Earth-Science Reviews 46 Ž1999.

167–185
www.elsevier.comrlocaterearscirev

Colonization of new habitats by benthic foraminifera: a review

)
Elisabeth Alve
Department of Geology, UniÕersity of Oslo, P.O. Box 1047 Blindern, N-0316 Oslo, Norway

Abstract

Colonization of new habitats, which have been established as a result of a catastrophic disturbance of the environment, is
one of the characteristic repetitive events throughout the Phanerozoic. In recent years, much attention has been paid to
investigations focusing on biological recovery of benthic habitats severely disturbed by human activity. In order to improve
our environmental and stratigraphical interpretations of such events, we need a more thorough understanding of the
processes involved in colonization by one of the most abundant and useful fossil groups, the benthic foraminifera. The
present review focuses on processes governing benthic foraminiferal dispersion and colonization patterns in modern
environments. For benthic foraminifera, the only active dispersal mechanism is through self-locomotion on or within the
sediment and this is considered to be efficient over short distances only. Several passive dispersal methods have been
suggested but two seem to be of more general importance. These are dispersal through release and transport of embryonic
juveniles and passive suspension and transport of various growth stages. Both are probably important for most benthic
foraminifera but the former is likely to be the main mechanism for attached, tubular and larger foraminifera, which are not
easily entrained at a later life stage. The latter seems to be a more important dispersion mechanism for benthic foraminifera
than previously realized. The colonization rate of soft-bottom substrates is closely related to the hydraulic regime in, and the
transit time from, the source area inhabited by species capable of colonizing the new habitat Žas long as food and other
environmental characteristics are not limiting factors.. The transit time depends on the speed of the transporting medium and
the distance from the source area. There seems to be two end-processes which can operate during the colonization,
depending on whether physically induced or biological processes are allowed to dominate. They are characterized by
different colonization patterns. In high energy environments Žbottom current velocities often ) 20 cmrs., a short transit
time may cause the major components of the nearest ambient seafloor assemblages to colonize the new habitat within days.
In this case the colonization is simply through a physical transfer of parts of the source community to the new habitat,
allowing no time for pioneer, opportunistic assemblages to develop. In low energy environments Žbottom current velocities
generally - 10 cmrs., the transit time is long for most species. Here, colonization follows the classic metazoan successional
pattern with an initial, high abundance pioneer assemblage strongly dominated by small opportunists followed by
development of assemblages with increasing numbers of specialized species and recovery can take from one to several years.
Initial lack of food Že.g., volcanic ash. or ‘hostile’ substrate properties Že.g., recently reoxygenated or severely contaminated
sediments. may delay colonization by months or even years. Small, infaunal species Žboth calcareous and agglutinated. are
among the first and most successful colonizers of soft bottom habitats from shallow waters to the deep sea. Throchospiral

)
Fax: q47-22-85-42-15; E-mail: elisabeth.alve@geologi.uio.no

0012-8252r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 0 1 2 - 8 2 5 2 Ž 9 9 . 0 0 0 1 6 - 1
168 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
agglutinated taxa are among the most abundant colonizers on deep sea hard substrates. q 1999 Elsevier Science B.V. All
rights reserved.
Keywords: benthic foraminifera; meiofauna; dispersal; colonization; succession; recovery
1. Introduction
Environmental disturbances have various degrees
of destructive impacts on benthic communities and
severe, large-scale disturbances can lead to defauna-
tion of existing sediments or establishment of new,
unoccupied habitats. Habitat disturbance or destruc-
tion may also cause species extinction and this is
most likely to happen in areas with high numbers of
rarely occurring endemic taxa ŽCulver and Buzas,
1998.. The initial faunal recovery processes and
subsequent succession following major disturbances
are referred to as colonization ŽLevin and DiBacco,
1995. and this is the topic considered in the present
paper, focusing on benthic foraminifera. Small-scale
disturbances Že.g., fishes stirring up the sea bottom,
animal tracks, faecal casts. of already occupied habi-
tats are not included. However, several aspects of the
colonization processes following large-scale distur-
bances also have implications for our understanding
of the dynamics and recovery patterns of small-scale
disturbances and are therefore of general interest and
applicability.
In the marine environment, severe disturbance
causing an appearance of new habitats ready for
colonization by benthic organisms is generally due to
one of the following three causes:
Ž1. Sudden depositional events such as turbidity
current deposits Že.g., flysch. and other mass-flow
deposits which typically occur along continental
margins and in fjords, deposition of submarine vol-
canic ash layers, and anthropogenic dumping activ-
ity.
Ž2. Sudden exposure of new azoic sea floor which
may be due to Ža. natural or human induced erosion
such as areas where the surface sediments have been
‘stripped’ off during mass-flow transport, Žb. benthic
storms Ži.e., strong currents., Žc. icebergs ploughing
into the sea bottom, or Žd. in more recent years,
anthropogenic dredging in coastal areas or possible
deep sea manganese nodule mining.
Ž3. Exposure of new azoic sea floor due to an
environmental change such as retreating ice fronts
and oxygenation following anoxic events Že.g.,
sapropels and reoxygenation following organic mat-
ter pollution abatement., whereas marine transgres-
sions probably operate too slowly to provide a lag
between exposure and colonization.
In the marine geological record of sudden deposi-
tional events there will be a succession from Ža. a
pre-disturbance deposit to Žb. a disturbance deposit
followed by Žc. the post-disturbance deposit. Units a
and c may contain in situ fossils whereas unit b will
either be unfossiliferous Že.g., volcanic ash layer. or
contain transported fossils Že.g., turbidites, although
they may contain post disturbance, infaunal taxa
which utilize organic matter in the turbidite layer
ŽRathburn and Corliss, 1994... The marine geologi-
cal record of sudden exposure of new azoic sea floor
may be represented by disturbance deposits without
fossils Že.g., as a result of anoxia or ice in contact
with the sea floor. followed by post-disturbance
deposits Žwith fossils.. However, events such as
benthic storms, and dredging may not leave a distur-
bance deposit but simply erode into older fossilifer-
ous deposits Žin which nothing is currently living.
upon which new deposits Žwith fossils. subsequently
accumulate Ži.e., create an hiatus.. From a geological
point of view, important paleoenvironmental infor-
mation can be obtained by high resolution studies of
sediments deposited just before, during, and after the
disturbance event Že.g., Rohling et al., 1997. but
detailed paleoenvironmental interpretations can only
be achieved through analyses of the fossil assem-
blages. In many cases, benthic foraminifera represent
the best fossil group for study because they are
usually the most abundant benthic organisms pre-
served. While the present review focuses on biologi-
cal observations of short-term Žin a geological per-
spective. colonization processes in modern environ-
ments, geological investigations are the only which
can provide more complete information about long-
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
term processes. However, in order to perform de-
tailed interpretations, it is necessary to establish
whether the sedimentary sequence is complete Ži.e.,
without hiatus. and whether the benthic community
recorded just after the event is redeposited or in situ.
In the latter case, valuable paleoenvironmental infor-
mation can be obtained only if we know how to
recognize and interpret foraminiferal colonization
patterns and this has to be based on a thorough
understanding of foraminiferal biology.
Marginal basins, such as the Mediterranean Sea,
which have undergone alternation between oxic and
anoxic conditions leading to sapropels Že.g., Rohling
et al., 1997; Schmiedl et al., 1998 and references
therein. present additional problems of scale com-
pared with the observations of modern processes.
Questions which might be posed include the follow-
ing.
Ø What is the source area of the colonizing
species? Are they from oxic refuges within the basin
or are they introduced from the adjacent open ocean?
If the latter is the case, was the post-sapropel circula-
tion the same as the present-day anti-estuarine circu-
lation in the Mediterranean; this would present a
major problem for transport of foraminifera.
Ø How rapidly does recolonization take place in
such previously hostile habitats? Is it diachronous or
near instantaneous on a geological timescale?
Ø How long does it take for the colonizing as-
semblages to reach comparable diversity and equata-
bility levels to those of the pre-sapropel assemblages
after re-establishment of well oxygenated condi-
tions?
These are questions that future studies of sapro-
pels might address in the light of the data from
modern environments reviewed in this paper.
In addition to these more traditional geological
applications, analyses of both live and dead benthic
foraminiferal assemblages have been shown to have
a good potential for studying anthropogenically in-
duced disturbance and recovery effects in marginal
marine environments Žreviewed in Alve, 1995a; for
discussion of environmental change using benthic
foraminifera as proxies, see also Murray, in press..
Consequently, detailed information concerning the
dynamics of benthic foraminiferal dispersal, colo-
nization, and recolonization patterns is also impor-
tant from an environmental management point of
169
view, for interpreting and understanding the ecologi-
cal implications of, and recovery from, anthro-
pogenically induced environmental stress Že.g., Elli-
son et al., 1986.. This concerns both short-term
biological monitoring evaluating impacts of physical
and chemical disturbance and environmental stratig-
raphy investigations ŽAlve, in press. recording im-
pacts over a longer time period Že.g., back to pre-in-
dustrial times..
There are numerous studies of benthic metazoan
colonization patterns both in lacustrine and marine
environments. The question arises: do benthic
foraminifera, being protists, follow the same patterns
of dispersal, colonization, and subsequent succession
as metazoans?
At present, there is only limited understanding of
the processes and biological dynamics of benthic
foraminiferal dispersal and colonization patterns, and
most publications so far have primarily focused on
the speed of colonization rather than on the pro-
cesses involved Že.g., see active vs. passive distinc-
tion below.. This review addresses the principal
environmental and biological processes which seem
to control dispersal and colonization of modern
foraminiferal assemblages in newly established, azoic
habitats in comparison with what is known of the
patterns for marine benthic metazoan invertebrates.
2. Dispersion
The dispersal phase of macrobenthic life histories
in the marine environment commonly occurs through
passive spreading of planktonic larval stages ad-
vected by currents Že.g., Grassle, 1978. and recolo-
nization studies have shown that pelagic larval re-
cruitment can account for 70–90% of all individuals,
especially of polychaetes and molluscs ŽMcCall,
1977; Santos and Simon, 1980; Diaz-Castaneda et
al., 1993.. However, movement by adults and juve-
niles through the water column have also been re-
ported Že.g., Chandler and Fleeger, 1983; Kern and
Bell, 1984.. In contrast to the macrofauna, most
meiofaunal taxa lack pelagic larvae and they are
known to enter the water column either passively
through entrainment, or actively through swimming
Žfor review, see Palmer, 1988a; Thistle et al., 1995..
Since benthic foraminifera do not have swimming
170 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
abilities, active entry to the water column is not
possible. Consequently, for most motile benthic
foraminifera, there are theoretically four different
ways of dispersion Žthree passive, one active.: Ž1.
release to the water column of gametes, zygotes, or
of embryonic agamonts or gamonts following sexual
and asexual reproduction, respectively; Ž2. adaption
to a meroplanktonic juvenile life stage with subse-
quent passive spread by currents; Ž3. self locomotion
along the sea floor; or Ž4. through passive Žphysi-
cally or biologically induced. entrainment into the
water column and subsequent transport of different
growth stages. For attached species, the former two
are most likely. Shallow water taxa may also be
transported by floating objects or larger marine ani-
mals Žfor discussion, see Myers, 1936., by birds, and
by human activity ŽLessard, 1980; Witte, 1994; Mc-
Gann and Sloan, 1996..
2.1. Release of propogules following reproduction
Dispersal of foraminifera can involve the release
of flagellate gametes to the seawater or the produc-
tion of amoeboid gametes ŽGrell, 1967.. Of the
foraminifera for which aspects of reproduction has
been studied, the majority have a life cycle in which
gametogenesis produces numerous biflagellated,
free-swimming gametes that are released directly
into the surrounding seawater ŽGoldstein, 1997..
However, gametes probably do not live long enough
Žhours to one or a few days?. to represent a primary
dispersal mechanism, and the farther they travel, the
lower the density of gametes and likelihood of fertil-
ization ŽS.T. Goldstein, pers. commun., 1998.. Also,
in some species Že.g., Spirillina ÕiÕipara, Patellina
corrugata., the haploid gametes are confined at all
times within an attached cyst implying that dispersal
cannot be accomplished in the gamete phase of their
life-cycle ŽMyers, 1936.. On the other hand, distribu-
tional and seasonal reproduction studies of the shal-
low water species Trochammina hadai suggest that
the sexual generation is more efficiently dispersed
than the asexual generation because the gametes are
released to and advected by the bottom water
ŽKitazato and Matsushita, 1996.. Some shallow wa-
ter species which live in close association with algae
have adapted to the seasonally fluctuating intensity
of turbulent coastal zones by alternating the different
stages of their life cycles between the sediments and
epiphytally on algae ŽErskian and Lipps, 1987. or
alternate between intertidal and subtidal habitats
ŽWalker, 1976.. Both involve passive dispersion of
adult individuals as well as of embryonic juveniles.
Some living larger foraminifera can withstand very
high current velocities of 3–4 mrs ŽSeverin and
Lipps, 1989., suggesting that they are not easily
entrained. This is probably due to a combination of
their large test size and ability to cling to the sub-
strate with their pseudopodia. Additionally, the fact
that larger foraminifera recolonize reef habitats fol-
lowing defaunation caused by for instance a cyclone
ŽCollen, 1996., suggests that they re-enter these habi-
tats as embryonic juveniles following reproduction in
adjacent areas. This mechanism probably also plays
an important role in the dispersal of many attached
taxa since they are not easily entrained but still have
shown to be among the most successful colonizers of
hard substrates Žsee Section 4..
It seems that dispersal by gametes may be effi-
cient over small distances Žmeters to hundreds of
meters., whereas zygotes and embryonic juveniles,
which probably have a density comparable to seawa-
ter and therefore are easily transported, are more
prone to disperse over larger distances. The first few
chambers of juvenile benthic foraminifera are often
thin and transparent and capable of increasing their
flotation by extending numerous filose pseudopodia,
so there is no reason why they should not remain
pelagic for days or possibly weeks ŽMyers, 1936..
However, more studies are needed, both for epifau-
nal and particularly for infaunal species which prob-
ably reproduce within the sediments Ži.e., no imme-
diate release of embryonic offspring to the water
column; e.g., Frankel, 1972., before further conclu-
sions concerning the importance of this mode of
dispersal can be drawn.
2.2. Meroplanktonic life stage
Occurrences of living benthic foraminifera in the
water column has led several authors to suggest that
some species have a meroplanktonic Ži.e., temporary
planktonic. stage in their life cycle we.g., BoliÕina
Õaughani ŽLidz, 1966.; Brizalina lowmani ŽHueni et
al., 1978.; various tide-pool species ŽWalker, 1976.x.
To the authors knowledge, a meroplanktonic life
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
stage has so far been proved in five genera only
ŽTretomphalus, Tretomphaloides, Millettiana, Cym-
baloporetta, and Rosalina. which build a float
chamber for use during their planktonic stage ŽLoeb-
¨
lich and Tappan, 1987; Ruckert-Hilbig, 1983.. This
is most probably an efficient dispersal method but
whether or not it is an adaptive strategy in species
other than those with a float chamber is left to be
proved. Consequently, until more information is
available, no conclusions can be drawn concerning
the more general importance of this mode of disper-
sion.
2.3. Self locomotion
In most environments, self locomotion along the
sea floor is probably a less efficient and very slow
process because foraminifera Žthose investigated so
far. move with a speed of - 1 mm per hour Žtypi-
cally deep-sea and bathyal species, e.g., Weinberg,
1991; Hemleben and Kitazato, 1995; Bornmalm et
al., 1997. up to a few millimeters per hour Žsome
shallow water species, e.g., Kitazato, 1988; Wet-
more, 1988. and because their movements are known
to be random Že.g., Jepps, 1942; Murray, 1963.,
implying that they do not actively track a new
habitat. However, tank experiments have indicated
that colonization of new habitats through self loco-
motion may occur over small distances of some tens
of centimeters within 7 days ŽSchafer and Young,
1977.. Consequently, due to the random and rela-
tively slow movement, this method is probably most
applicable to active colonization of small-scale dis-
turbed patches.
2.4. PassiÕe entrainment and transport of growth
stages
It is commonly known that once in suspension,
sediment particles can be carried for long distances
even at low velocities Žrelative to the velocities
needed to entrain them. and their physical behaviour
is mainly a function of the settling velocity. It is
reasonable to assume that the same holds true for
benthic foraminiferal tests and consequently, one of
the most important factors for dispersal of
foraminifera of various growth stages is the critical
shear velocities required to entrain Žsuspend. the
171
foraminifera in the source area, as well as the sur-
vival time of the entrained individuals.
Compared to other marine, major meiofaunal
groups Žcopepods and nematodes., living benthic
foraminifera seem to be the least easily suspended
ŽSherman and Coull, 1980.. This is not surprising,
since copepods are agile swimmers and nematodes
lack clinging appendages Že.g., Palmer and Molloy,
1986.. As pointed out by Severin and Lipps Ž1989.,
a living foraminiferan can use its pseudopodia to
anchor itself to the substrate, whereas entrainment of
a dead test is simply a function of the size, shape,
and density of the test in relation to the bottom
current velocity. Furthermore, in shallow water habi-
tats where wave action and turbulence impose a
physical stress on the organisms living there, differ-
ent adaptive strategies Žattachment, avoidance, test
robustness. are developed by the benthic foraminifera
to withstand transport Žsee discussion in Palmer and
Molloy, 1986; Erskian and Lipps, 1987.. Despite all
this, living benthic foraminifera have been reported
to occur abundantly in the water column and, as
discussed in Section 3, several studies have shown
that appearance of diverse, abundant assemblages on
new substrate can happen so quickly that settlement
of various growth stages, rather than settlement Žand
subsequent growth. of recently produced offspring,
is more likely to have been the major mechanism.
There is hardly any information on what bottom
current velocities are needed to entrain motile living
benthic foraminifera, but some information exists
concerning dead tests. Flume experiments have
shown that the mean traction velocities for dead tests
of common, free living, small Žnominal diameter
0.32–0.52 mm. species such as Quinqueloculina cf.
Q. Õulgaris, Islandiella subglobosa, Bulimina ac-
uleata, and UÕigerina peregrina are as low as 5.1,
5.4, 6.6, and 9.2 cmrs, respectively ŽKontrovitz et
al., 1978.. Consequently, bottom currents of at least
10–15 cmrs are probably needed to entrain living,
adult benthic foraminifera as long as their pseudopo-
dia are active and ‘clinging’ to particles outside the
test. On the other hand, foraminifera associated with
fluffy sediments, e.g., phytodetritus Žwhich is resus-
pended by bottom currents exceeding about 7 cmrs
Žat 1 m altitude; Lampitt, 1985.. are probably more
easily entrained and thereby have a higher dispersion
potential. Flume studies indicate that benthic
172 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
foraminifera suspended in bottom flows of about
4–9 cmrs can passively be transported into fiddler
crab burrows ŽDePatra and Levin, 1989.. In addition
to physically induced entrainment, biological distur-
bance Že.g., fiddler crabs, fish, flushing of burrows
by infaunal macrobenthos. can also suspend benthic
foraminifera. For example, passive transport of
foraminifera and other meiofauna has been shown to
be doubled due to fish activities ŽPalmer, 1988b..
Due to the fact that suspension transport of both
dead and living benthic foraminifera has important
implications for the taphonomic aspect of palaeoeco-
logical interpretations, comments will be given on
transport of dead tests as well as on living individu-
als.
2.4.1. Suspension transport of dead indiÕiduals
Storms have been shown to play an important role
in the suspension transport of benthic foraminifera
because there are several records of benthic
foraminifera in plankton samples taken during or
after such events but in several cases the majority of
individuals recorded are dead. For example, plankton
samples Žnet opening 76 mm. collected from the sea
surface and 10 m below the surface after a period of
storms in the English Channel had a ‘high content’
of dead benthic foraminifera, but only very thin-
walled types, showing a pronounced size sorting
Žmajority 150–200 mm in length or diameter accord-
ing to shape. were recorded ŽMurray, 1965.. Based
on the presence of only scattered live Žstained. indi-
viduals Ž) 76 mm. of benthic foraminifera in surface
water Ž40 m below the surface. samples and samples
from 5 m above the sea floor, the Western Ap-
proaches and the Western English Channel, Murray
et al. Ž1982. concluded that, even though dead tests
were abundant, suspension transport is not a
widespread means of dispersal of live benthic
foraminifera in that area. Suspension and transport of
‘probably dead’ benthic foraminifera has also been
reported from the North Sea where Leptohalysis
scottii Žas Reophax . occurs regularly during winter
and spring in plankton tows Žmesh size 270 mm.
collected at 10 m water depth ŽJohn, 1987.. Myers
Ž1936. noted that ‘‘it is not uncommon to find even
adult Foraminifera in plankton taken from the waters
of the littoral zone’’. During a 16-month survey of
sediment traps, suspended at 125 m water depth on a
mooring in 400 m of water on the eastern side of the
USA, Brunner and Biscaye Ž1997. recorded average
fluxes of 155 benthic testsrm2 per day from the
shelf to the slope during relatively calm spring and
summer periods, whereas fluxes of 29,000 and 50,000
testsrm2 per day were found in connection with a
winter storm. The transported benthic taxa were
typical of the continental shelf in that area and they
ranged in size from about 30 to 845 mm, with a
median size of 81–98 mm. Only a few living indi-
viduals were present in the whole data set ŽBrunner,
pers. comm., 1998.. Overall, this shows that trans-
port of benthic foraminiferal tests by water currents
may be substantial.
2.4.2. Suspension transport of liÕing indiÕiduals
In the above mentioned records, nearly all the
transported benthic foraminiferal tests were dead.
Considering the fact that in most marine environ-
ments, the densities of dead tests are generally one to
several orders of magnitude higher than those of
living individuals Že.g., Scott and Medioli, 1980;
Alve and Murray, 1997., it is not surprising that they
are also more common in the water column follow-
ing resuspension of surface sediments. However,
living individuals, representing various growth
stages, have also been reported from the water col-
umn. For example, Arnold Ž1964. collected some of
the individuals Ž Spiroloculina hyalina. used in his
culture studies ‘by a plankton net towed obliquely
from the surface to a depth of 140 ft’ in an area off
La Jolla where the water depth ranged from 120 to
160 ft. Lidz Ž1966. found living individuals of Bo-
liÕina Õaughani in plankton tows Ž62 mm mesh.
down to 15 m below the sea surface 0.5–3.5 km
offshore of California and also mentioned unpub-
lished records of living species of both BoliÕina and
BoliÕinita in plankton tows from the ‘deep ocean
water’ in the Catalina Basin Ž) 50 km offshore..
Living individuals of 12 benthic species were
recorded in plankton tows Ž72 mm mesh. collected
from the surface water just off Bodega Head, Cali-
fornia, in water depths to about 25 m ŽLoose, 1970..
The assemblage composition was the same as that
living in the intertidal community of the area but the
size range of the specimens was somewhat smaller
Ž250–500 mm diameter.. No quantitative abundance
data were available, but due to the fact that a fair
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
number of living individuals were found even though
‘the conditions under which the tows were made
probably represent a near minimum for energy and
turbulence’, it was inferred that ‘great numbers of
foraminifera could be transported’ during storms and
high energy conditions. Furthermore, in the Gulf of
Mexico, living individuals of Brizalina lowmani Ž)
400 individualsrm3 . were recorded in plankton tows
collected at 0–25 m water depth from the coast and
up to several tens of kilometer offshore ŽHueni et al.,
1978..
In a colonization experiment performed in rela-
tively shallow water Ž11–19 m. in the western Baltic
Sea, elevated colonization platforms Ž1.5–5.0 m
above the sea floor. were used to prevent active
locomotion of the foraminifera up and into the colo-
nization trays ŽWefer and Richter, 1976.. Samples
were collected monthly and the first recorded living
individuals were of intermediate size Žabout 200
mm., i.e., no juveniles and no adults, implying that
the primary dispersion of the foraminifera was
through suspension and lateral transport of individu-
als of intermediate growth stages. Both calcareous
and agglutinated forms were present but Elphidium
excaÕatum was by far the most abundant, and live
individuals of E. excaÕatum Žsize: 125–200 mm.
were also recorded in the water at that site.
A nice example showing that even big Žnearly 1
mm in diameter. taxa can be suspended, transported
into a new habitat, and continue to live there, was
shown in a colonization experiment carried out in
Sagami Bay, off Japan, at 1445 m water depth
ŽKitazato, 1995.. The sediment in this particular
colonization box consisted of artificial substrate made
of silt-sized glass beads. After 1 year of colonization,
a large individual of AlÕeolophragmium adÕena with
glass beads incorporated into the five last chambers
Žout of 11 chambers in the last whorl. was recorded
showing that it was alive and in its adult form when
it was transported into the colonization box. Another
part of the same experiment included colonization in
two boxes with defaunated ambient sea floor mud.
One was open, whereas the other was covered with a
plankton net Ž90 mm mesh. to exclude larger indi-
viduals from colonizing. Both shallow and deep
infaunal taxa colonized the open box, whereas no
stained foraminifera were found in the box covered
by the plankton net. Kitazato concluded that the
173
individuals probably had not entered the colonization
boxes as either zygotes or juveniles but had been
suspended and transported into the new habitat in
connection with benthic storms or possibly through
bioerosion by deep-sea fish. However, the possibility
that the plankton net had been clogged by sediment
and thereby decreased the efficient mesh size, cannot
be excluded.
The cited examples have shown that suspension
transport of individuals up to several hundred mi-
crons is not uncommon and that the transported
living individuals often represent the dominant
species inhabiting the sediments in the source areas.
We shall return to this point in the discussion of
colonization patterns.
The processes which lead to colonization Ždisper-
sion, transport, settling. operate all the time in ma-
rine environments and normally they contribute to
the changing pattern of species distributions and
variability in their abundance through time. How-
ever, the difference between ‘normal’ conditions and
colonization of azoic Žempty space. sediment is that
in the former the introduced individuals have to
compete with the pre-existing fauna whereas in the
latter this does not apply, at least in the initial stage.
3. Colonization of soft bottom substrates
Characteristic features of the dominant, metazoan
early colonizers include high reproduction capacity
and short life cycles Žr-strategistss opportunists. en-
abling efficient colonization Že.g., Koskenniemi,
1994.. The following specialization stage is charac-
terized by species with lower invasion ability, they
tend to have longer life cycles, and habitat selection
mechanisms are increasingly important to determine
the faunal distribution ŽK-strategistss equilibrium
species.. Some species occur later in the environ-
mental development due to initial lack of suitable
habitats and the impact of the species’ dispersion
ability on the community structure decreases dramat-
ically as more specialized species are introduced
ŽKoskenniemi, 1994.. The importance of species dis-
persal ability at the beginning and the increasing role
of the habitat Žand species interactions. later in the
succession has been shown for terrestrial inverte-
brates Že.g., Huhta, 1971. as well as for macro-
zoobenthos Že.g., Koskenniemi, 1994..
174 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
For benthic foraminifera, the current state of
knowledge is to a larger extent based on experiments
than on field observations. Recent studies Že.g.,
Smith, 1985; Kukert and Smith, 1992; Snelgrove et
al., 1995. have shown that several meio- and macro-
faunal colonization experiments have been fraught
with artifacts due to hydrodynamic effects and the
isolation of the experimental substrate from the am-
bient sediment by the sides and floor of the trays.
However, the present review has not attempted to
evaluate possible artifacts concerning the design of
the cited experiments.
Several of the colonization experiments dealing
with benthic foraminifera have focused primarily on
ecological aspects rather than the colonization pro-
cess proper. In these studies, information about the
colonization patterns has been obtained as a spin-off
and quantitative faunal data of the experimental and
ambient Ži.e., nearby in situ. assemblages are not
always available. In several cases, purely sand-sized
particles Ži.e., no mud. have been used in some of
the colonization trays, whereas other trays have con-
tained ambient sea floor sediments which have been
defaunated, mostly by freezing. Some of the pure
sand experiments will be discussed together with
studies of sediments with characteristics beyond the
‘normal’ marine range ŽSection 3.2. because the
well-established positive correlation between mud
and organic matter implies that pure sand represents
an extremely nutrient deficient habitat and, as such,
is not representative of most marine environments
Žfor macrofaunal responses to colonization in en-
riched versus unenriched sediments, see, e.g., Snel-
grove et al., 1996.. The same applies to recently
deposited volcanic ash layers. Studies concerning
anthropogenic dump sites and colonization following
anoxic events are also discussed in Section 3.2 be-
cause they initially represent chemically hostile habi-
tats.
3.1. Azoic ‘normal’ marine sediment
Experimental studies in coastal shallow water ar-
eas have shown that the initiation of colonization and
even establishment of assemblages with densities
and a faunal composition comparable to that of the
surrounding ambient benthic assemblages may occur
in only a few days to weeks. For example, Schafer
Ž1976. reported that re-establishment of the major
species occurred in colonization frames only 2 days
after emplacement at 13 m water depth in Nova
Scotia. In addition to the colonization of the sur-
rounding sea floor species, a strongly increasing
absolute abundance of living Ammonia beccarii and
Elphidium spp., which are characteristic infaunal
species of the more shallow areas, occurred a few
days later, just after a hurricane had passed. There
was no increase of the typical infaunal ambient
species, Eggerella adÕena, following this event. The
increase in only the shallower water species was
directly attributed to disturbance effects caused by
the hurricane.
At 65 m on the shelf off New Jersey, Ellison and
Peck Ž1983. found that defaunated ambient sedi-
ments Žmoderately well-sorted, medium–fine sand.
were completely colonized 10 weeks after emplace-
ment, and the faunal composition was comparable
with that after 43 weeks. In the same way as for the
shallow water studies, the colonization occurred in
proportions similar to that of the surrounding ambi-
ent fauna. There was no particular difference in the
faunal composition or density between the 0–1, 1–2,
and 2–3 cm levels in the sediments, and it was
inferred that colonization on and into the sediment
proceeded nearly simultaneously. A similar pattern
was recorded after 6 weeks in a colonization experi-
ment Žopen mud-filled box. conducted at 125 m
water depth off Florida ŽBuzas et al., 1989..
The cited examples show that in shallow water
coastal and inner shelf areas, the assemblage compo-
sition and faunal density may rapidly Žwithin days to
weeks. approach those of the ambient, surrounding
sea floor. In these instances, the major operating
mechanism seems to be simply a physical transfer of
parts of the surrounding sea floor assemblages into
the colonization trays, leaving no time for oppor-
tunistic, pioneer species to flourish. This nearly in-
stantaneous dispersal mechanism probably has im-
portant implications for maintenance of the homo-
geneity of faunal compositions in such areas. But
what mechanisms operate in calm, physically less
disturbed areas Že.g., fjords and the deep sea.?
Colonization experiments have recently been car-
ried out at 55–63 m water depth in different, well
oxygenated, parts of the Oslo Fjord, Norway, to test
macro- and meiofaunal responses to various concen-
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 175

open connection to the surrounding sediments. This

would have facilitated direct invasion by neighbour-
ing, free living organisms.
At two sites Žareas B and C., the numerical
density was significantly lower in the colonization
boxes compared to the ambient sea floor assem-
blages, whereas the difference was not significant at
the third site Žarea 1; Fig. 1.. Furthermore, the
number of species was significantly lower and Stain-
forthia fusiformis was 23–40% more abundant in the
colonization boxes compared to the ambient fauna
ŽFigs. 2 and 3.. This shows that the small, infaunal,
opportunistic S. fusiformis was the most successful
colonizer and that 6–7.5 months were not enough, in
this low energy environment, for recovery of the
community structures to ambient levels. Conse-
Fig. 1. Numerical density Žmean values and SD for replicates. of quently, it seems that different dispersal and colo-
live Žstained. benthic foraminifera in ambient seabed sediments nization patterns operate in high and low energy
and colonization boxes Žsurface 0–5 cm. from three stations in the
environments, and that only the latter opens for
Oslo Fjord, Norway.
opportunistic, pioneer species to flourish. In area C,
living tubular foraminifera, primarily Rhabdammina,
trations of heavy metals ŽAlve and Olsgard, in press; were abundant Žreplicates: 5.6, 10.4, and 15.5 stained
unpublished data.. As a spin-off from these experi- tubesr10 cm2 . on the ambient sea floor, whereas no
ments, information has also been obtained concern- living tubular individuals were present in the colo-
ing colonization patterns of benthic foraminifera Ž) nization boxes indicating that tubular taxa are late
63 mm fraction.. Bottom current velocities in these immigrants. Their large size and heavy tests must
areas are generally around 2 cmrs but higher values
can occur, particularly in connection with deepwater
renewals ŽEyvind Aas, pers. comm., 1998.. Data
presented here represent analyses of three replicate
cores Žsurface 0–5 cm. collected from colonization
boxes Žcore diameter 57 mm. and three from the
adjacent sea floor Žcore diameter 69 mm. at each of
three different stations. The colonization devices
consisted of 1.5 = 1.5 m aluminium frames, each
containing 16 propene plastic boxes Ž29 = 32 = 13
cm height.. The three Žof the 16. boxes, from each
frame, which were sampled for the foraminiferal
analyses presented here were filled Žto 2 cm below
the brim. with frozen, defaunated, ambient sediments
Žthe other boxes had ambient or contaminated sedi-
ments and will not be discussed here.. The frames
were left on the sea floor to colonize for 6 Žareas B
and C. and 7.5 Žarea 1. months. This experimental
design isolates the colonization sediments from the
Fig. 2. Number of live Žstained. species Žmean values and SD for
surrounding sediments. It therefore represents a closer replicates. of benthic foraminifera in ambient seabed sediments
analog to larger scale disturbances followed by colo- and colonization boxes Žsurface 0–5 cm. from three stations in the
nization of azoic sediments than if there had been an Oslo Fjord, Norway.
176 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
Fig. 3. Relative abundance Žmean values and SD for replicates. of
live Žstained. Stainforthia fusiformis in ambient seabed sediments
and colonization boxes Žsurface 0–5 cm. from three stations in the
Oslo Fjord, Norway.
require a very high shear velocity, compared to most
benthic foraminifera, in order to get suspended so
they probably disperse at a very early life stage.
Their absence in the colonization boxes may indicate
that they have a slow turnover rate and either had not
reproduced or at least not successfully settled into
the boxes.
An even more delayed colonization and recovery
pattern was recorded in the Baltic Sea experiment
ŽWefer and Richter, 1976. where living individuals
were found only occasionally during the first 8
months, and the faunal density did not approach that
of the surrounding environment until 13 months after
installation. It was speculated that this delay might
have been due to an absence of strong water move-
ments.
Compared to what was recorded in the open
coastal shallow water and shelf studies, the coloniza-
tion in these comparably tranquil, partly landlocked
areas, showed a pronounced time lag with recovery
times of more than 8 months. The strong dominance
of one opportunistic species in the low energy, as
opposed to the high energy environments, probably
represent the low equatability, low species diversity,
and high abundance pioneer assemblages characteris-
tic of metazoan invertebrate colonization.
In the deep sea, benthic macrofauna has been
shown to have a much slower colonization rate
compared to shallow water habitats Že.g., Grassle
and Morse-Porteous, 1987, and references therein..
However, more recent investigations suggest that
some events in the deep sea may occur more quickly
than once thought, particularly in response to differ-
ent kinds of food enrichment Že.g., Snelgrove et al.,
1994, 1996.. For benthic foraminifera, it is difficult
to make generalizations like this because their colo-
nization rates seem to a large extent to depend on the
hydraulic regime in the source area and on the speed
of the transporting medium but there is some evi-
dence that foraminifera colonize more rapidly than
macrofaunal invertebrates. In a colonization experi-
ment perfomed in the Panama Basin at 3900 m,
Kaminski et al. Ž1988. reported that, if the tubular
Dendrophrya arborescens is excluded from the cal-
culations, 9 months may be sufficient time for an
agglutinated foraminiferal fauna Ž) 297 mm. to re-
cover to background levels of abundance and diver-
sity after a disturbance Žthe macrofauna did not
recover.. The absence of tubular forms in the Panama
Basin colonization trays is in good agreement with
the above mentioned findings in Oslo Fjord, Nor-
way. In Sagami Bay, Japan, most species of the
ambient community recolonized defaunated ambient
mud after 1 year but here the assemblage sizes were
about 50 times smaller in the culture bottles com-
pared to those of the surrounding sea floor ŽKitazato,
1995..
3.2. Azoic sediments with characteristics beyond the
‘normal’ marine range
In addition to the recruitment rate of individuals
to the new substrate, the environmental character-
istics of the new habitat Že.g., nutrient flux, geo-
chemical composition. plays an important role for
the faunal recovery and development. Examples are
instances where there is an initial lack of food, such
as habitats emerging following volcanic ash deposi-
tion, and initially geochemically hostile sediments,
such as those emerging following dumping of pol-
luted sediments or reoxygenation of previously
anoxic areas.
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185 177

3.2.1. Initial lack of food
Colonization following the 1991 eruption of Mt.
Pinatubo on the Philippines, which caused a 2–6 cm
thick ash layer to be deposited in the South China
Sea Žcovering an area of at least 36,000 km2 ., has
been shown to take many years ŽHess and Kuhnt,
1996, 1997. and is still not complete. Investigations
3 and 5 years after the eruption showed that the
benthic foraminiferal community was still far from
recovery to background levels. However, the sedi-
ment prior to eruption was hemipelagic mud while
after the eruption it was volcanic ash so it should not
be expected that the post-eruption assemblage would
be the same. After 3 years, the recolonization fauna
observed in the top centimeter of ash was composed
entirely of infaunal forms, such as two species of
Reophax and one miliolid. Tubular forms, which had
been abundant before the eruption, were not present.
Five years after the eruption, the species diversity
had increased compared to 1994 Ž3 years. and the
first epifaunal saccorhizids and rhizamminids ŽFig.
4. were recorded ŽHess and Kuhnt, 1997.. Textularia
sp. was rarely present in the pre-eruption sediments
but made up a large portion of the dead assemblage
above the ash after 3 years. It was speculated that
this skinny Textularia and Reophax dentaliniformis,
which showed the largest abundances in the dead
surface assemblages, represented the pioneer stage of
a colonization succession and that they had been
outcompeted by later immigrants. Two species of
Reophax were the most successful colonizers here,
as was also the case in the Panama Basin experiment
ŽKaminski et al., 1988..
Surface samples Žnon-quantitative data. collected
during five austral summers following the 1970 vol-
canic eruption Žeruptions also in 1967 and 1969. on
Deception Island, Antarctica, also showed a slow
recovery of the benthic foraminiferal assemblages
ŽFinger and Lipps, 1981.. The assemblages recorded
in the caldera in 1972 were sparse, by 1973 the fauna
had undergone substantial enrichment and in 1974–
1976 the samples were rich in foraminifera, suggest-
ing that there was a considerable progressive, but
slow, repopulation of the devastated benthos.
Some of the field experiments which have in-
volved colonization of pure sand or glass beads seem

Fig. 4. Individuals of Rhizammina colonizing the areas ŽSouth China Sea. affected by the ashfall of the 1991 Mt Pinatubo volcanic eruption.
Photo taken by Michael Kaminski in June, 1998, during the RrV Sonne Cruise 132, station 11. Width of pictures 8 cm.
178 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
to illustrate that initially nutrient-deficient sediments
show a slowly recovering faunal development. In a
colonization experiment Žsand from a sand pit., con-
ducted during 6 weeks at 1 m water depth in the
Indian River, Florida, weekly sampling showed that
the densities of all taxa were significantly lower after
one and two weeks but that the densities ‘stabilized’
after 3 weeks and the colonization occurred in the
same rank order as the ambient fauna ŽBuzas, 1993..
It is not know whether or not reproduction occurred
in the colonizing sediments. This colonization pat-
tern resembles that described previously ŽSection
3.1. for high energy environemts with a physical
transfer of parts of the surrounding sea floor assem-
blages into the new habitat, i.e., no primarily biologi-
cally driven succession would be expected but rather
a successive introduction of whichever speciesrindi-
viduals were available for transport during the inves-
tigation period. A similar faunal development was
seen in the colonization of uncovered sand-filled
boxes in the Florida Ž125 m. experiment ŽBuzas et
al., 1989.. At greater depths ŽSagami Bay, 1445 m.,
in boxes with artificial substrates Žsilt-sized glass
beads., the densities of living individuals were only
one to two thirds of that of the open defaunated
ambient mud boxes after 1 year and the number of
species was accordingly lower whereas the diversity
ŽShannon Wiener index. was comparable ŽKitazato,
1995.. Stained individuals were recorded only in the
fluffy surface 5–10 mm which had been deposited
since the emplacement.
3.2.2. Geochemically ‘hostile’ sediments
The best way of establishing the rate of environ-
mental recovery following disturbance is to monitor
the faunal development. In some instances, the pre-
disturbed assemblage may colonize after some time
and to what degree this happens can be checked
through comparison with the fossil assemblages pre-
served in the pre-disturbed deposits. In other in-
stances, the environmental characteristics of the habi-
tat at the site have changed to such a degree that the
pre-disturbed assemblages are not the best adapted
any more. Alternatively, according to the ‘species
pool hypothesis’ of Buzas and Culver Ž1994., more-
or-less random subgroups of species will establish
themselves in the new habitat. Either way, the rate of
colonization will, to some extent, depend on the
geochemical characteristics of the new area.
Following initiation of sewage treatment in the
¨ River estuary, Sweden, it took about 1 year
Gota
before the benthic foraminifera exhibited its first
colonizers and even into the second year only Am-
monia beccarii and three allogromiid species were
recorded, whereas nematodes and larval forms of
macroinvertebrates were present already during the
initial phase of the recovery process ŽCato et al.,
1980.. A faster colonization was recorded at an
offshore dump site used for disposal of dredge spoil
rich in organic material, Chaleur Bay, Canada, where
Eggerella adÕena and Ammotium cassis had repopu-
lated most of the substrate after 1 month ŽSchafer,
1982.. Two years later, all localities were repopu-
lated, and the number of species and the standing
crop had increased from 13 to 37 and 3 to 27
individualsrcm3 , respectively.
In the geological record, there are numerous ex-
amples where colonization has occurred on sub-
strates which were previously anoxic. Such habitats
have completely different chemical and physical
properties compared to well-oxygenated sediments
and this probably has an impact on the colonization
patterns. For example, in Drammensfjord, Norway, it
took more than 1 year to colonize sediments which
had experienced over 5 years of anoxia ŽAlve,
1995b.. The opportunistic species Stainforthia
fusiformis was by far the most abundant and suc-
cessful colonizer of the previously anoxic habitats
both there and in Frierfjord, Norway ŽAlve, 1994..
On the other hand, only sparse living individuals of
Bulimina marginata, which is considered to be a
species tolerant of low oxygen Že.g., Rohling et al.,
1993., were present during the initial colonization
phase. The fact that B. marginata made up 45% of
the stained assemblage at this site 4 years later
ŽBernhard and Alve, 1996. shows that faunal recov-
ery after prolonged anoxia may take several years.
Furthermore, it suggests that B. marginata is a
slower colonizer of previously anoxic sediments than
S. fusiformis.
3.3. Discussion of colonization patterns
One of the fundamental aspects to consider for
understanding the processes controlling the coloniza-
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
tion pattern is the post-settlement responses by the
recruiting individuals. How do they respond when
introduced into a new habitat? If the settling environ-
ment is suitable for the species maintenance, do all
introduced species start reproducing soon after they
have settled, or do they wait until the season of the
year when most individuals normally reproduce? The
reproduction patterns in benthic foraminifera are very
complex and even though the life cycle is known for
about 50 species ŽLee et al., 1991., there is still a
poor understanding of how often they reproduce and
what actually triggers reproduction. Many seasonal
studies suggest that reproduction occurs once or a
few times a year Že.g., Lutze and Wefer, 1980;
Erskian and Lipps, 1987; Cearreta, 1988; Kitazato
and Matsushita, 1996.. Wefer Ž1976. suggested that
Elphidium excaÕatum had a growth period of about 3
months between each reproductive cycle. Boltovskoy
and Lena Ž1969. suggested that the life cycle of
small species probably is as short as 1 month, but
extremely rapid reproduction rates, just a few hours
after the gamonts leave the reproductive cyst, have
been reported in very small taxa ŽPawlowski and
Lee, 1992..
Most seasonal studies show that, even for species
which seem to go through one or several reproduc-
tion peaks per year, at least some juveniles are
present throughout the year, indicating that they
reproduce continuously Že.g., Nonion depressulus,
Murray, 1983; Ammonia beccarii, Basson and Mur-
ray, 1995; Stainforthia fusiformis, as Fursenkoina
fusiformis, Murray, 1992.. Most seasonal studies are
from shallow water areas but even though less is
known about reproduction rates in deep-sea species
Žsee Corliss and Silva, 1993., there are indications
that a similar pattern also applies to them. Some
deep-sea species have been documented to increase
their abundance within a period of 1–2 months, as a
response to increased fluxes of phytodetritus Že.g.,
Gooday, 1988; Gooday and Lambshead, 1989.,
whereas most of the metazoan meiofauna seem to
fail to exploit and utilize phytodetritus as rapidly as
the foraminifera ŽGooday et al., 1996.. On the other
hand, small individuals of common phytodetritus-ex-
ploiting species Že.g., Epistominella exigua. Ždif-
ficult to say for rarer species. are also present be-
tween the phytodetritus deposition events ŽA.J. Goo-
day, pers. commun., 1998.. This implies that even
179
though there are certain times of the year when
reproduction is particularly intense, small individuals
will always be available for transport and, theoreti-
cally, the individuals should also be able to continue
to reproduce in the new habitat, whether or not they
are introduced during their most reproductive phase.
Reproductive activity is generally thought to be
closely related to food availability. Different species
have their peak densities at different times of the
year and this may be a strategy for temporal parti-
tioning of food resources where those resources are
limited ŽCorliss and Silva, 1993.. Such partitioning
is not required in eutrophic areas where the abun-
dance of food is not a limiting factor. For example,
nutrient conditions were not considered to be one of
the controlling factors of reproduction for Trocham-
mina hadai as the phytoplankton production Ži.e.,
nutrient availability. was high throughout the year
ŽKitazato and Matsushita, 1996.. However, even in
eutrophic areas, reproduction may be seasonal if the
food supply is seasonal Žfor examples and discus-
sion, see Gooday and Rathburn, 1999 - this volume..
The species composition established in the new
area depends on the species pool in the source
areaŽs., the type and availability of food, and the
species’ ability to survive and reproduce in the new
habitat. It has been pointed out by several authors
that many benthic invertebrate larvae actively select
their site of settlement, i.e., habitat selection Že.g.,
Thorson, 1966; Butman, 1987; Woodin, 1991. and
larvae of polychaetes with sedentary adult stages
seem to be particularly good in discriminating be-
tween different substrates ŽGray, 1971.. Similar se-
lective behaviour was suggested for Glabratella or-
natissima ŽErskian and Lipps, 1987. but it is not
clear whether or not this applies to other species.
Pioneer macrobenthic colonizers are often typi-
cally epifaunal or shallow infaunal, whereas infaunal
groups which mix and aerate the sediments to greater
depths, colonize at a later stage ŽMcCall, 1977;
Rhoads et al., 1977.. For benthic foraminifera,
Schafer and Young Ž1977. suggested that free living
species with an epibenthic life style had a higher
susceptibility for redistribution than infaunal forms.
In this connection, it must be kept in mind that,
particularly in areas with variable inputs of liable
organic material, the vertical microhabitat position of
sediment-dwelling foraminifera is dynamic and do
180 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
not always show a consistent species specific depth
partitioning within the sediments Že.g., Linke and
Lutze, 1993; Jorissen et al., 1995.. However, in
shallow water habitats, species which are common
both within and below the surface 1–2 cm of sedi-
ment such as Ammonia beccarii Že.g., Goldstein and
Harben, 1993., Elphidium excaÕatum Že.g., Corliss
and Van Weering, 1993., and Fursenkoina fusiformis
Že.g., Alve and Bernhard, 1995., have been shown to
be among the first colonizers in defaunated sedi-
ments Žsee above mentioned case studies.. At a
bathyal site Ž1445 m., Kitazato Ž1995. recorded that
deep infaunal taxa were among the few species
which colonized his open, ambient sediment-filled
culture bottles. And finally, in the deep sea, infaunal
taxa such as skinny species of Textularia and some
Reophax species have been shown to be among the
first and most successful colonizers Žsee Section
3.2.1.. Consequently, typically infaunal rather than
epifaunal species seem to be among the first coloniz-
ers in environments ranging from shallow water to
the deep sea.
It seems that whether or not benthic foraminifera
follow the classic metazoan successional coloniza-
tion pattern to a great extent depends on the intensity
of the hydraulic regime in and the transit time Žwhich
in turn depends on current speed and transport dis-
tance. from the source area as well as on the envi-
ronmental characteristics Že.g., food availability. of
the new habitat ŽFig. 5.. In high energy environ-
Fig. 5. Generalized outline of dispersion of growth stages and colonization patterns of benthic foraminifera on soft-bottom substrates. The
‘transit time’ depends on the speed of the transporting medium and on the distance to source area.
ments, passive suspension and transport of various
growth stages dominate. Here the intensity of the
hydraulic regime in the source area is responsible for
which size fractions are thrown into suspension.
This, together with the transit time, controls whether
only the most easily suspended individuals or a more
representative and numerically larger fraction of the
source assemblage will be recruited. In areas with
frequent recruitment of most faunal elements of dif-
ferent growth stages, there is no time for oppor-
tunists to flourish and the recovery happens within
only a few days to weeks simply by a physical
transfer of parts of the surrounding sea floor assem-
blages into the new habitat Ži.e., the colonization
pattern is controlled by physical factors.. An excep-
tion may be if the new habitat is eutrophic and
thereby probably cause enrichment opportunists,
rather than the introduced assemblages, to flourish.
On the other hand, in low energy environments with
limited or only occasional recruitment Že.g., partly
enclosed basins., recovery may take more than one
year. When food and the physico-chemical properties
of the new habitat are not limiting factors, oppor-
tunists Že.g., Fursenkoina fusiformis. which are par-
ticularly suited for rapid exploitation of new habitats
will dominate during the initial colonization phase
Ži.e., the colonization pattern is primarily controlled
by biological factors.. The same colonization pattern
seems to apply when the transit is slow due to long
distance Žhundreds to thousands of kilometers. trans-
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
port over nutrient deficient areas Že.g., subsequent to
ash deposition.. We do not know how long the
foraminifera can survive in transit but the dispersal
and colonization may occur via stepping-stones such
as whale falls, as suggested to be the case for
hydrothermal vent and cold seep organisms ŽSmith et
al., 1989; Feldman et al., 1998. or other organically
enriched patches on the sea floor Žfor benthic
foraminiferal patterns associated with such patches,
see Gooday and Rathburn, 1999 - this volume..
4. Colonization of hard substrates
Colonization studies of hard substrates show that
foraminifera are one of the most successful coloniz-
ing groups. For instance, Abyssotherma pacifica was
the dominant taxon of all the organisms on one of
two recruitment plate arrays placed near a hydrother-
mal vent at 2600 m depth Ži.e., above CCD. in the
East Pacific for more than 3 years ŽVan Dover et al.,
¨
1988 Žas Foraminifera sp. 1.; Bronnimann et al.,
1989.. Here, it made up ) 25% of the total living
meio- and macrofauna Ži.e., 19 testsr10 cm2 .
whereas a relative abundance of only 3% was
recorded on the other, indicating a patchy coloniza-
tion pattern. However, the colonization of this species
must have taken more than 3–4 weeks, as it was not
recorded on arrays deployed for 23–26 days. Addi-
tionally, A. pacifica Žas ‘brown foraminifers’ but
species name confirmed by L.S. Mullineaux, pers.
comm., 1998. was one of the two far most numeri-
cally abundant species Žthe other was a ciliate. of all
taxa recorded on basalt colonization plates deployed
for 3 years in hydrothermal vent communities at
2505 m water depth, East Pacific Rise, with no
temperature anomaly ŽMullineaux et al., 1998.. This
shows that trochospiral agglutinated foraminifera like
A. pacifica can be significant components of the
benthic community that colonizes hard substrates in
deep-sea hydrothermal vent environments.
Manganese nodules represent a very common hard
substratum in the abyssal deep sea ŽMullineaux,
1988., and recolonization is an important topic when
considering manganese nodule mining. How long
would recovery take following disturbance? After 7
weeks of colonization at 1240 m water depth, the
181
abundance was higher on arrays exposed to low
current flow Žvelocities often - 5 cmrs. compared
to those exposed to higher flow Žvelocities up to tens
of centimeter per second., whereas no difference was
recorded after 2 years. These results show that
boundary layer flows affect both settlement and
post-settlement processes in this abyssal environ-
ment. Agglutinated foraminifera Žprimarily Trocham-
mina sp.. were the most abundant of all the coloniz-
ing organisms both after 7 weeks and 2 years which
is in accordance with the naturally occurring epifau-
nal assemblages on manganese nodules and crusts.
The fact that these attached foraminifera were abun-
dant on the manganese nodules after only 7 weeks
indicates that embryonic juvenilesŽ?. were available
in high numbers soon after deployment. Whether this
high availability is a commonly occurring phe-
nomenon or not is left for future studies to investi-
gate.
5. Conclusions
Our present state of knowledge concerning ben-
thic foraminiferal dispersal and colonization of new
habitats is based on both experimental and field
observations.
Dispersal through self locomotion and release of
gametes to the water masses may be significant over
short distances and the presence of a meroplanktonic
life stage has been reported for a few taxa only.
Consequently, these methods are not considered to
be of general importance for colonization following
large-scale disturbance. On the other hand, dispersal
through release of embryonic juveniles is considered
to be an important mechanism, and it is probably the
main mechanism for attached, tubular and larger
foraminifera, which are not easily entrained at a later
life stage. Finally, passive suspension and lateral
transport of various growth stages seems to be a
more important dispersion mechanism for benthic
foraminifera than has generally been appreciated.
This realization has an impact on our understanding
of the mode and rate of colonization of new soft
bottom habitats, which seems to be closely related to
the hydraulic regime in, and the transit time from,
the source area inhabited by species capable of colo-
nizing the new habitat. The transit time depends on
182 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
the speed of the transporting medium and the dis-
tance from the source area.
It is suggested that the speed and pattern of
colonization of soft bottom sediments are controlled
by to which extent physical or biological factors are
allowed to dominate. If high energy conditions Žbot-
tom current velocities ) about 20 cmrs. dominate
in the source area and the transit time for most
species which are likely to inhabit the new environ-
ment is short Žhours to days., colonization may
happen within days and ‘stabilization’ within days to
weeks Ždifferent from metazoan pathway.. The pro-
cess will simply be a physical transfer of parts of the
source community to the new habitat, leaving no
time for development of an opportunistic pioneer
assemblage. However, an exception is probably if
the new habitat is highly eutrophic. If the source area
is dominated by weak bottom water currents Ž- 10
cmrs., entrainment is rare and the transit time is
long Žweeks to months., allowing primarily embryos
and small individuals to be transported. This leads to
an initial establishment of a pioneer assemblage
strongly dominated by one or a few opportunistic
species Žsimilar to metazoan pathway., and recovery
can take from one to several years. The same colo-
nization pattern seems to apply when the transit is
slow due to long distance Žhundreds to thousands of
kilometers. transport over nutrient deficient areas
Že.g., subsequent to ash deposition.. We do not know
how long they can survive in transit but the dispersal
and colonization may occur via stepping-stones Žbe-
neficial temporary habitats connected to organically
enriched patches like whale carcasses..
The environmental properties of the new habitat
also have important impacts on the colonization pat-
tern. Recovery may be delayed for months or even
years due to initial lack of food Že.g., volcanic ash.
or ‘hostile’ substrate properties Že.g., recently reoxy-
genated or severely contaminated sediments.. In these
instances, the duration of the time lag depends on the
deposition rate of metabolizable organic matter and
on how quickly the sediment chemistry recovers to
an inhabitable level, respectively. Except for this
delay, recovery seems to depend on the hydraulic
regime and transit time in the same way as in more
‘normal’ marine settings.
Infaunal, small species are among the first and
most successful colonizers in new habitats from shal-
low water to the deep sea. In the deep sea, trochospi-
ral agglutinated taxa are among the most abundant
colonizers on hard substrates.
There is still a large gap in our knowledge of the
processes governing benthic foraminiferal dispersal
and colonization patterns. Considering the important
implications a closer understanding of these pro-
cesses have for paleoenvironmental interpretations,
biostratigraphic correlations, and for evaluating the
recovery rates following environmental disturbance,
this calls for intensified research. Only through a
combination of well-planned experiments and field
observations following unplanned natural ‘experi-
ments’ such as volcanic eruptions, anoxic events, or
mass-flow deposits, can we obtain a better under-
standing of the dynamics of benthic foraminiferal
colonization patterns.
Acknowledgements
I am very grateful to the organizing committee for
inviting me to present this paper at the ‘Cor Drooger
Symposium’, to Mike Kaminski for allowing me to
use one of his photos, and to John Murray, Andy
Gooday, Bert van der Zwaan, and the reviewers
Ahuva Almogi-Labin and Frans Jorissen for con-
structive comments on the manuscript.
References
Alve, E., 1994. Opportunistic features of the foraminifer Stainfor-
thia fusiformis ŽWilliamson.: evidence from Frierfjord, Nor-
way. J. Micropalaeontol. 13, 24.
Alve, E., 1995a. Benthic foraminiferal responses to estuarine
pollution: a review. J. Foramin. Res. 25, 190–203.
Alve, E., 1995b. Benthic foraminiferal distribution and recoloniza-
tion of formerly anoxic environments in Drammensfjord,
southern Norway. Mar. Micropaleontol. 25, 169–186.
Alve, E., in press. Environmental stratigraphy: a case study recon-
structing bottom water oxygen conditions in Frierfjord, Nor-
way, over the past five centuries. In: Martin, R.E. ŽEd..,
Environmental Micropaleontology. Plenum Press.
Alve, E., Bernhard, J.M., 1995. Vertical migratory response of
benthic foraminifera to controlled oxygen concentrations in an
experimental mesocosm. Mar. Ecol. Progr. Ser. 116, 137–151.
Alve, E., Murray, J.W., 1997. High benthic fertility and taphon-
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
omy of foraminifera: a case study of the Skagerrak, North Sea.
Mar. Micropaleontol. 31, 157–175.
Alve, E., Olsgard, F., in press. Benthic foraminiferal colonization
in experiments with copper contaminated sediments. J.
Foramin. Res.
Arnold, Z.M., 1964. Biological observations on the foraminifer
Spiroloculina hyalina Schulze. Univ. Calif. Publ. Zool. 72,
1–93.
Basson, P.W., Murray, J.W., 1995. Temporal variations in four
species of intertidal foraminifera, Bahrain, Arabian Gulf. Mi-
cropaleontology 41, 69–76.
Bernhard, J.M., Alve, E., 1996. Survival, ATP pool, and ultra-
structural characterization of benthic foraminifera from Dram-
mensfjord ŽNorway.: response to anoxia. Mar. Micropaleontol.
28, 5–17.
Boltovskoy, E., Lena, H., 1969. Seasonal occurrences, standing
crop and production in benthic foraminifera of Puerto De-
seado. Contr. Cushman Fdn. Foramin. Res. 20, 87–95.
Bornmalm, L., Corliss, B.H., Tedesco, K., 1997. Laboratory
observations of rates and patterns of movement of continental
margin benthic foraminifera. Mar. Micropaleontol. 29, 175–
184.
¨
Bronnimann, P., Van Dover, C.L., Whittaker, J.E., 1989.
Abyssotherma pacifica, n. gen., n. sp., a recent remaneicid
ŽForaminiferida, Remaneicacea. from the East Pacific Rise.
Micropaleontology 35, 142–149.
Brunner, C.A., Biscaye, P.E., 1997. Storm-driven transport of
foraminifers from the shelf to the upper slope, southern Mid-
dle Atlantic Bight. Cont. Shelf Res. 17, 491–508.
Butman, C.A., 1987. Larval settlement of soft-sediment inverte-
brates: the spatial scales of pattern explained by active habitat
selection and the emerging role of hydrodynamic processes.
Annu. Rev. Oceanogr. Mar. Biol. 25, 113–165.
Buzas, M.A., 1993. Colonization rate of foraminifera in the Indian
River, Florida. J. Foramin. Res. 23, 156–161.
Buzas, M.A., Culver, S.J., 1994. Species pool and dynamics of
marine paleocommunities. Science 264, 1439–1441.
Buzas, M.A., Collins, L.S., Richardson, S.L., Severin, K.P., 1989.
Experiments on predation, substrate preference, and coloniza-
tion of benthic foraminifera at the shelfbreak off the Ft. Pierce
Inlet, Florida. J. Foramin. Res. 19, 146–152.
Cato, I., Olsson, I., Rosenberg, R., 1980. Recovery and decontam-
ination of estuaries. In: Olausson, E., Cato, I. ŽEds.., Chem-
istry and Biogeochemistry of Estuaries. Wiley, Chichester, pp.
403–440.
Cearreta, A., 1988. Population dynamics of benthic foraminifera
˜ Estuary, Spain. Rev. Paleobiol.
in the Santona ´ 2, 721–724.
Chandler, G.T., Fleeger, J.W., 1983. Meiofaunal colonization of
azoic estuarine sediment in Louisiana: mechanisms of disper-
sal. J. Exp. Mar. Biol. Ecol. 69, 175–188.
Collen, J., 1996. Recolonization of reef flat by larger foraminifera,
Funafuti, Tuvalu. J. Micropalaeontol. 15, 130.
Corliss, B., Silva, K.A., 1993. Rapid growth of deep-sea benthic
foraminifera. Geology 21, 991–994.
Corliss, B.H., Van Weering, T.C.E., 1993. Living Žstained. ben-
thic foraminifera within surficial sediments of the Skagerrak.
Mar. Geol. 111, 323–335.
183
Culver, S.J., Buzas, M.A., 1998. Patterns of occurrence of benthic
foraminifera in time and space. In: Donovan, S.K., Paul,
C.R.C. ŽEds.., The Adequacy of the Fossil Record. Wiley, pp.
207–226.
DePatra, K.D., Levin, L.A., 1989. Evidence of the passive deposi-
tion of meiofauna into fiddler crab burrows. J. Exp. Mar. Biol.
Ecol. 125, 173–192.
Diaz-Castaneda, V., Frontier, S., Arenas, V., 1993. Experimental
reestablishment of a soft-bottom community-utilization of
multivariate analyses to characterize different benthic recruit-
ments. Est. Coast. Shelf Sci. 37, 387–402.
Ellison, R.L., Peck, G.E., 1983. Foraminiferal recolonization on
the continental shelf. J. Foramin. Res. 13, 231–241.
Ellison, R.L., Broome, R., Ogilvie, R., 1986. Foraminiferal re-
sponse to trace metal contamination in the Patapsco River and
Baltimore Harbour, Maryland. Mar. Pollut. Bull. 17, 419–423.
Erskian, M.G., Lipps, J.H., 1987. Population dynamics of the
foraminiferan Glabratella ornatissima ŽCushman. in northern
California. J. Foramin. Res. 17, 240–256.
Feldman, R.A., Shank, T.M., Black, M.B., Baco, A.R., Smith,
C.R., Vrijenhoek, R.C., 1998. Vestimentiferan on a Whale
Fall. Biol. Bull. 194, 116–119.
Finger, K.L., Lipps, J.H., 1981. Foraminiferal decimation and
repopulation in an active volcanic caldera, Deception Island,
Antarctica. Micropaleontology 27, 111–139.
Frankel, L., 1972. Subsurface reproduction in foraminifera. J.
Paleontol. 46, 62–65.
Goldstein, S.T., 1997. Gametogenesis and the antiquity of repro-
ductive pattern in the Foraminiferida. J. Foramin. Res. 27,
319–328.
Goldstein, S.T., Harben, E.B., 1993. Taphofacies implications of
infaunal foraminiferal assemblages in a Georgia salt marsh,
Sapelo Island. Micropaleontology 39, 53–62.
Gooday, A.J., 1988. A response by benthic foraminifera to the
deposition of phytodetritus in the deep sea. Nature ŽLondon.
332, 70–73.
Gooday, A.J., Lambshead, P.J.D., 1989. Influence of seasonally
deposited phytodetritus on benthic foraminiferal populations in
the bathyal northeast Atlantic: the species response. Mar. Ecol.
Progr. Ser. 58, 53–67.
Gooday, A.J., Rathburn, A.E., 1999. Temporal variability in
deep-sea benthic foraminifera: a review. Earth-Sci. Rev. 46,
187–212, this volume.
Gooday, A.J., Pfannkuche, O., Lambshead, P.J.D., 1996. An
apparent lack of response by metazoan meiofauna to phytode-
tritus deposition in the bathyal North-Eastern Atlantic. J. Mar.
Biol. Assoc. UK 76, 297–310.
Grassle, J.F., 1978. Diversity and population dynamics of benthic
organisms. Oceanus 21, 42–49.
Grassle, J.F., Morse-Porteous, L.S., 1987. Macrofaunal coloniza-
tion of disturbed deep-sea environments and the structure of
deep-sea benthic communities. Deep-Sea Res. 34, 1911–1950.
Gray, J.S., 1971. Factors controlling population localizations in
polychaete worms. Vie et Mil. 22, 707–721.
Grell, K.G., 1967. Sexual reproduction in protozoa. In: Chen, T.T.
ŽEd.., Research in Protozoology, Vol. 2. Pergamon, Oxford,
pp. 149–213.
184 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
Hemleben, C., Kitazato, H., 1995. Deep-sea foraminifera under
long time observation in the laboratory. Deep-sea Res. I 42,
827–832.
Hess, S., Kuhnt, W., 1996. Deep-sea benthic foraminiferal recolo-
nization of the 1991 Mt. Pinatubo ash layer in the South China
Sea. Mar. Micropaleontol. 28, 171–197.
Hess, S., Kuhnt, W., 1997. Deep sea agglutinated foraminifera as
important recolonizers of the 1991 Mt. Pinatubo ash layer in
the South China Sea. Abstract Vol., Fifth International Work-
shop on Agglutinated Foraminifera, Plymouth, UK.
Hueni, C., Monroe, J.A., Gevirtz, J., Casey, R., 1978. Distribution
of living benthonic foraminifera as indicators of oceano-
graphic processes of the South Texas outer continental shelf.
Trans. Gulf Coast Assoc. Geol. Soc. 28, 193–200.
Huhta, V., 1971. Succession in the spider communities of the
forset floor after clear-cutting and prescribed burning. Ann.
Zool. Fenn. 8, 483–542.
Jepps, M.W., 1942. Studies on Polystomella Lamarck ŽFor-
aminifera.. J. Mar. Biol. Assoc. UK 25, 607–666.
John, A.W.G., 1987. The regular occurrence of Reophax scottii
Chaster, a benthic foraminiferan, in plankton samples from the
North Sea. J. Micropalaeontol. 6, 61–63.
Jorissen, F.J., De Stigter, H.C., Widmark, J.G.V., 1995. A concep-
tual model explaining benthic foraminiferal microhabitats. Mar.
Micropaleontol. 26, 3–15.
Kaminski, M.A., Grassle, J.F., Whitlatch, R.B., 1988. Life history
and recolonization among agglutinated foraminifera in the
Panama Basin. Abh. Geol. B.-A. 41, 229–243.
Kern, J.C., Bell, S.S., 1984. Short-term temporal variation in
population structure of two harpacticoid copepods, Zausodes
arenicolus and Paradactylopodia breÕicornis. Mar. Biol. 84,
53–63.
Kitazato, H., 1988. Locomotion of some benthic foraminifera in
and on sediments. J. Foramin. Res. 18, 344–349.
Kitazato, H., 1995. Recolonization by deep-sea benthic
foraminifera: possible substrate preferences. Mar. Micropale-
ontol. 26, 65–74.
Kitazato, H., Matsushita, S., 1996. Laboratory observations of
sexual and asexual reproduction of Trochammina hadai Uchio.
Trans. Proc. Palaeontol. Soc. Jpn., N.S. 182, 454–466.
Kontrovitz, M., Snyder, S.W., Brown, R.J., 1978. A flume study
of the movement of foraminifera tests. Palaeogeogr., Palaeo-
climatol., Palaeoecol. 23, 141–150.
Koskenniemi, E., 1994. Colonization, succession and environmen-
tal conditions of the macrozoobenthos in a regulated, polyhu-
mic reservoir, western Finland. Int. Rev. Hydrobiol. 79, 521–
555.
Kukert, H., Smith, C.R., 1992. Disturbance, colonization and
succession in a deep-sea sediment community: artificial-mound
experiments. Deep-sea Res. 39, 1349–1371.
Lampitt, R.S., 1985. Evidence for the seasonal deposition of
detritus to the deep-sea floor and its subsequent resuspension.
Deep-sea Res. 32, 885–897.
Lee, J.J., Faber, W.W., Jr., Anderson, O.R. and Pawlowski, J.,
1991. Life cycles of foraminifera. In: Lee, J.J., Anderson, R.O.
ŽEds.., Biology of Foraminifera. Academic Press, London, pp.
285–334.
Lessard, R.H., 1980. Distribution patterns of intertidal and shal-
low-water foraminifera of the tropical Pacific Ocean. Cushman
Fdn. Foramin. Res., Spec. Publ. 19, 40–58.
Levin, L.A., DiBacco, C., 1995. Influence of sediment transport
on short-term recolonization by seamount infauna. Mar. Ecol.
Progr. Ser. 123, 163–175.
Lidz, L., 1966. Planktonic foraminifera in the water column of the
mainland shelf off Newport Beach, California. Limnol.
Oceanogr. 11, 257–263.
Linke, P., Lutze, G.F., 1993. Microhabitat preferences of benthic
foraminifera: a static concept or a dynamic adaptation to
optimize food acquisition? Mar. Micropaleontol. 20, 215–234.
Loeblich, A.R., Jr., Tappan, H., 1987. Foraminiferal Genera and
their Classification. Van Nostrand Reinhold, New York.
Loose, T.L., 1970. Turbulent transport of benthonic foraminifera.
Contr. Cushman Fdn. Foramin. Res. 21, 161–166.
Lutze, G.F., Wefer, G., 1980. Habitat and sexual reproduction of
Cyclorbiculina compressa ŽOrbigny., Soritidae. J. Foramin.
Res. 10, 251–260.
McCall, P.L., 1977. Community patterns and adaptive strategies
of the infaunal benthos of Long Island Sound. J. Mar. Res. 35,
221–266.
McGann, M., Sloan, D., 1996. Recent introduction of the
foraminifer Trochammina hadai Uchio into San Francisco
Bay, California, USA. Mar. Micropaleontol. 28, 1–3.
Mullineaux, L.S., 1988. The role of settlement in structuring a
hard-substratum community in the deep sea. J. Exp. Mar. Biol.
Ecol. 120, 247–261.
Mullineaux, L.S., Mills, S.W., Goldman, E., 1998. Recruitment
variation during a pilot colonization study of hydrothermal
X
vents Ž9850 N, East Pacific Rise.. Deep-sea Res. II 45, 441–
464.
Murray, J.W., 1963. Ecological experiments on foraminiferida. J.
Mar. Biol. Assoc. UK 43, 621–642.
Murray, J.W., 1965. Significance of benthic foraminiferids in
plankton samples. J. Paleontol. 39, 156–157.
Murray, J.W., 1983. Population dynamics of benthic foraminifera:
results from the Exe Estuary, England. J. Foramin. Res. 13,
1–12.
Murray, J.W., 1992. Distribution and population dynamics of
benthic foraminifera from the southern North Sea. J. Foramin.
Res. 22, 114–128.
Murray, J.W., in press. When does environmental variability
become environmental change? The proxy record of benthic
foraminifera. In: Martin, R.E. ŽEd.., Environmental Micropale-
ontology. Plenum.
Murray, J.W., Sturrock, S., Weston, J., 1982. Suspended load
transport of foraminiferal tests in a tide- and wave-swept sea.
J. Foramin. Res. 12, 51–65.
Myers, E.H., 1936. The life-cycle of Spirillina ÕiÕipara Ehren-
berg, with notes on morphogenesis, systematics, and distribu-
tion of the foraminifera. J. R. Micro. Soc. London 56, 120–146.
Palmer, M.A., 1988a. Dispersal of marine meiofauna: a review
and conceptual model explaining passive transport and active
emergence with implications for recruitment. Mar. Ecol. Progr.
Ser. 48, 81–91.
Palmer, M.A., 1988b. Epibenthic predators and marine meiofauna:
 E. AlÕe r Earth-Science ReÕiews 46 (1999) 167–185
separating predation, disturbance, and hydrodynamic effects.
Ecology 69, 1251–1259.
Palmer, M.A., Molloy, R.M., 1986. Water flow and the vertical
distribution of meiofauna: a flume experiment. Estuaries 9,
225–228.
Pawlowski, J., Lee, J.J., 1992. The life-cycle of Rotaliella ela-
tiana n. sp.: a tiny macroalgavorous foraminifer from the Gulf
of Elat. J. Protozool. 39, 131–143.
Rathburn, A.E., Corliss, B.H., 1994. The ecology of living
Žstained. deep-sea benthic foraminifera from the Sulu Sea.
Paleoceanography 9, 87–150.
Rhoads, D.C., Aller, R.C., Goldhaber, M.B., 1977. The influence
of colonizing benthos on the physical and chemical diagenesis
of estuarine seafloor. In: Coull, B. ŽEd.., Marine Benthos.
University of South Carolina, Belle Baruch Symposium, 113–
138.
Rohling, E.J., De Stigter, H.C., Vergnaud-Grazzini, C., Zaalberg,
R., 1993. Temporary repopulation by low-oxygen tolerant
benthic foraminifera within an Upper Pliocene sapropel: evi-
dence for the role of oxygen depletion in the formation of
sapropels. Mar. Micropaleontol. 22, 207–219.
Rohling, E.J., Jorissen, F.J., De Stigter, 1997. 200 Year interrup-
tion of Holocene sapropel formation in the Adriatic Sea. J.
Micropalaeontol. 16, 97–108.
¨
Ruckert-Hilbig, A., 1983. Megalospheric gamonts of Rosalina
globularis, Cymbaloporetta bulloides and Cymbaloporetta
miletti ŽForaminifera. with differently constructed swimming-
¨
apparatus. Tubinger ¨
Mikropalaontologische Mitteilungen 1,
1–69.
Santos, S.L., Simon, J.L., 1980. Marine soft-bottom cummunity
establishment following annual defaunation: larval or adult
recruitment? Mar. Ecol. Progr. Ser. 2, 235–241.
Schafer, C.T., 1976. In situ environmental response of benthonic
foraminifera. Geol. Surv. Canada, Pap. 76-1C, pp. 27–32.
Schafer, C.T., 1982. Foraminiferal colonization of an offshore
dump site in Chaleur Bay, New Brunswick, Canada. J.
Foramin. Res. 12, 317–326.
Schafer, C.T., Young, J.A., 1977. Experiments on mobility and
transportability of some nearshore benthonic foraminifera
species. Geol. Surv. Canada, Pap. 77-1C, pp. 27–31.
Schmiedl, G., Hemleben, C., Keller, J., Segl, M., 1998. Impact of
climatic changes on the benthic foraminiferal fauna in the
Ionian Sea during the last 330,000 years. Paleoceanography
13, 447–458.
Scott, D.B., Medioli, F.S., 1980. Quantitative studies of marsh
foraminiferal distributions in Nova Scotia: implications for sea
level studies. Cushman Fdn. Foramin. Res., Spec. Publ. 17,
1–58.
Severin, K.P., Lipps, J.H., 1989. The weight–volume relationship
185
of the test of AlÕeolinella quoyi: implications for the taphon-
omy of large fusiform foraminifera. Lethaia 22, 1–12.
Sherman, K.S., Coull, B.C., 1980. The response of meiofauna to
sediment disturbance. J. Exp. Mar. Biol. Ecol. 46, 59–71.
Smith, C.R., 1985. Colonization studies in the deep sea: are
results biased by experimental design? In: Gibbs, P.E. ŽEd..,
Proceedings of the 19th European Marine Biology Sympo-
sium. Cambridge Univ. Press, Cambridge, England, pp. 183–
189.
Smith, C.R., Kukert, H., Wheatcroft, R.A., Jumars, P.A., Deming,
J.W., 1989. Vent fauna on whale remains. Nature 341, 27–28.
Snelgrove, P.V.R., Grassle, J.F., Petrecca, R.F., 1994. Macrofau-
nal response to artificial enrichments and depressions in a
deep-sea habitat. J. Mar. Res. 52, 345–369.
Snelgrove, P.V.R., Butman, C.A., Grassle, J.F., 1995. Potential
flow artifacts associated with benthic experimental gear: deep-
sea mudbox examples. J. Mar. Res. 53, 821–845.
Snelgrove, P.V.R., Grassle, J.F., Petrecca, R.F., 1996. Experimen-
tal evidence for aging food patches as a factor contributing to
high deep-sea macrofaunal diversity. Limnol. Oceanogr. 41,
605–614.
Thistle, D., Weatherly, G.L., Ertman, S.C., 1995. Shelf harpacti-
coid copepods do not escape into the seabed during winter
storms. J. Mar. Res. 53, 847–863.
Thorson, G., 1966. Some factors influencing the recruitment and
establishment of marine benthic communities. Neth. J. Sea
Res. 3, 267–293.
Van Dover, C.L., Berg, C.J., Turner, R.D., 1988. Recruitment of
marine invertebrates to hard substrates at deep-sea hydrother-
mal vents on the East Pacific Rise and Galapagos spreading
center. Deep-sea Res. 35, 1833–1849.
Walker, D.A., 1976. An in situ investigation of life cycles of
benthonic midlittoral foraminifera. Maritime Sed. Spec. Publ.
1, 51–59.
Wefer, G., 1976. Environmental effects on growth rates of benthic
foraminifera Žshallow water Baltic Sea.. Maritime Sed. Spec.
Publ. 1, 39–50.
Wefer, G., Richter, W., 1976. Colonization of artificial substrates
by Foraminifera. Kieler Meeresforsch. 3, 72–75.
Weinberg, J.R., 1991. Rates of movement and sedimentary traces
of deep-sea foraminifera and Mollusca in the laboratory. J.
Foramin. Res. 21, 213–217.
Wetmore, K.L., 1988. Burrowing and sediment movement by
benthic foraminifera, as shown by time-lapse cinematography.
´
Rev. Paleobiol. 2, 921–927.
Witte, L.J., 1994. Man-made dispersal of microbenthos. Mar.
Micropaleontol. 23, 87–88.
Woodin, S.A., 1991. Recruitment of infauna: positive or negative
cues? Am. Zool. 31, 797–807.