & conservation; EVO, phylogeny & diversity; PHY, morpho-physiology; PRO, production;
and PAR, diseases & symbionts. The number of articles per year is given in parentheses. The figure
shows a progressive increase with time in the relative frequency of ECO papers.
1967 Nobel Laureate in Medicine for discoveries concerning the primary physiological
and chemical visual processes in the eye, used the crayfish in his elucidation of the role of
vitamin A in vision (Wald, 1967, 1968).
The crayfish’ important role as model organisms in scientific research is clear. Hart &
Clark (1987) have documented over 11 000 citations pertaining in some way to crayfish
from Aristotle to 1985. Since 1990, an average of 141 articles each year have focused on
crayfish (after Web of Science), including journals with a high impact such as Current
Biology (Issa & Edwards, 2006; Patullo & Macmillan, 2007; Aquiloni et al., 2008),
Nature (Scholtz et al., 2003), PLoS ONE (Van der Velden et al., 2008), Science (Barinaga,
1996; Lange, 1996; Yeh et al., 1996), and Trends in Neuroscience (Edwards et al., 1999).
Despite this relative prolificacy of published articles (a similar search in Web of Science
showed an average of only 39 published articles focused on Anomala Boas, 1880), the
range of crayfish species studied so far has been narrow, mainly on 164 of the 644
species described so far (Crandall & Buhay, 2008), which constitute less than 25% of
the known crayfish. Besides, over 75% of these studies were focused on just 10 species
with Procambarus clarkii (22%) largely prevailing over the others, 10% for Pacifastacus
leniusculus (Dana, 1852), 9% for Austropotamobius pallipes (Lereboullet, 1858), and 8%
for Cherax quadricarinatus (Von Martens, 1868). A bias can also be found in ecological
and conservation studies; although the Palearctic contains a lower number of described
crayfish species (38) than the Nearctic, Australasian, and Neotropical ecozones (382, 151,
and 64, respectively, Crandall & Buhay, 2008), the number of studies in the former ecozone
are decidedly higher (180 vs. 110 in 8 yr) with an average of 4.7 published articles per
species in 8 yr against 0.4, 0.3, and 0.2 in the Afrotropical, Nearctic, and Australasian
ecozones, respectively. The Afrotropics, with 9 described species, has been the subject of
0.1 studies per species in 8 yr, but the majority has focused on the introduced Procambarus
clarkii.
As research continues and our knowledge of crayfish rapidly grows, our expectation
and hope is that scientists will soon enlarge the array of species and ecozones of interest.
This will strengthen not only the role of crayfish as an important model organism of
modern biological studies, but will also provide the indispensable scientific basis for the
development of appropriate measures to protect the endangered freshwater ecosystems and
the organisms inhabiting these, crayfish included.
Diagnosis
Lobster-like habitus. Carapace thin, fused to thorax, forming branchiostegites enclosing
branchial chambers; moveable stalked eyes; biramous antennules; scale-like antennal
exopod; well-mineralized mandibles; plate-like maxillules and maxillae. First to third
thoracic appendages forming functional maxillipeds; fourth to eighth thoracic appendages
forming uniramous pereiopods, consisting of a pair of chelipeds and four pairs of
walking legs; propodus of the first three pairs of pereiopods extended (fixed finger),
forming a claw with the flexible dactylus (movable finger), particularly voluminous in the
chelipeds. Gonopores located on the coxae of the third (female) or fifth (male) pereiopod.
Gills trichobranchiate; pleurobranchs, arthrobranchs, and podobranchs; inhalant channels
between the appendage bases. Well-developed pleon clearly segmented; pleopods with two
flagelliform rami; second to fifth pleomeres of females bearing a pair of feathery pleopods;
first and second pleopods in males modified as copulatory appendages (gonopods).
Biramous uropods with paddle-like rami forming a tail fan with the telson. Development
direct with all the larval stages embryonized; the first juvenile stage without uropods.
EXTERNAL MORPHOLOGY
[C. S OUTY-G ROSSET ]
General habitus
Crayfish are bilaterally symmetrical, with a body plan typical of higher crustaceans. As
such, their body is covered by an exoskeleton and growth consists in periodic shedding
and replacement of the cuticle during ecdysis (Drach & Tchernigovtzeff, 1969; Hartnoll,
1982).
In dorsal view, the body of a crayfish is divided into two regions by a transverse dorsal
groove, the cervical groove: an anterior cephalothorax, covered by the carapace, and the
posterior, segmented pleon or tail (fig. 67.3). The unmodified appendages of crustaceans
are composed of a basal two-part protopod (coxa and basis) from which two rami arise, an
outer exopod and an inner endopod (McLaughlin, 1982). In the malacostracan pereiopod
276
F. GHERARDI ET AL.
Fig. 67.3. Dorsal and ventral diagrams of a stereotyped crayfish. [After M. Pöckl.]
there are usually five articles, forming the endopod: ischium, merus, carpus, propodus,
and dactylus. Epipods are attached to the proximal external part of the protopod and
projections (endites) arise from its inner margin. Epipods often function as gills while
endites of the mouthparts are modified for food transfer. The protopod is divided into a
coxa and a basis, as for all thoracic appendages.
The appendages of crayfish were described by Holdich (2002) and Arrignon (2004);
their structure and function are summarized in table I. Each somite bears a pair of ap-
pendages, five pairs of head appendages (preoral appendages: antennules and antennae,
postoral appendages: mandibles, maxillules or maxillae 1, maxillae or maxillae 2), three
pairs of maxillipeds, and five pairs of pereiopods. The pleon is composed of five somites,
each bearing a pair of pleopods. Appendages can be specialized for various functions,
such as food handling and consumption, respiration, sensory tasks, defense, locomotion,
or reproduction (Holdich, 2002).
Crayfish, as other decapods, may exhibit autotomy, the spontaneous shedding of
one or several appendages in response to injury or threat. Autotomy, which occurs in
a predetermined fracture plane (McVean, 1982), implies regeneration (Bliss, 1960). In
Cambarus propinquus (Girard, 1852), limb regeneration has been shown to accelerate
molting along with the growth of sensory neurons that re-establish the appropriate
connections with the neural network of the ventral nerve cord (Cooper, 1998).
Cephalothorax
In ventral view, the cephalothorax is composed of five anterior somites (the cephalon)
and eight posterior thoracic somites (the thorax). Anteriorly, the carapace bears a con-
spicuous anterior, median, pointed extension of the head region, the rostrum. The lateral
border of the rostrum exhibits suborbital ridges. Along with the orbital spines observed
on the anterior edge of the carapace, these structures are important in species identifica-
tion (Hobbs, 1989). Each orbit contains a movable eyestalk with a compound eye; this is
composed of thousands of repeating units called ommatidia, each of which functions as
a separate visual receptor (see section Internal Morphology). The cephalothorax has sen-
sory functions (antennae), feeding functions (chewing or grinding with mandibles, food
handling with maxillae 1 and 2), and locomotory functions (walking legs).
The respiratory apparatus of decapod crustaceans consists of numerous feathery gills,
a branchial chamber between the lateral carapace and the body that houses them, and
a water pump (scaphognathite) that generates a respiratory current over them. The
number of gills in crayfish is fixed at 17-18 pairs. The gills are epipods attached to the
coxa or the adjacent articulating membrane or pleurite of most thoracopods.
Pleon
The pleon consists of six somites and ends with the telson. The anus is located on
the ventral side of the telson. Each body segment (somite) is enclosed in four articulated
exoskeletal plates, or sclerites, that form a complete ring around the segment: dorsal
278
TABLE I
External morphology of crayfish [After Arrignon, 2004]
Appendage Structure Function
Protopod Exopod Endopod Epipod
C EPHALOTHORAX
Antennule 3 segments multisegmented multisegmented balance (statocyst):
ramus ramus chemo- and
mechanoreception
(setae)
Antenna 2 segments large scaphocerite multisegmented touch, taste, smell
Mandible asymmetrical, enlarged gnathobase 3-segmented palp chewing or grinding,
cleaning
coxa basis
Maxilla 1 membranous membranous food handling
Maxilla 2 2 foliaceous lobes 2 foliaceous lobes scaphognathite thin tip scaphognathite food handling
Maxilliped 1 large thin plate large thin plate long basis, reduced expanded manipulating foods
multisegmented towards mouth
F. GHERARDI ET AL.
Maxilliped 2 large small long basis, 5-segmented podobranches touch and breathing
multisegmented
Maxilliped 3 seto-branchial joined with ischiopod long basis, 5-segmented podobranches touch and breathing
multisegmented
Pereiopod 1 normal joined with ischiopod cheliped or claw
used in defense and
in catching/handling
food
Pereiopod 2 normal joined with ischiopod walking leg
Pereiopod 3 female gonopores joined with ischiopod walking leg
Pereiopod 4 normal joined with ischiopod walking leg
Pereiopod 5 male gonopores joined with ischiopod walking leg
TABLE I
(Continued)
Appendage Structure Function
Protopod Exopod Endopod Epipod
P LEON
Pleopod 1 endopod in males swimming
Pleopod 2 normal multi-segmented spermatophore male first two pairs
tube for sperm transfer
Pleopod 3 normal multi-segmented spermatophore female: carrying
tube eggs and juveniles
Pleopod 4 normal setose rami spermatophore egg attachment
tube
Pleopod 5 normal setose rami setose rami egg attachment
Pleopod 6 uropods setose rami setose rami swimming, escape
T ELSON (None) single structure, part
of tail fan; escape
INFRAORDER ASTACIDEA: FRESHWATER CRAYFISH
reaction; bears anus

279
tergite, ventral sternite, and laterally two pleurites. The tergite and pleurites are fused
together to form a hard arch of exoskeleton. On somites 2-6 the pleurites extend ventrally
past the body as side plates, or epimera, which together form a shallow ventral channel
below the body of the pleon. The sternites cover most of the ventral surface of the pleon
but the pleurites cover its lateral parts. For the most part sternites are thinner and more
flexible than tergites and pleurites. They are transparent and, in living specimens, the
pleonal musculature and nerve cord can be seen through them. The posterior margin of
each sternite, however, is thick and heavy.
Appendages
C EPHALON
Antennules. – The first antennae are located below the eyestalks. They are smaller
than the second antennae, with a 3-segmented basal stalk or peduncle from which arise
two slender, multi-articulate flagella. There is a statocyst in the basal article of each first
antenna. The two eyestalks are also on the anterior of the head. Each bears a conspicuous
compound eye at its distal end.
Antennae. – The biramous second antennae are long, each arising from a bi-articulated
protopod that consists of a proximal coxa and a distal basis. The short, wide exopod
is called the antennal scale, arising from the basis. The endopod, also arising from the
basis, has a short, thick basal peduncle of three articles and a very long narrow, whip-like
flagellum composed of many articles.
Mandibles. – The mandibles are calcified and equipped with well-developed muscles.
They have a large basal portion that bears a cutting edge on a medial lobe. A 3-segmented
palp arches over the cutting edge. The mandibles are involved in chipping and crushing.
Maxillules. – The first maxillae bear two broad endites and a narrow, larger, endopod.
Maxillae. – The second maxillae generate the water current that pumps water out of the
front of the branchial chamber. Its basal portion bears four flat, narrow endites, a slender
endopod, and a long scaphognathite (composed of exopod and epipod), the movement
of which generates the respiratory current through the branchial chamber.
T HORAX
Maxillipeds. – The anterior three pairs of thoracic appendages are biramous maxil-
lipeds. The first is long and narrow with a short endopod, the second is biramous but
smaller than the third, with an exopod longer than the endopod. The third maxillipeds are
anterior to the chelipeds. Each is large and intermediate in shape and size between the legs
of the pereion and the mouthparts of the head. Each has a large, stenopodous endopod
and a small filamentous exopod. The protopod is divided into a coxa and a basis, as for all
thoracic appendages. One function of the third maxillipeds is to protect the more delicate
appendages anterior to it.
Pereiopods. – The five somites of the pereion bear a total of 10 appendages, the
pereiopods. All pereiopods are uniramous: they lack the exopod while the endopod
is long and narrow. Pereiopods 1-3 are similar in structure, each bearing a prehensile,
or grasping, pincer, called chela. The chelae are composed of the movable dactyl that
opens and closes against a fingerlike distal process of the propodus. The first pereiopods,
because of the striking size of their chelae, are referred to as chelipeds. Chelipeds make
a fine example of allometric growth. In crayfish, the growth of chelae shows a form of
positive allometry, i.e., a progressive geometric growth in which the dependent variable
grows faster with respect to the body size, such as in Orconectes virilis (Hagen, 1870) (cf.
Aiken & Waddy, 1992) and Orconectes rusticus (cf. Garvey & Stein, 1993). The chelipeds
are sexually dimorphic (Snedden, 1990), possibly playing a role in sexual selection.
Pereiopods 4 and 5 have no chelae. The coxa of pereiopod 4 has a large membranous,
leaf-like epipod that is absent from pereiopod 5. Similar epipods are present on pereiopods
1-3 and maxilliped 3.
The female gonopores are located on the medial side of the coxa of pereiopod 3.
The male gonopores are the external openings of the vasa deferentia from the testes
and are found at the tip of the two short genital papillae on the medial surface of the
coxa of pereiopod 5. In Cambaridae, a conspicuous oval seminal receptacle, the annulus
ventralis (Hobbs & Jass, 1988) is located on the ventral surface of the female pereion
between the coxae of pereiopods 4 and 5. There, sperm are stored, sometimes for weeks
or months before fertilization. The annulus ventralis in Procambarus is surrounded by
flexible cuticle and is freely movable, in Orconectes it is inflexibly fused to the sternum
immediately anterior to it, and in Cambarus it is capable of a slight, hinge-like motion
between the anterior and more heavily sclerotized posterior portion.
P LEON
The appendages of the pleon articulate with the pleurites at the ends of the sternal arch.
Each appendage is a linear series of articles joined by flexible articulations. Appendages
may be biramous or uniramous. A biramous appendage has a basal article attached by its
proximal end to the body. The basal article is the protopod, which is often divided into
a coxa and basis. The two rami are an outer, or lateral, exopod and an inner, or medial,
endopod. The pleon serves for movement with five pairs of small limbs called pleopods
or swimmerets used for swimming. Typically, the pleopods beat to maintain a current of
water over the gills. Pairs 2-5 are biramous and are similar to each other, being narrow and
whip-like. The pleopods of females are better developed than those of males and are used
to carry the eggs, which are glued to the individual setae fringing the rami.
Pleopods. – The first pleopods of males are uniramous (named gonopods) and are
modified to serve as intromittent organs to transfer spermatozoa to the female. Unlike other
crayfish, adult male Cambaridae can belong to either Form I or Form II. The gonopods of
Form I males are sclerotized and hard, and suitable for intromission. Those of Form II
males are not sclerotized and soft, and cannot transfer sperm to the female. The Form I
gonopods have a species-specific shape that fits like a key into the annulus ventralis.
Gonopods of Form I in Procambarus usually terminate in more than two processes, in
Cambarus have two or less terminal processes and are bent at right angles to the shaft of
the pleopod, and in Orconectes have two or fewer processes and are not bent.
Uropods. – The uropods have a relatively small protopod and a biarticulate exopod
bearing a fringe of setae at the distal border of each of its rami. The rami plus the telson
make up the tail fan, which functions as a large paddle. With the fan deployed, flexure
of the powerful muscles of the pleon moves the fan rapidly forward under the body and
results in the generation of a forward jet of water that propels the animal backwards, the
so-called tail-flip.
INTERNAL MORPHOLOGY
[G. VOGT; includes Basic physiology and biochemistry]
Data on the general anatomy, physiology, and biochemistry of decapod crustaceans can
be found in the first four volumes of “Treatise on zoology – The Crustacea”, Schram’s
“Crustacea”, Bliss’ “The biology of Crustacea” (vol. 5), and Harrison’s “Microscopic
anatomy of invertebrates” (vol. 10). An extensive review of crayfish functional anatomy
considering the literature until the late 1990s is given in Holdich’s “Biology of freshwater
crayfish” (Vogt, 2002). A summary of these and an update are offered here.
Our picture of the structure and function of crayfish organs is mainly based on the inves-
tigation of a few species such as Astacus astacus (Linnaeus, 1758), Astacus leptodactylus
Eschscholtz, 1823, Pacifastacus leniusculus, Orconectes limosus (Rafinesque, 1817), Pro-
cambarus clarkii, Cherax destructor Clark, 1936, and Cherax quadricarinatus. In recent
years, the marbled crayfish has been added to this list. This emerging laboratory model is
the first parthenogenetic decapod described (Scholtz et al., 2003); it has been identified as
a parthenogenetic form of the slough crayfish, Procambarus fallax (Hagen, 1870), native
to Georgia and Florida, U.S.A. (Martin et al., 2010).
The location of the various organs in the crayfish’s body is illustrated in figs. 67.4
and 67.5. In the following, the organ systems are discussed with respect to structural-
functional relationships and, wherever appropriate, also with regard to freshwater adap-
tation, behavior, ecology, and evolution. Also emphasized are those structural-functional
phenomena, which have attracted the attention of general biology or applied sciences. The
material presented is based on the crayfish literature only and does not include generaliza-
tions made from other decapods. Due to space limitation, I have mainly cited the recent
literature. Readers interested in the older literature are referred to Vogt (2002).
Musculature
The musculature, the most voluminous tissue of crayfish and usually organized into
compact muscle bundles of up to several hundred fibers, is found in all parts of the
body but is particularly well developed in the posterior cephalothorax, the pleon, the
chelae, and the proximal articles of the pereiopods (fig. 67.6A). The muscles are either
attached to the inner side of the exoskeleton, the endophragmal skeleton, or chitinous
apodemes. Movements of the pleon and the limbs are usually effected by antagonistic
pairs of muscles, the flexors and extensors (fig. 67.6A). Exceptions of this general
Fig. 67.4. Schematic illustration of crayfish anatomy, showing main organs except musculature,
endocrine glands, and interoceptors. [After Vogt, 2002.]
Fig. 67.5. Transversal section of posterior cephalothorax of juvenile marbled crayfish, showing
organs in situ; arrow, ventral pericardial septum; arrowhead, ovary; bc, branchial chamber; bv,
branchiopericardial vessel; cu, cuticle; da, descending artery; ep, epidermis; gi, gills; he, heart; hg,
hindgut; ht, hepatopancreas tubule; li, ligament; mu, musculature; nc, nerve cord; pc, pericardial
cavity; sa, subneural artery. [After Vogt et al., 2009.]
Fig. 67.6. Musculature of crayfish. A, schematic illustration of thoracic and pleonal musculature;
B, ultrastructure of short-sarcomere fibers in claw musculature, showing typical features of cross-
striated musculature; C, scanning electron micrograph of muscle net around hepatopancreas tubule;
arrow, circular fibers; arrowhead, longitudinal fibers; cb, cell body of muscle cell. B, Cherax
destructor; C, Astacus astacus. [A, after Vogt, 2002; B, after West, 1997.]
scheme are found in the heart, hindgut, and hepatopancreas. The hepatopancreas tubules
are surrounded by a muscle net (fig. 67.6C), which appears particularly suitable to fill and
empty these blindly ending tubules. The hindgut has inner longitudinal and outer circular
muscle bands, which together generate peristaltic contractions that move the fecal strings
towards the anus (To et al., 2004). In the heart, the muscle fibers show a shears lattice-like
arrangement (fig. 67.7B), facilitating contraction of this hollow organ.
Skeletal, cardiac, and visceral musculature are generally cross-striated (West, 1997)
(fig. 67.6B). An exception is the poorly investigated musculature of the ovarian envelope,
which is multinucleate like the cross-striated musculature, but lacks stripes, thus resem-
bling smooth muscles (Vogt et al., 2004). Under the microscope, skeletal muscles appear
Fig. 67.7. Circulatory system of crayfish. A, schematic illustration of heart; B, histological section
of muscularis layer of heart, showing shears lattice like arrangement of muscle fibers (arrowhead);
arrows denote nodes of lattice; C, cardiac ganglion with cell bodies (cb) and axons (arrowhead)
of neurons; D, bulbus (bu) of heart (he) with valve (arrow), giving rise to dorsal abdominal
artery (daa) and descending artery (da); E, arteriole in hepatopancreatic hemal sinus (hs) lined
by an endothelium (en) only; F, hemal sinus between hepatopancreas tubules (ht) visualized by
hemocyanin immunofluorescence; gc, granulocytes; oc, oocyte; pc, pericardial cavity. B, C, E, F,
Astacus astacus; D, marbled crayfish. [A, B, C, E, F, after Vogt, 2002; D, after Vogt et al., 2009.]
composed of different fiber types varying in ultrastructure, histochemistry, and innervation

(West, 1997; Gruhn & Rathmayer, 2002). On the basis of their sarcomere length the muscle
fibers can be broadly categorized into three main types: short-sarcomere, intermediate-
sarcomere, and long-sarcomere fibers. Tonic fibers such as the superficial pleonal muscle
fibers, which are used for slow actions and postural activities, are mainly composed of
long sarcomeres. Phasic fibers such as the deep pleonal muscle fibers, which exert fast
contraction (tail flip) but low maximal tension, are mainly made up of short sarcomeres.
Giant sarcomeres were found in the claw closer muscles of Procambarus clarkii. These
sarcomeres are 8.3 μm long at rest, which is four times as long as vertebrate striated muscle
sarcomeres, and are extensible up to 13 μm (Fukuzawa et al., 2001).
The microscopic anatomy of crayfish muscles follows principally the scheme of cross-
striated musculature (Vogt, 2002) but shows peculiarities and intra-individual variation
with respect to the contractile apparatus, sarcomere matrix, and Ca2+ regulating system.
The contractile apparatus consists of actin, myosin, troponin, and tropomyosin. The
actin is rather uniform in all muscle fibers of crayfish, being structurally similar to
the actins of other animal taxa (Kang & Naya, 1993). The myosins, however, occur
in several isoforms and are at least partly responsible for the structural and functional
diversity of crayfish muscles (LaFramboise et al., 2000). However, even muscle fibers of
the same type can vary in the contractile apparatus as shown for fast fibers in the claw
and pleon of Cherax destructor, which differ in troponin composition and sensitivity to
Ca2+ (Koenders et al., 2004). The properties of the muscle fibers are not only determined
by the contractile apparatus but also by elastic proteins of the sarcomere matrix such
as the titins/connectins. These molecules connect the Z-line to the edge of the A-band
and are crucial for maximal extension and restoration of the normal sarcomere length.
In the claw closer muscle of Procambarus clarkii, a connectin with novel molecular
domains and features was detected, which allows the unusually high degree of stretching
described above (Fukuzawa et al., 2001). Even the Ca2+ regulating system (T-tubules,
sarcoplasmic reticulum, and Ca2+ -ATPase), which is essential for initiation and stopping
of muscle contraction, can vary considerably as shown for the phasic and tonic muscles of
Procambarus clarkii (cf. Ushio & Watabe, 1993).
The regulation of the muscles is well understood in some cases, but rather obscure in
others. The skeletal muscles are innervated by at least two axons, a glutamate releasing
excitatory and a GABA releasing inhibitory one, which lie side by side (DeMill &
Delaney, 2005). In the claw opener muscle of the walking legs of Astacus leptodactylus,
each muscle fiber is studded with approximately 2000 motor synapses and a smaller
number of inhibitory synapses. The hindgut musculature is also well innervated but differs
in several aspects from the skeletal muscles. It cannot experimentally be tetanized like the
skeletal muscles and has a myogenic pacemaker that induces slow contractions (Brenner
& Wilkens, 2001). Moreover, its longitudinal and circular muscle bands react differently to
myotropic peptides such as proctolin and crayfish peptide DF2 (Mercier & Lee, 2002). The
regulation of the muscle net around the hepatopancreas tubules is still a mystery, because
nerves have not been found in the hepatopancreas as yet (Vogt, 1994).
Crayfish muscles display a high degree of plasticity during ontogeny, molting, regen-
eration, and alteration of activity. For instance, in Procambarus clarkii identified fibers of
the superficial pleonal flexor increased in length from 20 μm at hatching to 400 μm in the
adult. The claw closer muscle of Orconectes rusticus includes only tonic long-sarcomere
fibers in the adults, but long- and short-sarcomere fibers in the pristine claw and the first
regenerate. Prior to ecdysis, the mass of the claw muscles of the chelipeds must be drasti-
cally reduced to be able to withdraw the chela through the narrow ischium-basis joint. This
reduction is caused by a specific mode of proteolysis, which reduces the thin actin con-
taining filaments to a higher degree than the thick myosin filaments (West, 1997; Mykles,
1999). Interestingly, despite the massive proteolysis of filaments, the contractile apparatus
is kept functional at all times. After ecdysis the fibers of all muscles must be elongated
to accommodate the new, larger exoskeleton. Stem cells, the so-called satellite cells, are
involved in this process in both skeletal and heart musculature (Martynova, 1993). Adapta-
tion of the musculature to increased activity is mainly achieved by structural and functional
modifications of the neuromuscular junctions (Cattaert & Le Ray, 2001).
Rapid movements of the musculature such as tail flipping generate electrical field po-
tentials that are positively correlated with the pleonal muscle mass (Patullo & Macmillan,
2004). Such traitorous signals may be detected by predators but are unlikely to be used for
communication among crayfish (Steullet et al., 2007).
The musculature is of great interest as a food commodity for humans. Its consistency,
biochemical composition, and nutritional value vary with the food and the physiological
status of crayfish (Pavasovic et al., 2007). Environmental pollutants can be deposited in
the musculature but, fortunately for the consumers, their concentrations are usually much
lower than in other organs (Guner, 2007). Some crayfish muscles have attracted broader
attention as research models or test systems. For instance, the pleonal muscles are used for
studying the principles of neuromuscular control (McCarthy & Macmillan, 1999) and the
claw muscles for investigating proteolysis (Mykles, 1999). The hindgut musculature has
for long been used as a pharmacological assay (Brenner & Wilkens, 2001).
Circulatory system
Crayfish have a well-developed open circulatory system responsible for the distribu-
tion of oxygen, nutrients, and hormones throughout the body, the transport of metabolic
waste products to the excretory organs, and the direction of immune defense components
to the infection sites. The vascular system becomes functional at about 40% of embryonic
development, when the heart starts beating, as shown in studies of the marbled crayfish.
The circulatory system is composed of the heart, arteries, arterioles, and hemal sinuses
(figs. 67.4 and 67.5). Two organs serve as pumps, the heart and, to a minor extent, the “cor
frontale”, which is a muscular extension of the ophthalmic artery (fig. 67.4) [but see chap-
ter 9 in volume 2 of this series]. The heart pumps the hemolymph into seven arteries, the
ophthalmic artery, the antennary arteries, the hepatopancreatic arteries, the dorsal pleonal
artery, and the descending artery (fig. 67.7A), which branch into smaller arteries and arte-
rioles supplying all organs and appendages. Some organs receive blood from two different
arterial systems. The antennary artery and the thoracic branch of the subneural artery, for
instance, supply the antennal gland (fig. 67.4). The arterioles discharge their blood into
hemal sinuses that surround and penetrate all tissues and organs (fig. 67.7F). The deoxy-
genated hemolymph from the organs and appendages is collected in the branchial sinuses
at the gill bases. It is then channeled through the gills, oxygenated, and transported to the
pericardial cavity via the branchiopericardial vessels (fig. 67.5), which are vessel-like
hemal sinuses.
The heart is located dorsally in the posterior cephalothorax (fig. 67.5) and is suspended
in the pericardial cavity by elastic ligaments (fig. 67.7A). The ventral septum of the
pericardium has a convex form (fig. 67.5) and includes eight pairs of muscles (fig. 67.7A).
Contraction of these muscles flattens the pericardial floor, resulting in an expansion of the
pericardial cavity and a simultaneous inflow of blood from the branchiopericardial vessels.
These events occur during contraction of the heart (systole), which increases the sucking
effect of the pericard. There are three pairs of ostia (fig. 67.7A) that control the inflow of
blood from the pericardial cavity into the heart and six valves that regulate its outflow from
the heart into the arteries. The ostia are controlled by compact circular muscle pads (Vogt,
2002), which close during systole and open during diastole. The semilunar flap valves
regulate blood flow from the heart to the arteries (fig. 67.7D) that open during systole and
close during diastole. All arteries with the exception of the dorsal pleonal artery and the
descending artery have their own valve. The latter two have a valve in common, which is
situated in the bulbus (fig. 67.7D). Each valve is composed of cross-striated musculature,
elastic fibers, and collagen fibers. Contraction of the muscle fibers stiffens the valve and
decreases blood flow through it.
The wall of the heart is composed of two layers, an outer adventitia and an inner
muscularis, which are separated by collagen fibers. The adventitia consists of large cells
that are filled with glycogen (Vogt, 2002), which may be mobilized during emergency
reactions and molting. The muscularis is made up of a network of cross-striated muscle
fibers that are either attached to each other (fig. 67.7B) or to the collagen fibers between
adventitia and muscularis. The arteries normally have no musculature and are composed of
an amorphous intima, a cellular endothelium, and a thick layer of collagen (Vogt, 2002).
The arterioles are lined by an endothelium only (fig. 67.7E). Sinuses are hemolymph
spaces lacking their own epithelium. They appear as narrow channels within tissues and
organs (fig. 67.11B), as broad lacunae (figs. 67.7F and 67.20D; see color insert) or as
vessel-like structures. Examples for the latter are found in the gills, and between gills and
pericardial cavity (fig. 67.5).
Reiber (1994) provided hemodynamic values for the cardiovascular system. For in-
stance, resting Procambarus clarkii kept at 25◦ C have a heart rate of 125 beats min−1 , a
stroke volume of 0.059 ml beat−1 , a cardiac output of 7.5 ml min−1 , a systolic pressure
in the heart chamber of 9.5 mm Hg, and arterial hemolymph flows of 1.3 ml min−1 in the
ophthalmic artery and of 5.2 ml min−1 in the descending artery.
The heart of adult crayfish is neurogenic, with four levels of regulation: the car-
diac ganglion, accelerating and inhibiting neurons, valve-regulating neurons, and neuro-
hormones (Harper & Reiber, 2001; Cooke, 2002). The cardiac ganglion is y-shaped and
located in the dorsal muscle layer of the heart with the legs of the Y opened cranially.
It includes 16 neurons with prominent cell bodies, which are wrapped in glial cells and
connective tissue (fig. 67.7C). Their axons branch to the muscle fibers of the muscularis
and the ostia, but not to the valves. The cardiac ganglion generates the basic rhythm of the
heart. This rhythm can be modulated by the accelerating and inhibiting nerves and neuro-
hormones from the pericardial organ, which can act on both the cardiac ganglion and the
heart muscles. The valves are regulated by separate nerves, which also branch to the mus-
cles of the pericardial floor (Vogt, 2002). This system can apparently regulate the stroke
volume and the distribution of blood among the various body regions. Interestingly, regu-
lation of the cardiac function differs between early juveniles and adults, because juveniles
do not react to experimental neurohormonal modulation (Harper & Reiber, 2001).
The hemolymph occupies approximately 27% of the body volume of crayfish and
consists of hemocytes (see Immune system) and plasma. Its total cation concentration
corresponds to 40% of sea water. Blood composition varies greatly, depending on the
animal’s activity status, molting stage, season, reproduction, etc. The most variable
substances in the hemolymph are sugars and lipids. The blood sugars occur mainly
as glucose and the lipids as high density lipoproteins, as demonstrated for Cherax
quadricarinatus (cf. Abdu et al., 2002). The most dominant protein in the hemolymph
is the oxygen carrier hemocyanin, which usually exceeds 90% of the protein fraction. The
rest includes the clotting protein and immune defense components. The hemocyanin is
synthesized in the hepatopancreas (Spindler et al., 1992) and forms a series of quarternary
structures composed of different subunits (Stöcker et al., 1988). The most frequent forms
are hexamers and dodecamers. Formation of polymers enhances the oxygen affinity of
hemocyanin.
Crayfish adapt to activity changes or environmental challenges such as toxicants,
hypoxia, increased temperature, or confrontation with conspecifics and predators by
alterations of the hemodynamic parameters (Schapker et al., 2002; Fedotov et al., 2006).
Periods of activity are generally characterized by a higher heart rate than the resting
periods, often resulting in a circadian rhythmicity of heart rate (Styrishave et al., 2007).
Long-term exposure to water-borne copper elicited a considerable reduction of heart rate
in Procambarus clarkii (cf. Bini & Chelazzi, 2006) as did hypoxia (Reiber & McMahon,
1998). During prolonged hypoxia, reduced heart rate was compensated by an increased
stroke volume, which maintained or even increased the cardiac output. A fascinating
long-term adaptation was observed in Astacus leptodactylus, which is able to modify
its hemocyanin pattern with temperature changes: the higher the temperature, the more
hexameres are present in the hemolymph at the cost of the dodecamers. This change is
caused by an alteration of gene expression for the various subunit types that built the
hexamers and covalently link two hexamers to a dodecamer (Decker & Föll, 2000). This
long-term adaptation of oxygen transport to temperature change is in sharp contrast to
short-term adaptation, which is regulated by modulation of the oxygen binding capacity of
the hemocyanins by protons, lactate, or urate.
The descending artery of crayfish is a hot candidate for becoming a model in research
on symmetry. This artery is normally unpaired and links the heart to the ventrally
located subneural artery (fig. 67.4), which supplies the mouthparts, chelipeds, walking
legs, nerve cord, and ventral thoracic and pleonal musculature with hemolymph. The
descending artery is an extraordinary structure because it originates dorsally from the
right or left subchamber of the bulbus, loops then on either side of the body around
the hindgut, traverses the ventral part of the body along the body mid-plane (fig. 67.5),
and terminates in an unpaired ventral vessel, which is also located in the body mid-
plane. In a genetically identical population of the marbled crayfish raised under identical
environmental conditions, this artery was either bilaterally symmetric (4.5% of specimens)
having dorsal branches on both sides of the hindgut, right asymmetric (45.1%), or
left asymmetric (50.4%), suggesting that symmetry variation is the result of stochastic
developmental events (Vogt et al., 2009). This organ may therefore be suitable to study
the mechanisms responsible for the maintenance and breaking of bilateral symmetry in
metazoans.
Immune system
Crayfish have an innate immune system, which provides rapid defense against infec-
tions in a generic way but does not confer long lasting immunity to the host. The im-
mune system includes hemolymph clotting, antimicrobial peptides, protease inhibitors,
phagocytosis, and, most importantly, melanization and encapsulation of pathogens and in-
fected tissue areas. Sealing of wounds by the clotting system is a first line of defense,
which keeps micro-organisms from entering the body. The crayfish clotting system con-
sists of a clotting protein and a transglutaminase that cross-links the clot (Theopold et
al., 2004). The clotting protein of Pacifastacus leniusculus is a dimeric protein consisting
of 210 kDa subunits. It is synthesized in the hepatopancreas and has no similarity to the
fibrinogen of vertebrates. The transglutaminase is released from the hemocytes and in-
jured musculature (Sritunyalucksana & Söderhäll, 2000). Phenoloxidase, the key enzyme
of the melanization-and-encapsulation process, can also participate in clot formation
under some conditions. Moreover, the broad-band protease inhibitor α2 -macroglobulin
is thought to be crosslinked to the clotting protein at the wound site to capture proteases
secreted by invading micro-organisms.
Another line of defense is provided by antimicrobial peptides. There are at least
five antibacterial peptides known from Pacifastacus leniusculus, three crustins, and two
astacidins (Jiravanichpaisal et al., 2007). The crustins are constitutively expressed by the
circulating hemocytes and kill Gram positive bacteria. Astacidin 1 is produced by cleavage
of a hemocyanin subunit under acidic conditions. It is 16 amino acid residues long and has
growth inhibiting effects on a broad range of Gram positive and Gram negative bacteria
(Lee et al., 2003). Release of astacidin 1 from hemocyanin is enhanced when crayfish are
injected with lipopolysaccharide or glucan, the typical components of bacterial and fungal
cell walls. Astacidin 2, a 14 amino acid residue peptide released from the hemocytes, is
effective against Gram positive and Gram negative bacteria as well (Jiravanichpaisal et al.,
2007). Crayfish have also defense mechanisms against viruses but these are only poorly
investigated. For instance, Pan et al. (2000) found antiviral activity in tissue extracts of
Procambarus clarkii that inhibited a variety of DNA and RNA viruses. Liu et al. (2006)
reported on the expression of an anti-lipopolysaccharide factor (ALF) in the hemocytes of
Pacifastacus leniusculus that can interfere with replication of white spot syndrome virus
(WSSV).
Invading micro-organisms usually sequester proteases, which must be eliminated from
the circulation because of their tissue-damaging effects. One mechanism of inactivation
is binding of protease inhibitors at the active site of the proteases. In the hemolymph
of Pacifastacus leniusculus there are at least two protease inhibitors of this type, which
are effective against fungal proteases: a subtilisin inhibitor and the trypsin inhibitor
pacifastin (Diéguez-Uribeondo & Cerenius, 1998). Another type of protease inhibitor is
α2 -macroglobuline, which is synthesized in the hemocytes. It is a broad-band molecular
trap that delivers the bound protease to phagocytotic hemocytes for degradation. The α2 -
macroglobulin of Astacus astacus is a disulfide bounded dimer and has an accessible
stretch of sequence with several cleavage sites for proteases. Cleavage of this region
induces a conformational change by which the protease is entrapped between the two
subunits of the molecule (Stöcker et al., 1991). Pacifastin and α2 -macroglobulin are
thought to have dual functions, inhibition of foreign proteases and regulation of the
enzyme cascade of the proPO system (see below). The α2 -macroglobulins comprise an
evolutionarily conserved arm of the innate immune system with similar structure and
function in major animal phyla (Armstrong, 2006).
Phagocytosis and melanization-and-encapsulation are cell mediated immune re-
sponses. There are three types of hemocytes in crayfish, hyaline cells, semi-granulocytes,
and granulocytes (Johansson et al., 2000; Giulianini et al., 2007). Hyaline cells are the
smallest of the three hemocytes, have a diameter of roughly 10 μm, and are character-
ized by a hyaline cytoplasm and tiny granules that are only visible under the electron
microscope. Granulocytes are the largest blood cells with diameters up to 20 μm. They in-
clude two populations of granules, large round ones and smaller elliptical ones (fig. 67.8B).
Semi-granulocytes are of similar size but include only small elliptical granules (fig. 67.8B),
which stain like the small granules of the granulocytes (Vogt & Rug, 1996). In Procam-
barus clarkii, hyaline cells are the most abundant hemocytes (75%), followed by the gran-
ulocytes (16%), and semi-granulocytes (9%) (Lanz et al., 1993). However, the number of
hemocytes and their relative frequency in the hemolymph can vary considerably and is
usually low during an infection (Johansson et al., 2000) because the hemocytes accumu-
late in the infected areas of the body and are spent for melanization and encapsulation of
the pathogens.
All types of hemocytes are produced in the hematopoietic tissue, which is located
dorsally on the stomach, in the hollow between cardiac and pyloric stomach (fig. 67.4).
In Astacus astacus the hematopoietic tissue consists of numerous lobules with tightly
packed stem cells and developing hemocytes (fig. 67.8A). These lobules are enveloped
by a meshwork of collagen fibers and are in close contact with hemal sinuses. Lack of
mRNA for pro-phenoloxidase in the cells of the hematopoietic tissue indicates that final
differentiation of the hemocytes is completed outside the hematopoietic tissue (Söderhäll
et al., 2003). It is believed that, under normal conditions, hemocytes are continuously
Fig. 67.8. Immune system of crayfish. A, histological section of hematopoietic tissue, showing
groups of differentiating hemocytes enclosed by collagen fibers (arrow); arrowheads, hemal sinuses;
B, ultrastructure of granulocyte with large (arrow) and small (arrowhead) granule types; C, early
stage of immune response against bacterial infection in hepatopancreas tubule; note concentration of
granulocytes (arrowheads) around tubule; D, advanced stage of immune response, showing enclosure
of degenerating hepatopancreas tubule (ht) by an inner melanin layer (arrow) and an outer layer of
aggregating hemocytes (arrowheads); E, degeneration of bacteria (arrow) in polymerizing melanin
mass; F, melanized fungus in cuticle; arrow denotes melanin layer; hs, hemal sinus; lu, lumen; n, cell
nucleus; sg, semigranulocyte. A-E, Astacus astacus; F, Pacifastacus leniusculus. [A, B, after Vogt,
2002; C, after Vogt & Rug, 1996; D, E, after Vogt, 2008c.]
released from the hematopoietic tissue. Release could experimentally be stimulated by

injection of β-1,3-glucan from the cell wall of fungi. Söderhäll et al. (2003) have developed
a method to culture hematopoietic tissue cells in vitro, which facilitates investigation of
hematopoiesis in crayfish.
Foreign material in crayfish is either phagocytized or isolated by melanization and
encapsulation. These reactions are mediated by the hemocytes. Apparently, all types of
hemocytes are to a certain degree capable of endocytosis (Giulianini et al., 2007). How-
ever, the hyaline cells are clearly the primary effectors of phagocytosis as shown in vitro
and in vivo (Vogt & Rug, 1996; Johansson et al., 2000; Giulianini et al., 2007). Melaniza-
tion and encapsulation constitutes the most important immune defense mechanism of cray-
fish (Sritunyalucksana & Söderhäll, 2000; Iwanaga & Lee, 2005; Cerenius et al., 2008).
The reaction is elicited by binding of pathogen associated molecules (lipopolysaccharide
in bacteria or β-1,3-glucan in fungi) to host recognition proteins, which are continuously
secreted from the hepatopancreas. This complex binds then to receptors of the hemocytes
and triggers their degranulation (Cerenius et al., 1994). The substances released, among
them pro-phenoloxidase, and further factors from the hemolymph provide a cascade of
proteases and inhibitors (proPO-system) that accomplish the controlled conversion of
pro-phenoloxidase into active phenoloxidase at the site of infection. The phenoloxidase
then generates melanin, which encloses the pathogens or the infected tissue areas. Cere-
nius et al. (2008) provides more detailed information on the various molecules involved in
the proPO-system.
The final result of the melanization and encapsulation reaction, which can also be
elicited by factors from damaged tissues, is either killing of the pathogen by melanization
(fig. 67.8F) or separation of the pathogen or damaged host tissue area by melanization
and encapsulation. The latter results in the formation of brown to black nodules, which are
composed of two layers, an amorphous inner melanin layer originating from the interaction
of the hemolymph and degranulating granulocytes (fig. 67.8C) and an outer cellular layer
mainly composed of semigranular hemocytes (figs. 67.8D and 67.20C; see color insert)
(Vogt & Rug, 1996). The enclosed pathogens and host tissue usually disintegrate as a
result of the cytotoxic action of intermediates of the melanin synthesis and the physical
shielding effect of the melanin layer (figs. 67.8D and 67.8E).
The crayfish immune system can be suppressed by environmental toxicants and
stimulated by certain food ingredients. For instance, exposure to episodic pulses of
aqueous aluminum increased the risk of infection in Pacifastacus leniusculus by impairing
the ability of the hemocytes to recognize and remove bacteria from the circulation (Ward
et al., 2006). On the other hand, glucans, lipopolysaccharides, and killed bacterial cells can
enhance individual components of the immune system as shown by in vitro experiments.
However, the use of such immunostimulants in crayfish culture is still controversially
discussed, because stimulatory effects in vitro do not necessarily translate into better health
when administered in large-scale outdoor culture (Smith et al., 2003).
Research on the immune system of crayfish has revealed some results, which go
beyond Astacida or Decapoda. For instance, pacifastin, first detected in Pacifastacus
leniusculus, is the eponymous prototype of the pacifastins, a new protease inhibitor
family that includes more than 40 members from crustaceans and insects (Kellenberger
& Roussel, 2005). Another example concerns cancer. Crayfish and other decapods are
significantly less affected by tumors than mammals, fish, insects, and bivalves, although
they have comparable life-spans and are exposed to similar carcinogenic impacts from the
environment and the food. The very low rate of carcinogenesis in decapods is apparently
related to peculiarities of their detoxification pathways, their immune system, and specific
mechanisms that ensure integrity of their stem cells throughout life (Vogt, 2008c).
Therefore, investigations on the immune response of crayfish to experimentally induced
neoplasias may contribute to the understanding of how an organism can successfully
prevent or control spontaneously and environmentally induced cell proliferation, which
may finally help to fight cancer in humans.
Respiratory system
The respiratory system is composed of the gills, which are located in the branchial
chambers at both sides of the cephalothorax (fig. 67.5) and serves for respiration and,
together with the antennal gland and digestive system, for osmoregulation, acid-base
homeostasis, and excretion of nitrogenous waste products. It also participates in removal
of particulate material from the hemolymph.
The gills attach near the bases of the five pairs of pereiopods and the three pairs of
maxillipeds (fig. 67.9A). According to their site of attachment, three types of gills are
distinguished. Pleurobranchs insert on the epimeral wall, arthrobranchs at the arthrodial
membrane between body wall and appendage, and podobranchs on the appendages.
Anatomically, crayfish gills are trichobranchiate, composed of a central axis that is
surrounded by up to 300 branchial filaments (fig. 67.9A, B). The pleurobranchs and
arthrobranchs of all crayfish families and the podobranchs of Parastacidae follow this
general scheme. The podobranchs of Astacidae and Cambaridae are more complex because
they have integrated an epipodal plate with a wing-like distal extension, the lamina
(fig. 67.9A). The number and arrangement of the gills varies among species and is
expressed in the branchial formula. The maximum number of gills per thoracomere
is four, for instance one podobranch, two arthrobranchs, and one pleurobranch in the
thoracomeres 5-8 of Astacus astacus. In most thoracomeres, however, there are fewer
gills. Particularly the pleurobranchs are often absent or rudimentary. For example, Astacus
astacus has a total of 18 functional and four rudimentary gills (Price et al., 1995; Bauer,
1998; Barradas et al., 1999; Batang & Suzuki, 2000; Vogt, 2002).
To allow exchange of gases, water must constantly flow over the gills. The water
current in the branchial chamber is created by beating of the scaphognathite, an exopod of
the second maxilla. This structure lies within the exhalant channel lateral to the mouthparts
(Lignot et al., 2005). Beating of the scaphognathite creates a forward ejection of water
below the antenna and a negative pressure in the branchial chamber, which causes water to
enter via inhalant channels between the limb bases. Dense, pappose setae fringing the limb
bases filter the inflowing water. The flow route of the water is directed over the mats of gill
filaments by the epipodites and laminae of the podobranchs. The frequency of ventilation
Fig. 67.9. Respiratory system of crayfish. A, arrangement of gills in gill chamber (podobranchs are
removed from pereiopods 1-3); arrow, lamina; arrowhead, gill filament; B, gill filaments (gf) and
intertwined setobranch setae (arrowheads); C, details of cleaning structures on setobranch seta; D,
electron micrograph of respiratory gill filament with thin cuticle and thin epithelium (ep); E, ion
transporting gill filament with much thicker cuticle and epithelium and extensive apical (arrow)
and basal membrane infoldings (bi); arrowhead, basal lamina; g, Golgi body; hs, hemal sinus; m,
mitochondrion. A, B, Procambarus clarkii; C, marbled crayfish; D, E, Astacus leptodactylus. [A, B,
after Bauer, 1998; D, E, after Barradas et al., 1999.]
depends very much on the status of activity, water temperature, and oxygen content of the
water. Adult Astacus astacus, for instance, have beating frequencies of the scaphognathite
of 44-150 beats min−1 and a ventilation volume of 0.2-0.8 litre · h−1 . Interestingly, the
scaphognathite beat is regularly reversed, for example in 2 of 112 beats in Procambarus
clarkii, which probably prevents blockage of the inhalant channels with debris (Reiber,
1994). Active ventilation starts during hatching, as observed in Procambarus clarkii and
in the marbled crayfish (Reiber, 1997a; Vogt, 2008a).
The vascular architecture and blood circulation of the gills have been investigated in
several species. Particularly good insight was obtained with latex casts (Dunel-Erb et al.,
1982). The deoxygenated hemolymph enters the gills from ventrolateral sinuses of the
thorax and flows then through the afferent vessels of the axis into the afferent vessels of
the filaments. Thereafter, it circulates through the lacunae where it is oxygenated. The
hemolymph leaves the gills via the efferent vessels of the gill filaments and axis and
is finally transported through the branchiopericardial vessels into the pericardial cavity
(fig. 67.5). The gills are composed of chief cells, pillar cells, connective tissue, and
nephrocytes. The chief cells make up the majority of the branchial epithelium, provide
a structural framework for the lacunae, synthesize the cuticle, and are responsible for all
molecular exchange activities. The connective tissue forms the septa between afferent and
efferent vessels in the axis and the filaments. Pillar cells are only present in the laminae
of the podobranchs and have a tensile role. Nephrocytes serve for hemolymph filtering
(Dickson et al., 1991; Barradas et al., 1999; Vogt, 2002).
Principally, each gill can be respiratory and ion-transporting, but both functions are
spatially separate, as shown for Procambarus clarkii and Astacus leptodactylus (cf.
Dickson et al., 1991; Barradas et al., 1999). Usually, the centrally located filaments of
a gill are ion-transporting and the marginal filaments are respiratory. The respiratory
epithelium is made up of extensions of the chief cells and has a diameter of only 2 μm
inclusive of the cuticle (fig. 67.9D), which is well within the range of the respiratory
epithelia of fish. With dimensions of this order, oxygen can easily be absorbed by
diffusion, facilitated by continuous blood circulation that creates a permanent oxygen
gradient. Astacus astacus can utilize 49-71% of the oxygen of the water. This efficiency is
comparable with that of cephalopods and fish. The thin respiratory epithelium is apparently
also used to eliminate CO2 and NH3 from the hemolymph. Ammonia/ammonium is the
major product of nitrogenous excretion in crayfish. A certain percentage of the CO2 and
NH3 may leave the gills as counterions of Cl− /HCO− + +
3 or Na /NH4 exchangers.
Because of the high permeability of the respiratory epithelia, there is a permanent
passive efflux of ions from the hypertonic hemolymph into the water. To compensate this
loss, ions are actively transported against the osmotic gradient back into the hemolymph.
The ion transporting epithelia, which are also made up of extensions of the chief cells, are
much thicker than the respiratory epithelia and are characterized by intense apical and basal
membrane infolding and plenty of mitochondria (fig. 67.9E). During intermolt the primary
concern is Na+ and Cl− balance, whilst around ecdysis the emphasis switches more to
Ca2+ regulation. Acid-base shifts that are caused by exercise and other conditions are
also compensated by branchial exchange of ions. Sodium apparently enters the epithelial
cells from the water via sodium channels in the apical membrane down an electrochemical
gradient that is generated by outward translocation of protons by V-ATPase. Transfer of
Na+ from the cell to the hemolymph is then affected by Na+ , K+ -ATPase located in the
extensive basal membrane infoldings (Mo & Greenaway, 2001; Kirschner, 2004). Ca2+
is probably transported via membrane potential dependent Ca2+ channels at the apical
membrane and basally located Ca2+ -ATPase and/or Na+ , K+ -ATPase (Gao & Wheatly,
2007). Waterborne silver interferes with ion transport in crayfish and results in decreased
influx and increased efflux of Na+ from the gill epithelium (Grosell et al., 2002).
A third function of the gills is apparently filtration of the hemolymph. In Pacifastacus
leniusculus this function was ascribed to the nephrocytes, which are large vacuolated
cells located in the walls of the efferent vessels. Ultrastructurally, they closely resemble
the podocytes of the antennal gland, having pedicels and a slit diaphragm. Due to
these structures and their ability to internalize ink particles from the hemolymph by
phagocytosis, they are thought to have a hemolymph filtering function. They may remove
particulate waste products and perhaps also viruses from the circulation, and eliminate
these by lysosomal degradation (Vogt, 2002). Martin et al. (2000) found a different mode
of removal of ink particles in the gills of Procambarus clarkii. There, injected ink particles
were phagocytosed by groups of hemocytes, which were then melanized and encapsulated.
Interestingly, these melanized nodules were attached to the inner surface of the gill cuticle
and removed from the tissue during the next molting.
The gills are intensely innervated but in Astacus leptodactylus electrophysiological
recordings revealed only mechanosensitive and proprioceptive functions (Ishii et al.,
1989). However, groups of oxygen-sensitive chemoreceptors are located in the walls
of the branchiopericardial vessels close to the gills. They respond to hypoxia and
hyperoxia and are also barosensitive. Ultrastructurally, they resemble the arterial chemo-
and baroreceptors of mammals (Kusakabe et al., 1991). In Procambarus clarkii, there
are apparently oxygen sensors in the branchial chamber, which selectively modulate
cardiovascular and ventilatory functions, but these receptors have not yet been identified
(Reiber, 1997b).
Cleaning of the gills is accomplished by the setobranch setae (fig. 67.9A, B)
and setae originating from the inner side of the branchiostegite (Bauer, 1998). These
setae are distributed between the gill filaments (fig. 67.9B) and are covered by rasping
microstructures (fig. 67.9C). Gill cleaning seems to act concomitantly with any type of
leg movement, because limb motion causes the setobranch setae to be jostled, scraping the
surfaces of the gill filaments. However, there is also a special gill cleaning behavior, limb
rocking, which is a stereotyped horizontal movement of the outstretched legs towards the
head in resting crayfish.
Two topics related to the respiratory system have recently gained broader attention,
the adaptation of crayfish to fresh water and the use of respiratory parameters for
the prediction of community changes under conditions of global warming. Invention of
hyperosmoregulation is one of the evolutionary keys of adaptation to fresh water, but
not all life stages of crayfish are able to hyperregulate. Crayfish embryos are unable to
osmoregulate during most of their development but are protected from the osmotic stress of
fresh water by their egg shell. The shift from osmoconformers to hyperregulators occurs
only during late embryonic development, i.e., hours or days before eclosion, as indicated
by the appearance of Na+ , K+ -ATPase in the differentiating cells of the gill filaments
of Astacus leptodactylus (cf. Lignot et al., 2005). Measurement of the respiration rate
at different experimental temperatures is regarded as a promising tool to predict which
species of crayfish in a given ecosystem will have bioenergetic advantages in the warmer
water bodies of the future (Whitledge & Rabeni, 2003). Such an approach may be of
particular value to assess the potential impact of subtropical invaders on temperate crayfish
under conditions of global warming.
Excretory system
Excretory organs eliminate metabolic wastes and xenobiotics and participate in the
regulation of blood homeostasis. In crayfish, these functions are distributed among the
gills, the digestive system, and the antennal gland. The latter is commonly considered
as the main excretory organ, although in crayfish it serves mainly for the discharge of
water that passively enters the body through the permeable gill epithelium. In order to
maintain the osmotic homeostasis of the hypertonic hemolymph, superfluous water must
permanently be withdrawn from the hemolymph and discharged from the body without
losing the electrolytes. This is done by the production of hypotonic urine in the paired
antennal glands. The gills excrete nitrogenous waste products, as described above.
The antennal glands are located in the anterior ventrolateral regions of the cephalotho-
rax (fig. 67.4) and open as elevated pores under the second antennae (fig. 67.11E). Each
antennal gland is a derivative of a single metanephridium linked to a rudimentary
coelom, the coelomosac. It consists of four morphologically distinct segments: coelo-
mosac, labyrinth, nephridial tubule, and bladder with nephropore (Schaffner & Rode-
wald, 1978; Fuller et al., 1989). In situ, this organization is not that obvious, because the
various segments are involuted into each other and covered by the bladder (fig. 67.10A).
In Astacus astacus and Procambarus clarkii, the antennal gland is supplied by two differ-
ent vessel systems (fig. 67.4) and two different nerves (Vogt, 2002). The ontogeny of the
antennal gland starts in early embryos; it becomes fully functional just before hatching, as
shown in Astacus leptodactylus (cf. Khodabandeh et al., 2005a, b).
The production of urine in crayfish is something special in Decapoda, in so far as
a hypotonic fluid is made from the ultrafiltrate of the hemolymph. Crayfish transferred
to higher salinities can shift to the production of urine isotonic with the hemolymph, as
shown for Procambarus clarkii (cf. Sarver et al., 1994). Synthesis of the urine includes
the processes of ultrafiltration, secretion, and reabsorption. The site of ultrafiltration is
Fig. 67.10. Schematic illustration of excretory system of crayfish. A, segments of antennal gland in
situ; B, coelomosac epithelium showing structures of ultrafiltration and way of ultrafiltrate (arrows);
n, cell nucleus. [After Vogt, 2002.]
Fig. 67.11. Excretory system of crayfish. A, ultrastructure of basal part of podocyte with pedicels
(pe), basal lamina (arrowhead), and slit diaphragm (arrow); B, histological section of labyrinth,
showing apocrine secretion (arrows); C, immunohistochemical demonstration of Na+ , K+ -ATPase
(arrows) in bladder (bl) and nephridial tubule (nt) of late embryo; D, release of urine plume, made
visible by intra-vascular injection of fluorescein; E, nephropore (arrow) and parts of fan organ in
juvenile; cs, coelomosac; em1, exopod of maxilliped 1; em2, exopod of maxilliped 2; hs, hemal
sinus; la, labyrinth; lu, lumen; us, urinary space; ys, yolk sac. A, Procambarus clarkii; B, Astacus
astacus; C, D, Astacus leptodactylus; E, marbled crayfish. [A, after Schaffner & Rodewald, 1978; B,
after Vogt, 2002; C, after Khodabandeh et al., 2005b; D, after Breithaupt & Eger, 2002.]
the coelomosac. Secretion of materials such as organic acids and heavy metals is mainly
performed by the epithelia of the coelomosac and the labyrinth, and reabsorption of ions,
glucose, and amino acids is carried out by the labyrinth, the nephridial tubule, and the
bladder. The bladder serves for accumulation and storage of the urine, e.g., for later use in
intraspecific communication. In adult Procambarus clarkii, the bladder can hold at least
0.4 ml. The urine is released through the nephropore, which is covered by an opercular
lip (fig. 67.11E). In Astacus astacus, the excretion of urine per hour amounts to roughly
0.2% of the body weight. The urine released corresponds to 30-40% of the primary urine
produced in the coelomosac. The rest of the primary urine is reabsorbed on its way to
the bladder. Considering that the hemolymph volume is 30% of the body weight, then
complete filtration of the hemolymph of a crayfish would last 2 to 2.5 days. The pH of the
urine is 6.6 compared to 7.8 of the hemolymph.
The coelomosac consists of a central chamber and numerous short, radiating tubules
that are closely intermingled with hemal sinuses. The single-layered coelomosac epithe-
lium is composed of podocytes that send out interdigitating foot processes, the pedicels
(Schaffner & Rodewald, 1978). These pedicels rest on a basal lamina and are bridged
by a slit diaphragm (figs. 67.10B, 67.11A). Both structures serve as mechanical filters
that are permeable for molecules up to 460 kDa and 70-150 kDa, respectively, as shown
for Procambarus clarkii (cf. Schaffner & Rodewald, 1978). It is highly probable that the
ultrafiltrate that is produced by these filtering structures takes its way into the coelomosac
lumen along the intercellular spaces (fig. 67.10B). There is, however, a second transcel-
lular transport route, which is mediated by basolateral endocytotic vesicles, intracellular
vacuoles, and apocrine secretion of such vacuoles (Vogt, 2002). This route is based on
chemical selection of particular molecules or substance classes rather than by mechani-
cal size selection, and Roldan & Shivers (1987) showed this is used for the elimination of
organic acids and heavy metals.
The segment following the coelomosac is the labyrinth; its epithelium is composed of
cuboidal to columnar cells that, unlike the coelomosac epithelium, possess a microvillous
border and basal invaginations of the plasma membrane. The labyrinth cells have
extensive surface blebbing (fig. 67.11B): blebs are thought to contain solutes (Fuller et al.,
1989), such as organic acids. The accumulation of organic acids in the lysosomal vacuoles
of the labyrinth gives the antennal gland its green color.
The nephridial tubule is highly convoluted and occupies the greatest portion of the
antennal gland (fig. 67.10A). In adult Procambarus clarkii, it has a length of 3 cm. It is
a specific adaptation to fresh water because in those marine decapods that produce urine
isotonic to the hemolymph this segment is lacking. The epithelial cells of the nephridial
tubule have no microvillous border but very intense basal invaginations associated with
numerous mitochondria, resembling the ion transporting cells of the gills. The basal
membrane includes Na+ , K+ -ATPase as immunocytochemically demonstrated in Astacus
leptodactylus (fig. 67.11C), and Ca2+ -ATPase (Khodabandeh et al., 2005b; Wheatly et
al., 2007). The bladder cells are usually flatter but have a similar ultrastructure and also
display intense Na+ , K+ -ATPase activity (fig. 67.11C) (Khodabandeh et al., 2005b). The
nephridial tubule and the bladder are the sites of ion reabsorption creating hypotonic urine.
Reabsorption rates of electrolytes in the antennal gland are 90-95% (Wheatly & Gannon,
1995). The final ionic concentration of the urine in intermolt crayfish is on average 22 mM
Na+ , 17 mM Cl− , and 1 mM Ca2+ . Glucose and amino acids penetrate the ultrafiltration
barriers but the urine is almost free of them. The sites and mechanisms of their reabsorption
have not yet been identified.
The antennal gland is also a main organ of detoxification of heavy metals and organic
xenobiotics. Lead injected into the hemolymph of Orconectes propinquus Girard, 1852
was exclusively detoxified in the antennal gland (Roldan & Shivers, 1987). The metal was
absorbed from the hemolymph by the coelomosac and labyrinth cells, and deposited in
lysosomes, which were then discharged by apocrine secretion and eventually excreted with
the urine. The continuous excretion of the lead-containing granules, and hence the absence
of excessive accumulation of the metal in the antennal gland, indicates that crayfish are not
suitable for a long-term monitoring of lead pollution. The antennal gland also possesses
cytochrome P450-dependent mixed-function oxygenases (MFO) (Jewell et al., 1997),
which play an important role in biotransformation of organic xenobiotics (James & Boyle,
1998). Using the polycyclic aromatic hydrocarbon benzo[a]pyrene as a test substance,
Jewell et al. (1997) found much higher MFO activity in the antennal gland of Procambarus
clarkii than in the hepatopancreas, the second important organ of detoxification of
xenobiotics. These authors also found differences in the generated metabolites, suggesting
that the detoxification pathways in the antennal gland and hepatopancreas are not identical
copies of the same machinery.
Urinary signals play a significant role in social interactions of crayfish. They are
used in the establishment of dominance hierarchies, male and female recognition, and
coordination of courtship, as shown in Astacus leptodactylus, Pacifastacus leniusculus,
and Procambarus clarkii (cf. Breithaupt & Eger, 2002; Simon & Moore, 2007; Berry
& Breithaupt, 2008; section Behavior). Moreover, predator-stressed crayfish can release
urinary signals that alarm conspecifics and cause them to move away from the source of
the signal (Zulandt Schneider & Moore, 2000). Chemical signaling can be modified by
changing the amount of urine released. For instance, urine release is higher at increased
levels of aggression and during stress. The pheromones discharged with the urine are not
yet identified but are probably hormones from the hemolymph that circulate in higher
concentrations under conditions of aggression or stress and, accordingly, pass the filters of
the coelomosac in higher amounts. The regulation of urine release may be facilitated by the
separate nervous regulation of the bladder and the capping structure of the nephropore. The
urine plume can be channeled in practically all directions in a variety of flow fields, and
even as water jets (fig. 67.11D). The motors for these movements are the forward-directed
gill current and, more importantly, the fan organ, which is composed of the feathered
exopods of the maxillipeds 1 to 3 (fig. 67.11E). This fan organ can produce water currents
away from the body but can also propel odor molecules from the surroundings to the frontal
sense organs of the crayfish, to scan the environment and to search for food (Breithaupt,
2001).
Digestive system
The digestive system is the most voluminous organ system of crayfish except for the
musculature (fig. 67.4) and is composed of three regions: the foregut including esophagus
and stomach, the midgut including midgut canal, midgut cecum and hepatopancreas, and
the hindgut (figs. 67.12 and 67.13A). A cuticle that is shed at each molt lines the foregut
and hindgut. The digestive tract serves for processing of the food, supply of the body
with metabolites, storage of nutrient and energy reserves, synthesis of blood proteins and
vitellogenins, and detoxification of xenobiotics.
The food is torn in pieces by the mouthparts, which are rich in cutting structures,
pestles, and mechano- and chemoreceptors (Garm, 2004). It is lubricated at the entrance
Fig. 67.12. Schematic illustration of digestive system of crayfish: a, antechamber of hepatopancreas;

cf, cardiac filter; cpfc, cardiopyloric filter channel; cpv, cardiopyloric valve; dlc, dorsolateral pyloric
channel; g, gastrolith; hiv, hepatopancreatic-intestinal valve; mpc, medial pyloric chamber; mt,
medial tooth; pf, pyloric filter; piv, pyloro-intestinal valve; rlt, right lateral tooth. [After Vogt, 2002.]
of the esophagus by mucus secreted from subtegumental glands (Brown, 1995). The
esophagus channels the food into the stomach but is also used for vomiting indigestible
food components that are too large to pass through the cardiopyloric valve. It is a short,
vertically oriented tube (fig. 67.12) with a deeply infolded inner surface and an extensive
musculature, which facilitate intake of larger food items. Close to the entrance into the
stomach there are two sensory fields, which in Astacus astacus consist of 40-60 sensilla
(Altner et al., 1986). Two chemoreceptors and one mechanoreceptor are harbored by each
sensillum. The chemoreceptors respond to gastric fluid and nicotinamide derivatives,
which are ubiquitous in living organisms. The mechanoreceptor reacts to stretch of the
esophageal wall.
The stomach is divided into two parts, the anterior cardiac stomach, which serves
for physical and chemical breakdown of the food, and the posterior pyloric stomach,
which filters the chyme (fig. 67.12). It is armed by a system of calcified cuticular ossicles
that support the gastric mill, participate in formation of the pyloric filter, and provide
attachment sites for the extensive musculature of the stomach. The gastric mill mainly
consists of two prominent lateral teeth with large denticles and one medial tooth attached
Fig. 67.13. Digestive system of crayfish. A, transversal section of cephalothorax of stage 1 juvenile,
showing yolk sac (ys), midgut (m), and developing hepatopancreas (he); B, section of gastrolith
pocket with partly resolved gastrolith; C, gastric mill composed of lateral teeth and medial tooth; D,
scanning electron micrograph of pyloric filter tubes; E, transversal section of hepatopancreas tubule,
showing unspecific esterase activity at cell apices (arrow) and at cell bases (arrowheads), indicating
absorption of nutrients from the lumen and delivery of metabolites to the hemolymph, respectively; F,
astacin immunofluorescence in Golgi bodies (arrow) of enzyme synthesizing F-cells (fc); G, storage
of glycogen (gl) and lipid (li) in hepatopancreatic R-cell; bc, B-cell; gc, gill chamber; hs, hemal
sinus; n, cell nucleus; nc, nerve cord; rc, R-cell. A, B, marbled crayfish; C, Orconectes limosus; D-
G, Astacus astacus. [A, B, after Vogt, 2008a; D, G, after Vogt, 2002; F, after Möhrlen et al., 2001.]
to the roof of the cardiac stomach (figs. 67.12 and 67.13C). These teeth are made up
of cuticle and are replaced by each molt. The basic movement of the gastric mill is
effected by a system of lever-like ossicles and relatively few muscles that drive this lever
system. Further muscles can then intervene to modify the basic movement, resulting in a
variety of cutting, grinding, and squeezing movements (Böhm, 1996). Basically, the gastric
mill of crayfish seems to be adapted to omnivory because even detritus-feeding cave-
dwelling crayfish have denticulate teeth. In the anterior part of the cardiac stomach there
are two lateral pouches, which synthesize the gastroliths (fig. 67.13B). These calcium-
storing structures first appear in hatchlings. They are then formed prior to each molting
and completely resolved after ecdysis (Shechter et al., 2008). Gastroliths are a specific
adaptation to fresh water, where calcium is less available than in seawater. In former times,
gastroliths were popular drugs in traditional medicine and mainly used for treatment of
pyrosis.
The cardiac stomach is always filled with a brownish, bitter tasting digestive fluid,
which can easily be withdrawn with a pipette. In adult Astacus astacus, this fluid has an
average pH of 5.6 and a volume of about 0.4 ml per stomach. It includes 50 mg protein
per ml and comprises a variety of digestive enzymes and a fat emulsifier (Vogt et al.,
1989). When the food enters the cardiac stomach, it is mixed with this fluid and repeatedly
masticated until a chyme with a fluid consistency is created. This chyme is then transported
to the hepatopancreas via the cardiopyloric filter channels and thereby filtered twice, a
first time by the cardiac filters located in the floor of the cardiac stomach and then a second
time by the pyloric filters. The solids are transferred through the cardiopyloric valve into
the medial chamber of the pyloric stomach, and from there via the midgut to the hindgut
(fig. 67.12).
The pyloric stomach is a complicated structure subdivided into three stories, a dorsal
chamber with the dorsolateral channels, a medial chamber, and two ventral chambers
(Vogt, 2002). Each of the ventral chambers includes a press plate and numerous filter
tubes covered by dense mats of setae (fig. 67.13D) that retain particles larger than 50-
100 nm. These filter tubes terminate in the antechamber of the hepatopancreas. The medial
chamber of the pyloric stomach serves for formation of the fecal pellets. The role of
the dorsal chamber and the dorsolateral channels is still obscure. These compartments
supposedly transport fluid back to the stomach that is squeezed out from the fecal bolus.
However, they may also serve for a retrograde transfer of the gut content to the stomach
for reprocessing as I have repeatedly observed in transparent shrimps. The entire foregut is
under the control of the stomatogastric nervous system, which includes the stomatogastric
ganglion, the esophageal ganglion, and the commissural ganglia as higher centers (Böhm,
1996; Skiebe, 2003).
The midgut is functionally less significant than other parts of the digestive tract because
it is very short (fig. 67.12), in contrast to the conditions in most other decapods. The
midgut probably produces the peritrophic membrane that envelops each fecal pellet.
The midgut cecum is a relic of an embryonic connection between midgut and yolk sac
(fig. 67.13A). Despite this luminal connection, the main digestive tract is apparently not
involved in yolk digestion of late embryos and the first postembryonic life stages. Its
breakdown is rather accomplished by the yolk sac epithelium that seems to secrete the
necessary enzymes, first of all trypsin (Luo et al., 2008). Thus, digestion of yolk in the yolk
sac and digestion of food in the digestive tract can occur concomitantly, which facilitates
transition from endogenous to exogenous feeding in crayfish. In the astacids this transition
occurs in postembryonic stage 2 and in the cambarids and parastacids in stage 3 (García-
Guerrero et al., 2003; Vogt, 2008a).
The hindgut transports the feces to the exterior, harbors bacterial symbionts, is
involved in rapid uptake of water after ecdysis, and seems to contribute to ion- and
osmoregulation. Cross sections of the hindgut of Astacus astacus typically show six
longitudinal folds, which are lined by a relatively thick cuticle and a single-layered
epithelium that is composed of one columnar cell type without microvilli. Exterior to the
epithelium follows a thick layer of spongy connective tissue and longitudinal and circular
musculature. This musculature produces peristaltic and antiperistaltic movements. Two
nerves originating from the terminal ganglion run on either side of the hindgut and
regulate activity of this organ (Vogt, 2002; To et al., 2004). The hindgut of crayfish
often harbors a remarkable microflora. In Astacus astacus, Astacus leptodactylus, and
Pacifastacus leniusculus from Lithuania, a total of 350 bacterial strains have been
identified, mainly Pseudomonas, Aeromonas, and Enterobacteriaceae (cf. Mickėnienė,
1999). Their concentration amounted to 106 -108 bacteria per gram gut content. In
Pacifastacus leniusculus, this microflora produced 18 essential amino acids, which may
contribute to crayfish nutrition.
The hepatopancreas can be considered as the central organ of metabolism in crayfish
because it executes intestinal, hepatic, and pancreatic functions. It synthesizes digestive en-
zymes, lipid emulsifiers, blood proteins, and vitellogenins, absorbs the nutrients, provides
other organs with metabolites, and stores nutrient and energy reserves. It also participates
in detoxification of heavy metals and organic xenobiotics. The hepatopancreas occupies
most of the thoracic cavity and is composed of two half organs, which are linked to either
side of the pyloric stomach (fig. 67.4). Each half organ consists of hundreds of blindly
ending tubules, which fuse to form collecting ducts that finally terminate in the antecham-
ber (fig. 67.12). The hepatopancreas tubules are composed of a single-layered epithelium
that is enveloped by a close-meshed muscle network and surrounded by hemolymph (figs.
67.6C, 67.7F, 67.13E, and 67.20D; see color insert). The epithelium includes five cell
types, embryonic (E-cells), resorptive (R-cells), fibrillar (F-cells), blister-like (B-cells),
and midget (M-cells) (Vogt, 1994, 2002). R-, F-, and B-cells bear a microvillous border
and have contact to both the luminal and hemolymph side of the tubule. The E-cells, which
are exclusively located at the blind ends of the tubules, give rise to R-, F-, and B-cells. The
origin of the M-cells has not yet been clarified. As they age, the hepatopancreas cells are
gradually pushed down the tubules by mitotic pulses of the E-cells, generating a distinct
age gradient along the tubules. Migration of the cells from the tip of the tubule to the an-
techamber, where they are discharged from the epithelium, lasts approximately two weeks.
The nutrients are mainly absorbed by the R-cells as indicated by radioactive tracers
and temporal monitoring of the histochemical patterns of those enzymes that are involved
in final breakdown and intracellular conversion of the nutrients (fig. 67.13E). The
nutrients are absorbed in molecular form probably by carriers for monosaccharides, amino
acids, and dipeptides. The R-cells are also major storage sites for lipids and glycogen
(fig. 67.13G). These reserves are used during starvation, molting, and vitellogenesis. Lipids
are secreted from the R-cells into the hemolymph as high density lipoprotein particles
(HDL), which include phospholipids as a major lipid component. In Cherax destructor,
this HDL has a molecular mass of 95 kDa (Abdu et al., 2000).
The hepatopancreas synthesizes a broad variety of carbohydrases, lipases, and pro-
teinases including cellulase and astacin that can cleave native collagen without prior acidic
denaturation (Vogt et al., 1989; Vogt, 2002; Crawford et al., 2005). The digestive enzymes
are synthesized in the F-cells as shown by immunocytochemistry (fig. 67.13F). After syn-
thesis in the rER (rough endoplasmic reticulum) and passage through the Golgi bodies,
the enzymes are directly discharged into the hepatopancreas lumen and transferred to the
cardiac stomach, where they await the next meal in an active form (Vogt et al., 1989;
Vogt, 2002). There is no intracellular storage within zymogen granules as in the vertebrate
pancreas. Astacin is certainly the best investigated of all crayfish enzymes. It occurs in a
concentration of 1 mg per ml in the gastric fluid. It is a zinc-endopeptidase composed of
200 amino acids and has a molecular mass of 22 614 Da. Its gene has been sequenced and
its three-dimensional structure resolved (Geier et al., 1997; Vogt, 2002). Astacin is synthe-
sized as an inactive pro-enzyme and is activated on its way to the stomach (Möhrlen et al.,
2001). When Astacus astacus was fed with a single portion of meat, the cardiac stomach
was emptied in the following 3-4 hours and refilled with new digestive fluid after about
4-5 hours (Vogt et al., 1989). A similar pattern of refilling of the stomach with digestive
fluid was observed in Cherax quadricarinatus (cf. Loya-Javellana et al., 1995).
The function of the B-cells is still obscure, but there is evidence that they may
be involved in synthesis and recycling of lipid emulsifiers (Vogt, 2002). The M-
cells are individually located at the hemal side and show the typical ultrastructure of
a peptide synthesizing endocrine cell (fig. 67.17A). They either regulate neighboring
hepatopancreas cells or the activity of the muscle net, which has no neuromuscular
synapses (Vogt, 1994).
The hepatopancreas is also a major site of detoxification of xenobiotics. Heavy metals
are mainly removed by storage excretion either in the R-cells or F-cells. For instance,
copper is deposited as inert sulphite in the lysosomes of the R-cells. Iron, in contrast, is
mainly accumulated in the F-cells and only to a lower degree in the R-cells (Roldan &
Shivers, 1987; Vogt, 2002). Such lysosomal granules usually accumulate in the cells with
increasing age and leave the epithelium in the antechamber region, where the aged cells
disintegrate. In feeding crayfish, the turnover period of the hepatopancreas cells is about 2
weeks and, accordingly, the heavy metal load of the hepatopancreas reflects 2 weeks only.
In starving crayfish, however, the mitotic activity is almost suspended resulting in a longer
retention time of the metals in the hepatopancreas. Heavy metals can also be detoxified by
binding to cytoplasmic metallothioneins as shown for cadmium, which induced expression
of a 12 kDa metal-binding protein in Procambarus clarkii (cf. Del Ramo et al., 1989). The
hepatopancreas of crayfish is also capable of detoxifying organic compounds with the help
of cytochrome P450. This can be deduced from the occurrence of cytochrome P450 in the
hepatopancreas (James & Boyle, 1998) and its induction after injection of TCDD (2,3,7,8-
tetrachloro-dibenzo-p-dioxin) in Pacifastacus leniusculus (cf. Ashley et al., 1996).
Feeding experiments with the marbled crayfish revealed that food is internalized and
processed only from juvenile stage 3. The reason for this rather late onset of active food
uptake in crayfish becomes clear from data on the development of the digestive tract and
the mouthparts (Vogt, 2008a). The pyloric filters are well developed in stage 1 already,
whereas the gastric mill has sclerotized teeth only from stage 2. The mouthparts, however,
are only sparsely studded with setae in this life stage and appear not yet ready for the
processing of food. The hepatopancreatic cell types are discernable in stage 1 but only
the R-cells seem to be functional. They accumulate increasing amounts of lipid droplets,
reflecting a gradual transfer of energy carriers from the yolk sac to the hepatopancreas
via the hemolymph. García-Guerrero et al. (2003) made a similar observation in Cherax
quadricarinatus. The other hepatopancreatic cell types are active only from stage 3.
Hammer et al. (2000) measured an increase of the specific activities of three digestive
enzymes, α-amylase, trypsin, and non-specific esterase, in Procambarus clarkii before
food was internalized for the first time, indicating that the molecular digestive competence
is attained shortly before the onset of feeding in stage 3.
Three topics are briefly outlined at the end of this section, which are either unique
in the animal kingdom or of broader biological significance. The first issue concerns
the hindgut of stage-1 juveniles of Cambaridae. During molting into stage 2, the cuticle
of the hindgut is shed later than the exoskeleton, thereby generating the anal thread.
This structure acts as a safety line that secures the freshly molted juvenile to the
maternal pleopods via the hooked-in stage-1 exuvia (Vogt, 2008a). The second topic is
the astacins, a protein family that is widespread in the animal kingdom, among them the
bone morphogenetic protein of humans (Möhrlen et al., 2006). Astacins have in common
that they act in the extracellular space either freely or membrane-bound. However, they
have remarkably different functions such as digestion of nutrients, regulation of the
extracellular matrix, wound healing, or breakdown of the egg envelope during hatching.
Their eponymous prototype, which was used to reveal basic data and the three-dimensional
structure, is the digestive enzyme astacin from Astacus astacus (cf. Vogt, 2002). A third
topic of broader interest is the preferred feeding of brooded juveniles on maternal feces
and food particles that fall down from the mouthparts of the mother (Vogt, 2008a). This
behavior may be evoked by the weaker consistency or smaller size of these food sources
but could also be a measure to acquire symbiotic bacteria or to learn, which food is best
suitable. If that peculiar behavior is innate, it would be a simple mechanism to transmit
knowledge on salubrious food sources across generations.
Reproductive system
The reproductive system is located in the posterior cephalothorax between peri-
cardium and intestine (figs. 67.4, 67.5) and consists of the gonad, two descending ducts,
and the gonopores. There are additional external reproductive organs, like the glair glands
and the annulus ventralis in females, and the gonopods in males. The appearance of the
gonads and their extension in the body depend on age and reproductive status of the indi-
viduals. In hatchlings they are already present but very small. In adults they are periodically
enlarged during the breeding seasons and change color according to the maturation stage
of the germ cells. In cambarids, the sexes can be distinguished from juvenile stage 4.
The female reproductive system is composed of the ovary, the oviducts, and the
gonopores on the coxae of the third pereiopods (figs. 67.15A, 67.20A; see color insert).
In Astacidae and Cambaridae, the ovary is trilobed, consisting of two anterior branches and
an unpaired posterior branch (fig. 67.15A), but in Parastacidae it is composed of two lobes
that are grown together in the middle (Noro et al., 2008). The oviducts arise laterally at the
ovary and run straight down to the gonopores (fig. 67.15A). They lead the oocytes to the
exterior and synthesize a milky fluid of unknown identity prior to spawning. The annulus
ventralis is only found in Cambaridae. It is a cuticular spermatheca that originates from
the posterior part of the seventh sternite (Vogt et al., 2004). Glair glands are present in the
females of all families and are located on the underside of the pleon inclusive of the tail
fan. These whitish glands become periodically active during the reproductive seasons and
are involved in the attachment of the eggs to the pleopods. They are good indicators of
forthcoming spawning.
In hatchlings of the marbled crayfish, the ovary is so small that it can be detected
only on histological sections (Vogt, 2007). It contains only one or two pre-vitellogenic
oocytes. Oviducts are not yet present at that time. The number of oocytes increases during
the following life stages and amounts to a few dozen in stage 6. Primary vitellogenesis,
which is characterized by the accumulation of yolk and enlargement of the oocytes, starts
in stage 7. First spawning usually occurs around the fifteenth postembryonic life stage.
Formation of the annulus ventralis and the gonopores was first visible in stages 4 and 5,
respectively (Vogt et al., 2004).
Each branch of the ovary is made up of the ovarian envelope, the interstitium, oogenetic
pouches, oocytes, the ovarian epithelium, germaria, and the ovarian lumen (fig. 67.14A).
The ovarian envelope consists of muscle cells, collagen fibers, elastic fibers, and hemal
sinuses. The muscle cells are multinucleate but non-striated. The ovarian envelope is thin
in pre-vitellogenic females and increases in thickness with each spawning. Oogenetic
pouches are formed by segments of the ovarian epithelium that bulge towards the ovarian
interstitium and transform into follicle epithelia whilst colonized by oocytes (figs. 67.14A
and 67.15B). The interstitium between the oogenetic pouches and the ovarian envelope is
a loose meshwork of musculature, connective tissue, and hemal sinuses.
The germaria are concentrated in the central part of the ovarian lobes and bulge from
the ovarian epithelium towards the lumen. They include the oogonia and produce the
oocytes. In the marbled crayfish, three stages of oocytes could be clearly distinguished
due to their size and staining properties (Vogt et al., 2004). Previtellogenic oocytes have
a diameter of ca. 20 to 100 μm, stain deeply violet with Azan, and are found either in
the germaria or in the ovarian lumen (figs. 67.15B and 67.20B; see color insert). Primary
vitellogenic oocytes have a diameter of ca. 100 to 250 μm, stain pale orange to red and are
located in the oogenetic pouches (figs. 67.15B and 67.20B; see color insert). Secondary
vitellogenic oocytes measure 250 to 1300 μm and stain blue to purple (Vogt et al., 2004).
Fig. 67.14. Schematic illustration of reproductive system of crayfish. A, architecture of ovary; B,

spermatozoon with extended radial arms. [A, after Ando & Makioka, 1998; B, after Vogt, 2002.]
Growth of the oocytes is predominantly characterized by the deposition of lipid and

yolk globules (fig. 67.15C). The lipid is used by the developing embryo as an energy
source and the yolk as a source for proteins, lipids, and carbohydrates. The yolk mainly
consists of vitellin, a lipoglyco-carotenoprotein, which in Cherax quadricarinatus is com-
posed of subunits of 75-177 kDa (Khalaila et al., 2004). Serrano-Pinto et al. (2004) found
in the same species two vitellins with native molecular masses of 440 and 470 kDa. The
oocytes are apparently able to synthesize yolk from primary vitellogenesis (fig. 67.15C)
until ovulation, but during secondary vitellogenesis yolk precursors, the vitellogenins, are
additionally produced in the hepatopancreas, secreted into the hemolymph, transported to
the ovary, absorbed by the follicle cells, and transferred to the oocytes (Abdu et al., 2002;
Vogt, 2002; Serrano-Pinto et al., 2004). Serrano-Pinto et al. (2004) analysed the cDNAs
from the hepatopancreas and ovary of Cherax quadricarinatus and found that there are
at least two different vitellogenin genes. It is not known whether the follicle cells serve
only for transcytosis of the vitellogenins or whether they participate in their processing.
In any case, these cells act as mediators because the oocytes have no direct contact to the
hemolymph (fig. 67.15C). The constituents of the lipid droplets also originate from the
hepatopancreas and are transported to the ovary via the hemolymph (Vogt, 2002).
The male reproductive system is composed of the testis, two vasa deferentia, and
the gonopores on the coxae of the fifth pereiopods. Astacids and cambarids additionally
have paired gonopods, which are composed of the first and second pleopods. Like the
ovary, the testis is Y-shaped in Astacidae and Cambaridae and composed of two parallel
lobes in the Parastacidae (Vogt, 2002; López Greco et al., 2007). It is lined by a cortex
of connective tissue and includes numerous seminiferous tubules and collecting ducts that
terminate in the vasa deferentia. The seminiferous tubules include Sertoli cells and various
developmental stages of germ cells (fig. 67.15D) (Krol et al., 1992). Spermatogenesis
Fig. 67.15. Reproductive system of crayfish. A, female reproductive system composed of y-shaped
ovary (ov), oviducts (od), and gonopores (arrow) at coxae of 3rd pereiopods; B, histological section
of ovary, showing primary vitellogenic oocytes (po) in oogenetic pouches and previtellogenic
oocytes (arrowhead) in ovarian lumen (ol); arrow denotes invasion of oogenetic pouch by previtel-
logenic oocyte; C, electron micrograph of oocyte, showing synthesis of yolk particles (arrowhead)
in rough endoplasmic reticulum (rer) and deposition of yolk granules (yg) and lipid droplets (ld)
in cytoplasm; note interdigitation of microvilli (arrow) of oocyte and neighboring follicle cell (fc); D,
is synchronous within individual seminiferous tubules but can vary between the tubules
as shown for Procambarus clarkii (fig. 67.15D). The spermatogonia divide and undergo
meiosis, thereby developing through primary and secondary spermatocytes into spermatids
(Hinsch, 1993). The spermatids then develop into mature spermatozoa by formation of the
acrosome and radial arms, condensation of the chromatin and elimination of a considerable
part of the cytoplasm, inclusive of cell organelles. The Sertoli cells are in close contact with
the germ cells throughout differentiation and appear to play a role in resorption of excess
cytoplasm from the differentiating spermatocytes. They are probably also involved in the
production of the mucopolysaccharide capsule that envelops each spermatozoon.
The vasa deferentia are highly convoluted ducts that arise from each side of the testis
and open at the gonopores. They are lined by a single-layered secretory epithelium and
serve for packaging of the sperm into spermatophores (fig. 67.15E) and storage of
the spermatophores until mating. The mature spermatophore consists of a central sperm
mass and a three-layered wall (López Greco & Lo Nostro, 2008). During the mating
season, spermatophores are deposited either on the ventral surface of the females or, in
cambarids, in the annulus ventralis. Following ejaculation, the spermatophore becomes
gradually hardened in the water. Such spermatophores are resistant to environmental stress,
which helps the sperm to survive the days or weeks between mating and spawning. The
free spermatozoa are aflagellate and follow in general the scheme given for reptantian
decapods (fig. 67.14B) (Krol et al., 1992). Their acrosome consists of subcompartments
that vary in structure and staining behavior (fig. 67.15F). Radial arms are present in
Astacidae and Cambaridae but are lacking in Cherax (cf. Beach & Talbot, 1987). Their
number varies greatly among species. For instance, Procambarus clarkii has 4 arms
and Astacus astacus has more than 20 arms. These arms extend after the release of the
spermatozoa from the spermatophore. Upon contact with the egg, the acrosome penetrates
the chorion and propels the nucleus into the egg.
Spawning and fertilization of the eggs is accompanied by a remarkable sequence of
events and behaviors of the female (Vogt & Tolley, 2004). It is initiated by formation of a
fertilization pouch by bending the pleon towards the underside of the cephalothorax. This
pouch is then filled with a gelatinous mass that probably originates from secretions of the
glair glands and perhaps also from the oviducts. Thereafter, the sperm is mobilized from
the spermatophores and mixed with the released oocytes. Release of the spermatozoa
from the spermatophores is achieved either mechanically by the female or, more likely,
by chemical dissolution of the spermatophore wall in the specific environment of the
fertilization pouch. Finally, the fertilized oocytes are attached to the pleopods for
section of testis showing seminiferous tubules with Sertoli cells (sc), spermatogonia (arrow),
spermatocytes (sp), and spermatids (arrowhead); E, group of spermatozoa (arrow) in vas deferens
surrounded by epithelial secretions (es); F, spermatozoon with nucleus (n), acrosome (a) and confined
radial arms (arrow); hs, hemal sinus; in, interstitium; m, mitochondrion; n, cell nucleus; oe, ovarian
envelope. A-C, marbled crayfish; D, Procambarus clarkii; E, F, Astacus astacus. [A, B, C, after Vogt
et al., 2004; D, after Krol et al., 1992; E, F, after Vogt, 2002.]
brooding. Attachment of the eggs requires rolling and turning movements of the female
and can last many hours (Vogt & Tolley, 2004).
Intersexes, which occasionally occur in a broad range of species from all crayfish
families (section Reproduction), usually have male and female external sex characteristics
but only rarely mixed male and female gonads. Typically, such ovotestes are composed
of one active testicular lobe and one ovarian lobe containing oocytes arrested in the
previtellogenic stage (Sagi et al., 2002). They are probably the result of a unilateral
dysfunction of the androgenic gland. Ovotestes with histological signs of regression of the
testicular tissue and partial replacement by ovarian tissue were found in three specimens
of the putative protandric hermaphrodite Parastacus defossus Faxon, 1898 from the wild
(Noro et al., 2008). However, the complete transformation of a functional testis into a
functional ovary, or vice versa, has not yet been demonstrated for any crayfish specimen.
Endocrine system
The endocrine system of crayfish consists of organs that are either of neuronal or
epithelial origin. The neuroendocrine organs are usually composed of two parts, a
hormone producing somata cluster (fig. 67.17B) and a hormone releasing neurohemal
organ, which consist of hemal sinuses and the axon terminals of the neurosecretory cells
(fig. 67.17C). Examples of neuroendocrine organs are the X-organ sinus gland system,
the post-commissural organ and the pericardial organ. The epithelial endocrine organs
are composed of groups of modified epithelial cells (fig. 67.17D), which release their
hormones into adjacent hemal sinuses. The mandibular organ, Y-organ, and androgenic
gland belong to this type. The crayfish hormones are mainly peptides, steroids, amines,
and terpenoids. Peptide hormone producing cells are ultrastructurally recognized by high
amounts of rER, mitochondria, and hormone storing granules (fig. 67.17A).
The location of the endocrine organs in the crayfish’s body is illustrated in fig. 67.16.
The X-organ sinus gland is the master gland of the endocrine system, comparable to
the pituitary gland of vertebrates. It produces not only effector hormones acting di-
rectly on the target tissues, but also glandotropic hormones that regulate other hor-
mone glands. The X-organ sinus gland is located in the eyestalk (fig. 67.16) and is com-
posed of neurosecretory neurons that have their somata in the X-organ (fig. 67.17B) and
their axon terminals in the sinus gland (fig. 67.17C) (Gorgels-Kallen et al., 1982; Fin-
german, 1992). Release of the hormones in the sinus gland is under neuronal control.
The X-organ is composed of 150-200 somata and synthesizes a variety of metabotropic,
chromatophorotropic, and glandotropic peptide hormones such as the crustacean hyper-
glycemic hormone (CHH), molt inhibiting hormone (MIH), gonad or vitellogenesis in-
hibiting hormone (GIH/VIH), mandibular organ inhibiting hormone (MOIH), red pig-
ment concentrating hormone (RPCH), and pigment dispersing hormone (PDH). The
metabotropic and glandotropic hormones are members of the CHH-peptide family and
are structurally similar (Chang, 2001). For instance, the CHH and MIH of Procambarus
bouvieri (Ortmann, 1909) consist of 72 amino acid residues and differ in only seven amino
Fig. 67.16. Schematic illustration of endocrine system of crayfish. Endocrine organs are drawn in
solid black; h, heart; p, pericard; t, testis. [After Vogt, 2002.]
acids (Aguilar et al., 1996). CHH induces hyperglycemia but can also increase osmolal-
ity and Na+ content of the hemolymph (Serrano et al., 2003). MIH and MOIH inhibit
the activity of the Y-organs and mandibular organs, respectively, and VIH inhibits ovarian
development.
CHH is the best investigated hormone of the CHH-family. It enhances the hemolymph
glucose level in periods of high activity and emergency situations (Fanjul-Moles, 2006).
CHH immunoreactive cells first appear in hatchlings and amount to 35-40 in the mature
X-organ. In Cherax destructor there are two CHH genes, which can produce a total of
four CHH peptides by posttranslational isomerization (Bulau et al., 2003). The CHH is
synthesized in the X-organ as pre-pro-enzyme carrying a signal peptide of 26 amino acids,
a pro-peptide of 33 amino acids, and an active peptide of 72 amino acids. Release of CHH
from the sinus gland is regulated by neurotransmitters, notably GABA and serotonin, and
is probably also under negative feedback control by the glucose level of the hemolymph
(Lee et al., 2001). In Orconectes limosus the average level of CHH in the hemolymph was
1.3 × 10−11 M rising up to 1.25 × 10−10 M within a few minutes under stress conditions
(Kummer & Keller, 1993).
The content of CHH and glucose in the hemolymph of crayfish fluctuates and is
generally higher during periods of activity (Kallen et al., 1990). In the nocturnal Astacus
leptodactylus, synthesis of CHH in the X-organ started to increase 2 hours before darkness.
Bursts of CHH release from the sinus gland were then noted after onset of darkness. CHH
can act on several tissues, but the hepatopancreas and the musculature seem to be the
main targets. During transport from the sinus gland to the target organs CHH is apparently
bound to hemocyanin subunits (Kallen et al., 1990). In the hepatopancreas, CHH binds to
receptors of the plasma membrane, which transduce the signal via cAMP and cGMP and
Fig. 67.17. Endocrine system of crayfish. A, ultrastructure of peptide hormone synthesizing M-

cells with abundant rough endoplasmic reticulum (rer), mitochondria (m), and hormone containing
granules (arrow); B, cell bodies (arrows) of X-organ stained with CHH-antibodies; C, electron
micrograph of sinus gland, showing hemal sinuses (hs) and axon terminals (at) filled with hormone
granules (arrow); D, histological section of androgenic gland (ag) attached to vas deferens (vd); n,
cell nucleus; g, Golgi body. A, Astacus astacus; B, Orconectes limosus; C, D, Procambarus clarkii.
[A, after Vogt, 1994; B, after Gorgels-Kallen et al., 1982; C, D, after Fingerman, 1992.]
finally elicit the release of glucose from the glycogen stores of the R-cells (Kummer &
Keller, 1993). In vivo, release of glucose is detectable 10 to 20 minutes after injection of
CHH and attains a maximum after about 2 hours. CHH also seems to stimulate release of
fatty acids and phospholipids from the hepatopancreatic lipid stores (Santos et al., 1997).
RPCH and PDH are short peptides of 8 and 18 amino acid residues, respectively,
and act on chromatophores (Rao, 2001). Both hormones are synthesized in the X-organ
but also in other parts of the nervous system, suggesting that they play an additional
role as neuromodulators. In crayfish, their main function is apparently regulation of the
distal pigments of the compound eye, which do not directly respond to light. Instead,
light induces a neurohormonal reflex that is mediated by RPCH and PDH. RPCH induces
a retraction of the distal pigments to the darkness-adapted state, thereby enhancing the
photon-catching capacity of the rhabdom. PDH induces the opposite, namely migration
of the shielding pigments to a light-adapted state limiting the access of strong light to
the sensitive rhabdom (Porras et al., 2001). Regulation of the epidermal chromatophores
by RPCH and PDH seems to be less significant, because crayfish lack a physiological
color change typical of many shrimps. Instead, they display a so-called morphological
change of pigmentation, which involves quantitative alterations of the chromatophores and
qualitative changes of the pigments over weeks and months (Rao, 2001).
The post-commissural organ is an unpaired neurohemal organ associated with the
post-esophageal commissure (fig. 67.16). In Cherax destructor and Procambarus clarkii, it
was found to contain several neuropeptides in high concentrations, for instance allatostatin,
crustacean cardioactive peptide (CCAP), FMRFamide, proctolin, and orcokinins. These
hormones or neuropeptides are apparently involved in modulation of the stomatogastric
nervous system and thus in regulation of the activity of the stomach muscles (Skiebe,
2003).
The paired pericardial organs lie in the pericardial cavity (fig. 67.16) and consist
of several nerve trunks originating from the thoracic ganglia and extending through
the pericard. They terminate at the ostia in extensive arborizations. The pericardial
organs release CCAP, serotonin, octopamine, dopamine, and FMRFamides. All of these
neuropeptides can act as heart beat modulating hormones but may have additional
functions elsewhere in the body. CCAP is a cyclic nonapeptide and has a cardioexcitatory
effect (Chung et al., 2006). In Orconectes limosus, the hemolymph level of CCAP
increased more than 100-fold in the active phase of ecdysis, suggesting that this hormone
may also be involved in molting and may account for some of the changes in physiology
and behavior seen during ecdysis (Phlippen et al., 2000). CCAP is also released from
neurons of the terminal ganglion and elicits pronounced myotropic effects on the hindgut
(Audehm et al., 1993).
The Y-organs are located posteriolaterally to the esophagus (fig. 67.16) and appear
like hypertrophied parts of the epidermis. They are involved in regulation of somatic
growth and regeneration. The Y-organs synthesize the steroid 20-hydroxyecdysone and
derivatives, which elicit molting when secreted in higher concentrations. The Y-organs
undergo cyclical alterations during the molting cycle and are particularly thick during the
premolt stage. The ecdysone titer is low during intermolt and increases sharply during
premolt (Dell et al., 1999). For instance, in Orconectes limosus the intermolt value of
0.29 ng ecdysone per g fresh weight of crayfish increased to a maximum of 56.9 ng g−1
in premolt stage D2 and dropped back to 9.5 ng g−1 prior to ecdysis. The Y-organs are
negatively regulated by the molt inhibiting hormone (MIH) from the sinus gland, which in
Orconectes limosus is a 75 amino acid protein (Bulau et al., 2005). Its ecdysteroidogenesis
suppressing signal to the Y-organ is mediated via the cGMP pathway (Nakatsuji et al.,
2006). In Procambarus clarkii, the titer of MIH in the haemolymph was 6.53 fmol ml−1
at intermolt and dropped to 1.25 fmol ml−1 at premolt. Ecdysteroid production during
intermolt is apparently also under negative feedback control by circulating ecdysteroids
(Dell et al., 1999).
The mandibular organs are located close to the esophagus (fig. 67.16) and secrete the
terpenoid hormone methyl farnesoate (MF), which is chemically similar to the juvenile
hormone of insects. MF is involved in the regulation of morphogenesis and reproduction
of crayfish. Oral application of MF to Procambarus clarkii females resulted in enhanced
maturation of the ovaries, suggesting that MF acts as a gonadotropin in crayfish (Laufer et
al., 1998). In adult male Procambarus clarkii, MF was shown to be involved in shaping of
Form I and Form II, the two different morphotypes of male cambarids. If the hemolymph
level of MF is low prior to molting, reproducing Form I types with large chelae and spines
on the ischium of the third and fourth walking legs are formed. Non-reproducing Form II
types with smaller chelae and no spikes are produced at increased levels of MF (Laufer
et al., 2005). Synthesis of MF is negatively regulated by the mandibular organ inhibiting
hormone (MOIH) from the X-organ sinus gland system.
The androgenic glands are present only in males and are closely associated with the
vasa deferentia (figs. 67.16 and 67.17D). In Cherax destructor, they consist of cords
of epithelial cells that are attached to the vas deferens by connective tissue (Fowler &
Leonard, 1999). The androgenic gland cells show the typical ultrastructure of a protein
synthesizing cell. Their hormone promotes development of the testis and secondary
male characters. It also seems to influence behavior, because in Cherax quadricarinatus
implantation of androgenic glands into females induced male courtship displays and false
copulations (Barki et al., 2003). However, a complete change of gender resulting in the
development of functional gonads of the opposite sex has not yet been obtained, neither
by implantation, or andrectomy of the androgenic gland. In Cherax quadricarinatus
the androgenic hormone is apparently a protein of 176 amino acids related to the
insulin/insulin-like growth factor family (Manor et al., 2007).
There is evidence that further endocrine tissues, hormone release areas and hormones
exist in addition to the well-investigated ones. This can be inferred from the detection of
small neurohemal areas in the perineural sheaths of some nerves in Cherax destructor (cf.
Skiebe, 2003) and of solitary, endocrine M-cells in the hepatopancreas of Astacus astacus
(fig. 67.17A) (Vogt, 1994). Among the hormones that were measured in the hemolymph
and tissues of crayfish but not intensely investigated, are vertebrate-type sexual hormones
and glucocorticoids (Mackevičienė & Chibisova, 1995), prostaglandins, and insulin-like
growth factors (IGF). The prostaglandins E2 and F2α are synthesized in the ovary and
are thought to play a role in ovulation by acting on the musculature of the ovarian
envelope (Spaziani et al., 1995). IGF was shown to stimulate glycogen synthesis in the
hepatopancreas and the musculature of Cherax quadricarinatus and may therefore be
considered as an antagonist of the CHH (Richardson et al., 1997). In the case of the
vertebrate-type steroids it is unknown whether they are produced by the crayfish itself,
or acquired from the environment.
Crayfish exhibit a variety of circadian rhythms in their physiology and behavior (see
section Behavior), which require pacemakers and modulating hormones. Apparently
there are several pacemakers in the central nervous system, particularly in the protocere-
brum. Photoreceptor cells, either located in the retina of the compound eye or in the brain,
act in the entrainment of the clock (Bobkova et al., 2003; Solís-Chagoyán et al., 2008).
Blue light seems to be the main environmental signal for synchronization of the pacemak-
ers. It is perceived by a special photopigment, the cryptochrome CRY (Fanjul-Moles et
al., 2004). The hormone melatonin from the eyestalk can modulate the circadian rhythms
of crayfish probably by acting on both the photoreceptor cells and the pacemakers in the
brain. It sends a signal of darkness to the circadian clock (Solís-Chagoyán et al., 2008).
A highly topical issue related to endocrinology of crayfish and other decapods is the
disturbance of the endocrine system by environmental endocrine disruptors (Rodríguez
et al., 2007). Exposure of embryos of the marbled crayfish to water-borne methyl-
testosterone resulted in prolonged embryonic development, reduced hatching success, and
reduced growth of the juveniles, and caused severe malformations of the appendages in
juveniles (Vogt, 2007). These effects are apparently related to the ability of testosterone to
interfere with ecdysteroid control of development and molting, by acting as an ecdysteroid
receptor antagonist. Histological examination of the testosterone treated specimens at later
ages revealed that the androgen had no long-term effects on the development of the ovary
and did not induce sex reversal as claimed for other decapods.
Nervous system
Crayfish are very popular models in neuroscience, because their nervous system is
easily accessible, is composed of relatively few neurons, and remains functional in vitro
for longer periods of time. The nervous system is the first of the internal organ systems to
appear. At about 35% of embryonic development, the neuromeres of the brain emerge
simultaneously and the neurons start to differentiate by extending neurites, as shown for
Cherax destructor and the marbled crayfish (Vilpoux et al., 2006). The other neuromeres
follow sequentially in an anterior-posterior gradient. The mature nervous tissue includes
sensory neurons, motor neurons, interneurons, and glia cells. The cell somata of the
neurons are mainly located in the sense organs or in the ganglia. The axons are bundled
within nerves or, in the ganglia, within tracts. Both the ganglia and the nerves are enveloped
by a layer of connective tissue and are pervaded by hemal sinuses. The ganglia inclusive of
the brain are typically organized into peripheral groups of cell somata, central neuropils
composed of axons, dendrites, and synapses, and axonal tracts that link the neuropils to
each other (Mulloney et al., 2003).
The ventrally located central nervous system is composed of segmental ganglia and
connectives, starting with the brain and ending with the terminal ganglion (fig. 67.4).
The brain is located in the anterior cephalothorax and is followed by the subesophageal
ganglion, five thoracic, and six pleonal ganglia. The right and left ganglia of each somite
are fused into a single unit but their paired origin remains visible on histological sections.
All ganglia inclusive of the brain send out nerves to the periphery. The connectives of both
body sides lie close together (fig. 67.5) and are separate only between the thoracic ganglia
3 and 5, where the descending artery penetrates the nerve cord (fig. 67.4). The thoracic
part of the nerve cord is located in the sternal sinus and is protected by the endophragmal
skeleton. The pleonal part lies unprotected underneath the hindgut (Vogt, 2002).
The brain includes at least 80 000 neurons (Elofsson, 1986), which are organized into
neuropils, cell clusters, and axonal tracts (fig. 67.18A) (Sandeman et al., 1992). It can
be subdivided into protocerebrum, deutocerebrum, and tritocerebrum, reflecting its
origin from three pairs of segmental ganglia (Vilpoux et al., 2006). The protocerebrum
includes the optic ganglia of the eyestalk and some rostral neuropils and cell clusters
of the brain. It appears to be mainly responsible for processing of visual inputs and
Fig. 67.18. Nervous system of crayfish. A, immunocytochemical demonstration of serotonin recep-

tors in cell clusters (arrows) of the brain; B, ramification of giant serotonin immunoreactive neurite
(ne) in glomeruli (gl) of olfactory lobe (ol) and accessory lobe (al); C, cell bodies (cb) of neurons
in stomatogastric ganglion visualized by Lucifer yellow backfill; D, arborizations of interneuron (in)
and lateral giant (lg) from the lateral giant escape reflex circuit; contact zones (arrowheads) are iden-
tified by dye-coupling; E, newborn cells (arrows) in brain visualized by BrdU immunocytochemistry;
ax, axon; pc, protocerebrum; dc, deutocerebrum; tc, tritocerebrum. A, C, D, Procambarus clarkii; B,
E, Cherax destructor. [A, after Spitzer et al., 2005; B, after Sandeman & Sandeman, 1994; C, after
Skiebe, 1999; D, after Antonsen & Edwards, 2003; E, after Sullivan & Beltz, 2005.]
control of the endocrine system via regulation of the X-organ sinus gland system. The
deutocerebrum includes the olfactory lobes, accessory lobes, antennular neuropils, and
associated cell clusters. It is mainly responsible for the processing and integration of
olfactory and hydrodynamic inputs (Mellon, 2005). The tritocerebrum comprises the
antennary neuropils, the commissural ganglia and the postesophageal commissure, and
mainly serves for processing of hydrodynamic and other mechanical modalities, regulation
of the stomatogastric nervous system, and secretion of neuropeptides. The accessory lobes
are the biggest structures in the brain of crayfish (figs. 67.18A, B), which is in contrast to
the conditions of many other decapods (Sandeman et al., 1992). Their function has not yet
been clarified, but it is known that they receive higher-level visual, olfactory and tactile
inputs (Mellon, 2000). Some authors have related the conspicuousness of the accessory
lobes to the nocturnal life of crayfish. The brain gives rise to five paired nerves, the optic,
oculomotor, antennular, anntenary, and tegumentary nerves, and two unpaired nerves that
link the brain with the neural network of the esophagus.
The subesophageal ganglion, the thoracic ganglia and the pleonal ganglia are histo-
logically similar (Mulloney et al., 2003). The subesophageal ganglion originates from
longitudinal compression of six pairs of neuromeres during late embryonic development
(Vilpoux et al., 2006) and is composed of approximately 7000 neurons (Elofsson, 1986).
It has 11 pairs of nerves, coordinates the activity of the mouthparts and maxillipeds, and
supplies the antennal gland, the thoracic musculature, and the heart. The thoracic ganglia
(ganglia of thoracomeres 4 to 8) mainly control the movements of the chelipeds and walk-
ing legs. Each thoracic ganglion includes about 2000 neurons and usually has three pairs of
nerves, which innervate the legs, the segmental body musculature, the integument, and the
heart (Mulloney et al., 2003). Each walking leg is innervated by roughly 80 motorneurons,
which have their cell bodies in the thoracic ganglion of the same thoracomere, and includes
more than 2000 sensory neurons and 200-300 interneurons (Cattaert & Le Ray, 2001). In
Pacifastacus leniusculus, the muscles of the walking leg distal to the coxa are innervated by
14 excitatory and three inhibitory neurons only. The other motorneurons supply the levator,
promotor, remotor, and depressor muscles of the leg (fig. 67.6A) (Faulkes & Paul, 1997).
The thoracic ganglia not only receive sensory inputs from chemoreceptors, mechanore-
ceptors, and proprioceptors of the legs, but also from chemoreceptors, baroreceptors, and
proprioceptors of the gills, and proprioceptors of the thoracic musculature.
The pleonal ganglia possess only 630 neurons each (Mulloney et al., 2003). The
pleonal ganglia 1 to 5 have three pairs of nerves supplying the swimmerets, pleonal
musculature, and pleonal mechanoreceptors. The sixth pleonal ganglion or terminal
ganglion, which develops from the longitudinal compression of two pairs of neuromeres
and an anomalous terminal component, has six paired nerves and one unpaired nerve
and innervates the uropods, telson, and hindgut. The pleonal ganglia control three
types of motor activity, maintenance of posture, tail flipping, and rhythmic beating
of the swimmerets. In Pacifastacus leniusculus, approximately 200 of the neurons of
each ganglion are motorneurons, most of them innervating the swimmerets (∼70 per
swimmeret). In Cherax destructor, each of the posture controlling superficial extensor and
flexor muscles and the tail flip generating deep extensor and flexor muscles (fig. 67.6A) is
innervated by a minimum of five excitatory and one inhibitory motorneurons (McCarthy
& Macmillan, 1999). The pleonal ganglia receive sensory inputs from the proprioceptors
of the pleonal musculature and the thousands of sensory setae on the pleon and tail fan.
The terminal ganglion additionally includes somata of neurosecretory neurons that project
to neurohemal areas around the hindgut and anus.
Some ganglia like the esophageal ganglion, stomatogastric ganglion, and heart ganglion
are unpaired and are located outside the ventral nerve cord. The esophageal ganglion and
the stomatogastric ganglion are situated at the anterior surface of the esophagus and on
top of the cardiac stomach, respectively. Together with the two commissural ganglia of
the tritocerebrum, they form the stomatogastric nervous system that controls movements
of the esophagus, gastric mill, and pyloric filters (Skiebe, 2003). The cardiac ganglion is
the least compact ganglion and is located in the dorsal wall of the heart (Cooke, 2002). It
generates the basic heart beat.
A broad spectrum of neuroactive molecules has been identified in the nervous tissue
of crayfish that act either as neurotransmitters or as neuromodulators. These include
the amino acids glutamate and GABA, the peptides CCAP, RPCH, PDH, proctolin,
allatostatin, enkephalines, tachykinins, orcokinins, FMRFamides, and SIFamides, the
monoamines dopamine, octopamine, noradrenaline, 5-hydroxytryptamine (serotonin), and
histamine, the choline derivative acetylcholine, and the gases nitric oxygen and carbon
monoxide (Watson et al., 2000; Skiebe, 2003; Araki et al., 2004; Yasuda-Kamatani &
Yasuda, 2006; Rieger & Harzsch, 2008). There are many reports on the distribution of these
molecules in different parts of the nervous system, but in most cases it is not clear whether
they function as transmitters or as neuromodulators. Examples for neurotransmitters
are glutamate and GABA, which act in the excitatory and inhibitory synapses of the
neuromuscular system, respectively (Watson et al., 2000). A neuromodulatory function
has been proven for serotonin, which is involved in functional alterations of the lateral
giant escape reflex (see below). Information on the gradual appearance of the neuroactive
substances during ontogenesis and their possible role in formation of the nervous system
is found in Rieger & Harzsch (2008).
One of the topical directions of neurological research in crayfish focuses on the
establishment of structural-functional relationships in small neuronal networks. Complete
wiring diagrams are essential to understand the interplay between nervous system and
organ function or nervous system and behavior. Particularly suitable models for this type
of research due to their small number of neurons are the cardiac ganglion (fig. 67.7C),
which has 16 neurons (Cooke, 2002), and the stomatogastric ganglion (fig. 67.18C),
which has 19 to 26 cell bodies in Cherax destructor and Orconectes limosus (cf. Skiebe,
2003). Another common model is the lateral giant escape circuit that mediates a
coordinated escape triggered by an attack to the pleon (Antonsen & Edwards, 2003).
This circuit is composed of the paired lateral giant interneurons of the pleonal segments,
afferents from mechanosensory setae of the pleon and proprioceptors of the tail fan,
and efferent pre-motor interneurons and motor neurons (Edwards et al., 2002). The
extension of individual neurons in neuronal networks can be visualized by backfilling
with dye of cut axons (fig. 67.18C). The neuropeptides they produce can be identified
by immunocytochemistry (fig. 67.18B) or mass spectrometry. The chemical stimulus
they respond to may be determined either by immunocytochemical identification of their
receptors (fig. 67.18A) or by electrophysiological recordings from identified neurons
after stimulation with neuroactive substances. Connection patterns between neurons are
made visible by differential dye coupling, which is based on differences in the ability
of intracellular dye markers to pass through the gap junctions of electrical synapses
(fig. 67.18D).
A second topical direction of neurological research investigates the structural dynam-
ics of the crayfish brain. One target is the olfactory lobe, which in the adult crayfish is
made up of about 200 cone-shaped areas of densely packed synaptic fields, the olfactory
glomeruli (fig. 67.18B). These glomeruli receive the sensory afferents of the olfactory
aesthetascs on the outer branch of the first antenna that branch extensively throughout the
glomeruli. They also include dendritic arborizations of neurons clustered laterally in the
midbrain, which additionally ramify within the accessory lobe (fig. 67.18B). After each
molting, several new aesthetascs are added to the first antenna, each of them containing
roughly 100 olfactory receptor neurons. The axons of all of these new sensory neurons
grow towards the olfactory lobe and are integrated into the glomeruli, resulting in an en-
largement of this part of the brain and alteration of its wiring pattern (Sandeman & Sande-
man, 2003; Schmidt, 2007). If the first antenna is repeatedly removed on one side of the
body the olfactory lobe ipsilateral to the lesion remains much smaller than its companion
on the healthy side, as demonstrated in Procambarus clarkii (cf. Mellon & Tewari, 2000).
Crayfish cannot only enlarge their brain by integration of new afferent axons,
but also by the production of new neurons, which makes them suitable models to
investigate life-long neurogenesis in detail (Schmidt, 2007; Sullivan et al., 2007). Using
Procambarus clarkii as an experimental animal, Sullivan et al. (2007) have found that
new neurons in the brain originate from precursor cells, which reside in a special area
of the brain, the neurogenic niche. From there, they migrate to their site of destination
and give rise to new neurons, resembling closely the situation in higher vertebrates.
Sullivan & Beltz (2005) discovered that newborn cells in the adult brain of Cherax
quadricarinatus (figs. 67.18E and 67.20F; see color insert) can differentiate into distinct
neuronal types and that neurogenesis also occurs in the optic neuropils. Most interestingly,
Song et al. (2007) observed higher survival of newborn neuron precursors in dominant
Procambarus clarkii compared to subordinates. In juveniles of Cherax destructor, rearing
under prolonged enriched conditions (communal rearing, large containers) resulted in
higher proliferation and survival of neurons than rearing under impoverished conditions
(individual rearing, small containers) (Sandeman & Sandeman, 2000), suggesting that
social and environmental factors can elicit structural alterations of the crayfish brain.
A third topical direction of neurological research in crayfish deals with the adapta-
tion of neuronal networks to environmental challenges, or, in other words, the neural
basis of behavior. Crayfish possess a variety of neuronal networks of different structural
complexity and functional plasticity. Tail flipping is among the simplest and most stereo-
typed motor programs and walking is the most complex and variable one (Cattaert & Le
Ray, 2001). Neuronal networks can generate motor patterns in the absence of any sensory
feedback but adaptation of this command to the actual situation requires the integration
of sensory feedback. On the molecular basis, adaptation is achieved by neuromodulation,
which changes the excitability of neurons or the effects of synapses, and thereby extends
the performance range of neuronal circuits (Edwards et al., 2002). Neuromodulation can
affect the properties of sensory receptors, central neurons, motor programs, or chemical
and electrical synapses. It amplifies or reduces the normal response either for a brief or an
extended period of time. Reviews on the plasticity and modulation of motor programs are
available for pleonal positioning (Larimer & Moore, 2003), the escape reflex (Edwards et
al., 2002; Shirinyan et al., 2006), swimmeret movements and walking (Cattaert & Le Ray,
2001), movements of the gastric mill (Skiebe, 2003), and dominance hierarchy formation
(Edwards et al., 2003).
A rather well investigated example for the plasticity of a neuronal circuit is the lateral
giant escape reflex and its habituation, which is a simple form of learning. This escape
reflex is initiated by a tactile stimulus on the pleon, which initiates a single spike in the
lateral giant interneurons that activates motor neurons to produce a highly stereotyped
tail flip. It is modulated by serotonin, which produces opposite effects at high and low
concentrations and rapid and slow exposures. For instance, slowly applied serotonin
facilitates (amplifies) responses of the lateral giants in socially isolated crayfish and in
new dominant and subordinate animals. Facilitation is retained in the dominants during
two weeks of continuous pairings of the crayfish but gradually changes to inhibition in
the subordinates. These and other effects of serotonin modulation appear to result from
changes in the serotonin receptor patterns on the neurons involved. Detailed information
on the modulation of the crayfish escape circuit and the neural basis of dominance
hierarchy formation is found in Edwards et al. (2002, 2003). Shirinyan et al. (2006)
found that descending input from higher ganglia is needed to induce crayfish escape
reflex habituation, but once established habituation persists even after the rostral ganglia
inclusive of the brain are disconnected. This indicates that lower level neural circuits are
reprogrammed through transient interaction with higher ganglia (Shirinyan et al., 2006).
Two topics are outlined at the end of this section due to their general biological
relevance, the determination of crayfish age by lipofuscin deposits in the brain, and sleep
in crayfish. Lipofuscin is a universal pigment deriving from the auto-oxidation of cellular
components. Its amount has been shown to increase with age in the vertebrate brain.
By quantification of lipofuscin in the olfactory lobes of Pacifastacus leniusculus from
known age classes, Belchier et al. (1998) have shown that lipofuscin is linearly correlated
with age, producing much more accurate age estimates than conventional body size-based
procedures. Sleep, a distinct state of reduced activity, irritability, and attention, is well
established in vertebrates but evidence for sleep in invertebrates is still meager. A specific
form of slow wave electrical activity of the brain characterizes sleep in mammals. Ramón
et al. (2004) have measured such slow waves in the brain of Procambarus clarkii, which
had particularly high thresholds to mechanical stimulation, a common behavioral indicator
of sleep. Since this slow wave pattern was different from the waking rest pattern, it is quite
obvious that crayfish can sleep.
Sense organs
Crayfish have numerous exteroceptors and interoceptors that provide information
from the external and internal world to the central nervous system. Exteroceptors are
the eyes, aesthetascs, corrugated setae, and tactile and hydrodynamic setae on the
appendages and various parts of the exoskeleton. The interoceptors include propriocep-
tors, which relay information about the position and motion of the body, and chemo- and
baroreceptors, which monitor blood pressure and the chemical state of the hemolymph
and gastric fluid (Vogt, 2002). Some sense organs like the statocysts exert both extero-
and interoceptive functions. Crayfish can also sense electrical fields, as shown for Pro-
cambarus clarkii and Cherax destructor, but their behavioral thresholds are very high,
suggesting that crayfish do not use electroperception in locating and identifying con-
specifics or prey (Steullet et al., 2007). Thermo-, magneto- or pain-receptors have not
yet been identified. Practically all external sense organs of crayfish emerge in the first
postembryonic life stages, and in cambarids most of them are fully functional only from
stage 3, as shown in the marbled crayfish (Vogt, 2008a). These sensory deficiencies of the
early juvenile stages may explain prolonged brood care in crayfish, which is unique among
Decapoda (cf. Vogt & Tolley, 2004).
There are two well-established photoreceptive systems, the compound eyes and the
terminal ganglion, and a rather obscure one, the intercerebral ocelli. The compound
eyes are responsible for normal vision and are thus involved in exploration of the
environment and food searching. There is recent evidence that the eyes also play an
important role in recognition and memory of individuals (Van der Velden et al., 2008). The
terminal ganglion includes a pair of photosensitive neurons, which react to illumination
with onset of walking, even in blind cave-dwelling crayfish (Rodríguez-Sosa et al., 2006).
Intracerebral ocelli were found in the protocerebrum of species from all crayfish families
(Bobkova et al., 2003). These ocelli are made up of 4-5 photoreceptor cells with rhabdom-
like structures and photopigment, but lack dioptric structures. In Pacifastacus leniusculus,
as much as 14 ocelli were identified in a single brain. These hidden receptors may play a
role in entrainment of circadian rhythms (Fanjul-Moles et al., 2004).
The compound eyes are located on the eyestalk and can be moved in all directions
by oculomotor muscles. They are composed of rectangular ommatidia (fig. 67.19D)
consisting of the dioptric apparatus, a photosensitive retina, screening pigments, and
tapetum cells (Vogt, 2002). All optical elements inclusive of the retina differentiate
from the surface epithelium. The optic primordia appear at about 55-60% embryonic
development and are structurally complete in stage 2 juveniles, as shown in Procambarus
clarkii and the marbled crayfish (Hafner et al., 2003; Vogt & Tolley, 2004). Adult Astacus
astacus can have more than 3000 ommatidia per eye. The dioptric apparatus includes an
outer cornea, which pre-focuses the light, and an inner crystalline cone, which guides
the light to the retina. The retina consists of seven cells, which project their photo-pigment
carrying microvilli towards the centre of the ommatidium forming the rhabdom. An eighth
retinular cell of smaller size does not participate in the formation of the rhabdom. The
retinular cells also include the proximal screening pigments, which respond directly to
light with intracellular movements. The axons of the retinular cells are bundled and project
to the lamina ganglionaris of the eyestalk. Cells containing the distal screening pigment
surround the crystalline cone and the retina, and mediate the light- and darkness-adapted
state of the eye via RCPH and PDH. Tapetum cells are located basally between the retinular
Fig. 67.19. Sense organs of crayfish. A, olfactory aesthetascs on outer flagellum of 1st antenna; B,
gustatory corrugated setae on chela of 2nd pereiopod; C, hydrodynamic setae on inner flagellum of
1st antenna; D, rectangular ommatidia of compound eye; E, statolith (sl) and mechanoreceptive setae
(arrow) with setules (arrowhead) in statocyst of juvenile; F, abdominal stretch receptor organ with
receptor muscles (r) and sensory neurons (arrows). A-E, marbled crayfish; F, Astacus leptodactylus.
[A, B, after Vogt et al., 2008; C, D, after Vogt & Tolley, 2004; E, after Vogt, 2008a; F, after Purali,
2005.]
cells and serve for reflection of light to the rhabdom. They cause the typical eye glow of
crayfish at night.
The eyes of crayfish are superposition eyes that can adapt to a broad range of light
intensities by position changes of the distal screening pigments. At strong light the
pigments separate the ommatidia from each other, thus creating a mosaic image that is
particularly suited to detect moving objects. At low light the pigments retract and allow
light rays from several ommatidia to superimpose on a single rhabdom, resulting in the
formation of a superposition image, which promotes vision in the night. The superposition
focus is created by mirror optics, the reflection of light rays by crystals in the outer walls
of the crystalline cones of several ommatidia (Land, 2000). Crayfish eyes are sensitive
to polarized light, facilitating both navigation and the recognition of moving transparent
objects (Tuthill & Johnsen, 2006; Glantz, 2007; Glantz & Schroeter, 2007). They should
also be able to discriminate color, because there are at least two receptor types with
overlapping spectral ranges but behavioral evidence for color vision is lacking. During
summer, the retina of Procambarus clarkii expresses mainly rhodopsin with a maximal
absorption at 530 nm (green) and a second pigment absorbing at 440 nm (violet) (Hafner
et al., 2003; Porter et al., 2007). The rhodopsin is located in the main rhabdom and
the 440 nm pigment in the isolated eighth retinular cell. This pigment is thought to
provide crayfish with UV sensitivity during summer. In the winter months, Procambarus
clarkii has rhodopsin and, to a higher degree, porphyropsin as visual pigments (Zeiger
& Goldsmith, 1993). Porphyropsin is widespread among aquatic animals and has an
absorption maximum at 567 nm (yellow).
Cave-dwelling crayfish usually display different grades of reduction of the eyes and
corresponding areas of the brain. However, Procambarus cavernicola and Procambarus
oaxacae reddelli Hobbs, 1973 have possibly developed a new tactile or hydrodynamic
function for their obsolescent eyes, because they have feathered setae on their corneae,
which is exceptional in crayfish (Mejía-Ortíz & Hartnoll, 2006).
Sensilla concerned with chemoreception are mainly concentrated on the first antennae
(antennules), mouthparts, and pereiopods. The chemoreceptors on the antennules mainly
serve for sensing odorants coming from distant sources (olfaction), whereas the receptors
on the mouthparts and pereiopods perceive molecules by direct contact with the source
(gustation). Recently, further chemosensory setae have been identified on the chelae
of male Orconectes rusticus, which perceive female odors (Belanger et al., 2008).
Reproductive Form I males had significantly more such setae on their chelae than non-
reproductive Form II males. Aside from these external chemoreceptors, there are also some
internal chemosensors known, for instance oxygen receptors in the branchiopericardial
vessels (Ishii et al., 1989) and chemosensilla in the esophagus (Altner et al., 1986; Vogt,
2002).
The olfactory organ of crayfish is composed of the outer flagella of the antennules
and serves for food searching, testing of the water quality, and social interactions. With
the help of the fan organ and the swimmerets, crayfish can create currents that bring
distant odor molecules from all directions to the sensory structures of the head (Denissenko
et al., 2007). These movements and the flickering of the olfactory flagella are typical
behaviors associated with olfaction. The flagella are equipped with numerous aesthetascs
(fig. 67.19A) that increase in number by each molt and can exceed 150 per antennule in
adults. In Cherax destructor and the marbled crayfish the aesthetascs emerge in the second
postembryonic stage (Sandeman & Sandeman, 2003; Vogt & Tolley, 2004). Aesthetascs
are blunt setae with a thin cuticle, lacking a terminal pore (fig. 67.19A). They house the
dendrites of bipolar olfactory receptor neurons that have their somata clustered in a sensory
ganglion at the base of the corresponding aesthetasc. The axons of the more than 100
receptor neurons of each aesthetasc run within the antennular nerve to the deutocerebrum
and terminate in the olfactory lobe (Sandeman & Sandeman, 2003). The antennules are
occasionally damaged during agonistic interactions but can regain their full function after
two to three molts, as shown in Orconectes sanborni (Faxon, 1884) (Mccall & Mead,
2008). Comparison of the surface-dwelling Orconectes cristavarius Taylor, 2000 and the
cave-dwelling Orconectes australis packardi Rhoades, 1944, revealed longer antennules
and longer aesthetascs relative to the body size in the subterranean species, but a higher
total number of aesthetascs in the epigean species (Ziemba et al., 2003).
The gustatory corrugated setae (= fringed setae) are located on the inner margins of
the propodus and dactylus of pereiopods 1-3 (fig. 67.19B) (Vogt, 2008a; Vogt et al., 2008).
In Austropotamobius torrentium (Schrank, 1803), each corrugated seta contains eight
receptor cells with long dentritic segments that extend to the tip of the seta where a small
pore is found (Altner et al., 1983). Two receptors respond to strong mechanical stimuli,
one reacts to amino acids, one to amines, two to pyridines, and two to plant extracts.
The amino acid receptor is stimulated by a broad variety of amino acids, except for those
having voluminous hydrophobic or negatively-charged side chains. In the omnivorous
Procambarus clarkii, the most effective stimuli were trehalose and leucine, followed by
cellobiose, glycine, and glucose. When trehalose was applied in concentrations higher than
10 μM, the food testing clasp frequencies of the chelae of the second and third pereiopods
increased significantly (Corotto et al., 2007). Comparison of the corrugated setae of 44
species from all crayfish families with respective setae of 73 species from other major
groups of Decapoda revealed that corrugated setae are confined to crayfish and can thus be
regarded as an autapomorphy of Astacida Scholtz & Richter, 1995 (cf. G. Vogt, unpubl.).
They are strikingly different from the homologous hedgehog-setae of Nephropidae Dana,
1852 and related structures of Thaumastochelidae Bate, 1888 and Enoplometopidae De
Saint Laurent, 1988, which are regarded as the closest relatives of freshwater crayfish.
Mechanoreceptors are distributed all over the crayfish’s body (Vogt, 2002). They
are particularly frequent on the antennae, mouthparts, pereiopods, and tail fan. These
mechanoreceptive setae have hydrodynamic and tactile functions, and serve for exploration
of the environment, social interaction, and control of the pressure exerted by the chelae and
mouthparts. Further mechanoreceptors are found inside the body and are associated with
the joints of the appendages, musculature, ventral nerve cord, esophagus, and stomach.
These mechanoreceptors are involved in coordination of posture, escape reflexes, and
walking, and measure the filling state of the stomach. Special mechanoreceptive organs
are the statocysts, which are located in cavities of the body but remain connected with the
outer world.
The statocysts are located in the basal articles of each antennule (Hertwig et al., 1991;
Takumida & Yajin, 1996). They maintain balance and sense gravity, high frequency
vibrations, and perhaps also angular accelerations. Each statocyst consists of a chitinous
chamber with a dorsal aperture covered by setae. The center of the statocyst is occupied by
a statolith composed of tiny sand grains and debris that are glued together by mucus from
tegumental glands located at the floor of the statocyst. The statolith is surrounded by up to
100 sensory setae, most of them being attached to the statolith (fig. 67.19E). All sensory
setae have a similar shape but differ in size and diameter. They have a feathered shaft and
a peculiar construction of their base (Vogt, 2002), which allows shearing movements in
one direction only. The shearing forces are exerted by the statolith and transmitted via a
cuticular lever to a sensory complex composed of ciliate neurons and enveloping cells.
In Astacus leptodactylus the largest group of setae is crescent-shaped and discriminates
different tilts during rotation about the roll axis (Lemmnitz & Wolff, 1990). A second
group of transversally oriented setae discriminates tilts about the pitch axis, and a third
longitudinally arranged group that is not attached to the statolith may sense angular
acceleration. Statocysts are also sensitive to vibrations in the higher frequency range up
to 2000 Hz, as shown for Orconectes limosus (cf. Breithaupt & Tautz, 1990), suggesting
that crayfish can hear to a certain degree. However, there is no evidence that crayfish use
sound for communication (Popper et al., 2001). The statocysts are renewed at each molt
and must be refilled with sand grains and debris after ecdysis, which is done with the
chelae of the second pereiopods.
Hydrodynamic stimuli provide information on the direction of water flow but also on
the movement of conspecifics, prey, and predators. Hydrodynamic receptors are found on
the antennae, carapace, pleon, tail fan, chelipeds, and walking legs. They can be smooth
like those on the inner flagella of the antennule (fig. 67.19C) and the flagella of the
second antennae (Sandeman, 1989), or feathered. They vary in length between 0.1 and
2 mm and can perceive a broad range of frequencies, depending on the length of the
seta. Most setae respond to frequencies lower than 150 Hz, which is within the range
of moving fish and crayfish (Breithaupt & Tautz, 1990). A special hydrodynamic sensor
of crayfish is the tail fan, which can measure very small water displacements coming
from all directions (Douglass & Wilkens, 1998). The hydrodynamic setae on the second
antennae probably also participate in the tactile sense, together with the proprioceptors. In
Cherax destructor, there are more than 7000 setae on each antenna but not all of these are
innervated (Sandeman, 1989). The tactile sense is used for thigmotactic navigation and
scanning of other crayfish during encounters (McMahon et al., 2005).
Further mechanoreceptive structures are the muscle receptor organs (MROs), the
chordotonal organs (COs), and cuticular stress detectors (CSDs). MROs are composed
of a sensory neuron functionally allied with a single muscle fiber (fig. 67.19F) and occur
in the pleon, thorax, thoraco-coxal joints of the limbs, and the mandible (Macmillan &
Field, 1994; Purali, 2005). They measure the tonus of muscles and contribute to feedback
control of posture and movements like tail flipping. COs are located in each limb joint and
contribute to coordinated movements of the appendages (Clarac, 1990; Vogt, 2002). They
are usually composed of an elastic strand of connective tissue that attaches proximally to
the muscle tendon and distally to the cuticle of the next article. Each strand includes 20
to 100 bipolar sensory neurons with ciliate dendrites ending in scolopidia. They monitor
changes in joint movements via strand length alterations. CDSs are located in the basis-
ischium region of the pereiopods and respond to externally and internally induced stress.
They consist of one or two receptor strands that insert on a soft part of the cuticle (Vogt,
2002). Within the strands, there are groups of bipolar sensory neurons terminating in
scolopidia. CDSs are involved in posture of the legs and probably also in autotomy.
Some sense organs of crayfish have attracted the attention of general or applied
biologists. For instance, the pleonal stretch receptor organs (MROs) of crayfish are
probably the most intensely studied mechanoreceptors of the animal kingdom, because
they are easily accessible and have very large sensory cells (fig. 67.19F) (Purali, 2005).
They provide excellent models to study fundamental problems of mechanotransduction
and to investigate the interplay between internal motor generators and external sensory
systems (Rydqvist et al., 2007). The neurons of these MROs are also used to explore the
mechanisms of photodynamic therapy. This technique elicits death of cells under light
exposure via dye-mediated oxygen stress and is successfully used for treatment of cancer
(Fedorenko & Uzdensky, 2008). It is also applied in experimental neurophysiology for the
selective destruction of neurons in order to study their role in complex neuronal networks.
The mechanoreceptors on the tail fan have been used to investigate the phenomenon
of stochastic resonance in biology (Douglass et al., 1993; probably the most frequently
cited crayfish paper). When an optimized random noise, which can be produced by a noisy
environment or the sensory neurons themselves, is added to sub-threshold signals, such
weak signals can reach the threshold so that they can be perceived by the sense organs.
Apparently, biological systems have evolved the capability to exploit stochastic resonance
but this phenomenon is also of great importance in chemistry, physics, and techniques.
Another topic of applied interest is the mirror optics of the compound eye of crayfish. This
optical principle has evoked ideas for the construction of a new type of X-ray telescope
and a collimator to produce a parallel beam from an X-ray source, which might be useful
in forming ultrafine microcircuits on a chip (Land, 2000).
In the last two decades, great progress was made in the understanding of structure-
function relationships of crayfish organs. This progress was mainly due to ingenious
experimental designs and the application of modern morphological, physiological, and
molecular techniques. Major deficiencies are the low number of species investigated and
the poor knowledge on crayfish genetics. Examination of a broader spectrum of the over
600 described species of crayfish would certainly reveal new results, particularly if those
species came from extreme environments like brackish water, semi-terrestrial habitats, or
caves (Crandall & Buhay, 2008).
Genomics and proteomics in crayfish are still in their infancy and far beyond that
of penaeid shrimps. However, first attempts to identify genes and their products by
cDNA microarrays were successfully accomplished using the hepatopancreas of Cherax
destructor as a model organ (Shechter et al., 2007). Likewise, genes were successfully
transferred into the oocytes of Pacifastacus leniusculus (cf. Sarmasik et al., 2001),
suggesting that the production of transgenic crayfish for research is principally feasible.
The broader application of such techniques would certainly enhance our knowledge on the
structure and function of crayfish organs.
REPRODUCTION AND DEVELOPMENT

[C. S OUTY-G ROSSET – with the assistance of J. C ARRAL , J. R EYNOLDS & G. VOGT]
Crayfish are gonochoristic, and there is evidence that sex is determined by a WZ-ZZ
scheme with the males being the homogametic sex (Parnes et al., 2003). However, sex
chromosomes have not yet been identified among the numerous small chromosomes of
crayfish, which can vary in number in the diploid state between 116 in Astacus astacus
and 376 in Pacifastacus leniusculus trowbridgii (Stimpson, 1857), the highest value ever
recorded in Metazoa (Tan et al., 2004). Mating occurs at a particular phase of the molt
cycle, most often during intermolt. Males of Astacidae deposit spermatophores near the
openings of the female gonoducts (at the base of the third pereiopods) and use the first two
pairs of modified pleopods (gonopods) to guide the placement of the spermatophores. In
contrast, male Cambaridae extrude sperm onto the annulus ventralis, at the entrance of a
tubular sperm-storage organ at the posterior end of the female seventh thoracic sternites.
In Parastacidae, where the first pair of pleopods is vestigial in males, mating is brief and
the female then distributes the deposited sperm between the walking legs (Holdich, 2002).
Fertilization occurs some time after copulation, when the eggs, spermatophores, and
a sticky fluid denoted as ‘glair’ are released into a temporary brood chamber created by
females curling their pleon. Each egg is attached by a flexible stalk to an individual seta.
Egg clutches remain attached to the female pleopods for weeks or months until hatching.
Development is direct, the young hatching as juvenile instars and passing through the
stages of zoea or nauplius while still in the egg. Juveniles remain attached to their mother
for a number of days, during which they may molt once or twice. Once they leave their
mother, they begin adult life and reach maturity within a few months to several years,
according to the species.
Based on their reproductive biology and life-history patterns, crayfish species have
been classified into two groups: summer or winter brooders, broadly corresponding to
‘r-selected’ and ‘K-selected’ species, respectively [terms derived by Adams (1980) after
MacArthur & Wilson (1967)]. The average life span of crayfish is one to several years. In
Europe (table II), indigenous species are K-selected, whereas introduced species (such as
Orconectes limosus or Cherax albidus Clark, 1936) are included in the summer group.
Species of crayfish indigenous to Europe are less fecund, mature at a larger size, and
occupy a narrow range of habitats with slow growth rate and a longer life span (Reynolds,
2002). In U.K. populations of Austropotamobius pallipes, for example, mating occurs in
October, involving a long and arduous copulation that may sometimes be lethal, followed
by egg laying in early November (Brewis & Bowler, 1985). Eggs are carried by females
until the following July-August when hatching occurs.
On the other hand, introduced species have the ability to undergo multiple spawnings
during the breeding period, to mature at a small size, to be highly fecund, and to occupy
a large range of ecosystems (Reynolds, 2002). The semi-terrestrial burrowing crayfish
Parastacoides tasmanicus tasmanicus (Erichson, 1846) in southwestern Tasmania, attains
sexual maturity at a relatively late age (3-5 years) and large size (25-30 mm cephalothorax
length); it has a long life span (<10 years) and a slow and variable growth rate (Hamr
& Richardson, 1994). Males reach sexual maturity at a smaller size than do females.
Mating and spawning, which closely follow the female molt, occur in early autumn when
males and reproductive females pair in burrows; eggs are carried over winter and hatch
early the following summer; young remain attached to their mother until mid summer.
Mature females exhibit a biennial molting and breeding cycle, an apparently unique
strategy among parastacid crayfish, which probably is a consequence of the cooler climatic
conditions in Tasmania.
330
TABLE II
Reproductive and population dynamic characteristics of crayfish in Europe: the first five are native, the others are introduced from North America (the
next six) and Australia (the last two) [After Souty-Grosset et al., 2006]
Species Longevity (yr) Age at maturity Size at maturity Egg incubation Egg number
Begins Ends
1. Astacus astacus 20 16 mo-5 yr 62-85 mm October-November May-July 90-260
2. Astacus leptodactylus 5+ 3-4 yr 66 mm October-December Late May-July 200-650
3. Astacus pachypus ? 3 yr 60 mm November-December March-April 70-240
4. Austropotamobius pallipes 10+ 2 yr 40-60 mm Autumn April-May 50-200
5. Austropotamobius torrentium 10+ 3-5 yr 35-50 mm May Mid July 40-100
6. Pacifastacus leniusculus 20 2-3 yr 60-90 mm October End July 200-400
7. Procambarus clarkii 1+ <1 yr 40 mm Two generations per yr 600
F. GHERARDI ET AL.
8. Procambarus sp. 2 <1 yr 40 mm All the yr round up to 270

9. Orconectes limosus 4 1-2 yr 35 mm Several generations per yr 400
10. Orconectes virilis 4 1-2 yr 27 mm Autumn July 490
11. Orconectes rusticus 3-4 1 yr 23 mm February-June March-July 80-575
12. Cherax destructor 3-6 <1 yr 60 mm Five times a yr in aquaria 350
13. Cherax quadricarinatus 4-5 <1 yr 110 g All the yr round 300-1000
Cambarid species, such as the red swamp crayfish Procambarus clarkii, can exhibit
very flexible patterns of reproduction helping to make it one of the most invasive crayfish
in the world (reviewed in Gherardi, 2006). This species can have at least two reproductive
periods (in autumn and spring). Mating takes place at any size from 4 to over 12.5 cm,
with the production of 50-600 eggs. Newly hatched crayfish remain with their mother in
the burrow for up to eight weeks (Ackefors, 1999).
The picture is not always so clear-cut. This is the case in the gilgie, Cherax quinque-
carinatus (Gray, 1845), endemic to southwestern Western Australia, that occupies a wide
range of permanent and temporary aquatic environments (Beatty et al., 2005). Patterns of
reproduction and population biology were determined from monthly collections of gilgie
in Bull Creek, southwestern Western Australia. The species matures at a relatively small
size, with 50% of females and males maturing at 24 and 31 mm cephalothorax length,
respectively. The majority of females began to spawn at the end of their second year. The
ovarian and pleopodal fecundities are relatively low compared to other crayfish species of
similar size, being on average 82 and 77, respectively. Cherax quinquecarinatus under-
goes an extended spawning period, from late winter to late summer (August to February),
with three spawning events facilitated by short brood and rapid gonadal recovery periods;
these traits are consistent with other crayfish species able to tolerate temporary environ-
ments. Cherax quinquecarinatus thus shows life history characteristics of both a summer
(r-strategist) and a winter (K-strategist) brooder.
Sexual maturation
Crayfish pass through 11-15 molts before reaching sexual maturity, through an environ-
mentally controlled process leading to oogenesis and spermatogenesis. Age at maturity
varies according to the species and to the region. For example, Pacifastacus leniusculus
matures earlier in central Finland (1 year; Kirjavainen & Westman, 1995) than in Sweden
(2 years; Abrahamsson, 1971). In the case of cool-water species, such as the parastacid
Paranephops zealandicus (New Zealand), the age at maturity may be more than six years.
In captive males of Austropotamobius pallipes, a correlation between frequency of
mating and decrease in vasa deferentia weight was found (Woodlock & Reynolds, 1988),
but in wild males the weight of the vasa deferentia was highly variable, the data suggesting
that at least one third of adult males may not have mated in the wild. All females appear to
have spawned, whether or not they had mated, with an average of 85% reduction in ovary
weight over the reproductive season. At 50 days after spawning, pleopodal egg counts were
on average 81% of ovarian counts in the laboratory and only 61% of the ovarian counts in
the field. Average ovarian egg size was positively correlated with female size, and larger
females had a wider range of egg sizes than smaller ones.
Ovarian development is generally a process in three stages: pre-vitellogenesis, primary
vitellogenesis, and secondary vitellogenesis. In the spiny cheek crayfish Orconectes
limosus, the gonadosomatic index, expressed in fresh weight of the gonads as a percentage
of the weight of the whole body, ranges between 0.11 and 0.79% (with a minimum in
July and a maximum in September) in males, and from 0.25 to 6.15% (with a minimum in
July and a maximum in April) in females (Kozak et al., 2007). Egg extrusion takes place
in mid April. Between April and May, dissection indicated both the presence of mature
oocytes and of oocytes undergoing resorption. The volume of oocytes gradually decreased
in summer and increased between winter and spring from 0.2 mm at the beginning of
the reproductive cycle to 1.8 mm immediately before shedding the eggs. Ovarian eggs
averaged 141 ± 52 in number. The ovary was most often brown, but it was white in June
and July, and orange in August and September. Mating started in October and continued
through the winter.
In Procambarus clarkii, field and laboratory observations suggest that temperature
controls the onset of ovarian development, which is also accelerated by the increase in
day length (Daniels et al., 1994). The photoperiodic induction of ovarian maturation in
this species seems to be mediated by extra-retinal photoreception (Fanjul-Moles et al.,
2001).
Sex determination and sex ratios

Sex determination is mediated by the hormones secreted by the androgenic glands;
in their absence, vitellogenesis may occur. Surgical experimental procedures and implan-
tation have demonstrated the importance of the androgenic gland in controlling differen-
tiation of the testis and the male secondary sexual characters (section Internal morphol-
ogy). Ovaries auto-differentiate in the absence of these glands, if lost during development;
growth and maturation are controlled by methyl farnesoate produced by the mandibular
gland.
Sex ratios in most natural crayfish populations are close to 1 : 1 (Abrahamsson, 1971;
Mason, 1975), observed changes from this ratio generally being due to female-male
differences in seasonal activity and/or in their catchability. After copulation, females
seclude themselves in a shelter for a relatively long time during egg incubation, whereas
males remain active. As an example, only 24% of the trapped Austropotamobius pallipes
in an Irish lake during winter were females (Matthews & Reynolds, 1995); after the
release of the juveniles, however, in July, the sex ratio in traps was 1 : 1. Recently, Manor
et al. (2007) analysed the sex ratio of Orconectes virilis (an indigenous species) and
Orconectes rusticus (an invasive species) in northern Michigan. While it was 1 : 1 in
the latter species, Orconectes virilis females were more abundant than males. External
factors like differential mortality or differential movement might cause the observed bias
in Orconectes virilis.
Intersexes, parthenogenesis, and hybridization

There are a few exceptions to the typical gonochorism in crayfish. Intersex individuals
showing male and female characters occur regularly in species from all crayfish families
but are particularly frequent in Parastacidae (cf. Sagi et al., 2002; Rudolph et al., 2007;
Noro et al., 2008). In Cherax quadricarinatus, such intersexes have been shown to be
genetic females but functional males (Parnes et al., 2003). The intersex characteristics can
be limited to the external morphology, e.g., the presence of male and female gonopores,
but can also extend to the gonads, resulting in the parallel occurrence of oviducts and vasa
deferentia or even the development of ovotestes. In the South American genus Parastacus,
the presence of male and female gonopores in the same individual is common and can
encompass all individuals of a population (Noro et al., 2008). True hermaphroditism,
the simultaneous or sequential functioning of male and female reproductive organs in
the same individual, is rare in crayfish. It was found in Parastacus nicoleti (Philippi,
1882), Parastacus defossus, Samastacus spinifrons (Philippi, 1882) and Virilastacus
rucapihuelensis Rudolph & Crandall, 2005 (cf. Rudolph et al., 2007; Noro et al., 2008).
In Parastacus defossus, 7 out of 72 gonads investigated were ovo-testes, which were
interpreted as transitional stages from males to females. Protandric hermaphroditism in
this species may be an adaptation to fossorial life and low population density (Noro et al.,
2008).
At present, little is known on the factors that elicit intersexuality in crayfish. The case
of intersexuality described in Cherax quadricarinatus by Sagi et al. (1996) was considered
as a unique model for the study of the role of the androgenic gland in the regulation of
sex differentiation in crustaceans. Implantation of the androgenic gland into females and
its surgical removal from males suggest that intersexuality can result from the absence or
malfunctioning of one of the androgenic glands in males (Sagi et al., 2002). However, it is
an open question whether such functional degenerations occur spontaneously or whether
they are induced by environmental factors or parasites. Examples for the latter are provided
by the shrimp, Hippolyte inermis Leach, 1815, where sex reversal is caused by compounds
from ingested benthic diatoms, and by some amphipods and isopods, where feminization is
induced by the bacterium Wolbachia, a widespread bacterial manipulator of reproduction
in arthropods.
Exciting contributions to our knowledge on crayfish reproduction come from hybridiza-
tion experiments and the detection of parthenogenesis in crayfish. Hybridization of
Cherax rotundus Clark, 1941 females and Cherax albidus males consistently produced
only male progeny, whereas the reciprocal cross produced both male and female progeny
(Lawrence et al., 2000). This approach is of interest for yabby aquaculture, due to faster
growth of the male hybrids. Parthenogenesis was detected in the marbled crayfish in 2003
and was at that time the first case in Decapoda (cf. Scholtz et al., 2003). Recently, Yue
et al. (2008) reported on the occurrence of four natural clones of Procambarus clarkii in
China, suggesting that parthenogenesis may be more widespread in crayfish. The marbled
crayfish, or Marmorkrebs, first appeared in the aquarium trade in the mid 1990s, is an all-
female species, and produces genetically identical offspring (Vogt et al., 2004; Martin et
al., 2007; Vogt et al., 2008). It is a parthenogenetic form of the slough crayfish Procam-
barus fallax (cf. Martin et al., 2010), which coexists with the genetically similar Procam-
barus alleni (Faxon, 1884) in some subtropical sloughs of Florida. At present, there are
two genetic systems available in the Marmorkrebs-Procambarus fallax kinship, the gono-
choristic and genetically diverse wild type and the parthenogenetic and genetically unifom
Marmorkrebs (Martin et al., 2007; Vogt et al., 2008). This unique genetic system provides
outstanding biological material for research on alteration of the genome, physiology and
behavior during transition from gonochorism to parthenogenesis.
In support of a number of reports of interspecific mating in crayfish (Reynolds, 2002),
evidence was found of hybridization between two species of North American crayfish.
Using morphological and allozyme comparisons between three species from allopatric
and sympatric populations, Perry et al. (2001) found no evidence of hybridization between
the indigenous Orconectes virilis and both a second indigenous species, Orconectes
propinquus, and the introduced Orconectes rusticus. However, numerous morphologically
intermediate crayfish between Orconectes propinquus and Orconectes rusticus occurred
at sympatric sites, and many of these individuals showed allozymes diagnostic for both
species in allopatry. Over 6% of the crayfish at one sympatric site were putative F1
hybrids, 4% were putative F2 individuals (hybrid × hybrid origin), and 13% were putative
backcrosses (product of hybrid × parental matings). This is the first genetic documentation
of hybridization between a resident crayfish species and an invader. Hybridization may be
a common phenomenon in crayfish, and genetic mechanisms may be threats to indigenous
crayfish.
Embryonic development
Rathke (1829), Lereboullet (1862), Reichenbach (1877, 1886), Huxley (1880), and
Morin (1886) carried out early studies of embryonic development in astacids in the 19th
century. Sixteen stages of embryonic development from before spawning to the first
postembryonic molt and their chronology were described in the astacids Astacus astacus
and Austropotamobius torrentium, and in the cambarids Cambarus rusticus (cf. Busch,
1940) and Cambarus bartonii sciotensis Rhoades, 1944 (cf. Zehnder, 1934).
Celada et al. (1985, 1987) reported the external images and chronology of the embry-
onic stages of Pacifastacus leniusculus by means of optical microscope techniques and
scanning electron microscope (SEM), respectively. A similar study using SEM techniques
was performed for Austropotamobius pallipes (cf. Celada et al., 1991) (fig. 67.21). Con-
sidering intervals of 5% of the total time between fertilization and hatching, Sandeman &
Sandeman (1991) and García-Guerrero et al. (2003) provided a morphological description
of the embryonic development in Cherax destructor and Cherax quadricarinatus, respec-
tively. Scholtz & Kawai (2002) in Cambaroides japonicus (De Haan, 1841) and Alwes &
Scholtz (2006) in the Marmorkrebs, described some aspects of embryonic and postembry-
onic development.
Fig. 67.21. Microphotographs taken using a stereoscopic microscope NIKON SMZ 10. Images
correspond to Austropotamobius pallipes eggs fixed in alcoholic Bouin (J. M. Carral, J. D. Celada,
J. R. Pérez, and M. Sáez-Royuela). A, Phase III: blastosphere; B, Phase VI: embryo with circular
gastral furrow; C, Phase IX: embryo with naupliar appendages; D, Phase X: embryo with Anlagen
of masticatory appendages; E, Phase XI: embryo with Anlagen of pereiopods; F, Phase XII: embryo
with pulsating heart; G, Phase XIII: embryo with strongly developed eye pigment; H, Hatching:
Stage 1 juvenile.
In all studies on different crayfish species, the images of the embryonic stages are
similar, even when the duration of incubation is highly variable. In the wild, periods of
embryonic development are markedly different between astacids (around 6 months) and
cambarids (<1 month) (Reynolds et al., 1994). In each species, temperature is the main
factor influencing the duration of embryonic development; for example, incubation of
Austropotamobius pallipes lasts 82 days at 15.5◦ C and 139 days at 11◦ C (Carral, 1990;
Celada et al., 1991).
A knowledge of embryonic phases and their chronology has allowed for the intensifi-
cation of reproduction under culture conditions. The application of thermal treatments at
certain stages of embryonic development was shown to be a key factor in improving yields
of the final stage 2 juveniles in both maternal (Celada et al., 1998; Pérez et al., 1998a, b)
and artificial incubation (Carral et al., 1988, 1992; Pérez et al., 1998a, b, 1999). Once
artificial incubation had become feasible, egg storage from 28 days up to 3 months and
egg transport were successfully performed (Celada et al., 2000, 2001; Pérez et al., 2003).
Pérez et al. (2003) identified a critical embryonic phase that limits the duration of storage,
when they reported high mortalities when stored eggs reached phase XII (embryo with pul-
sating heart). Recently, Melendre et al. (2007) recommended incubating batches of eggs
with similar stages of embryonic development in order to avoid losses of stage 2 juveniles
derived from the coexistence of stages 1 and 2 at the end of the artificial incubation.
ECOLOGY
[F. G HERARDI]
Crayfish can be found in a wide variety of freshwater habitats: lakes, rivers, swamps,
cave pools, temporary ponds, and estuaries all provide suitable abiotic and biotic con-
ditions for their survival (Nyström, 2002). However, the pattern of crayfish distribution
varies greatly, depending on the physiological tolerance of each single species to physico-
chemical factors, e.g., water temperature, salinity, pollution, and to their changes, its resis-
tance to physical disturbance, and its ability to face predation and competition.
A comparison between the European stone crayfish, Austropotamobius torrentium,
and the North-American red swamp crayfish, Procambarus clarkii, is emblematic in
this respect. Austropotamobius torrentium was recently added to Annex II of the EU
Habitats Directive as a species requiring special conservation measures: many cases of
local extinction have in fact been recorded across its entire distribution range (central and
southeastern Europe) (Souty-Grosset et al., 2006). It is a stenoecious species, inhabiting
a small range of habitats where it exhibits a narrow tolerance to several environmental
factors. Typically, the species is confined to brooks, small streams, and headwaters
in mountainous areas that provide appropriate shelter, such as cobbles and pebbles
(Souty-Grosset et al., 2006). It avoids water velocities >25 cm s−1 and requires water
temperatures >8◦ C in summer, with an optimum between 14 and 18◦ C and an upper limit
of 23◦ C. It does not occur in warm, organically enriched and polluted watercourses, or
in stagnant waters with muddy sediments. Bank side shrubs and trees are common and
provide the required shade, leaf litter, and shelter (Souty-Grosset et al., 2006).
Procambarus clarkii was recently added to the list of the 100 worst alien species
in Europe (DAISIE, 2008) because of its well-documented invasive potential (Gherardi,
2006). From its native range (north-eastern Mexico and south-central U.S.A.), it has been
successfully introduced into all continents, except Australia and Antarctica; it has become
dominant in many introduced ecosystems and rapidly expands (Gherardi, 2006). Contrary
to Austropotamobius torrentium, it is a euryecious species. While in its native range
Procambarus clarkii is most abundant in seasonally flooded wetlands (Huner, 2001), in the
introduced range it can be found in all types of water bodies, including rivers and streams,
temporary streams and ponds in Portugal, trout streams in Oregon, rice fields in Spain
and Portugal, permanent lakes in Nevada, Switzerland, and Kenya, and irrigation systems
in Italy (Huner, 2001). The species faces low water and dry periods by retreating into
burrows (Huner & Barr, 1991) and low water oxygen concentrations (below 2 mg L−1 )
by using atmospheric oxygen (Huner & Barr, 1991). It is found in waters ranging from
brackish (10 ppt in salinity) to fresh water. Molting rate appears to be highest at relatively
high temperatures (22-30◦ C). Populations have been found from culture ponds with a total
hardness <5 mg mL−1 (with an optimum over 50 mg mL−1 ) and with pH lower or higher
than the optimal 6.5-8.5 (Huner, 2001).
The two examples above are illustrative in showing that the responses of a given species
to the various features of the habitat reflect its possible conservation status or invasive
behavior. Understanding the ability of crayfish to tolerate changes in water temperature,
salinity, and hydrological regimes, to resist pollution, and to face habitat degradation
and simplification, will help us anticipate their overall responses to global change: and
hopefully will help us find a solution. In the latest years, the number of studies investigating
crayfish habitat requirements has increased (Trouilhé et al., 2007 and Benvenuto et al.,
2008 in Astacidae; Flinders & Magoulick, 2007 in Cambaridae; Jowett et al., 2008 in
Parastacidae), but more attention is needed, in particular for some still understudied taxa
and regions, e.g., the genus Astacoides in Madagascar (Jones et al., 2007). Determining the
environmental factors that affect the abundance and production of crayfish is also important
from an economic point of view, when crayfish species are used as aquaculture/fisheries
commodities.
Below is a summary of our present knowledge of the relationships between some abiotic
and biotic factors of the habitat, and crayfish distribution and abundance in an environment
subject to changes. This is followed by an examination of the feeding habits of crayfish
and their position in the food web, along with their direct and indirect effects on other
trophic levels.
Crayfish in their habitat

The ability to tolerate changes in water temperature varies greatly within the families
and to a lesser extent between families (Nyström, 2002). However, members of Astacidae
appear to have lower upper lethal temperature tolerance limits than several species from
Cambaridae, the latter seemingly being favored in the face of global warming. Temperature
tolerance limits have been identified for several crayfish in the laboratory (Nyström, 2002),
but in natural conditions crayfish may adopt behaviors that allow them to resist extreme
values. For instance, when water temperature exceeds its thermal tolerance (>39◦ C),
Orconectes rusticus finds refuge in burrows at a significantly cooler temperature (about
6◦ C lower) (Mundhal, 1989).
Since temperature influences several stages in the crayfish life cycle (see Reynolds,
2002 and references therein), this factor will probably have a strong impact on population
size from year to year. However, few studies address the importance of temperature for
crayfish abundance, mostly due to a lack of long-term data. In a lake in southern Sweden,
both climatic- and density-dependent factors were found to influence the population size of
both the indigenous Astacus astacus (present in the lake until 1974 when it went extinct due
to the crayfish plague) and Pacifastacus leniusculus (introduced in 1985) (Olsson, 2008).
The application of a modified Rickert model to better explain the recorded fluctuations in
the crayfish population showed that winter temperature two years previous to catch was
positively correlated with the abundance of large adult crayfish, while crayfish density in
the previous year influenced the catch of the following summer.
A warmer climate and the resulting effect on precipitation are predicted to alter the
salinity of freshwater and estuarine ecosystems. Some crayfish species may survive in
brackish water areas for several weeks: Astacus leptodactylus, Austropotamobius pallipes,
and Procambarus clarkii tolerate salinities up to 21 ppt (Holdich et al., 1997) and Cherax
quadricarinatus up to 12 ppt (Jones, 1995). However, growth in, e.g., Cherax destructor
at salinities above 6 ppt (Mills & Geddes, 1995) and reproduction in, e.g., Astacus
leptodactylus at salinities above 7 ppt (Holdich et al., 1997) appear to be inhibited in all
species studied so far.
Crayfish responses to a second indirect effect of global warming in many regions, the in-
creased rate of desiccation, are both physiological and behavioral. Crayfish ability to face
desiccation is particularly crucial in the Mediterranean countries, where the phenomenon
is exacerbated by the massive abstraction of water for human use. A mechanism that cray-
fish may adopt to adapt to aquatic oxygen depletion is a switch to air as an oxygen source.
Severely hypoxic Orconectes rusticus, for example, were described to climb the vegeta-
tion and reach the water surface, where they thrusts one branchial chamber into the air and
use the scaphognathite to pass air across the gills (McMahon & Wilkes, 1983). Similar
responses have been reported for other crayfish species (Wheatly & Taylor, 1981). The air
breathing capability is a property of temporary or permanent burrowers. Three species of
American burrowers, Fallicambarus fodiens (Cottle, 1863), Cambarus diogenes diogenes
(Girard, 1852), and Procambarus clarkii spend, at least in the laboratory, the majority of
the time either moving or resting above the water line, or at the surface of the water with the
inhalant apertures of the branchial apparatus in the air (MacMahon & Hankinson, 1993).
In times of drought, the water table may well fall below the ability of crayfish to burrow. In
the relatively high humidity conditions found in their natural burrows, species of Cherax
and Procambarus clarkii can survive periods in excess of 28 days without any access to
free water (Huner, 1989). On the contrary, Procambarus clarkii exposed to room air of
about 50% RH shows mortality after 3-7 days of exposure (McMahon, 2001).
The third indirect effect of global warming is the increased variability and intensity
of rainfall events that may modify disturbance regimes by changing the magnitude and
frequency of floods. The ability of crayfish to withstand periods of floods in streams
and rivers varies between species and life stages, juveniles being particularly prone to
be washed away (Smith et al., 1996). In non-burrowing crayfish, such ability is increased
by heterogeneous habitats (see below) that can provide refuges, such as cobbles, stones,
and submerged tree roots.
Human activities contribute greatly to the chemical pollution of fresh waters by means
of mining operations, sewage from urban areas, industrial effluents, fertilizers, and the
use of biocides (Nyström, 2002). Pollutants may also enter aquatic systems through
atmospheric deposition. Thus, in several regions crayfish are exposed to both inorganic
chemicals, such as sulphur dioxide (acid rains), fertilizers (eutrophication), and metals, as
well as man-made organic chemicals, such as pesticides, polycyclic aromatic hydrocarbons
(PAHs), polychlorinated bi-phenyls (PCBs), and pharmaceuticals.
The effects of acidification on crayfish are several (France, 1983): (1) direct lethal
effects (most crayfish species are affected by water at a pH below 5.5; Appelberg,
1989); (2) reproductive failure (Appelberg, 1984); (3) decreased resistance to diseases
(experimental acidification of a lake in Canada increased the frequency of Orconectes
virilis infected by the lethal microsporidian Thelohania contejeani); and (4) increased
vulnerability to predation (low exoskeleton rigidity due to disturbed calcium metabolism
in acidified lakes may increase the risks of predation).
Similarly complex are the effects of eutrophication on crayfish populations. If on the
one hand, the addition of phosphorous and nitrogen from human sewage run-off from
agriculture areas could raise productivity of the systems and thus crayfish production,
on the other hand, increased mineralization of organic material reduces the oxygen
concentration. Crayfish tolerance to low oxygen concentrations may vary among species
(Hobbs & Hall, 1974), but some crayfish species, e.g., Orconectes virilis and Procambarus
clarkii, can shift to air breathing as described above. Eutrophication is often accompanied
with toxic algal blooms. There is evidence that crayfish ingest phytoplankton (Gherardi &
Lazzara, 2006) and accumulate toxins such as microcystin-LR in their tissues and organs
(Tricarico et al., 2008), but short term consumption of cyanobacteria, such as the benthonic
Oscillatoria sancta and the planktonic Microcystis aeruginosa, had no detectable effect on
either Pacifastacus leniusculus (cf. Lirås et al., 1998) or Procambarus clarkii (cf. Tricarico
et al., 2008).
The effects of chemicals, e.g., metals, detergents, oils, pesticides, etc., on crayfish
species have been analysed under controlled laboratory conditions (Hobbs & Hall, 1975).
Under exposure of mercury, cadmium, and lead, a reduced activity of the central nervous
system acetylcholinesterase (AChE) was observed in Procambarus clarkii (N.B.: AChE is
an enzymatic biomarker commonly used to denote exposure to organo-phosphate insecti-
cides) (Devi & Fingerman, 1995). A review of 183 acute toxicity tests with 97 organic
toxicants revealed that the degree of toxicity is dependent on the chemical compound
(organophosphate and organochlorine insecticides are the most toxic), crayfish life stage
(juveniles are more susceptible than the adults), and the species involved (Orconectes is
more sensitive to these than is Procambarus) (Eversole & Seller, 1996). Some field studies
attempted to link chemical contamination observed or suspected in the environment with
bioaccumulation of toxicants, such as heavy metals or PCBs, DDT, and DDE in crayfish
organs and tissues, particularly in the gills, exoskeleton, and hepatopancreas [in: Cambarus
bartonii bartonii (Fabricius, 1798) in Canada, Alikhan et al., 1990; Orconectes limosus in
the Netherlands, Schilderman et al., 1999; Austropotamobius pallipes and Procambarus
clarkii in Italy, Gherardi et al., 2002] or variations in DNA profiles (in Orconectes rusticus
in Ohio; Krane et al., 1999). In some instances, crayfish have been used as model systems
to investigate the physiological responses of organisms to toxicants such as in Cambarus
diogenes diogenes (cf. Grosell et al., 2002) and as bioindicators of chemical pollution (Pro-
cambarus clarkii in southern Spain; Vioque-Fernández et al., 2007). Because of the cray-
fish susceptibility to insecticides, various attempts have been made to use these chemicals,
including organic compounds (Peay, 2006), in order to eradicate unwanted populations of
crayfish from aquatic habitats. This is a matter of concern today. Strong ecological side-
effects are to be expected, since not only crayfish but also other invertebrates and even
fishes may be susceptible to these substances, with serious effects on the integrity of the
whole ecosystem. Besides, the peak insecticide concentrations needed in open water to kill
a given pest are usually far greater than the toxic levels of that pest as defined in the lab-
oratory. In sum, the transfer of laboratory toxicity data for insecticides to field conditions
is often associated with a number of uncertainties that need to be carefully addressed on a
case-by-case basis, before any significant conclusion can be researched (Souty-Grosset et
al., 2006).
Human activities have extensively affected freshwater habitats, leading to their
constant degradation loss, or simplification: channelization of streams, silt deposits, ash
wastes, and sawmill operations have all been reported to be directly responsible for the
extinction of several crayfish populations (Nyström, 2002). There is increasing evidence
that the heterogeneity of the pristine landscape offers physical protection and food to
crayfish. Cobbles and macrophytes provide shelter for non-burrowing crayfish, along with
submerged roots, fallen branches, and large woody debris from the riparian vegetation
(Naura & Robinson, 1998; Benvenuto et al., 2008), and may reduce predation on juveniles
and minimize the risk of cannibalism during molting among adults. Instead, the physical
protection of burrowing crayfish depends on levee areas and on soil suitability, i.e., small
particles and free water (Huner & Barr, 1991). Riparian vegetation furnishes also shade that
maintains low water temperatures and is a source of allochthonous plant detritus. To cite
an example, populations of Cambaroides japonicus were found in streams characterized
by high percentages of early successional species in the riparian vegetation and at reaches
with abundant boulders (Usio, 2007) as a confirmation that the distribution and abundance
of crayfish populations largely depend on both riparian vegetation and shelter. Similarly,
an outdoor stream channel experiment showed that habitat complexity, more than the
presence of adults, affects the recruitment of juvenile Pacifastacus leniusculus, reducing
competition for food and shelter and aggressive interactions between juveniles (Olsson &
Nyström, 2009).
The human-mediated introduction of species outside their native range is a form
of biological pollution that often affects the distribution and abundance of indigenous
crayfish. For example, brown trout (Salmo trutta Linnaeus, 1758), introduced to New
Zealand in the 1860’s to benefit sport fishing, has affected the distribution of the indigenous
crayfish Paranephrops planifrons White, 1842 and Paranephrops zealandicus due to
its intense predation, particularly on small individuals (Townsend, 2003; Olsson et al.,
2006). The vulnerability of Paranephrops planifrons to trout may in part reflect its
inability to respond to the chemical cues released by the non-indigenous fish; in contrast,
it exhibits antipredatory behavior towards the indigenous eels (Shave et al., 1994). In
many areas, non-indigenous crayfish compete, either directly (with overt aggression)
or indirectly (through exploitative competition), with indigenous crayfish species and
eventually replace them. For example, the competitive superiority of the non-indigenous
Pacifastacus leniusculus has led to the decline of the Shasta crayfish, Pacifastacus fortis
(Faxon, 1914) in northern California (Light et al., 1995). Pacifastacus leniusculus’ larger
body size (which is a determinant of dominance in agonistic interactions and decreases
the vulnerability to gape-size limited predators), along with its ability of interspecific
matings and to win competition for shelters, has contributed to the decrease in population
abundance of the indigenous Astacus astacus in Sweden (Söderbäck, 1991, 1994). Similar
mechanisms explain the replacement of Orconectes sanborni, Orconectes propinquus,
and Orconectes virilis by the invasive Orconectes rusticus in North America (Hill &
Lodge, 1994, 1999). The decline of indigenous species, such as the European species, may
be facilitated by the transmission of lethal parasites, e.g., Aphanomyces astaci, by non-
indigenous species (Pacifastacus leniusculus and Procambarus clarkii) (section Parasites
and diseases).
Feeding habits
Crayfish are the largest and amongst the longest lived invertebrates in many fresh-
water communities, and often occur at high densities. Most species can be regarded as
keystone consumers (Nyström et al., 1996) due to the important roles they play as both
predators and detritivores (Whitledge & Rabeni, 1997). They also constitute the main prey
of several species, including fish, birds, and otters. Hence, crayfish population decline may
profoundly affect the functioning of the entire ecosystem on the one hand, and the intro-
duction of potentially invasive crayfish may have serious consequences for the structure of
freshwater food webs on the other (Gherardi, 2007).
Crayfish feed on a variety of food items: detritus, algae, macrophytes, invertebrates
(including other crayfish), eggs and larvae of amphibians, fish, and fish eggs. The
omnivorous habits of crayfish can be inferred from the structure of their mouthparts and
their ability to grasp food items with their walking legs (section External morphology).
They are also able to locate potential prey using mechano- and chemoreceptors that allow
them to perceive hydrodynamic disturbances (Breithaupt et al., 1995) and chemical cues
(Tierney & Atema, 1988), respectively, produced by other organisms.
Information about crayfish feeding derives from gut (foregut) content data, behavioral
observations in natural habitats, laboratory choice experiments, assimilation data, and
stable isotope ratio analyses (Nyström, 2002). However, these different methods, even if
applied to the same species or to the same population, may provide contradictory results.
This is well illustrated by the example below regarding the feeding habits of Procambarus
clarkii in its introduced range in Italy. In experimental cages kept for three weeks in a lake
in Tuscany, the species showed to be a voracious consumer of the hydrophytes Nymphoides
peltata and Potamogeton filiformis and of the pond snail Haitia acuta (Draparnaud, 1805),
but not of Utricularia australis and the mosquito fish Gambusia affinis (Baird & Girard,
1853) (cf. Gherardi & Acquistapace, 2007). Its inability to prey on fish contrasts with the
results of other studies (Renai & Gherardi, 2004; Leite et al., 2005). Gut content analyses
from wild crayfish collected in several invaded habitats showed that by far the larger
portion (30-65%) of crayfish guts, with a slight variation across seasons, was composed of
plant detritus followed by fresh plants and animal remains (Gherardi & Barbaresi, 2008).
On the contrary, from a series of choice test experiments in the laboratory, Procambarus
clarkii always selected Urtica sp. when offered fresh plants, a choice that does not reflect
the availability of plants in the habitat. Surprisingly, crayfish even clearly preferred Urtica
sp. over dead earthworms, notwithstanding the higher nutritional value and assimilation
efficiency of the latter (Gherardi & Barbaresi, 2007).
Discrepancies in the results of different studies are not surprising. In part, these can
be a consequence of the use of different methods. For example, gut content analysis
data, although being highly informative for comparative studies, might be biased by the
different digestion rate of the various food items and only give information on recent
crayfish feeding activity. Laboratory experiments may not reflect crayfish feeding in their
natural habitat and may be too short to reveal the importance of nutrients that could be, in
contrast, essential for survival and growth in the long run (Nyström, 2002). The analysis
of carbon and nitrogen isotopes has the merit to provide information on assimilated food
sources over a long period of time: ratios of carbon (13 C/12 C) reflect the assimilated diet
of an organism, whereas ratios of nitrogen (15 N/14 N) are also used to define the trophic
position of an organism. For example, as shown in a study by Whitledge & Rabeni (1997)
in a stream in North America on Orconectes punctimanus (Creaser, 1933), terrestrial plant
detritus appeared to contribute to the diet of the species by 80% according to gut content
analysis, but much less according to the isotope ratio data. Other stable isotope analyses
have pointed out the importance of invertebrates as a food source for crayfish (Olsson et
al., 2008).
However, contradictory results may for a large part be due to the high variability
of crayfish feeding in their natural habitats, and to several other factors affecting that.
Although typically being described as generalists and opportunists (Gherardi & Barbaresi,
2008), most crayfish species act as selective feeders (Nyström & Strand, 1996). The
criteria adopted to make choices are several and sometimes difficult to understand
(Cronin et al., 2002). They include the availability of the various food items in the wild
(Nyström & Pérez, 1998), their morphology, and structure that affect the time to process
them. Thin-shelled species of snails are preferred to thick-shelled species by Pacifastacus
leniusculus (cf. Nyström et al., 1999). Submerged macrophytes are preferred over more
robust emergent species (Chambers et al., 1991) for their nutritional value (detritus is a
highly effective food for crayfish for its “microbial conditioning” or “chemical-defense
leaching”; Newman, 1991). Assimilation efficiency is important, e.g., rainbow trout eggs
are preferred to zebra mussels by Orconectes virilis (cf. Love & Savino, 1993), as well
as their possible content such as chemical defenses (tannins; Bolser et al., 1998). Factors
other than quality and morphology might also determine crayfish food choice, such as
the availability of cover or protection from predators (Damman, 1987), the consumer’s
state or hunger (Cronin & Hay, 1996), the consumer’s prior feeding experience (Dorn et
al., 2001), and the abundance of alternative foods (Chambers et al., 1990). Differences
in feeding may also be related to crayfish sex and activity, and to population density,
crayfish being forced to switch to less preferred items in the presence of strong competition
pressure by conspecifics (Bondar et al., 2005) and to increased cannibalism (Nyström,
2002). An ontogenetic shift of the diet was also described in several species, e.g., in
Austropotamobius pallipes, as reported by Gherardi et al. (2004), with juveniles being
more carnivorous than the adults, and only gradually shifting towards a more vegetarian
diet with growth (Momot, 1995).
Crayfish in the food web

Being omnivorous, adult crayfish influence the structure of food webs in a complex
way through direct or indirect trophic effects. These effects are most often density
dependent (Charlebois & Lamberti, 1996) with some notable exceptions in the case of
invasive species (Gherardi & Acquistapace, 2007). Fig. 67.22 is an attempt at summarizing
the trophic links that crayfish may produce in littoral zones of ponds and lakes (see also
Nyström, 2002; and Gherardi, 2007). These links, however, may vary in function of the
species composition of the community and the presence of introduced predators (Nyström
et al., 2001), conditions that make any generalization provisional.
Typically, adult crayfish affect the biomass of organic detritus (link 1, fig. 67.22) and
of macrophytes (link 2, fig. 67.22). In their turn, changes in detritus and macrophyte
biomass may have multiple non-trophic effects on the community, because of their role of
either protective cover and substrate, or breeding sites for a multitude of organisms, such
as other invertebrates, fish, amphibians, and birds (Rodríguez et al., 2005).
When grazing is intense, as in the case of dense populations of invasive crayfish
species, macrophyte abundance is subject to a drastic decline (Gutiérrez-Yurrita et al.,
1998). A substantial loss of macrophyte biomass is also due to non-consumptive plant
clipping and uprooting by crayfish (Gherardi & Acquistapace, 2007). Apparently, the
destruction of much more plant tissue than the crayfish can eat should induce a positive
effect to the system, because fragmentation produces nutritious, coarse particulate organic
matter (CPOM). However, in nutrient-rich conditions macrophyte destruction is generally
followed by a switch from a clear to a turbid state, dominated by growth of surface
Fig. 67.22. Food web links (those numbered are discussed in the text) in a littoral zone of a lake
or pond. Arrow thickness denotes the hypothesized strength of the interactions. The most important
interactors in the food web are in bold.
microalgae, like Microcystis aeruginosa (cf. Rodríguez et al., 2003). In its turn, this may
lead to a decrease in benthic primary production due to reduced light penetration.
Little is known about the effects of crayfish on the abundance and composition of
surface microalgae (link 3, fig. 67.22) (but see Gherardi & Lazzara, 2006). On the
contrary, information is available on their positive (+) or negative (−) effects on periphytic
algae (link 4, fig. 67.22). Crayfish may (1) consume and dislodge periphyton during
feeding, movement, or burrowing (−), (2) reduce the abundance of algivorous invertebrates
(or vertebrates), which can indirectly increase algal abundance (+) (Luttenton et al.,
1998), (3) fertilize periphyton with their feces (+) (Charlebois & Lamberti, 1996), and
(4) consume or destroy macrophytes on which some algae grow (−) (Lodge et al.,
1994). Because snails are both the prey primarily affected by crayfish (link 5, fig. 67.22)
and the most important grazer group among the many other grazing taxa, crayfish may
indirectly generate an increased abundance of microalgae by relieving them from the
grazing pressure of snails (link 6, fig. 67.22).
Similarly complex are the effects that adult crayfish have on the biomass and species
richness of macroinvertebrates (links 7, 8, and 9, fig. 67.22). Several mechanisms
may come into play (Charlebois & Lamberti, 1996), i.e., (1) consumption, (2) increased
drift through prey escape and incidental dislodgment by their foraging, and (3) possible
inhibition of invertebrate colonization. Gastropods are the taxon most affected by adult
crayfish (link 6, fig. 67.22) and are sometimes eliminated by invasive species (Wilson et
al., 2004). The direct impact of adult crayfish on non-snail macroinvertebrates (links 7
and 8, fig. 67.22) largely depends on the life-history and behavior of each single species.
In lentic waters, crayfish predation is weak on species that: (1) move quickly enough to
escape tactile-feeding crayfish, e.g., isopods, amphipods, some dipterans, heteropterans,
and coleopterans, (2) circumvent crayfish recognition ability by living in cases, e.g.,
trichopterans, or (3) avoid contact by living in the sediment, e.g., some dipterans (Lodge
et al., 1994; Nyström et al., 1996; Stenroth & Nyström, 2003). Indirect effects are also
many, as listed below. Through consumption and destruction of macrophytes, crayfish
can alter littoral habitats, leading to declines in macrophyte-associated taxa (Nyström
et al., 1996). Crayfish may also influence detrital substrates through bioturbation and
feeding: the reduction in detritus has potential consequences for zoobenthic communities,
particularly collector-gatherers, e.g., some ephemeropterans, trichopterans, and dipterans.
Finally, crayfish predation upon other macroinvertebrate predators such as odonate larvae
could reduce their abundance, subsequently allowing an increase in the abundance of their
prey, or they can compete with, e.g., odonates for prey resources (McCarthy et al., 2006).
Crayfish are exposed to a wide range of predators, including conspecifics (cannibalism
is frequent in dense populations but mostly directed to juveniles or molting individuals)
and other crayfish species (Pacifastacus leniusculus was found to prey on Astacus
leptodactylus and Austropotamobius pallipes; Holdich et al., 1995). Several species
of aquatic invertebrates, such as dragonfly larvae (e.g., Dye & Jones, 1975), fishes,
amphibians, and reptiles are all known predators of juvenile and adult crayfish, but few
seem to have a significant effect on crayfish abundance (Nyström, 2002). Exceptions
are possibly eels: in Swedish lakes, the abundance of Astacus astacus catches was
inversely proportional to the production of eels (Svärdson, 1972). To face predation by
fishes, crayfish have evolved several behaviors that range from the ability to recognize
chemicals released by some fish species (Hirvonen et al., 2007) and by injured con- and
heterospecifics (see section Behavior) and the adoption of a nocturnal activity pattern
to minimize encounters with diurnal predators (Hamrin, 1987), to reducing exposure by
hiding in shelters or occupying shallow parts of streams and pools (Benvenuto et al., 2008).
Crayfish can also be an important food source for several species of mammals, such as
the otter (Delibes & Adrían, 1987) and mink (Smal, 1991), as well as birds. In southern
Spain, the introduced Procambarus clarkii is abundantly preyed by at least six species of
birds; the diet of white storks, night herons, and little egrets is composed for up to 80% of
crayfish in summer (Rodríguez et al., 2005). Similarly, in the Camargue (southern France),
the Procambarus clarkii population density is highly predictive of the abundance of the
Eurasian bittern, Botaurus stellaris Linnaeus, 1758 (cf. Poulin et al., 2007). However, the
effects of mammal and bird predators on crayfish abundance are less well studied than that
of predatory fish. Even fewer is known about the impact that the simultaneous presence of
multiple predators may exert on crayfish populations (Nyström, 2002).
In conclusion, two points should be stressed. First, each single crayfish species can
be found along a gradient of morphological, physiological, and behavioral adaptations
between truly stenoecious and truly euryecious. In the face of global change and in the
need of prioritizing our conservation efforts, it seems crucial to know which species is
less vulnerable to changes in water temperature, salinity, and hydrological regimes, to
pollution, to habitat degradation, and to invasions by non-indigenous species. Second,
since crayfish play a key role in freshwater communities, the introduction of crayfish in
areas without any indigenous ecological equivalent is expected to induce complex and
often unpredictable changes in the food web (Gherardi, 2007). When non-indigenous
crayfish species replace an indigenous ecological equivalent, the overall effect may be
similarly strong if, once introduced, crayfish are capable of building high densities and/or
of reaching large size (Gherardi, 2007). All this might support the conclusion that any
attempt to slow down the ongoing process of extinction of species on one hand, and the
spread of invasive populations on the other, should be rooted in an in-depth knowledge of
crayfish ecology.
BEHAVIOR
[F. G HERARDI]
Since Huxley (1880), crayfish have served as excellent model organisms in ethological
studies (Gherardi, 2002). Notwithstanding their relatively simple physiological hardware,
behavior in crayfish is sophisticated enough to test general hypotheses about resource
acquisition, social dominance, mate selection, and individual recognition. Thus, from
a theoretical perspective, the study of crayfish behavior has largely contributed to refining
our general understanding of the ways the behavioral machinery works in invertebrates.
Behavioral studies incorporate a variety of disciplines, including genetics, ecology,
evolution, and physiology. Here, the emphasis will be on the ultimate causes of behavioral
phenomena, i.e., focused on the evolutionary history of behavior and on its adaptive
value in terms of individual fitness, but proximate questions dealing with the immediate
causation of behavior will be also raised. It seems axiomatic that, from an adaptive
perspective, behavior contributes to raising the relative fitness of crayfish by increasing
their ability to avoid sources of stress, e.g., thermal extremes, dehydration, and predators;
and to acquire and maintain primary resources, e.g., food, shelter, and mates.
Habitat selection
Habitat selection is the behavioral process determining the non-random distribution
of individuals among habitats. It is obviously crucial for an animal to make “decisions”
in this respect, since only in an appropriate habitat it will accomplish its vital functions
(survival, growth, and reproduction) and will avoid the stress inflicted by extreme environ-
mental conditions (section Ecology). Increasing attention is directed today to investigate
the different patches of the habitat that crayfish occupy. For example, a radio-telemetric
study showed that the noble crayfish, Astacus astacus, uses most frequently alder tree
roots or driftwood accumulations; further habitat requirements were water flow velocity
of <20 cm s−1 , a depth of 15-50 cm, the presence of stones, gravel and silt, an irregular,
steep or overhanging shoreline, and shade (Bohl, 1999). A second important objective of
recent studies is to understand how intra- and interspecific competition might affect habi-
tat selection in crayfish populations. Crayfish distribution among microhabitats is size-
partitioned in Austropotamobius pallipes (cf. Benvenuto et al., 2008): small individuals
were found most often in stream edges characterized by shallow water and a high avail-
ability of submerged roots, whereas large individuals use deeper waters, usually associated
with boulders. Forms of habitat segregation have been shown when congeneric species live
in syntopy. For example, in the same river in North America, Orconectes immunis (Hagen,
1870) inhabits mud-bottomed pools within the river, nearby ponds and sloughs, whereas
Orconectes virilis occurs primarily in swifter sections of the stream with rocky bottoms
(Bovbjerg, 1970). Choice experiments in the laboratory indicated that both species prefer
rocky substrates, but that when they occur together, the more aggressive Orconectes virilis
displaces Orconectes immunis from the better microhabitats.
Choosing the time to be active

Crayfish are expected to confine their general activity to appropriate temporal
windows within the daily and/or yearly cycle. Alternatively, to cope with the periodical
changes in the environment, they should change their habitat or migrate to other
areas. Several studies centering on the basic question of rhythmicity in crayfish activity
discussed the long-lasting problem of biological clocks (reviewed in Gherardi, 2002).
Instead, only few studies examined the timing of locomotory activity from an eco-
ethological perspective (Page & Larimer, 1972). Field and laboratory data revealed that, in
the majority of the crayfish populations/species examined so far, activity is concentrated
during nocturnal hours in, e.g., Astacus astacus (cf. Cukerzis, 1988; Styrishave et al.,
2007), Austropotamobius pallipes (cf. Barbaresi & Gherardi, 2001), Orconectes virilis (cf.
Hazlett et al., 1974), and Pacifastacus leniusculus (cf. Flint, 1977; Styrishave et al., 2007).
Indeed, nocturnal habits offer the advantages of both minimizing the risks of being preyed
upon by diurnal predators, and matching the activity of their prey. Only a few species seem
to depart from this general pattern. To cite one example, catches of Procambarus clarkii
in its introduced range in Tuscany reached a maximum after sunset in summer, but over
50% of crayfish were active during daytime in spring, and the few crayfish active in winter
were diurnal (Gherardi et al., 2000). As a confirmation, a laboratory study failed to show
significant differences in Procambarus clarkii’s locomotion between day- and night-time
(Gherardi et al., 2000).
For crayfish populations inhabiting higher latitudes, seasonal changes in the environ-
ment result in alternate periods of favorable and unfavorable conditions for the expression
of their general activity and life cycle patterns, the warmer or wetter periods being typ-
ically the more favorable, viz., in Austropotamobius pallipes (cf. Barbaresi & Gherardi,
2001), Austropotamobius torrentium (cf. Troschel et al., 1995), Pacifastacus leniusculus
(cf. Flint, 1977), and Procambarus clarkii (cf. Gherardi et al., 2001). The switch from pe-
riods of intense activity to periods of low or null activity and vice versa relies on several
pieces of information, mostly provided by day length, temperature, and food availability,
but the links between crayfish behavior and changes in their environment may be complex.
For example, the drastic slowing down of Procambarus clarkii’s locomotion in autumn
recorded during a radio-telemetric study in Italy, was only in part explained by the paral-
lel but more gradual decrease in air and water temperatures, water depth, and day length
(Gherardi et al., 2002).
Migrations are also known to occur in order to face seasonal changes in the environ-
ment in the home water bodies, often in association with reproduction. For example, Or-
conectes virilis females move downstream after having released the juveniles in summer,
and return upstream in autumn prior to overwintering in burrows (Hazlett et al., 1979).
In general, decreasing light and decreasing temperature seem to induce migration (e.g., in
Pacifastacus leniusculus in Lake Tahoe; Flint, 1977).
Avoidance of predators
Since many crayfish species tend to be more active at night, and predators of crayfish
often have generalist and opportunistic feeding habits, it seems advantageous for a species
to use chemical information about predation risks. Information may be given by the
odor of potential aquatic predators, i.e., fishes (Blake & Hart, 1993). Similarly informative
are some chemical stimuli, still of unknown nature (Acquistapace et al., 2005), released
by disturbed conspecifics (e.g., Zulandt Schneider & Moore, 2000), or contained in the
hemolymph emitted by injured conspecifics (“alarm odors”, e.g., Hazlett, 1994). All
these substances may cause appropriate changes of behavior in the alerted individuals by
inducing avoidance of their source areas, freezing or reduced activity, watchful posture,
and increased use of refuges (Hazlett, 1994).
This antipredatory ability is widely diffused among crayfish but the proximate
mechanisms are still open to debate. On the one hand, an innate responsiveness to
eel odors, which can be retained even in allopatry, has been suggested for the noble
crayfish (Hirvonen et al., 2007). On the other hand, many studies by B. A. Hazlett and
coworkers have elegantly proven that several species of crayfish can learn the smell of
potential predators by associating them with the alarm odors from conspecifics (Hazlett
& Schoolmaster, 1998). Crayfish exhibit predation-avoidance behaviors to formerly
neutral odors, such as those produced by nonpredatory fish, like goldfish, Carassius
auratus (Linnaeus, 1758) (Acquistapace et al., 2003), or to odors of potential prey, such
as gyrinid beetles and Campeloma decisum (Say, 1817) snails (Hazlett, 2007), when these
are initially paired with alarm odors. The history of previous exposure to predators
seems also to be important in determining responsiveness to alarm odors: the odors of
crushed conspecifics were treated as feeding signals by Procambarus clarkii populations

from aquaculture ponds, in which predation risks are minimal (Acquistapace et al., 2004).
If confronted with species that are not expanding their ranges, potentially invasive
species such as Orconectes rusticus and Procambarus clarkii are significantly quicker
in responding to the alarm substances emitted by crayfish of other species (Hazlett et
al., 2003) and can remember a learned association longer (Hazlett et al., 2002). This
“invasives-are-smarter” phenomenon allows crayfish to cope with new types of predators
in a novel environment, being a remarkable feature of the behavioral flexibility that
characterizes the biology of invasive species.
Burrowing
Sources of physical and biological stress can be avoided by hiding in natural shelters,
e.g., crevices in rocks, or in burrows. Along with protection against thermal extremes and
dehydration, shelters and burrows offer refuge against predators, conspecifics included,
thus representing a vital resource during some delicate phases of the crayfish life history,
e.g., when they reproduce and molt.
Burrowing crayfish are known since at least the Mesozoic (Hasiotis et al., 1999)
and are particularly abundant in Cambaridae. Interestingly, species reported to be non-
burrower in their native range may turn out to be burrower in the invaded areas, such as
Pacifastacus leniusculus in Britain (Guan, 1994). Burrowing species have been originally
classified into three categories (Hobbs, 1942). Primary burrowers are those crayfish that
spend almost their entire life below the ground surface, occasionally moving about at the
surface (to find food or mates). Their burrow systems are complex and rarely communicate
with open waters. A typical primary burrower is the prairie crayfish, Procambarus
hagenianus (Faxon, 1884), inhabiting the eastern and central Mississippi and western
Alabama. Fourteen species of terrestrial crayfish of the genera Engaeus and Geocharax
live permanently in burrows in marshes, river banks or hilltop areas in Australia. Burrows
may be over 1 m deep and entrances are often marked by a chimney of mud pellets, up to
45 cm high (Suter & Richardson, 1977).
Secondary burrowers occupy burrows during dry periods in areas that are inundated
seasonally. Burrows can be simple, usually consisting of a vertical passageway that may
slope gently or descend in an irregular spiral. Abundant information is available for
a typical secondary burrower, Procambarus clarkii. Field evidence (increased burrow
density with time without a parallel increase of the population size, short time of burrow
occupancy, and intense digging activity; Ilhéu et al., 2003) led Barbaresi et al. (2004) to
hypothesize a “consumeristic use” of the burrows in this species. In fact, at the end of its
foraging excursions, Procambarus clarkii constructs a new burrow, instead of returning to
the old one. The absence of burrow fidelity in this species is apparently a paradox, if one
considers the potentially high energy cost of digging, the vital role played by burrows in the
biology of this crayfish, and its homing ability (see below). Once left vacant, burrows may
collapse causing structural damages to the banks (and economic costs for their restoration).
Tertiary burrowers only burrow either in the winter or during drought conditions
and, in a few cases, during their breeding season. Those associated with permanent water
bodies dig simple, sub-vertical passages in the bottoms. Some stream-dwellers construct
highly elaborated burrows, apparently digging below mean water level and extending
galleries in all directions. The genus Orconectes comprises tertiary burrower species,
such as Orconectes causeyii Jester, 1967, living in permanent, well-oxygenated ponds in
the southwestern U.S.A. Among Parastacidae, Cherax destructor behaves as a tertiary
burrower, inhabiting farm ponds and irrigation canals where water temperature drops
during winter or the water table falls down, whereas the congeneric Cherax tenuimanus
Smith, 1912 rarely burrows.
Food acquisition
Feeding behavior has been described for several crayfish species, e.g., in Cambarus
bartonii bartonii (cf. Dunham et al., 1997), in Procambarus mexicanus (Erichson, 1846)
(cf. Hernández-Muñoz et al., 1999), and in several other species of Procambarus (cf.
Caine, 1975). A detailed description of in situ foraging was given for Austropotamobius
pallipes in a pristine stream in Italy (Gherardi et al., 2001); the species behaves as a time-
minimizer by limiting its foraging excursions to one hour per night, when it traverses
relatively small areas in comparison to other freshwater decapods, e.g., the river crab,
Potamon fluviatile (Herbst, 1785), cf. Gherardi et al. (1989). Energy and nutrient intake
were however maximized in the two sexes, males choosing vegetable detritus and females
choosing moss. Plant debris is one of the main sources of energy and proteins available to
many members of the stream community (section Ecology); moss, although relatively poor
in carbon, shows a higher digestibility (96%) than detritus (89%); periphyton growing on
it may represent an additional food source for the crayfish; its morphology (occurring in
‘bite-size’ pieces) makes its handling easier and thus reduces manipulation time.
Movement
Movement has multiple biological functions, being used both to locate life-supporting
resources and to avoid physical or biological stress. Many studies have analysed locomo-
tion of individual crayfish in different species, populations, and habitats. Crayfish were in-
dividually marked in various ways, ranging from holes punched in their telson or uropods
(Abrahamsson, 1965) or burn spots applied to their cephalothorax using soldering irons
(Abrahamsson, 1965) to radioactive tags (Merkle, 1969), implanted microchips (Guan &
Wiles, 1997), radio transmitters (Gherardi & Barbaresi, 2000; Robinson et al., 2000), and
passive integrated transponder (PIT) tags (Bubb et al., 2006a).
All data collected so far showed a relatively complex pattern of movement. A popu-
lation may exhibit a marked inter- (Hazlett et al., 1974) and intra-individual variability in
locomotory speed. Individuals were found to alternate peaks of higher locomotory activ-
ity (‘wandering’ phases) with long periods of scarce mobility (‘stationary’ phases), during
which movement was confined within a small area (Gherardi et al., 2002; Barbaresi et
al., 2004). The extent of movement may depend on several factors, such as season, sex,
and size (Barbaresi et al., 2004), and even the crayfish’s familiarity with the area might
influence it.
Movement may be more intense in potentially invasive rather than in indigenous
crayfish species, as a confirmation that invaders are better dispersers than the species
they displace. In addition, movements may allow the invasive species to make better use
of patchy resources than indigenous species do; this ability, coupled with their higher
agonistic potential (see below), may contribute to the observed replacement. In a river
in England where in 2003 the invasive signal crayfish Pacifastacus leniusculus and the
indigenous Austropotamobius pallipes still co-existed, clear inter-specific differences in
spatial behavior were found (Bubb et al., 2006a). The median distance moved per day by
signal crayfish, as assessed by radio-telemetry, was over twice that of Austropotamobius
pallipes, and dispersal from the release location was significantly higher in the former
species. However, even in invasive species the intensity of movement may show marked
inter-population differences. For example, in an invaded low-land river in England, radio-
tagged Pacifastacus leniusculus was recorded to cover up to 190 m per day on average
and to occupy a home range of 3000 m2 (Guan & Wiles, 1997). This datum contrasts
with the more sedentary behavior found using PIT telemetry in a population of the same
species inhabiting an upland river in northern England (Bubb et al., 2006b). The majority
of crayfish remained close to the release location, reaching an average distance of 36 m,
with a few crayfish moving up to 345 m. Similarly, a population of Procambarus clarkii
inhabiting rice fields in southern Spain showed, as monitored by radio-telemetry, a massive
use of space with a locomotory speed of up to 4 km d−1 (Gherardi & Barbaresi, 2000).
This figure is significantly higher if compared to the speed of other invasive populations
of the same species, either studied with the same technique (0.3-76.5 m d−1 in Tuscany,
Barbaresi et al., 2004; 1-11 m d−1 in southern Portugal, Gherardi et al., 2002), or with the
mark-recapture method (0.6-1.5 m d−1 , in Tuscany, Gherardi et al., 2000).
Aside from current, no other orientation mechanism has been implicated in any study of
movement. However, in the laboratory Cherax destructor showed to learn the topography
of the environment and to retain this information for a certain time. Crayfish displayed
a quick habituation to any configuration of the experimental tank, as revealed by the
reduction of their locomotory activity after repeated exposures to it, mostly relying upon
tactile inputs from the antennae to detect topographical changes in the environment (Basil
& Sandeman, 2000). In a more recent study, Barbaresi & Gherardi (2006) provided
evidence of Procambarus clarkii’s ability to home, at least in laboratory conditions.
Homing performances rely on this species’ capability to learn and to remember the
topography of the familiar environment for at least 16 hours.
Reproduction
M ATING
Mating has been described in several crayfish species. In Austropotamobius pallipes, it
consists of three sequential phases, i.e., contact, turning of the female, and mounting by
the male (Villanelli & Gherardi, 1998). Mate acceptance by the female is denoted by her
freezing during the contact phase, which determines the subsequent success of copulation.
The active role that the female plays in mating is also known for Cherax quadricarinatus,
in which females almost invariably initiate mating by approaching the male (Barki &
Karplus, 1999). In neither Austropotamobius pallipes (cf. Villanelli & Gherardi, 1998)
nor Cherax quadricarinatus (cf. Barki & Karplus, 1999) overt male-female aggression
was evident. In contrast, Austropotamobius pallipes females may be even killed by the
males before or after mating, at least in a laboratory setting (Woodlock & Reynolds, 1988).
Male-female fighting occurs in several other species (Orconectes rusticus, cf. Berrill &
Arsenault, 1984; Pacifastacus trowbridgii Stimpson, 1857, cf. Mason, 1970; Procambarus
clarkii, cf. Ameyaw-Akumfi, 1976). Similarly, inter-male competition for a female seems
to be frequent in both Cambaridae (Orconectes rusticus, Berrill & Arsenault, 1982;
Snedden, 1990) and Astacidae (Austropotamobius pallipes and Pacifastacus trowbridgii,
cf. Mason, 1970; Gherardi et al., 2006). In laboratory groups of Austropotamobius pallipes,
larger males even went so far as to kill the smaller males in the presence of a receptive
female (Woodlock & Reynolds, 1988). As a result of this larger male dominance, small
males typically are hardly involved in copulations (Berrill & Arsenault, 1984; Gherardi et
al., 2006). Behavioral observations and genetic investigations revealed multiple matings
and multiple sired broods in crayfish. Analysis of 15 wild broods of Orconectes placidus
(Hagen, 1870) with the microsatellite technique proved that most of the females had mated
with two to four males. However, even in multiple-mated females, 80% and more of
the brood descended from one male (Walker et al., 2002). This effect may be explained
by partial removal of the deposited spermatophores of first-mating males by second-
mating males, as observed in Austropotamobius pallipes (cf. Galeotti et al., 2008). Another
interesting feature of Austropotamobius pallipes males is their ability to adjust the volume
of their ejaculate to the size of the female, i.e., to their presumed reproductive capacity
(Rubolini et al., 2006).
S EXUAL SELECTION
Consistent with Charles Darwin’s theory of sexual selection (1871), animals select
mates that allow them to maximize their reproductive success (Andersson, 1994).
Females, who invest in a few costly gametes, are highly choosy, whereas males, who
produce large numbers of cheap sperm, are usually limited in their reproductive output
only by the frequency of mating (Trivers, 1972). Because of this inter-sexual difference in
investment, selection gives rise to ‘reluctant’ females on the one hand, and ‘ardent’ males
with exaggerated morphological and/or behavioral traits on the other.
These traditional ideas have been abundantly discussed in the crayfish literature and
only in part confirmed. Females of a wide array of species were found to select mates
with large body size: Astacus astacus (cf. Furrer, 2004), Austropotamobius pallipes
(cf. Villanelli & Gherardi, 1998; Gherardi et al., 2006), Orconectes rusticus (cf. Berrill
& Arsenault, 1984), and Procambarus clarkii (cf. Aquiloni & Gherardi, 2008a). This
preference might have evolved because: (1) large males are relatively more fertile with
respect to smaller individuals (though in Austropotamobius pallipes the volume of the
ejaculates decreases with increasing male size; Rubolini et al., 2006), and (2) being
dominant in intra-sexual competition, they offer the females high-quality vital resources,
such as breeding burrows, though Orconectes rusticus females are known to extrude and
brood their eggs in isolation (Berrill & Arsenault, 1982). Indirect benefits, yet to be
investigated, may be those hypothesized by the “good genes” model, i.e., a large size
might be the expression of high quality genes and females, mating with a large male, will
transmit this quality to their offspring (Hunt et al., 2005); or by the “runaway selection”
model, i.e., a slight ancestral preference for large males might have led to both an increased
frequency of hereditary “large-body genes” in males and a female preference for large
males (Weatherhead & Robertson, 1979). Indeed, Procambarus clarkii females invest
relatively less (in terms of the size/weight of eggs and juveniles) when they are forced
to copulate with small males (Aquiloni & Gherardi, 2008b).
Large chelae serve as powerful weapons during fights; it is thus expected that they
are subject to sexual selection (Villanelli & Gherardi, 1998). This statement has been
questioned in both Austropotamobius pallipes (females who mate with small, large-
clawed males lay larger eggs than the females who mate with large, small-clawed males;
Galeotti et al., 2006) and Procambarus clarkii (females do not show any preference when
simultaneously offered similarly-sized males with large and small chelae; Aquiloni &
Gherardi, 2008a). Chelar symmetry also has no apparent effect on mate choice, at least in
Procambarus clarkii (cf. Aquiloni & Gherardi, 2008a), whereas asymmetric chelae may
decrease the ability of males to win fights and to secure females for copulation (Rubolini et
al., 2006). Some male ornaments, such as a soft, uncalcified red patch on the outer surface
of the cheliped propodi in mature males of the redclaw crayfish Cherax quadricarinatus,
have been suggested to serve as choice criteria. The location of this vulnerable soft
membrane on the weapon used for fighting renders this structure a handicap for the male;
however, the red patch is also a honest signal of male quality, since its color, derived from
carotenoids obtained from the diet, may vary from bright red in males in good condition
to pale orange in malnourished males (Karplus et al., 2003). Finally, the importance that
the male hierarchical status might play in sexual selection is also controversial. Although
it has been proven that crayfish recognize the social status of conspecifics from their odor
(see below), Procambarus clarkii females make a choice between equally-sized dominant
or subordinate individuals only after having eavesdropped on them fighting (Aquiloni &
Gherardi, 2008a; Aquiloni et al., 2008a).
Due to their polygynous habit and the long time needed to produce sperm, males
may be limited in their sperm supply. This might induce on the one hand the females to
choose non-sperm-depleted males (but no evidence has been collected so far; Aquiloni &
Gherardi, 2008a) and, on the other hand, the males to evolve forms of mate selection.
A long copulation time, large investment in sperm production, and restricted mating
periods (less than one month in Austropotamobius pallipes; Villanelli & Gherardi, 1998)
might also induce male choosiness. Indeed, a study on Procambarus clarkii showed that
males select large females (Aquiloni & Gherardi, 2008a), who are relatively more fecund.
In fact, egg number increases with body size, e.g., Astacus astacus (cf. Cukerzis, 1988),
Astacus leptodactylus (cf. Köksal, 1988), Austropotamobius pallipes (cf. Rubolini et al.,
2006), and Procambarus clarkii (cf. Noblitt et al., 1995). Males should also evolve means
to reduce the risk of sperm competition that may lead to a decreased probability of
paternity. This is a common phenomenon in polygamous crayfish species, in which sperm
is stored before fertilization. When fertilization is external, e.g., on the female pleon as
in Astacidae, males either deposit their spermatophore on top of the first (Woodlock &
Reynolds, 1988) or feed on those deposited by the previous mates (Villanelli & Gherardi,
1998; Galeotti et al., 2007). In Cambaridae, by contrast, spermatophores are inserted into
a seminal receptacle (annulus ventralis) at the female seventh thoracic sternites (section
Reproduction and development), which makes sperm inaccessible for subsequent males.
In those cases, sperm competition may be avoided by adjusting the length of copulation
as a function of the female mating status (suggested for Orconectes rusticus, cf. Snedden,
1990), depositing a mating plug in the opening of the receptacle (suggested for Orconectes
rusticus, cf. Crocker & Barr, 1968), removing the plug of a previous male with copulatory
stylets (Berrill & Arsenault, 1984), or selecting virgin females (proven in Procambarus
clarkii, cf. Aquiloni & Gherardi, 2008a) and defending them.
S PECIES , SEX , AND MATE RECOGNITION

To minimize the loss of time and energy inflicted by non- or scarcely productive
matings, both sexes should have evolved the ability to recognize the “right” mate, i.e., a
reproductive conspecific of the other sex denoting in its phenotype to be of high quality.
To do so, crayfish typically rely on pheromones. Indeed, this taxon has an efficient
system for broadcasting and detecting chemical stimuli (Moore & Bergman, 2005). This
has been confirmed by studies investigating recognition between syntopic species, e.g.,
Orconectes virilis and Orconectes propinquus (cf. Tierney & Dunham, 1982, 1984). When
this mechanism fails, mating may occur between males and females of two different
species, resulting in either reproductive interference (between Austropotamobius pallipes
and Astacus leptodactylus or Pacifastacus leniusculus in England; Holdich et al., 1995) or
hybridization (with the eventual genetic assimilation of one species, as in the case of the
invasive Orconectes rusticus replacing Orconectes propinquus Girard, 1852 in Michigan;
Perry et al., 2001).
Pheromones are also involved in sex recognition. Receptive females of several species
(Cambarus robustus Girard, 1852, Orconectes propinquus, Orconectes virilis, and Pro-
cambarus clarkii) are known to emit sex pheromones (Ameyaw-Akumfi & Hazlett, 1975;
Ameyaw-Akumfi, 1976), using urine as the more likely medium of transmission (see
below); pheromones are primarily detected by the inner rami of the male antennules
(Ameyaw-Akumfi & Hazlett, 1975), but also chemosensory setae on male major chelae
may play a role (Belanger & Moore, 2006). Chemical stimuli seem to be also involved in
communicating readiness to mate in reproductive pairs (Simon & Moore, 2007).
However, recent studies pinpoint the bimodal nature of sex recognition in crayfish:
crayfish rely on both smell and sight but the relative importance of chemical and visual cues
varies between sexes. In some species, e.g., Procambarus clarkii, chemical recognition
seems to be a male prerogative (Aquiloni et al., 2008b). Indeed, the male is the sex
typically involved in mate search in crayfish, and olfactory stimuli provide long-distance
information that is particularly advantageous in the turbid waters where this species lives.
By contrast, in species that inhabit clearer waters, such as Austropotamobius pallipes,
males use both olfaction and vision (Acquistapace et al., 2002). Contrary to males,
Procambarus clarkii females seem to make more extensive use of vision, although visual
stimuli are not sufficient to identify the sex of a conspecific: visual stimuli should be
combined with the odor of a male to suppress female aggressiveness (Aquiloni et al.,
2008b).
Similarly complex is the female recognition of a high-quality mate: visual and chemical
stimuli combined are used by females of Procambarus clarkii to choose a large male,
whereas sight alone or odor alone of an individual of the other sex, independently of its
size, elicit aggression (Aquiloni & Gherardi, 2009). The sight of a mate of a larger size is
not per se an index of the “best” partner but this must be confirmed by chemical stimuli
that, in their turn, inform about the species, the sex, and the reproductive condition of the
potential mate.
PARENTAL CARE AND JUVENILE BEHAVIOR

Parental behavior in crayfish is relatively complex with respect to that found in
other decapods (Aquiloni & Gherardi, 2008d). Females of several crayfish species show
forms of maternal care of increasing complexity, from egg grooming (Bechler, 1979),
pleopod beating (Levi et al., 1999), removal of non-viable eggs and juveniles (Aquiloni &
Gherardi, 2008d), to increased aggressiveness (Fiegler et al., 1995), inhibition of egg and
juvenile cannibalism (Figler et al., 1997), decreased locomotion (Hazlett et al., 1979), and
burrowing (Hazlett, 1983). The extent of male participation in the care for eggs/juveniles
is still unclear. Ameyaw-Akumfi (1976) found that egg- and juvenile-bearing Orconectes
virilis females take refuge in the burrows constructed by their mates. Cohabitation between
mates in the same burrow was suggested for Procambarus clarkii (Ameyaw-Akumfi
& Hazlett, 1975) and Procambarus acutus acutus (Girard, 1852) (cf. Ameyaw-Akumfi,
1976), whereas communal burrows inhabited by family groups have been described for
species of Engaeus (cf. Suter & Richardson, 1977).
Some crayfish species are also known to extend their care to potentially self-sufficient
juveniles in a form of “extended parental care” (Thiel, 1999). For a period ranging
between a few weeks and 3-4 months or more (in Procambarus clarkii, cf. Huner & Barr,
1991, and Paranephrops zealandicus, cf. Whitmore & Huryn, 1999), juveniles remain first
attached to their mother’s pleon using transient structures (Vogt & Tolley, 2004) and then
freely crawl onto her body. Weaning consists in the young definitively leaving their mother
and digging their first burrows at some distance from hers or, in Engaeus, in digging side
branches from the mother’s burrow (Suter, 1977).
During their association with the mother, juveniles often swim or walk a few centime-
ters or more away from the female on feeding forays, to return rapidly to the mother upon
any disturbance. In some species, the juveniles are facilitated in their return behavior by
a typical posture assumed by the mother, the “spoon-like telson” posture (Aquiloni &
Gherardi, 2008d). Species-specific pheromones, possibly combined with visual stimuli
(Aquiloni & Gherardi, 2008d), mediate the interaction between juveniles and maternal
females (Little, 1975, 1976). Third stage juveniles of at least five species were found to
avoid the water conditioned by males or non-berried females, but orient instead towards
water in which recently berried females had been held, irrespective of those being or not
their biological mother.
Agonistic behavior
From an evolutionary perspective, agonistic behavior may be regarded as a behavioral
tool that contributes to enhancing the survival and/or the reproductive effort of the
individuals that interact (Moore & Bergman, 2005). Agonistic interactions in crayfish were
first described by Bovbjerg (1953); in Orconectes virilis that author identified four types of
interactions: Avoidance – the subordinate animal retreats from a higher-ranked individual;
Threat – an approach with outspread chelae in strike position; Strike – a unilateral
aggression, in which the aggressor approaches with outspread chelae, which are thrust
suddenly at one another; and Fight – the most dramatic contact between two crayfish, the
locking chelae and using the walking legs for leverage. Subsequent studies detailed the
behavioral patterns, showing their relatively large number [19 in Orconectes virilis vs. 15
in Poecilia reticulata Peters, 1859; 17 in Parus major Linnaeus, 1758; and 18 in Cynomys
ludovicianus (Ord, 1815)] (cf. Rubenstein & Hazlett, 1974) and their complex organization
in well defined sequences of information flow (Gherardi & Pieraccini, 2004). A form of
submissive posture, with the body held flat against the substrate and the chelipeds held
forward with the fingers only slightly spread, was described for Procambarus clarkii
(cf. Huner & Barr, 1991). Males of Procambarus clarkii were even shown to engage in
a pseudocopulatory behavior, possibly to indicate their dominance relationship (Issa &
Edwards, 2006).
Primary resources, such as food, shelter, and mates, constitute the ultimate deter-
minants of aggression. Starvation for one week results in increased activity (and in more
frequent social contacts) in the crayfish Orconectes virilis (cf. Hazlett et al., 1975). Three
species of Orconectes tested in the laboratory with natural substrata providing shelter were
engaged in very few interactions (Capelli & Munjal, 1982) and a similar reduced aggres-
sion was recorded in Orconectes rusticus under natural conditions when shelters are abun-
dant (Martin & Moore, 2007). As discussed above, male crayfish also fight for the access
of a female (Gherardi et al., 2006).
Through these types of interactions, dominance hierarchies are typically established
in groups of crayfish composed of either conspecifics, e.g., Austropotamobius pallipes (cf.
Tricarico et al., 2005), Procambarus acutus acutus (cf. Gherardi & Daniels, 2003), and
Procambarus clarkii (cf. Copp, 1986), or heterospecifics, e.g., Austropotamobius pallipes
vs. Procambarus clarkii (cf. Gherardi & Cioni, 2004), and Procambarus acutus acutus
vs. Procambarus clarkii (cf. Gherardi & Daniels, 2004). A large number of studies has
invariably proven the superior competitive ability of invasive species over resident crayfish
[Söderbäck, 1995; Vorburger & Ribi, 1999; Usio et al., 2001; Nakata & Goshima, 2003;
but not in Astacopsis franklinii (Gray, 1845) vs. Cherax destructor in Tasmania, Elvey et
al., 1996].
In most instances, agonistic interactions between two crayfish progressively escalate

until one of the opponents withdraws. A typical escalation advances through several stages
of intensity, starting with threat displays, then ritualized aggression with restrained use of
the claws, and finally brief periods of unrestrained combat (Bruski & Dunham, 1987).
Dominance in crayfish depends on a multitude of factors, either intrinsic or extrinsic,
including body size (Bovbjerg, 1953; Edsman & Jonsson, 1996), size of the weapons
(chelae: Bovbjerg, 1953; Bywater et al., 2008; but see Wilson et al., 2007), sex (Ranta
& Linström, 1993), morphotype (Guiasu & Dunham, 1998), physical state (Ranta &
Linström, 1992), the use of some agonistic displays (Levenbach & Hazlett, 1996; Guiaşu
& Dunham, 1997, 1999), knowledge of resource value (Bergman & Moore, 2003), prior
ownership of resources (burrows: Edsman & Jonsson, 1996), prior residence (Peeke et al.,
1995), past social history (Daws et al., 2002), and observation of other crayfish fighting
(Zulandt et al., 2008). The proximate causation of dominance hierarchies may also include
changes in serotonin levels, which have been shown to produce heightened aggressive
states (Huber et al., 2001). If intrinsic causation is responsible for agonistic interactions, a
crayfish with a prior winning experience may function as a “successful” fighter and thereby
fights more readily in future agonistic interactions. In fact, recent wins and losses in a
series of fights alter the likelihood of winning subsequent interactions, despite an apparent
disparity in size between opponents that would otherwise serve as an accurate predictor of
the outcome (Daws et al., 2002). However, high levels of serotonin were found to be not
sufficient per se to determine and maintain a high dominance status: injecting solutions
of serotonin and octopamine, which contrary to serotonin lead to decreased aggression
in crayfish (Livingstone et al., 1980), into the hemolymph of subordinate and dominant
Procambarus clarkii, respectively, Tricarico & Gherardi (2007) recorded a change in
aggressiveness as expected, which, surprisingly, was not accompanied by a significant
change in their chelar force and in their hierarchical status.
The advantages of reaching a superior social status include the maintenance of a
greater distance from neighbors in natural conditions, thus allowing an exclusive use of
resources (Martin & Moore, 2007), the acquisition of shelters when these are limited, and
an increased access to available food and mates (Capelli & Hamilton, 1984; Herberholz
et al., 2007; but see Fero et al., 2007). Consequently, dominant crayfish are expected to
gain increased fitness with respect to their subordinates, due to the utilization of these
benefits. However, a constant use of agonistic interactions to establish and reinforce social
hierarchies might theoretically lead to great energetic costs and to the risk of injuries. In
practice, this is minimized by the appearance, over sequential encounters, of a “viscosity”
in the social system (“social inertia”; Guhl, 1968): the opponents are less prone to engage
in combats and the subordinates avoid to approach the dominants, so that hierarchies
require little overt aggression to be maintained.
Three possible mechanisms, not mutually exclusive, have been used to explain the
phenomenon of social inertia. First, it has been hypothesized that the changes observed in
the behavior of dominant and subordinate individuals are the result of “winner and loser
effects”, e.g., in juvenile Astacus astacus (cf. Goessmann et al., 2000) and in Procambarus
clarkii (cf. Daws et al., 2002). The second mechanism assumes that hierarchies are kept
stable through a form of “true” individual recognition, i.e., the ability to discriminate one
individual on the basis of one or more identifying cues and to associate this to experiences
of victories or defeats from preceding encounters with that particular individual. Except
for the dubious record in Cambarellus shufeldtii (Faxon, 1884) (cf. Lowe, 1956), this
apparently refined form of recognition has not yet been described in crayfish. However,
clues that might support its existence in crayfish come from the recent study of Seebacher
& Wilson (2007) in Cherax dispar Riek, 1951: when the chelae of the original winners
were disabled, the winners kept on winning against the same opponents; this effect
disappeared when previous winners encountered unfamiliar individuals. In the third
mechanism, opponents do not need to have met each other in advance but are able to
recognize their reciprocal aggressive status by means of the cues that are under the control
of their physiological condition. Evidence of status recognition is abundant in the crayfish
literature (Copp, 1986; Gherardi & Daniels, 2003). Indeed, the large majority of crayfish do
not form social groups (except Engaeus) and typically display a low degree of site fidelity
(Robinson et al., 2000), and therefore their probability of encountering the same individual
repeatedly in general is low. As a consequence, true individual recognition is apparently
useless in reducing the costs of extended fights. Conversely, status recognition may be
a cheap, efficient, and presumably reliable mechanism to assess an opponent’s fighting
ability also in the absence of other information, such as asymmetries in phenotypic traits.
The discussion is still open about the sensory modality used by crayfish to commu-
nicate their status. Most likely candidates are chemical signals released with the urine
through the nephropores at the base of the antennae (Zulandt Schneider et al., 1999; Zu-
landt Schneider & Moore, 2000; section Internal morphology). This is corroborated by the
facts that: (1) the presence of urine increases olfactory sampling through antennule flicking
during fights (Ameyaw-Akumfi & Hazlett, 1975), (2) the direction of gill currents can be
controlled by the animal (Bergman et al., 2005), (3) urine is released most often during so-
cial interactions (Breithaupt & Eger, 2002), (4) the winner releases urine more often than
the loser (Breithaupt & Eger, 2002), and (5) when crayfish are deprived of the ability to
detect odors by the obstruction of chemoreceptors or are prevented to release urine, ago-
nistic bouts increase in duration and intensity, and the predictability of the eventual winner
is altered (Zulandt Schneider et al., 2001; Bergman et al., 2003). However, attempts made
to isolate the putative “pheromone of status” have failed so far (The et al., 2004).
It appears that the long-term exposure of a naïve crayfish to olfactory cues from
conspecifics can alter its subsequent agonistic behavior: it will behave as a dominant
if exposed to odors from subordinates and as a subordinate if exposed to odors from
dominants (Bergman & Moore, 2005). This result pinpoints the complex interactions that
exist between the several extrinsic and intrinsic factors into play. Chemical detection may
feed back onto the nervous system, leading to an avalanche of changes in the nervous
system and in the neurochemistry of the receiving crayfish (references in Moore &
Bergman, 2005). In their turn, these intrinsic changes may be expressed extrinsically in
the quality of the urine-borne chemicals emitted by the transmitter crayfish – and in the
meaning that receiving crayfish give to them.
There is, however, robust evidence that crayfish also use visual cues to recognize their
social partners (possibly at the individual level). A recent study by Van der Velden et al.
(2008) showed that Cherax destructor is able to learn some “facial” features of an opponent
and to behave accordingly when offered a second time with this familiar individual; more
than one cue is needed to recognize an individual, and all of them should have a relatively
wide variability within the population, such as the facial width. The previous social history
of an individual is also influential: crayfish kept in isolation prior to the experiment were
unable to recognize familiar opponents.
In conclusion, it should be stressed that there are several aspects that make the
knowledge of crayfish behavior particularly important from an applied perspective. On
the one hand, it provides insights into how to manage threatened species and invasive
populations (Sutherland, 1998). For example, the control of invasive species by the use
of, e.g., the sterile male release technique should be preceded by a thorough knowledge
of their mating system and reproductive potential (Aquiloni et al., 2009). On the other
hand, information on crayfish behavior provides relevant suggestions for the aquaculture
industry of how to make farming more efficient on the side of human economy and
more “humane” on the side of animal ethics. For example, aggressive behavior in farmed
crayfish is problematic when it physically damages stock and reduces quality: an increase
in habitat complexity tends to reduce the number of agonistic interactions and the total
time spent fighting in Cherax destructor (cf. Baird et al., 2006). Finally, from a theoretical
perspective, the study of crayfish behavior opens avenues of research in some heatedly
debated fields of modern ethology, such as social behavior. The discovery of a complex
system of communication in this typically “non-social” taxon pinpoints a direction for
future research, that is expected to reveal further surprises.
PARASITES AND DISEASES

[J. D IÉGUEZ -U RIBEONDO]
Studies on pathogens and their associated diseases have surprisingly been more
numerous in crayfish than in any other invertebrate taxon. This might be the result of
the wide interest in the so-called “crayfish plague”, a disease that has wiped out many
populations of European crayfish since 1860. The urgent need for both identifying the
causative agent of this disease and preventing its spread has led to a proliferation of studies
(see reviews in Alderman & Polglase, 1988; Cerenius & Söderhäll, 1992; Edgerton et al.,
2002, 2004; Dieguez-Uribeondo et al., 2006). As a consequence, today the agent of the
crayfish plague, the oomycete Aphanomyces astaci, is amongst the best known pathogens
of invertebrates; similarly, knowledge of the crayfish immune system approaches that of
a privileged model organism in invertebrates, Drosophila melanogaster Meigen, 1830
(cf. Cerenius & Söderhäll, 2003). Investigations on crayfish parasites and diseases have
also provided important findings in the fields of evolution, phylogeny, and systematics.
For example, molecular studies on crayfish parasites, such as Psorospermium spp. and
Thelohania spp., have contributed to an understanding of the phylogenetic roots of fungi

and animals (Ragan et al., 1996; Lom et al., 2001).
Indeed, the “on risk of extinction” status of the indigenous crayfish species in Europe
and the increasing interest in crayfish farming in Australia and U.S.A. have made
pathology an emerging field of crayfish research. In fact, knowledge of diseases will help
us restoring threatened populations of crayfish on the one hand, and setting the basis for
successful farming on the other. However, little is known about the diseases caused by
abiotic factors, such as adverse environmental conditions, poor nutrition, or exposure to
water-borne toxicants (Evans & Edgerton, 2002).
This review will briefly focus on the most important parasites and commensals found
to infect or infest crayfish (summarized in table III).
Aphanomyces astaci (crayfish plague)

Aphanomyces astaci Schikora is a fungal-like organism and an obligate parasite
of crayfish (see reviews in Cerenius & Söderhäll, 1992; Söderhäll & Cerenius, 1999;
Diéguez-Uribeondo et al., 2006). It causes the “crayfish plague”, a disease that has
devastated the native European species of crayfish since the middle of the 19th century.
This species is endemic to North America and has been categorized as among the 100
“world’s worst” invaders by the Invasive Species Specialist Group (ISSG) of the World
Conservation Union (IUCN) (http://www.issg.org/).
The history of the spread of the crayfish plague in Europe has been described in detail
by Alderman (1996). Crayfish plague outbreaks are characterized by mass mortalities
of indigenous European crayfish, but appear not to affect other animals. It is suspected
that Aphanomyces astaci was introduced into Europe, and specifically into Italy, through
imports of the North American crayfish species Orconectes limosus. Many events of
plague outbreaks started after 1969 as a consequence of the introduction of other North
American crayfish species, i.e., the signal crayfish Pacifastacus leniusculus and the red-
swamp crayfish Procambarus clarkii (cf. Huang et al., 1994; Diéguez-Uribeondo et al.,
1997; Lilley et al., 1997; Oidtmann et al., 1997; Vennerström et al., 1997; Diéguez-
Uribeondo & Söderhäll, 1999). The parasite was introduced into South America, Asia,
and Africa together with Procambarus clarkii. The crayfish indigenous to Australia are
known to succumb to Aphanomyces but, fortunately, its crayfish carriers have not yet been
introduced into that continent.
The life cycle of Aphanomyces astaci is well known (see reviews in Cerenius &
Söderhäll, 1992; Söderhäll & Cerenius, 1999; Diéguez-Uribeondo et al., 2006). It forms
characteristic spore-balls (fig. 67.23B) that release swimming zoospores, the infective
units. The zoospore lands on the surface of the cuticle of a crayfish and germinates; in
the European and Australasian species, the parasite spreads rapidly through the cuticle,
which results in the crayfish’s death within 6-10 days (Unestam & Weiss, 1970; Unestam,
1972). In the North American species, however, the parasite elicits a rapid and strong
immune reaction upon penetration of the cuticle; as a consequence, melanin is deposited
on the hyphae (Unestam & Weiss, 1970) (fig. 67.23C). This reaction is the result of the
TABLE III
Most important pathogens causing diseases in crayfish
Pathogen Type of Disease Infection Described in

organism site crayfish species:
Aphanomyces astaci Oomycetes Crayfish plague Cuticle Astacus spp.
(fungal-like) Austropotamobius spp.
Orconectes virilis
Pacifastacus leniusculus
Procambarus clarkii
Saprolegnia parasitica Oomycetes Saprolegniasis Cuticle Astacus astacus
(fungal-like) Austropotamobius pallipes
Orconectes virilis
Procambarus clarkii
Saprolegnia dilina Oomycetes Saprolegniasis Eggs Austropotamobius pallipes
(fungal like) in eggs Pacifastacus leniusculus
Thelohania spp. Microsporidian Porcelain Possibly Astacus spp.
disease digestive Austropotamobius spp.
tract Cambarellus spp.
Cherax spp.
Orconectes virilis
Paranephrops spp.
Psorospermium spp. Mesomycetozoa Psorospermiasis Unknown Astacus spp.
Austropotamobius spp.
Cherax spp.
Orconectes spp.
Procambarus clarkii
Intranuclear bacilliform Virus – Gut Astacus astacus
viruses (IBVs) Austropotamobius pallipes
Cherax spp.
White spot Virus White spot – Astacus spp.

virus (WSSV) disease Austropotamobius spp.
Cherax spp.
Orconectes spp.
Procambarus clarkii
activation of part of the crayfish immune system, the prophenoloxidase activating system.
The melanization reaction in the cuticle represents the first line of defense against the
invading parasite (Söderhäll & Cerenius, 1992). In fact, melanin, which is produced by
the enzyme phenoloxidase, PO, has fungistatic effects and prevents the growth of micro-
organisms (Söderhäll & Ajaxon, 1982). The enzyme PO is constitutively expressed in
North American crayfish but it has to be induced in European species (Cerenius et al.,
2003). The higher resistance of the North American species appears to be the result of
Fig. 67.23. A, black melanized spot on the sub-pleonal cuticle of the North American freshwa-
ter crayfish, Pacifastacus leniusculus, as a consequence of Aphanomyces astaci infection (cray-
fish plague) [photo by J. Diéguez-Uribeondo]; B, micrograph of characteristic spore balls of
Aphanomyces astaci that will release the infective zoospores [photo by J. Diéguez-Uribeondo]; C,
micrograph of a melanized hyphe of Aphanomyces astaci growing in the cuticle of the North Ameri-
can carrier species of crayfish, Pacifastacus leniusculus [photo by J. Diéguez-Uribeondo]; D, porce-
lain disease, characterized by intense white color in the sub-pleonal muscles due to accumulation of
Thelohania contejeani spores [photo by I. Dyková]; E, Psorospermium haeckeli, typical sporocyst
isolated from Astacus astacus muscle tissue [photo by P. Henttonen]; F, white spot virus symptoms
in Pacifastacus leniusculus [photo by K. Söderhäll].
a form of coevolution of the parasite with its host (Unestam & Weiss, 1970; Unestam,
1972). Thus, the North American species Orconectes limosus, Pacifastacus leniusculus,
and Procambarus clarkii have been shown to carry this parasite in their cuticle (see review
in Diéguez-Uribeondo et al., 2006), and they can die when they are immune-compromised
(see reviews in Cerenius & Söderhäll, 1992; Söderhäll & Cerenius, 1999). The dense
deposits of melanin in the North American crayfish can be macroscopically seen as “black
spots” (fig. 67.23A), which are the most suitable areas when trying to isolate the parasite.
However, melanin reaction is not specific of the crayfish plague, and the presence of such
spots does not necessarily indicate an infection with Aphanomyces astaci.
Identification of Aphanomyces astaci and diagnosis of the crayfish plague are difficult
(Cerenius et al., 1988), due to Aphanomyces species being morphologically indistinguish-
able. Today, however, with the advent of molecular techniques, a PCR-specific test has
been developed to aid classical approaches (Oidtmann et al., 2006; Ballesteros et al., 2007;
Kozubíková et al., 2008). The use of RAPD-PCR has led to the identification of four dis-
tinct genotypes of Aphanomyces astaci (Huang et al., 1994; Diéguez-Uribeondo et al.,
1995).
Thanks to the many studies on the biology of Aphanomyces astaci, today we know
that: (1) crayfish are the only carriers of the disease and the parasite survives only a few
days outside its host; and (2) the spores of Aphanomyces astaci only survive for a limited
time and have no resting stages. As a consequence, if crayfish disappear, the crayfish
plague fungus disappears as well. North American crayfish, in their capacity of permanent
Aphanomyces astaci carriers and producers of vast numbers of plague spores, are the prime
vehicle of the parasite, but also humans, favoring the spread of crayfish, are efficient factors
of its dispersion. Thus, introductions of crayfish into the wild or for aquaculture purposes,
the trade of live crayfish, and their uncontrolled fishing are the typical situations that cause
a rapid and efficient dispersion of the pathogen.
Thelohania contejeani (porcelain disease)

The porcelain disease is caused by the microsporidian, Thelohania contejeani Hen-
neguy (see review in Diéguez-Uribeondo et al., 2006). It is a chronic disease, resulting
in the death of the affected animals and occasionally leading to mass mortalities both in
wild populations and in aquaculture. Crayfish may take one-two years to die from this
infection. The term “porcelain” arises from the intense whitish color of the sub-pleonal
cuticle, produced by the accumulation of Thelohania spores in muscles and in other or-
gans (fig. 67.23D). This stage can be macroscopically recognized but corresponds to an
advanced stage of the infection. Asymptomatic animals cannot be recognized by eye. This
disease has been reported in Europe (Astacus astacus, Austropotamobius pallipes), in Aus-
tralia (Cherax destructor), and in North America (Pacifastacus leniusculus). However, the
exact identity of these microsporidians from these different hosts has not yet been exam-
ined.
The biology and histopathology of this parasite have been described in detail (Lom et
al., 2001). Thelohania spores serve for the transmission of the parasite; the infection seems
to begin in the digestive tract. However, the mode of migration to the sites of proliferation
is still unknown. Crayfish get infected by eating infected animals. The spores are known to
be resistant and to survive for a prolonged time, even for months. However, transmission
trials using animals harboring the spores failed. Pleonal tissues or claw skeletal muscles
get parasitized more frequently; when muscle cells get heavily infected, the plasmalemma
breaks and the parasites spread in the body. Although there were reports of cellular
reactions in the form of capsules around the spores in the attacked muscles, no signs of
any effective defense reaction by the host have been ever described.
Since the prevalence of this parasite can be high in some populations (for example, in
Europe the prevalence of Thelohania contejeani varies from 0.1% to 30%) and the infected
animals will eventually die, there is an urgent need to develop rapid and efficient techniques
for its identification. This should help us prevent its spread in the wild, thus ensuring
Thelohania-free animals for aquaculture. Research on factors inducing the development of
porcelain disease and on control measures are also needed.
Psorospermium haeckeli
Psorospermium haeckeli (Hilgendorf) is one of the first parasites described in crayfish,
being exclusive to them. For years, this organism has been considered enigmatic for its
unresolved phylogenetic position. In 1996, Ragan et al. (1996) found that Psorospermium
belongs to the DRIPs clade (= Mesomycetozoa), close to the animal-fungal dichotomy.
There are no macroscopic signs of infection by Psorospermium, so that its pathogenicity
was initially put into question. Several studies, however, have shown that Psorospermium
haeckeli can activate the crayfish immune system (Cerenius et al., 1991; Thörnqvist &
Söderhäll, 1993). Its presence has been related to decreased catches of Astacus astacus
(cf. Söderhäll, 1988). It may induce an acute plague in Pacifastacus leniusculus (cf.
Diéguez-Uribeondo et al., 1993; Thörnqvist & Söderhäll, 1993) and produce mortality
during molting and in aquaculture conditions (Vey, 1979, 1986; Söderhäll, 1988).
Psorospermium has been found in Astacidae, Cambaridae, and Parastacidae. Six
different morphotypes of the genus Psorospermium have been described, one in Australia
(Herbert, 1987; Edgerton et al., 1995; Henttonen, 1996; Evans & Jussila, 1997), two in
Europe (Vogt & Rug, 1995), and three in North America (Henttonen et al., 1992, 1994;
Henttonen, 1996). Molecular studies on ribosomal ITS DNA of Psorospermium forms
from Europe and North America suggest a wide genetic diversity (Bangyeekhun et al.,
2001), these forms thus being different species with a diverse degree of pathogenicity and,
possibly, host specificity.
The main stage of Psorospermium described in the literature is the resting sporocyst
(fig. 67.23E). This has a three-layered shell with an interior receptacle with lipid globules
(Vogt, 1999a). In the host crayfish, the number of Psorospermium haeckeli sporocysts
is highest in the collagenous layer of the thoracic arteries and in the surrounding
subepidermal connective tissue (Herbert, 1987; Evans et al., 1988; Henttonen et al., 1992,
1994; Edgerton et al., 1995; Vogt & Rug, 1995). Vogt (1999a) described the life cycle of
Psorospermium haeckeli. Briefly, an amoeboid stage forms typical resting sporocysts in a
spore receptacle that eventually will be released giving rise to the amoeboids. However,
many questions remain to be answered. The infection mechanism of Psorospermium is
unknown. According to Vogt & Rug (1999), the infection takes place in the digestive tract,
but other authors have suggested that this occurs through the soft cuticle via penetration
of the amoeboid stages. Additionally, the intervention in Psorospermium’s life cycle of
intermediate hosts has been questioned and never tested (Vogt, 1999a).
Viral diseases
Research on crustacean viruses has recently gained increasing interest due to the pos-
sible role of crayfish as vectors of harmful viruses for wild populations and aquaculture
stocks of crustaceans and fishes. Viruses have been described in a number of decapods,
including shrimps and crabs (see reviews in Edgerton et al., 2002; Diéguez-Uribeondo et
al., 2006). The viruses described so far in crustaceans belong to or are related to a wide
variety of families, such as the Baculoviridae, Birnavirus, Bunyaviridae, Herpesviridae, Iri-
doviridae, Picornaviridae, Parvoviridae, Reoviridae, Rhabdoviridae, Togaviridae, Totiviri-
dae, and a new virus family, Nimaviridae (cf. Brock & Lightner, 1990; Adams & Bonami,
1991; Lightner, 1993; Vogt, 1996; Van Hulten et al., 2001; Yang et al., 2001; Edgerton et
al., 2002). The first natural viral infection of crayfish was reported by Anderson & Prior
(1922), and others have been described since then. These viruses belong to 6 main groups
(Edgerton et al., 2002; Evans & Edgerton, 2002; Edgerton, 2003): (1) Intranuclear Bacil-
liform Viruses (IBVs) and White Spot Syndrome Virus (WSSV); (2) Parvo-like viruses;
(3) Birnavirus (infectious pancreatic necrosis virus, IPNV); (4) Reo-like virus; (5) Toti-like
virus; and (6) Picorna-like virus.
Of these, IBVs are the most important viruses that infect crayfish, while only in
the laboratory was Astacus astacus shown to act as a vector for IPNV. The most
intensively investigated viruses are the WSSV, responsible for the white spot disease
that has caused serious economic losses in shrimp production worldwide, with mortality
rates even reaching 100% (Flegel, 1997). WSSV has a wide range of hosts and can
affect almost all species of shrimps, other crustaceans, and insects. Crayfish, e.g., species
of Procambarus, Orconectes punctimanus, Cherax destructor, Pacifastacus leniusculus,
Astacus astacus, and Austropotamobius pallipes, were recently reported to be susceptible
to WSSV (Jiravanichpaisal et al., 2001, 2004; Edgerton, 2004, 2005). More importantly,
crayfish seem to serve as reservoirs for WSSV and possibly for other crayfish-associated
viruses (fig. 67.23F). The possibility of cross infections of viruses from shrimps to crayfish
pinpoints the dangers of introducing an alien organism into a new ecosystem, which may
have extremely deleterious consequences.
Epibionts
Branchiobdellidans, or crayfish worms, are leech-like oligochaetes and obligate ec-

tosymbionts (Tannreuther, 1915), living primarily on Astacoidea (cf. Brinkhurst & Gelder,
2001). These worms are not considered to be harmful, but their presence might decrease
the market value of crayfish. Branchiobdellidans are best described as ectocommensals,
living on the exposed exoskeleton of the host and displaying an opportunistic, omnivorous
diet, e.g., diatoms, detritus, and small invertebrates. The gill chamber habitat appears to be
obligate for a small number of species, including Branchiobdella astaci Odier, 1823 and
Branchiobdella hexodonta Grube, 1888. Observations by Grabda & Wierzbicka (1969)
support, at least, a partial parasitic association of Branchiobdella hexodonta with its hosts,
as probably true for other, similar gill-dwelling species. Other studies have used the dam-
aged gills of hosts as evidence for branchiobdellidan parasitism, but damage may also
result from (secondary) bacterial or fungal infections.
Ectosymbiont populations range in number and complexity, from over 1800 branchiob-
dellidans of the same species on a single host (Vogt, 1999b) to about 100 specimens from
eight species of five genera in a single crayfish (S. R. Gelder, unpubl. obs.). Ecological
studies on various branchiobdellidan-host associations have provided basic information,
which shows variations based on climate, season, habitat, and other parameters.
Other parasites and diseases

Occasionally, less conspicuous diseases can be observed in crayfish. These can be
caused by a broad range of organisms, i.e., bacteria, fungi, or other fungal-like organ-
isms (see reviews in Edgerton et al., 2002; Diéguez-Uribeondo et al., 2006). Thus, some
chitinolytic bacteria and fungi have been related to the burn spot disease. A number
of bacteria (Gram negative, i.e., Acinetobacter, Aeromonas, Citrobacter, Flavobacterium,
Pseudomonas, and Vibrio, and Gram positive ones, i.e. Corynebacterium, Bacillus, Micro-
coccus, and Staphylococcus) can cause asymptomatic bacteraemia or bacterial septicaemia
to crayfish. Shell disease or burn spot disease is caused by chitinolytic Gram negative bac-
teria including Pseudomonas sp. and fungi such as Ramularia sp., Didimaria cambari, or
Fusarium spp. Metazoan parasites that can cause infections are mainly species of dige-
neans that have crayfish as a second, intermediate host. Most of these metazoan parasites
can cause diseases in crayfish, if they are present in high numbers or in vital organs. Finally,
two fungal-like organisms, Saprolegnia parasitica and Saprolegnia diclina (Oomycetes),
have been found infecting crayfish under stress conditions, or infecting crayfish eggs, re-
spectively.
Crayfish pathology has gained increasing interest due to crayfish aquaculture and
the risk of devastation of Australasian crayfish by the crayfish plague and other dis-
eases. Pathogens, especially oomycetes, viruses, and branchiobdellidans, mainly disperse
through the introduction of non-indigenous crayfish in the wild or for aquaculture pur-
poses, the trade of live crayfish, and their uncontrolled fishing. Knowledge on diseases
and their vectors will help us setting the basis for successful farming on the one hand, and
preventing the extinction of threatened populations of crayfish on the other.
CONSERVATION
[C. S OUTY-G ROSSET]
Preserving freshwater biodiversity means preserving many abiotic and biotic prop-
erties of the habitat, such as the physical structure of the catchment, flow regime, wa-
ter quality, and indigenous communities. The dependence of threatened organisms on the
good status of their habitat pinpoints the links between nature conservation on the one
hand, and human health and well being on the other. This is particularly true for crayfish,
large and long-lived invertebrates, which act as important predators and detritivores and are
prey for fishes and other organisms. They play a key role in the functioning of freshwater
ecosystems (section Ecology).
Since the 19th century, the distribution of crayfish has become restricted and
fragmented due to various factors, including human degradation of habitats and water
quality. Crayfish are highly threatened by dam construction, water pollution, erosion,
siltation, and in-stream gravel dredging, and, in particular, the introduction of non-
indigenous crayfish, the parasites they harbor and other non-native species (Gherardi,
2007). In turn, the recorded decline of indigenous crayfish populations has adverse
effects on the functioning of the ecosystems and largely affects provisioning, regulating,
supporting, and cultural services. The loss of indigenous species may have negative
impacts on their predators, such as salmonids and other fish taxa, otters, and water birds,
with cascading effects on their prey and on the aquatic plants. Foraging and grazing by
crayfish boost primary productivity and are important in nutrient and energy cycling. In
their absence, macrophytes may overgrow, leading to decreased oxygen content and thus
to degraded water quality. Otters (a flagship species) and salmonids (bioindicators) are also
influenced directly by the deterioration of water quality.
In Europe, thousands of populations of indigenous crayfish have been lost or have been
replaced by North American species (Gherardi & Holdich, 1999); a similar pattern is
going on in North America (Lodge et al., 2000). In part, replacement of indigenous by
non-indigenous species has been driven by competition between crayfish and differential
predation by fishes. Particularly in Europe, the crayfish plague, due to the oomycete
Aphanomyces astaci (section Parasites and diseases) has been responsible for the loss of
entire indigenous populations.
The many threats to indigenous crayfish differ for their relative importance among eco-
regions or countries, as shown in Europe (table IV). The conservation of European crayfish
implies knowledge of their current distribution (Souty-Grosset et al., 2006), recognition of
their ecological requirements, and maintenance of the best environmental quality for their
well being. However, to set conservation priorities, there is a need for the application of
molecular methods that might allow a thorough understanding of the genetic structure and
phylogeography of a species. The conservation and exploitation of some species of socio-
economic importance (for example, the noble crayfish Astacus astacus) are perceived
today as not being mutually exclusive, but controlled fishery is an essential tool for their
preservation (Taugbøl, 2004; section Economic value).
Conservation status in different countries

E UROPE
Today, most crayfish species have been categorized for their conservation status within
the Red Data List produced by IUCN (the International Union for the Conservation of
Nature and Natural Resources). In Europe, the three indigenous Astacidae, Astacus asta-
cus, Austropotamobius pallipes, and Austropotamobius torrentium, are listed as vulnera-
ble (IUCN, 2007). In response to the Convention on Biological Diversity (Rio de Janeiro,
368
TABLE IV
Importance of various threats to indigenous crayfish populations among different ecoregions or countries of Europe (0, none; 1, low; 2, medium; 3,
high; ?, no information). The listed species refer to those, for which the given information is most relevant (AUP = Austropotamobius pallipes;
AUT = Austropotamobius torrentium; ASA = Astacus astacus) [Information based on Schulz & Schulz, 2004 and Souty-Grosset et al., 2006]
Ecoregion: Alpine Atlantic Central Eastern Mediterranean Scandinavia
Threat France Britain Ireland Czechia Germany Poland Estonia/Latvia Italy Portugal
Crayfish plague 2/3 3 3 3 2 2 1 2 1 3 3
Other diseases ? ? 2 2 ? ? 1 ? ? ? ?
Non-indigenous species 2/3 3 3 3 3 3 3 3 3 3 3
Predators 1 1 2 1 2 2 2 2 1 2 1
Exploitation 1 1 1 0 1 1/2 1 3 2 2 1
Habitat alterations 2 2/3 2 1 2/3 3 2 2 2 1 1
Water level reductions 1 21 ) 2 2 1 1/2 2 2 1 3 1
F. GHERARDI ET AL.
Eutrophication 2 1 1 1 1 1/2 3 2 1 1 1/2

Acidification 1 1 1 0 2 1 1 1 1 1 1/2
Toxicants 2/3 3 2 2/3 2 ? 2/3 3 3 2 1
Land-use 2/3 3 2 2/3 2 3 2 3 2 3 2
Fragmentation 3 3 2 1 3 3 1 3 2 1 2
Species ASA, AUP, AUP AUP AUP AUP ASA, AUT ASA ASA ASA AUP AUP ASA
1 ) Relevant for the Mediterranean region of France.
1992), Austropotamobius pallipes was included in annexes II and V of the Directive for the
Conservation of Natural Habitats and Wild Flora and Fauna (92/43/EEC and 97/62/EU) as
a species requiring management plans; for this species, the designation of Special Areas
of Conservation (SAC) is foreseen by the European network Natura 2000.
Conservation of European crayfish also suffers from a confused taxonomy. In fact,
when a species, legally recognized as threatened, is shown to be a complex or is split
into sub-species or sibling species, the legal status of its protection becomes unclear. It
takes time and resources to get relevant legislation rewritten and passed, and the outcome
may be unpredictable. This is the case in the Austropotamobius pallipes species complex
(Fratini et al., 2005; Bertocchi et al., 2008). A different case regards the species used as
commodities, such as Astacus astacus. Ancient culinary traditions have led this species to
be overexploited in Scandinavia. To face this problem, non-indigenous crayfish species,
together with their load of parasites, have been introduced into the wild for commercial
purposes, thus worsening the already difficult situation. Additionally, land-use planning
led to both pollution and physical damage of the environment that indirectly exerted
negative impacts on crayfish populations. Only in 1998 was a national action plan for the
noble crayfish conservation put into force. Since August 2003, the Species Protection Act
prohibits all import, transportation, and the keeping of live non-indigenous crayfish; new
legislation for assessing protected areas for the noble crayfish is continuously improved by
the government.
Today, the Habitats Directive and the Water Framework Directive provide a basic
framework for nature conservation in European freshwater ecosystems. Development tar-
gets and evaluation of surface water quality in the Water Framework Directive are based
on biotic indicators of good water quality, such as crayfish. Crayfish are also regarded
as heritage or flagship species (Füreder & Reynolds, 2004; Gherardi et al., 2004). As a
consequence, their conservation demands knowledge of their current distribution, recog-
nition of the species’ requirements, and maintenance, as far as possible, of the pristine
environments. Recognition of the value of exploitable species, e.g., Astacus astacus, can
be expressed through controlled fishing, which provides an impetus for continued con-
servation (Edsman & Smietana, 2004), although poaching is still widespread. Traditional
fishing methods have evolved, and modern fisheries are now managed for sustainable ex-
ploitation of Astacus (cf. Skurdal & Taugbøl, 2002). In most areas with Astacus astacus,
there is a long-standing tradition of crayfish catching and eating so that the use of indige-
nous crayfish for recreation may help their protection and may prevent illegal stocking
with non-indigenous species. The knowledge and attitudes of local people thus are key
factors.
Various other management practices have been supported by private or public enter-
prises, including habitat restoration (Rogers et al., 2002), restocking, introductions to new
areas, hatcheries (Schulz et al., 2002), and exclusion zones for non-indigenous species,
such as the so-called “no-go areas” in Great Britain (Holdich, 2003).
AUSTRALIA
Australia is a hot spot of crayfish diversity (Parastacidae), but the majority of species
are listed as endangered. They often have restricted distributions, low mobility, and exact
habitat requirements, making them very vulnerable to disturbance of their habitats. For
example, the so-called giant lobster, Astacopsis gouldi, the world’s largest freshwater
invertebrate, endemic of northern Tasmania, is a flagship species with great potential
for ecotourism, if adequately protected. It is listed as vulnerable under the Environment
Protection and Biodiversity Conservation Act (1999) and the Tasmanian Threatened
Species Protection Act (1995). The Murray crayfish, Euastacus armatus (Von Martens,
1866), is the second largest crayfish in the world, reaching weights of 3 kg. The Murray
crayfish is classified as threatened in the Australian Capital Territory and South Australia,
and is listed as vulnerable by IUCN (2004), also being considered as functionally extinct.
Another example is Engaeus granulatus Horwitz, 1990, a small crayfish with a <10 cm
average body length. The species only occurs in seven isolated areas of north central
Tasmania, where it occupies seeps, wetlands, and stream banks (Doran, 2000; Nelson,
2003). It is listed as endangered under the Tasmanian Threatened Species Protection Act
(1995).
N ORTH A MERICA
North America has the richest diversity of Cambaridae and Astacidae in the world
(section Phylogeny). The majority of crayfish species lives in the east of the Rocky
Mountains and in the southeastern states. Many live in streams, rivers, and lakes, while
others are restricted to springs, swamps, and underground waters (cave crayfish). About 65
species of crayfish are endangered, threatened, or listed as species of special conservation
concern, and 48% of indigenous crayfish species are in need of protection. These numbers
are best estimates only: the exact status of crayfish endangerment or extinction rates in
the United States is largely unknown, because very few population surveys have been
completed.
A FRICA
In Madagascar, the four endemic Parastacidae species are harvested by local people
for subsistence use and small-scale trade (Jones et al., 2006). Astacoides granulimanus
Monod & Petit, 1929 provides the majority of the catches. Community-based conservation
(through transfer of harvesting rights and responsibilities for forest management to
local communities) is central to a new conservation paradigm in Madagascar. This
recognizes the communities’ long term interest in their natural resources and offers an ideal
opportunity for those concerned with the sustainability of crayfish harvest to implement
management tools (such as size limits and no-take zones).
A SIA
In Japan, the only native crayfish, Cambaroides japonicus, has been declining dramat-
ically in the past few decades (Usio, 2007). Fishless streams associated with boulder sub-
strates in deciduous forest are important conservation areas for this species. Such habitats
may be limited in the headwater areas of pristine deciduous forests, which are disappear-
ing at an accelerating rate following deforestation. Major problems in conserving Cam-
baroides japonicus come from the lack of laws protecting it and its trade as an aquarium
pet.
Methods and policies

Several methods are available to assess conservation priorities. Along with the tradi-
tional method of quantifying species richness, generic richness, and critical species, newer
methods of phylogenetic and genetic diversity have been applied. For example, the “In-
terim Biogeographic Regionalisation Plans for Australia” (IBRA) assessed areas for con-
servation from the richness of freshwater crayfish species and their phylogenetic and ge-
netic diversity (Thackway & Cresswell, 1995). The two methods agreed to a large extent in
their ranking of areas, showing that the northwest coast of Tasmania and the southeastern
portion of the continent were of the highest priority for conserving the greatest amount of
diversity.
Ecosystem services have become an important issue in biodiversity policy. Recognizing
and highlighting the links between biodiversity and ecosystem services will contribute in
convincing stakeholders to reduce unacceptable losses in ecosystem services (Kettunen
& Ten Brink, 2006). Few are the examples that pinpoint the multiple values of biodiversity
and ecosystem services and scarce are the documented cases where biodiversity loss has
led to a demonstrated loss/degradation of ecosystem services. Among the case studies
reported, crayfish appear to be one of the most imperiled taxonomic groups in fresh waters
with over 30% of the species being threatened or endangered. The ecosystem services
affected by the decline of native crayfish populations include provisioning services (food
provision through declines in fisheries and rearing, and loss of traditional recreational
fishing); regulating and supporting services (water purification, nutrient cycling, and
primary productivity); and cultural services (recreation, ecotourism, and education).
Consequently, with no envisaged long-term benefits of such losses, and with various
ecological and socio-economic benefits that may be gained by the protection of these
indigenous species, the preservation of crayfish is of crucial importance.
Legislation is essential for effective conservation; indeed, it is in place in most countries
to protect indigenous crayfish (Vigneux et al., 2002; Edsman & Smietana, 2004), but
in many cases it has not been fully successful in preventing the further destruction of
populations. The efficacy of legislation is in fact often questioned (Holdich & Pöckl, 2005)
and different controls between countries will particularly affect species in trans-national
catchments. The way in which existing legislation is applied may also vary, and difficulties
can arise as a result of the different interpretations of what an indigenous crayfish species
is (Sibley, 2004).
Unsustainable land use practices and development decisions have resulted in unforesee-
able detrimental effects on the environment. Consequently, the ability of indigenous cray-
fish to recover has diminished and their populations continue to decline. The worst-case
scenario predicts that in the future almost all watersheds suitable for crayfish will become
inhabited by non-indigenous crayfish species, at least in Europe. Education of citizens
might be one of the most effective means for preserving species and habitats (Reynolds
& Puky, 2005), particularly in the case of decapod crustaceans, one of the most threat-
ened taxa, as evidenced by the high proportion of vulnerable or endangered species listed
(IUCN, 2007).
ECONOMIC IMPORTANCE
[F. G HERARDI]
The various uses that man has always made of crayfish are well documented since
ancient times. In Europe, their long-lasting importance to humans is reflected in the
several sayings, toponyms, family names, mythology, superstitions, fables, and tales in
which crayfish appear (Skurdal & Taugbøl, 2002). Crayfish were the subjects of paintings,
e.g., appearing in Italian Renaissance frescoes featuring the Last Supper (fig. 67.24;
see color insert), sculptures, and novels. Some of their parts, particularly their “stones”
(gastroliths), were even used in popular medicine (Swahn, 2004); in astrology, particularly
in the Renaissance, crayfish often symbolize the sign of Cancer. The high value as food
of some species, particularly of the noble crayfish Astacus astacus, is known since the
Middle Ages. In Central Europe, the tradition to eat the noble crayfish started at least
as early as the 1200s; there are reports of the consumption of enormous quantities of
crayfish: for instance, at the wedding of the Polish Princess Jadviga and Prince Jerzy in
1392, 75 000 crayfish were eaten in 8 days (Kulesh et al., 1999). In Scandinavia, crayfish
were regarded as injurious and poisonous until the 1500s; the interest in crayfish started
with the Wasa kings who sponsored the introduction of Astacus astacus from Germany
into Swedish lakes (Skurdal & Taugbøl, 2002). Notwithstanding the negative publicity
given by Carl von Linné, who regarded crayfish as insects and thus unsuitable to eat
(“Diaeta Naturalis”, 1733), the interest in crayfish as food increased across Sweden and
was transferred from the aristocracy to the middle and lower classes: today, crayfish
parties in Sweden are world famous and crayfish are regarded as culinary icons. In the
19th century, the demand for crayfish increased in Europe and their commercial harvesting
became an industry, particularly in Germany and Russia (Ackefors & Lindqvist, 1994).
Between 1853 and 1879, more than 5 million crayfish were yearly consumed in Paris
alone (Skurdal & Taugbøl, 2002).
The increased economic interest for crayfish inevitably led to their overharvesting
and to poaching that, along with the spread, since 1860, of the crayfish plague (section
Parasites and diseases), caused a rapid decrease of the available stocks. To cope with
the large demand of crayfish, their supply was first shifted to Astacus astacus imported
from the Baltic, Russia, and Finland (Skurdal & Taugbøl, 2002), then to non-indigenous
species introduced from outside Europe. The first species used to replace noble crayfish
in the European market was the narrow-clawed crayfish Astacus leptodactylus, harvested
in Turkey and largely exported to Western Europe until 1986 (5000 tonnes in 1984); this
crayfish, however, was highly susceptible to the plague. Safer in this respect appeared
to be the plague-resistant crayfish species from North-America, i.e., the signal crayfish
Pacifastacus leniusculus introduced in the 1960s to northern Europe (Taugbøl & Johnsen,
2006) and the red swamp crayfish Procambarus clarkii introduced in the 1970s to southern
Europe (Gherardi, 2006). The unwanted consequence of these introductions was that
these species, along with producing negative impacts on indigenous species, communities,
and ecosystems, were themselves vectors of Aphanomyces astaci (section Parasites and
diseases), thus making the situation for the remaining extant indigenous stocks even worse.
This is well illustrated by the story of the introduction of signal crayfish to Europe
(Taugbøl & Johnsen, 2006). In 1960, a small batch of signal crayfish was introduced
from California to Sweden. Trials were successful and in 1967-1969 a large number of
signal crayfish was imported from the U.S.A. and introduced into Swedish and Finnish
waters. Further introductions, especially of juveniles from Sweden, were made into many
European countries. The signal crayfish is well established in Sweden at present, where
it occurs in approximately 3000 localities. In addition, and at least until 2006, it has been
recorded in 25 European countries. A similar story could be told for Procambarus clarkii
(cf. Gherardi, 2006).
A commercial consequence of these introductions (for the ecological consequences,
see section Ecology) was that, of the total annual catch of crayfish in Europe (about
4200 tonnes in 1994) and of the total yield from aquaculture (about 160 tonnes in 1994)
(Ackefors, 1999), Astacus astacus comprises only about 290 tonnes (2-3%) of the total
catch, and 27% of the total production, whereas the most abundantly harvested and farmed
crayfish is Procambarus clarkii (fig. 67.25). However, notwithstanding its relatively low
Fig. 67.25. Production of crayfish per species in Europe (data from Ackefors, 1999).
yield, the noble crayfish constitutes 10-20% of the value of the total crayfish harvest. In
Scandinavia, for example, consumers are willing to pay higher prices for the indigenous
rather than for non-indigenous species (Holdich, 1999): the cost of fresh Astacus astacus
(paid to the farmer: US$ 40 kg−1 ) doubles the cost of fresh Pacifastacus leniusculus (paid
to the farmer: US$ 20 kg−1 ) and can be even 40 times higher that the cost of imported
frozen red swamp crayfish (paid to the U.S.A. farmer: US$ 1-3 kg−1 ).
In some countries, the aims of offering economic benefits to local people and of
diversifying agriculture by introducing non-indigenous species resulted in a miserable
“flop”. Despite the original aim of crayfish farmers in Britain to produce signal crayfish
for export to the Scandinavian market, most of the exports are now being made with
crayfish harvested from natural waters (Holdich, 1999). In Italy, the red swamp crayfish
has been exploited in the Massaciuccoli Lake (Tuscany) since the 1990s, but this industry
has met with very little success due to the low demand for crayfish from the Italian market
(Barbaresi & Gherardi, 2000). Similarly, in Africa, very few of the several projects that
led to crayfish importations since the 1960s are to be regarded as successful: today less
than 40 metric tonnes of Procambarus clarkii are fished annually, exclusively for local
consumption (mainly tourism) (Smart et al., 2002).
A different story is to be told for North America. There is not much information about
the original consumption of crayfish as food, but the most consumed crayfish of the
world today, the red swamp crayfish Procambarus clarkii, figured in the lore of both the
Attakapa and Houma tribes in southern Louisiana; the Houma used crayfish as their tribal
symbols (Huner, 2002). There is mention of crayfish exploitation by European immigrants
to Louisiana as early as the 1700s, and written records of commercial exploitation are
available from the late 1800s (Huner, 2002).
In Louisiana, the catch of the red swamp crayfish improved in the 1960s, reaching
landings of over 30 000 tonnes in favorable years (Huner, 2002). Commercial crayfish
farming developed in the 1950s: by the late 1960s about 4800 ha was in cultivation, by
1980 some 22 000 ha, and by 1986 more than 50 000 ha, with an average annual harvest
of 30 000-40 000 tonnes (Huner, 2002). Cultivation of Procambarus clarkii is practiced
in most states in the southern U.S.A., but at levels generally less than 700 metric tonnes
on 1000 ha in any particular state. In 1999, the U.S.A. produced about 50 000 tonnes of
crayfish, primarily in Louisiana, of which 30 000-35 000 tonnes came from aquaculture.
These figures were kept stable until the 2005 hurricanes that caused a crisis in the crayfish
industry. Threats to the North American crayfish industry are coming today from the
competition in the market, primarily by the People’s Republic of China, into which
Procambarus clarkii was introduced in the 1930s; in 2002, Chinese crayfish production
exceeded that of the U.S.A. with at least 70 000 tonnes per year, harvested for export as
peeled tail meat (Huner, 2002). A second potential competitor is Spain, now producing
3000-5000 tonnes of crayfish per year: Procambarus clarkii from Spain has appeared in
the U.S. market since 2000.
The above stories from Europe and North America underpin some interesting points of
discussion about the economic importance of crayfish, as follows.
(1) A very small fraction of species dominates the market: Procambarus clarkii (and
to a less extent Procambarus zonangulus Hobbs & Hobbs, 1990), Pacifastacus leniusculus,
Astacus leptodactylus, and Astacus astacus. To these, four species of the Australian
genus Cherax are to be added: Cherax albidus and Cherax destructor (the yabby, from
central Australia), Cherax quadricarinatus (redclaw, from northern Australia), and Cherax
tenuimanus (marron, from south-western Australia); all of these are farmed commercially
both in Australia and overseas (Lawrence & Jones, 2002). There are other species with
some potential of entering the market, such as the North American Cambarus robustus (cf.
Guiaşu, 2002), Orconectes limosus, Orconectes rusticus, and Orconectes virilis (cf. Hamr,
2002).
(2) The scientific interest in some species reflects their economic value. Of the 2537
articles focused on crayfish and published in peer-reviewed journals since 1990 (see
Introduction), about one third (32%) were focused on the two most important species
in commerce, Procambarus clarkii and Pacifastacus leniusculus (whereas the number of
crayfish species described up to now in the world amounts to over 600; Crandall & Buhay,
2008).
(3) The main economic value of crayfish is typically associated with production, but
little is known about their current consumptive use, i.e., their use as a subsistence diet at
a local scale. A study on the exploitation of four species of Astacoides by local people in
Madagascar showed that more than 50% of the 47 households in a village were directly
involved in crayfish harvest, which contributed US$ 2382 to the local economy in 2003-
2004, an important sum in the context of local incomes; subsistence use was widespread,
particularly by children to whom crayfish may be an important protein source (Jones et al.,
2006).
(4) The economic interest in crayfish has inevitably led to overharvesting many
species. This contributes to the constant decline recorded over the latest decades in the
populations of many crayfish species all over the world. To circumvent this problem,
wise management criteria should be applied. The cornerstone of fish management for
years has been the concept of maximum sustained yield (MSY): theoretically, it is the
largest yield/catch that can be taken from a species’ stock over an indefinite period to
ensure that populations continue through time, while still allowing a sustainable harvest.
However, MSY application requires a considerable amount of knowledge about biology,
ecology, and demography of each single population, but these data most often are difficult
to obtain. Harvest legislations are in force in many countries today. Most of these pose
restrictions to catch on the basis of size, sex, total harvest, fishing season, capture method,
and effort. In Europe and North America, legislation varies between countries and even
within countries. For example, the minimum size restriction for Pacifastacus leniusculus
is 92 mm total length in Oregon and California, 100 mm in Sweden, and 120 mm in France.
However, some of these restrictions may have more to do with what is more appropriate
for human consumption than for the biology of the species. Similarly, the regulation of
crayfish stocking, import, and cultivation varies considerably between countries.
(5) A sustainable aquaculture is regarded to be the best solution to meet market de-
mand without affecting wild stocks. Although farming methods have been well developed,
at least for the red swamp crayfish (Huner, 2002), the aquaculture production of species
that are more exigent (in terms of water conditions and food requirements) and more sus-
ceptible to diseases is still insufficient. Today, Astacus astacus is farmed in 13 European
countries (Westman et al., 1990) but these practices are developed at a very small scale,
with generally simple technologies (Skurdal & Taugbøl, 2002). To improve crayfish pro-
duction, more knowledge is needed in fields such as feeding and nutritional requirements,
water quality, diseases, behavior, etc.
(6) The introduction of non-indigenous species has certainly provided economic
benefits to several countries: it helped to restore the productivity of indigenous stocks,
e.g., in Sweden; compensate for their lack, e.g., in Spain; or develop extensive or semi-
intensive cultivation systems, e.g., in the People’s Republic of China (Ackefors, 1999).
However, once introduced for stocking and aquaculture and kept in outdoor ponds, crayfish
of several species are able to escape into the wild, where they can establish self-sustaining
populations and spread (Gherardi, 2007). Their invasiveness can be quantified by the
induced decrease in biomass and species richness of macroinvertebrates, macrophytes,
and periphyton and by their contribution to the decline of invertebrate taxa, including
indigenous crayfish species, and of amphibians and fish as well (Gherardi, 2007). Today,
the list of species that are causing concern in the introduced areas includes Pacifastacus
leniusculus in California (U.S.A.), Europe, and Japan, Orconectes limosus in Europe,
Orconectes rusticus in North America, Procambarus clarkii in Africa, California, Europe,
and Japan, Astacus leptodactylus in some European countries, and Cherax destructor in
Africa and Australia (Gherardi, 2007). Other species, such as Cherax quadricarinatus in
Ecuador, are expected to lead to problems in the near future (Gherardi, 2007).
Invasive crayfish may also inflict direct costs to the society. Procambarus clarkii is
a recognized pest in rice cultures in Portugal (in 2004, the recorded decrease of 6% in
profits in the “Baixo Mondego” area was exclusively due to crayfish: Anastácio et al.,
2005). The extensive burrowing by several crayfish is a problem in agricultural fields
and in other areas, e.g., lawns, golf courses, levees, dams, dykes, and in rivers and lakes
(e.g., Anastácio & Marques, 1997). In Africa, Procambarus clarkii was reported to spoil
valuable fish (tilapia and largemouth bass) caught in gill nets (up to 30% of the catch) and
to damage fish nets (De Moor, 2002). Costs of control and remediation may be elevated,
amounting to US$ 4.5 million for the reintroduction of Pacifastacus fortis (led to local
extinction by the introduced Procambarus clarkii) in California, and GB£ 100 000 for
the attempt to eradicate Pacifastacus leniusculus from Scotland (Gherardi, 2007). Finally,
non-indigenous crayfish may inflict other societal costs due to the potential harm they
pose to human health. Procambarus clarkii often lives in areas contaminated by sewage
and toxic industrial residues, and may have relatively high heavy metal concentrations in
its tissues (Geiger et al., 2005). It also consumes cyanobacteria that may produce lethal
animal and human intoxications (Carmichael, 1988). Its potential to transfer contaminants
to their consumers, including man, thus is high.
(7) Crayfish may provide economic values to humans other than being a gourmet
food. They may control some pests or diseases. Stocking of Cambarus bartonii bartonii
and Cambarus robustus may be a strategy for the management of nuisance macrophytes
in Ontario lakes (Guiaşu, 2002); these species even have the potential to feed on and
control nuisance populations of the zebra mussel and the clam Corbicula Megerle von
Mühlfeld, 1811 (cf. Covich et al., 1981; Hazlett, 1994); because of its feeding on the
pulmonate snails Biomphalaria Preston, 1910 and Bulinus Müller, 1781 known to host
Schistosoma mansoni and Schistosoma haematobium, the introduction of Procambarus
clarkii is expected to control the spread of human schistosomiasis in Africa (Mkoji et al.,
1999). Crayfish may be also used as a blueprint for the synthesis of medicines or of other
substances useful to human activities; research is moving to disclose the possible values
in them. For instance, the neurons of the stretch receptor organs (MROs) of the pleon are
used to explore the mechanisms of photodynamic therapy (section Internal morphology):
this technique elicits death of cells under light exposure via dye-mediated oxygen stress,
and is successfully used for treatment of cancer (Fedorenko & Uzdensky, 2008). Another
topic of applied interest is the mirror optics of the compound eye of crayfish: this optical
principle has evoked ideas for the construction of a new type of X-ray telescope and a
collimator to produce a parallel beam from an X-ray source, which might be useful in
forming ultrafine microcircuits on a chip (Land, 2000). The crayfish’s key role in food
webs (section Ecology) justifies their enormous ecological value, both as prerequisites
for the proper functioning of ecosystems and because of the multiple services they offer
to man. The multitude of studies focusing on crayfish (see Introduction) reflects their
scientific value and the various textbooks (e.g., Huxley, 1880) in which they are used to
explain the anatomy and physiology of crustaceans (and arthropods in general) denote their
educational value. Finally, the crayfish’s value as amenities is explicit in the large number
of “fans” across the world, including people that keep crayfish as household pets, e.g., in
Japan. They serve for human recreation also in an indirect way, being the primary food
of important sport fishes, such as smallmouth and largemouth bass in North America, or
being sold as fish baits (Guiaşu, 2002).
(8) There is another, less obvious economic value of crayfish, which is independent of
the goods and services they either directly or indirectly provide to humans. It is their in-
trinsic value that comes from simply knowing that they exist, i.e., existence value, or that
they may be left behind for the next generation, i.e., legacy value. As such, intrinsic value
is difficult to measure and never assessed in crayfish, but it may provide per se the rationale
for protecting this taxon without the need of conjuring up images of cooked crayfish.
PHYLOGENY AND BIOGEOGRAPHY

[K. A. C RANDALL]
There are over 600 described species of crayfish worldwide (fig. 67.26; table V)
(Crandall & Buhay, 2008). Taxonomically, they are organized into two superfamilies, the
Northern Hemisphere Astacoidea and the Southern Hemisphere Parastacoidea. Astacoidea
contain three families: the extant Cambaridae (with by far the most species diversity,
containing over 420 species within 12 genera), and Astacidae with three genera and 17
species and subspecies (Hobbs, 1989); and the fossil Cricoidoscelosidae containing a
378
F. GHERARDI ET AL.
Fig. 67.26. Geographic distribution of the global diversity of crayfish. The Northern Hemisphere center of diversity is in the southeastern United States,
whereas the Southern Hemisphere center of diversity is in southern Victoria, Australia.
TABLE V
Summary of critical species that contributed to the basic phylogenetic framework of Astacidea. With
total number of described crayfish species by taxon, where † indicates a genus that contains fossil
taxa and †† indicates a genus that is known exclusively from fossils
Family Genus Species

A STACIDAE Latreille, 1802 Astacus Fabricius, 1775 3
17 species Austropotamobius Skorikov, 1808 6
Pacifastacus Bott, 1950 8
C AMBARIDAE Hobbs, 1942 Barbicambarus Hobbs, 1969 1
424 species Bouchardina Hobbs, 1969 1
Cambarellus Ortmann, 1905 17
Cambaroides Pallas, 1972 7
Cambarus Erickson, 1846 95
Distocambarus Hobbs, 1981 5
Fallicambarus Hobbs, 1969 18
Faxonella Creaser, 1933 4
Hobbseus Fitzpatrick & Payne, 1968 7
Orconectes Cope, 1972 89
Palaeocambarus Taylor, Schram & Shen, 1999 †† 1
Procambarus Ortmann, 1905 † 177
Troglocambarus Hobbs, 1942 2
C RICOIDOSCELOSIDAE Cricoidoscelosus Taylor, Schram & Shen, 1999 †† 1
Taylor, Schram & Shen, 1999
1 species
PARASTACIDAE Huxley, 1879 Astacoides Guérin-Méneville, 1839 9
178 species Astacopsis Huxley, 1879 † 3
Cherax Erichson, 1846 45
Engaeus Erichson, 1846 39
Engaewa Riek, 1967 5
Euastacus Clark, 1939 43
Geocharax Clark, 1936 2
Gramastacus Riek, 1972 1
Lammuastacus Aguirre-Urreta, 1992 †† 1
Ombrastacoides Hansen & Richardson, 2006 11
Palaeoechinastacus Martin et al., 2008 †† 1
Paranephrops White, 1842 † 2
Parastacus Huxley, 1879 8
Samastacus Riek, 1971 1
Spinastacoides Hansen & Richardson, 2006 3
Tenuibranchiurus Riek, 1951 1
Virilastacus Hobbs, 1991 3
Total 620
single species (Taylor et al., 1999; Shen et al., 2001). Parastacoidea are composed of a
single family, Parastacidae, consisting of 15 extant genera and two fossil genera, totaling
over 170 species.
Present distribution and areas of endemicity

The most species-rich family of crayfish, Cambaridae, is distributed in North America
east of the Rocky Mountains, north into southern Canada, and south through Mexico
and, surprisingly, in Asia. The Asian endemic genus Cambaroides is a bit of an enigma
biogeographically, morphologically, and phylogenetically (see below), although Schram
(2001: 15, fig. 14) did offer a paleobiogeographic viewpoint that could serve to mitigate
the enigma. Some phylogenetic analyses place it weakly with the European species (which
makes more biogeographic sense), but a good sampling of Cambaroides to place into a
robust phylogenetic analysis has yet to occur. Astacidae are distributed west of the Rocky
Mountains (mainly in the Pacific Northwest) and in Europe (fig. 67.26). In Parastacoidea,
11 of the 17 genera are found in Australia. The remaining genera are distributed in southern
South America (three extant genera and one fossil genus with 13 species distributed in
southern Chile, Uruguay, and southern Brazil), New Zealand (with one endemic genus
and two described species), and Madagascar (with one endemic genus and nine described
species).
The greatest species diversity in crayfish occurs in the southern Appalachian Mountains
of the southeastern United States. This region is also home to a number of other highly
endemic and highly endangered freshwater species, including fishes, salamanders, snails,
and mussels. Based on phylogenetic results and biogeographic analyses, much of the
species diversity in Cambaridae is of relatively recent origin (compared to Parastacidae)
(Crandall et al., 2000a) and seems to have been driven by isolating effects of pre- and
post-Pleistocene river drainage changes (Crandall & Templeton, 1999). Population genetic
studies of species groups are beginning to unravel the evolutionary mechanisms associated
with driving this amazing diversity (Fetzner & Crandall, 2003; Buhay & Crandall, 2005;
Finlay et al., 2006; Apte et al., 2007; Schultz et al., 2008). Such studies support the notion
of much cryptic diversity within many of the species groups (Buhay et al., 2007; Schultz
et al., 2007; Mathews et al., 2008; Crandall et al., 2009).
The Southern Hemisphere crayfish have a center of diversity in southeast Australia.
These taxa (at least the genus-level divisions) appear to be much older in origin relative
to the Northern Hemisphere taxa. These genera appear to form well-defined monophyletic
groups (Crandall et al., 2000b) as a result. The species richness of many of these genera
appears to be the result of vicariance and dispersal with isolation events (Ponniah &
Hughes, 2004).
Phylogeny and historical processes

Crayfish are a monophyletic group and a sister taxon to the clawed lobsters from
the superfamily Nephropoidea (cf. Crandall et al., 2000a), and together Nephropoidea,
Astacoidea, and Parastacoidea make up the infraorder Astacidea Latreille, 1802 within
the suborder Macrura Reptantia Bouvier, 1917 (fig. 67.27). While there has been some
debate about the sister taxon to crayfish [Thalassinidea (suggested by Scholtz & Richter,
1995) versus other members of Astacidea], most recent treatments (both molecular and
Fig. 67.27. Phylogenetic relationships among the global crayfish showing the strongly supported
division between the two superfamilies of the Northern Hemisphere (Astacoidea) and the Southern
Hemisphere (Parastacoidea). The phylogeny also clearly supports the crayfish as a monophyletic
group, sister to the clawed lobsters (Homarus, Nephrops, Nephropsis). The phylogeny was estimated
using a Bayesian approach with a model of evolution determined using ModelTest. The phylogeny
was estimated from a combined data set of 28S, 18S, H3 (nuclear), and 16S, 12S (mtDNA) data.
Support values at the nodes represent results from bootstrap (top value, based on 1000 replications)
and posterior probabilities (bottom values, ×100).
morphological) clearly support the clawed lobsters as sister to crayfish with the spiny
lobsters as the next closest group, all distinct from thalassinideans (Crandall et al., 2000a;
Rode & Babcock, 2003; Porter et al., 2005; Tsang et al., 2008; fig. 67.27). Note also
that Astacidae and Parastacidae appear to form well-supported monophyletic groups, but
the Cambaridae is problematic due to the placement of the genus Cambaroides outside
the main family clade. However, using a maximum likelihood approach (not shown),
Cambaroides falls basal to the remaining clade of Cambaridae, which would result in a
monophyletic Cambaridae as well. Note the weak bootstrap support for the placement
of the genus Cambaroides relative to the rest of Cambaridae and Astacidae. This particular
evolutionary question will take more samples (of Cambaroides in particular) to achieve the
desired resolution. Similar ambiguity resulted from a morphological analysis that showed
Cambaroides falling basal to both the Cambaridae and Astacidae (cf. Braband et al., 2006).
While much work has been done in terms of testing the monophyly and sister group
relationships among the crayfish and their allies, relatively little work has been published
on the phylogenetic relationships among the genera of crayfish. We have extensively
sampled the Northern and Southern Hemisphere genera of crayfish and the Southern
Hemisphere crayfish form reasonably distinct monophyletic groups (Crandall et al.,
2000a). Parastacidae form three distinct clades with one containing genera from Tasmania
(Spinastacoides, Ombrastacoides, Astacopsis Huxley, 1879), south and eastern Australia
(Euastacus), and New Zealand (Paranephrops) (fig. 67.27). The next clade contains genera
from South America (Parastacus, Samastacus, Virilastacus) and Madagascar (Astacoides).
The third clade contains the remaining genera from Australia, including the Western
Australia endemic genus Engaewa. A more extensive treatment of the phylogenetic
relationships among the Southern Hemisphere crayfish is currently being developed by
the Crandall laboratory.
To a large extent, the lack of a solid genus level phylogeny for crayfish is reflective of
the fact that initial studies have shown that many of the genera (especially in Cambaridae)
do not form monophyletic groups, thereby requiring relatively complete taxonomic
sampling to perform reasonable phylogenetic analyses (Sinclair et al., 2004). This is a
difficult task, given the large number of species of crayfish – especially in the Northern
Hemisphere. Nevertheless, the Crandall laboratory in Utah has been actively attempting
to articulate the phylogenetic relationships among all crayfish – with a current focus
on obtaining samples from the species-rich Cambaridae. Our current results show the
difficulty of this task and the lack of monophyly of many (most) of the genera; none of
the species-rich genera of Cambarus, Orconectes, and Procambarus form monophyletic
groups. Ironically, the cave Orconectes (the type for the genus) falls well embedded within
the Cambarus clade; whereas, a clade of cave Cambarus (Cambarus tartarus Hobbs
& Cooper, 1972, Cambarus aculabrum Hobbs & Brown, 1987, and Cambarus setosus
Faxon, 1889) clusters basal to the genus Cambarellus. While we now have extensive
samples of genera from Cambaridae (including Cambarus, Cambarellus, Barbicambarus,
Procambarus, Orconectes, Fallicambarus, Faxonella, Hobbseus, and Distocambarus), we
are still lacking many of the species that make up these genera and will continue to
sample in an attempt to represent nearly all species from the family before we attempt
a complete revision of the genera within the family. However, these preliminary results
clearly support the need for such a study to identify the evolutionary groups relating
various species. Indeed, many of the evolutionary groups supported by this phylogeny
show great geographic concordance.
Given their geographic distribution and the strong support for a monophyletic origin,
crayfish must have originated in Pangaea by at least the Triassic period (185-225 mya).
The separation of the two crayfish superfamilies represents the splitting of Pangaea
into northern (Laurasia) and southern (Gondwana) land masses around 185 mya. This
separation is clearly seen in the estimates of crayfish phylogenetic relationships. The
antiquity of the crayfish is supported by recent fossil evidence from Colorado and Utah,
with fossil crayfish and burrows associated with Permian and Early Triassic (265 mya)
deposits (Hasiotis & Mitchell, 1993). Furthermore, the phylogenetic connection of the
Southern Hemisphere crayfish represented in southern South America, Madagascar,
New Zealand, and Australia corresponds to the distribution patterns of the predatory
dinosaur group Abelisauridae (cf. Sampson et al., 1998). Likewise, deposits of Southern
Hemisphere crayfish and trace fossils are found from the Triassic and Cretaceous in South
America (Patagonia) (Bedatou et al., 2008) and Australia (Martin et al., 2008). Thus,
crayfish offer further support for the hypothesis suggesting extended contact between
these land masses and the antiquity of the lineage (Hobbs, 1988; Scholtz & Richter,
1995; Crandall et al., 2000a). A recent study dating the divergence times of the crayfish
based on a relaxed molecular clock calibrated with six independent calibration points
suggested a divergence time of 183 mya (179-185 mya) between the Northern and
Southern Hemisphere crayfish, consistent with the breakup of Pangaea (Breinholt et al.,
2009). The divergence of the major clades of Parastacidae occurred around 159 mya (143-
171 mya); whereas, the divergence between Astacidae and Cambaridae was only 90 mya
(63-125 mya). Indeed, this study shows that the genera of Cambaridae are particularly
young, which, coupled with their species diversity, could be a cause of their taxonomic
confusion with respect to their evolutionary history.
Clearly much remains in terms of a complete understanding of the evolutionary
history of the crayfish. Yet the last 10 years have seen significant advances in our
understanding of the phylogenetics of many subgroups of crayfish as well as their major
structure overall. These studies have provided a foundation for comparative studies of
morphological evolution, which have themselves illuminated aspects of phylogenetic
relationships. Likewise, these studies have laid the foundation for important conservation
work on crayfish and their highly endangered freshwater habitats (Crandall, 1998). We
anticipate that the coming years will provide some stability in the major relationships and a
taxonomic revision of the Northern Hemisphere crayfish to better reflect their evolutionary
history. We also anticipate the continued discovering of new species of these wonderful
and curious organisms.
SYSTEMATICS
[C. S OUTY-G ROSSET]
The basic taxonomy of the Infraorder Astacidea has been detailed by Hobbs between
1974 and 1994, at least as far as the freshwater forms are concerned. For the superfamilies
Nephropoidea Dana, 1852, Glypheoidea Winkler, 1883, and Enoplometopidae De Saint

Laurent, 1988, we refer to chapter 66 in volume 9B of the present series.
The diagnosis of the two superfamilies of Astacoidea and Parastacoidea is based on the
description of the carapace, the form of sternal plates and podobranchia, the branchial
formula, and the differences between the first pleopods of males and females. Both
superfamilies lack a dorsomedian longitudinal suture or a ridge in the cardiac and posterior
gastric regions of the carapace; their sternal plate between the fifth pereiopods is not fused
with the sternal complex anteriorly.
Until the publication of the “Illustrated checklist of the American crayfishes (Decapoda:
Astacidae, Cambaridae & Parastacidae)” in 1989, Hobbs, basing himself on morphological
criteria, described many new taxa, including one new family (Cambaridae), 38 new genera
and subgenera, and 286 species. After Hobbs (1974), crayfish taxonomy was updated to
generic level (see Fitzpatrick, 1983; Fetzner & Crandall, 2002; Taylor, 2002), with the
more recent efforts incorporating allozymes (Horwitz & Adams, 2000), and 16sDNA
sequences from the mitochondrial genome (Pedraza-Olvera et al., 2004). Molecular studies
have also discovered a wealth of cryptic species that likely represent units of evolution.
Their identification is thus highly relevant for conservation purposes (Crandall et al.,
2000c; Fetzner & Crandall, 2003). Scholtz & Richter (1995) have suggested the name
Astacida, which would include Astacoidea and Parastacoidea.
Superfamily A STACOIDEA Latreille, 1802
Articles of the lateral ramus of the antennule bear two clusters of aesthetascs (except
in Cambaroidinae Villalobos, 1955, in which there is only one); branchial formula
is 16 + ep; 17 + ep; 18 + 2r + ep; or 18 + 3r + ep (ep: epipod; r: rudimentary),
podobranchiae of the first three pereiopods not differentiated into branchial and
epipodite portions; males have first pleopods with a single sperm groove, groove
may be present or absent in females, second pleopods of males show a spiral element
frequently borne on a subtriangular lobe; telson divided by a transverse suture almost
always, and usually completely. Species live in fresh waters but some migrate into
salt waters for part of their life cycle.
A STACIDAE Latreille, 1802
Some articles of the lateral rami of the antennules bear two clusters of aesthetascs;
branchial formula 18 + 2r + ep or 18 + 3r + ep; ischia of male pereiopods lack
hooks; females lack first pleopods and annulus ventralis (sclerites present but lack
sinus and fossa); males never exhibit cyclic dimorphism, distal portion of the male
first pleopods rolled to form a cylinder, distalmost part contracted to form either
tube or produced into two simple, spoon-like lobes.
C AMBARIDAE Hobbs, 1942
Some articles of the lateral rami of the antennules bear 1 or 2 clusters of
aesthetascs; branchial formula 18 + 3r + ep; 17 + ep or 16 + ep; ischia of one
or more of 2nd -4th pereiopods with hooks; female first pleopods and annulus
ventralis may be present or absent; males exhibit cyclic dimorphism, male first
pleopods either bear medially shallow sperm grooves, or distal portions tightly
folded with distal end of sperm groove opening on one of 2-4 terminal elements.
†C RICOIDOSCELOSIDAE Taylor, Schram & Shen, 1999
Rostrum with rounded base and lateral spines; blade-like scaphocerite; no ischial
hooks on pereiopods; rounded pleomeral pleura; first pleopod styliform, remain-
ing pleopods annulate; telson not divided by a transverse suture.
A single species, Cricoidoscelosus aethus, from the Jurassic, Jehol Group of
northeastern China.
Superfamily PARASTACOIDEA Huxley, 1879
Articles of the lateral ramus of antennules bear never more than one cluster
of aesthetascs; branchial formula ranges between 12 + epr + 5r and 21 + ep
(epr: rudimentary epipod), epipodite of the first maxilliped usually with branchial
filaments, podobranchiae of the first three pereiopods differentiated into branchial
and epipodite portions; first pleopods absent, second pleopods of males similar to
third; telson never completely divided by a transverse suture.
PARASTACIDAE Huxley, 1879
Diagnosis the same as for the superfamily.
ACKNOWLEDGEMENTS
The principal organization and editing of this chapter has been the responsibility of FG
and CS-G. Prof. Frederick Schram is warmly acknowledged for his invitation to participate
in this exciting project and for his helpful comments on our manuscripts. We thank also
Dr. Manfred Pöckl (Section 2), Dr. Dyková, Dr. P. Henttonen, and Dr. K. Söderhäll
(Section 7), and J. Breinholt and H. Bracken (Section 10) for providing pictures. Dr.
José Carral and Dr. Julian Reynolds were of great help in commenting on and providing
information for the Reproduction and Development section. FG’s work was supported by
the University of Florence, JDU’s work by the Spanish Ministry of Education and Science
(REF-200730I009 and CGL2006-12732-C02-01/BOS), and KAC’s work by NSF (grant
EF-0531762). FG and KAC acknowledge their students for their dedicated work over the
last 10 years. The University of Poitiers and CNRS supported the work of CS-G.
A PPENDIX
Cited animal taxa

A NOMALA Boas, 1880
A STACIDA Scholtz & Richter, 1995
A STACIDAE Latreille, 1802
A STACIDEA Latreille, 1802
A STACOIDEA Latreille, 1802
Astacoides Guérin, 1839

Astacoides granulimanus Monod & Petit, 1929
Astacoides madagascarensis (H. Milne Edwards & Audouin, 1839)
Astacopsis Huxley, 1878
Astacopsis franklinii (Gray, 1845)
Astacopsis gouldi Clark, 1936
Astacus Fabricius, 1775
Astacus astacus (Linnaeus, 1758)
Astacus leptodactylus Eschscholtz, 1823
Austropotamobius Skorikov, 1908
Austropotamobius pallipes (Lereboullet, 1858)
Austropotamobius torrentium (Schrank, 1803)
Barbicambarus Hobbs, 1969
Biomphalaria Preston, 1910
Botaurus stellaris Linnaeus, 1758
Bouchardina Hobbs, 1969
Bulinus Müller, 1781
C AMBARELLINAE Laguarda, 1961
Cambarellus Ortmann, 1905
Cambarellus shufeldtii (Faxon, 1884)
C AMBARIDAE Hobbs, 1942
C AMBARINAE Hobbs, 1942
Cambaroides Faxon, 1884
Cambaroides japonicus (De Haan, 1841)
C AMBAROIDINAE Villalobos, 1955
Cambarus Erichson, 1846
Cambarus aculabrum Hobbs & Brown, 1987
Cambarus hamulatus (Cope, 1881)
Cambarus bartonii bartonii (Fabricius, 1798)
Cambarus bartonii sciotensis Rhoades, 1944
Cambarus diogenes diogenes (Girard, 1852)
Cambarus propinquus (Girard, 1852)
Cambarus robustus Girard, 1852
Cambarus rusticus Girard, 1852 [now in Orconectes]
Cambarus setosus Faxon, 1889
Cambarus tartarus Hobbs & Cooper, 1972
Campeloma decisum (Say, 1817)
Carassius auratus (Linnaeus, 1758)
Cherax Erichson, 1846
Cherax albidus Clark, 1936
Cherax destructor Clark, 1936
Cherax dispar Riek, 1951
Cherax quadricarinatus (Von Martens, 1868)
Cherax quinquecarinatus (Gray, 1845)
Cherax rotundus Clark, 1941
Cherax tenuimanus Smith, 1912
Corbicula Megerle von Mühlfeld, 1811
C RICOIDOSCELOSIDAE Taylor, Schram & Shen, 1999
Cynomys ludovicianus (Ord, 1815)
Distocambarus Hobbs, 1981
Engaeus Erichson, 1846

Engaeus granulatus Horwitz, 1990
Engaewa Riek, 1967
E NOPLOMETOPIDAE De Saint Laurent, 1988
Euastacus Clark, 1936
Euastacus armatus (Von Martens, 1866)
Fallicambarus Hobbs, 1969
Fallicambarus fodiens (Cottle, 1863)
Fallicambarus devastator Hobbs & Whiteman, 1987
Faxonella Creaser, 1933
Gambusia affinis (Baird & Girard, 1853)
Geocharax Clark, 1936
Gramastacus Riek, 1972
Gramastacus insolitus Riek, 1972
Haitia acuta (Draparnaud, 1805)
Hippolyte inermis Leach, 1815
Hobbseus Fitzpatrick & Payne, 1968
N EPHROPIDAE Dana, 1852
N EPHROPOIDEA Dana, 1852
Ombrastacoides Hansen & Richardson, 2006
Orconectes Cope, 1872
Orconectes australis packardi Rhoades, 1944
Orconectes causeyii Jester, 1967
Orconectes cristavarius Taylor, 2000
Orconectes harrisonii (Faxon, 1884)
Orconectes immunis (Hagen, 1870)
Orconectes incomptus Hobbs & Barr, 1972
Orconectes limosus (Rafinesque, 1817)
Orconectes luteus (Creaser, 1933)
Orconectes placidus (Hagen, 1870)
Orconectes propinquus Girard, 1852
Orconectes punctimanus (Creaser, 1933)
Orconectes rusticus (Girard, 1852)
Orconectes sanborni (Faxon, 1884)
Orconectes virilis (Hagen, 1870)
Pacifastacus Bott, 1950
Pacifastacus fortis (Faxon, 1914)
Pacifastacus leniusculus (Dana, 1852)
Pacifastacus leniusculus trowbridgii (Stimpson, 1857)
Paranephrops White, 1842
Paranephrops planifrons White, 1842
Paranephrops zealandicus (White, 1847)
PARASTACIDAE Huxley, 1878
PARASTACOIDEA Huxley, 1878
Parastacoides Clark, 1936
Parastacoides tasmanicus tasmanicus (Erichson, 1846)
Parastacus Huxley, 1878
Parastacus defossus Faxon, 1898
Parastacus nicoleti (Philippi, 1882)
Poecilia reticulata Peters, 1859
Potamon fluviatile (Herbst, 1785)

Procambarus Ortmann, 1905
Procambarus acutus acutus (Girard, 1852)
Procambarus alleni (Faxon, 1884)
Procambarus cavernicola Mejía-Ortíz, Hartnoll & Viccon-Pale, 2003
Procambarus clarkii (Girard, 1852)
Procambarus fallax (Hagen, 1870)
Procambarus hagenianus (Faxon, 1884)
Procambarus mexicanus (Erichson, 1846)
Procambarus oaxacae reddelli Hobbs, 1973
Procambarus zonangulus Hobbs & Hobbs, 1990
Salmo trutta Linnaeus, 1758
Samastacus Riek, 1971
Samastacus spinifrons (Philippi, 1882)
Schistosoma haematobium (Bilharz, 1852)
Schistosoma mansoni Sambon, 1907
Tenuibranchiurus Riek, 1951
T HALASSINIDEA Latreille, 1831
T HAUMASTOCHELIDAE Bate, 1888
Troglocambarus Hobbs, 1942
Virilastacus Hobbs, 1991
Virilastacus rucapihuelensis Rudolph & Crandall, 2005
Cited botanical and other non-animal taxa at species level
Aphanomyces astaci Schikora
Didimaria cambari
Microcystis aeruginosa (Kützing) Lemmerman
Nymphoides peltata (S. G. Gmelin) Kuntze
Oscillatoria sancta (Kützing) Gomont.
Potamogeton filiformis Pers.
Psorospermium haeckeli (Hilgendorf)
Saprolegnia diclina Humphrey
Saprolegnia parasitica Coker
Thelohania contejeani Henneguy
Utricularia australis R. Br.
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Infraorder astacidea Latreille, 1802 P.O. : The freshwater crayﬁsh

Article · January 2010

Catherine Souty-Grosset Javier Diéguez-Uribeondo

SEE PROFILE SEE PROFILE

The user has requested enhancement of the downloaded file.

INFRAORDER ASTACIDEA LATREILLE, 1802 P.P.:

FRANCESCA GHERARDI, CATHERINE SOUTY-GROSSET, GÜNTER

Contents. – Introduction – Overview – Diagnosis. External morphology – General habitus –

1 ) Manuscript concluded June 2009.

© Koninklijke Brill NV, Leiden, 2010 Crustacea 9A (67): 269-423

reaction; bears anus

composed of different fiber types varying in ultrastructure, histochemistry, and innervation

released from the hematopoietic tissue. Release could experimentally be stimulated by

Fig. 67.12. Schematic illustration of digestive system of crayfish: a, antechamber of hepatopancreas;

Fig. 67.14. Schematic illustration of reproductive system of crayfish. A, architecture of ovary; B,

Growth of the oocytes is predominantly characterized by the deposition of lipid and

Fig. 67.17. Endocrine system of crayfish. A, ultrastructure of peptide hormone synthesizing M-

Fig. 67.18. Nervous system of crayfish. A, immunocytochemical demonstration of serotonin recep-

REPRODUCTION AND DEVELOPMENT

8. Procambarus sp. 2 <1 yr 40 mm All the yr round up to 270

Sex determination and sex ratios

Intersexes, parthenogenesis, and hybridization

Crayfish in their habitat

Crayfish in the food web

Choosing the time to be active

crushed conspecifics were treated as feeding signals by Procambarus clarkii populations

S PECIES , SEX , AND MATE RECOGNITION

PARENTAL CARE AND JUVENILE BEHAVIOR

In most instances, agonistic interactions between two crayfish progressively escalate

PARASITES AND DISEASES

Thelohania spp., have contributed to an understanding of the phylogenetic roots of fungi

Aphanomyces astaci (crayfish plague)

Pathogen Type of Disease Infection Described in

White spot Virus White spot – Astacus spp.

Thelohania contejeani (porcelain disease)

Branchiobdellidans, or crayfish worms, are leech-like oligochaetes and obligate ec-

Other parasites and diseases

Conservation status in different countries

Eutrophication 2 1 1 1 1 1/2 3 2 1 1 1/2

Methods and policies

PHYLOGENY AND BIOGEOGRAPHY

Family Genus Species

Present distribution and areas of endemicity

Phylogeny and historical processes

Nephropoidea Dana, 1852, Glypheoidea Winkler, 1883, and Enoplometopidae De Saint

Cited animal taxa

Astacoides Guérin, 1839

Engaeus Erichson, 1846

Potamon fluviatile (Herbst, 1785)

C ERENIUS, L., Z. L IANG, B. D UVIC, P. K EYSER, U. H ELLMANN, E. T. PALVA, S. I WANAGA &

F EDORENKO, G. M. & A. B. U ZDENSKY, 2008. Dynamics of ultrastructural changes in the isolated

G ROSELL, M., C. J. B RAUNER, S. P. K ELLY, J. C. M C G EER, A. B IANCHINI & C. M. W OOD, 2002.

H ASIOTIS, S. T., M. F. M ILLER, J. I SBELL, L. E. BABCOCK & J. W. C OLLINSON, 1999. Triassic

J ONES, J. P. G., F. B. A NDRIAHAJAINA, N. J. H OCKLEY, K. A. C RANDALL & O. R. R AVOA -

KOZUBÍKOVÁ, E., A. P ETRUSEK, Z. Ď URIŠ, M. P. M ARTÍN, J. D IÉGUEZ -U RIBEONDO & B.

M C M AHON, A., B. W. PATULLO & D. L. M ACMILLAN, 2005. Exploration in a T-maze by the

O IDTMANN, B., S. G EIGER, P. S TEINBAUER, A. C ULAS & R. W. H OFFMANN, 2006. Detection of

P ÉREZ, J. R., J. D. C ELADA, J. G ONZÁLEZ, J. M. C ARRAL, M. S ÁEZ -ROYUELA & R. F ERNÁN -

RUDOLPH, E. H., F. A. R ETAMAL & A. W. M ARTÍNEZ, 2007. Partial protandric hermaphroditism in

S CHOLTZ, G., A. B RABAND, L. T OLLEY, A. R EIMANN, B. M ITTMANN, C. L UKHAUP, F.

S IMON, J. L. & P. A. M OORE, 2007. Male-female communication in the crayfish Orconectes

— —, 1986. Disease problems during aquaculture of freshwater Crustacea. — Freshwater Crayfish,