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Symbiotic association between caprellids

(Amphipoda: Caprellidae) and the


scorpionfish Scorpaena mystes (Pisces:
Scorpaenidae)

Valentina Fernández-Del Valle, Cristian


Moisés Galván-Villa, José Luis Arreola-
Robles & Manuel Ayón-Parente

Symbiosis

ISSN 0334-5114
Volume 71
Number 1

Symbiosis (2017) 71:65-68


DOI 10.1007/s13199-016-0428-5

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Author's personal copy
Symbiosis (2017) 71:65–68
DOI 10.1007/s13199-016-0428-5

SHORT COMMUNICATION

Symbiotic association between caprellids


(Amphipoda: Caprellidae) and the scorpionfish
Scorpaena mystes (Pisces: Scorpaenidae)
Valentina Fernández-Del Valle 1 & Cristian Moisés Galván-Villa 1 &
José Luis Arreola-Robles 2 & Manuel Ayón-Parente 1

Received: 4 June 2015 / Accepted: 29 May 2016 / Published online: 6 June 2016
# Springer Science+Business Media Dordrecht 2016

Abstract Caprellid amphipods are common epibionts on a 1 Introduction


variety of invertebrates as well as vertebrates but little is
known on their life cycle in respect to their macrofaunal hosts. Caprellid amphipods, also called skeleton shrimps for their
This manuscript describes the permanent symbiotic associa- appearance, are small marine crustaceans that have a great
tion between Caprella suprapiscis amphipods and the importance for marine ecosystems (Guerra-García et al.
scorpionfish Scorpaena mystes. A total of 303 individuals of 2009). Caprellids are common epibiotic organisms that have
the caprellids including 134 males, 88 females, and 81 juve- a well-adapted morphology to attach to a variety of substrates
niles were found associated with seven out of eleven individ- and associated with other invertebrates such as echinoderms,
uals of S. mystes collected along the Bahía Chamela, Jalisco, hydroids, bryozooans, sponges, gorgonians, and crustaceans
Mexico (central Mexican Pacific Ocean). The size of the (Guerra-García 2001); also they can be found associated with
caprellids ranged from 0.8 to 9 mm total length. The number vertebrates as fishes, sea turtles, and whales (Mori and Yamato
of caprellids per fish do not depend on the size of the hosts as 1993; Aoki and Kikuchi 1995; Rowntree 1996; Galván-Villa
there is no correlation between the total length of the fishes and Ayón-Parente 2015).
and the number of caprellids. Our data suggests that the sym- The associations between caprellids and other species are
biotic association of C. suprapiscis with S. mystes is obliga- determined principally by feeding interactions or protection.
tory and ectocommensal. The caprellids are located on the Many species are able to feed directly on the substrates where
dorsal surface of the fishes, mainly in the head portion. They they cling on, mainly on hydroids and algae that also provide
likely benefit from the association by filter-feeding and scrap- protection from their predators (Vázquez-Luis et al. 2009;
ing mucous secretions or settled material from the surface of Lacerda and Masunari 2011). Available reports on associa-
their host as well as by improved dispersal. tions between fish and caprellid amphipods are very scarce.
However, caprellid amphipods are important prey and a natu-
ral dietary component for many coastal fish species because of
Keywords Crustacea . Association . Symbiosis . their high level of fatty acids, cosmopolitan distribution, fast
Ectocommensal . Pacific Ocean growth, ability to reach high population densities, and the
wide environmental tolerance (Caine 1989; Guerra-García
et al. 2004; Woods 2009). Furthermore, the present work aims
* Cristian Moisés Galván-Villa to document the symbiotic relationship between caprellid am-
gvc07765@cucba.udg.mx phipods and scorpionfishes in the Tropical Eastern Pacific.

1
Laboratorio de Ecosistemas Marinos y Acuicultura, Departamento de
Ecología, CUCBA, Universidad de Guadalajara, Camino Ing.
2 Materials and methods
Ramón Padilla Sánchez 2100, Las Agujas, 45110 Zapopan, Mexico
2
Instituto Tecnológico de Monterrey, Campus Guadalajara
This study was conducted at Bahía Chamela, Jalisco,
(ITESM-GDL), Av. General Ramón Corona 2514, Nuevo México, Mexico (central Mexican Pacific Ocean), from October
45201 Zapopan, Mexico to December 2013. Scorpionfishes Scorpaena mystes
Author's personal copy
66 V.F.-D. Valle et al.

Fig. 1 Caprellids associated to


Scorpaena mystes, a Caprellids in
upright-clinging behavior to body
surface of a scorpionfish, b Male
and female adults of Caprella
suprapiscis, c Head region of
male adult showing the anteriorly
projection, d Detail of gnathopod
2 of male adult

Jordan and Starks (1895) were collected by SCUBA 3 Results and discussions
diving at five localities along the bay (19°31–34´N;
105°05–07´W) from 5 to 7 m depth (for details see A total of 11 scorpionfishes Scorpaena mystes were examined
Galván-Villa and Ayón-Parente 2015). Fishes were col- (ranging in length from 11 to 22.5 cm). Only one species of
lected with a net bag, posteriorly placed in a bucket caprellid amphipod (Caprella suprapiscis Galván-Villa and
with seawater. All fishes were transported to the labo- Ayón-Parente 2015) recently described was found associated
ratory of the UNAM-Chamela station and maintained with S. mystes. A total of 303 caprellids were collected includ-
alive for 24 h for examination of caprellids and taking ing 134 males, 88 females (65 non-ovigerous and 23
measures until returning to the sea. Caprellids were col- ovigerous), and 81 juveniles. The caprellids were found main-
lected directly with forceps and preserved in 70 % eth- ly around the eyes and head of the host, less occurrence on
anol. Identification and counting were made later in the posterior body portion were found (Fig. 1a). Relationship be-
Laboratory of Marine Ecosystems and Aquaculture tween total length of fishes and number of caprellids was not
(LEMA in spanish), Universidad de Guadalajara found (r2 = 0.07, n = 13, p > 0.05). Only seven fishes had
(UdeG), in Zapopan, Jalisco, Mexico. caprellids (54 % prevalence) and the abundance of caprellids
Caprellids were separated in males, females, and juve- per fish ranged from one to 109 individuals on a single fish
niles. Males were identified by the absence of the brood (mean 43 ± 51, n = 7) (Fig. 2a).
pouches and the distal position of gnathopod 2. Females In general, females were smaller than males and not all
were identified by the presence of brood pouches and the females were mature but a high proportion were breeding
anterior position of gnathopod 2 on pereonite 2. Other during sampling months (October–December). The overall
smaller individuals lacking those distinct sexual characters sex ratio for caprellids was 1:0.65 (male/female). Total num-
were defined as juveniles (Guerra-García et al. 2000). Each ber of males was significantly higher than females (χ2 = 9.53,
individual was measured from the anterior margin of the n = 7, p < 0.05). In almost all of the fishes, more males oc-
head to the posterior margin of the telson (total body curred than females with exception of one. The proportion of
length) using a stereomicroscope with a graduated eyepiece ovigerous females to total females was significantly smaller
(8x and 32x). The relationship between the density of than that for non-ovigerous females (χ2 = 20.04, n = 7,
caprellids and total length of scorpionfishes was determined p < 0.05). The sizes of the males ranged from 2.6 to 9 mm
by applying a linear regression analysis. The sex ratio of total body length (mean 4.7 ± 1.4), females from 2.6 to 7 mm
the caprellid population was estimated and the significance (mean 4.5 ± 1.0), and juveniles from 0.8 to 3.2 mm (mean
in deviations were assessed by the Chi-square test. 2.3 ± 0.5) (Fig. 2b).
Author's personal copy
Symbiotic association between caprellids and scorpionfishes 67

dispersion behaviour where the caprellid Caprella grahami


readily crossed from one starfish Asterias forbesi to another
one upon contact.
Most of the caprellids were found clinging around the eyes
and head of the scorpionfish, attaching with the anterior
appendages and prehensile pereiopods, adaptations that
provide a powerful hold to the host. Takeuchi and Hirano
(1995) described that Bupright^ and Bparallel^ are the two prin-
cipal postures seen in the genus Caprella, the first group in-
habits environments with little wave action grasping the sub-
stratum with pereiopods V-VII, while the Bparallel^ group at-
tach to macroalgae exposed to strong wave action using
gnathopod I and pereiopods V-VII with the body somites
straight to the substratum. In situ observations indicate that
C. suprapiscis use the Bupright^ attachment, which facilitates
the filter-feeding mechanism waiting for food particles to be
caught with antennae and gnathopod setae. They could also
feed on material that settles on their hosts or by scraping mu-
cous secretions off the surface of the fish as it has been reported
for caprellid-starfish associations (Patton 1968). Further studies
on gut contents and feeding behaviour of these species are still
needed to reveal further clues. Another advantage for these
caprellids is protection due to behaviour of the host, venomous
fin-spines for self-defense of the fish that reduce possibilities of
predation, and the mimicry with the skin flaps, where the
caprellids match the background with a similar color pattern
and get protection by being less visible to predators (see
Fig. 1a–d).
The presence of C. suprapiscis in most of the
Fig. 2 Frequency of caprellids, a Variation in abundance of males, scorpionfishes shows that this species is well associated to
females, and juveniles of Caprella suprapiscis for each scorpionfish, b them. Visual records in other locations suggest the association
Sex ratio in total number of individuals of Caprella suprapiscis collected of caprellid amphipods with S. mystes throughout the Pacific
over all scorpionfish. Lines represents the mean body size and standard
coast of Mexico and the Gulf of California (Arreola-Robles
deviation of each group
pers. obs.). However, confirmation of the caprellid species
associated to scorpionfishes in other localities is wanting and
According to Vader’s (1983) associations types between it is probable that C. suprapiscis occurs along the distribution
caprellids and sea anemones observations suggest that of S. mystes in the Tropical Eastern Pacific.
C. suprapiscis is an obligatory ectocommensal. This type of
association was designated because on some of the Acknowledgments Thanks to Eduardo Ríos for field support, to Jorge
scorpionfishes C. suprapiscis were found at all stages of de- Vega from UNAM-Chamela station for facilities, Diego Moreno for his
help during fieldwork, Alberto Fernández for English revision, and Wim
velopment, which indicates that they live on the host their
Vader for providing us bibliographic material. Also thanks to Harald
entire life cycle. Nonetheless, it seems that the presence or Gruber and one anonymous reviewer for helpful comments. Financial
absence of caprellids has no effect on the scorpionfish, and it support for the sampling process through the project JF023-CONABIO
does not offer any evident benefits or disturbances. and P3E2013-UdeG.
Due to the capacity to move off the scorpionfishes, it is
possible that caprellids are using it as a mean of transportation
to facilitate the finding of food and for dispersion. These ben- References
efits are described between caprellids and some echinoderms
(Patton 1968; Volbehr and Rachor 1997; Wirtz 1998; Lindsay Aoki M, Kikuchi T (1995) Notes on Caprella andreae Mayer, 1890
and Takeuchi 2008). Dispersion of caprellids among (Crustacea, Amphipoda) from the caparace of loggerhead sea turtles
in the East China Sea and in Kyushu, Japan. Proc Jap Soc Syst Zool
scorpionfish individuals probably takes place during the re- 53:54–61
productive period of fish when male and female mate Caine EA (1989) Caprellid amphipod behavior and predatory strikes by
(Galván-Villa pers. obs.). Patton (1968) described similar fish. J Exp Mar Biol Ecol 126:173–180
Author's personal copy
68 V.F.-D. Valle et al.

Galván-Villa CM, Ayón-Parente M (2015) Caprella suprapiscis sp. nov. Antennarius striatus (Shaw & Nodder, 1794). Nanki-Seibutu 35:
(Crustacea: Amphipoda: Caprellidae) from the Pacific coast of 41–46
Mexico. Zootaxa 3956(4):569–578 Patton WK (1968) Feeding habits, behavior, and host specificity of
Guerra-García JM (2001) Habitat use of the Caprellidea (Crustacea: Caprella grahami, an amphipod commensal with the starfish
Amphipoda) from Ceuta, North Africa. Ophelia 55(1):27–38 Asterias forbesi. Biol Bull 134:148–153
Guerra-García JM, Corzo J, García-Asencio I, García-Gomez JC (2000) Rowntree VJ (1996) Feeding, distribution, and reproductive behavior of
Seasonal fluctuations of Phtisica marina slabber (Crustacea: cyamids (Crustacea: Amphipoda) living on humpback and right
Amphipoda: Caprellidea) in estuarine zone of Southwest Spain. whales. Can J Zool 74:103–109
Pol Arch Hydrobiol 47:527–531 Takeuchi I, Hirano R (1995) Clinging behavior of the epifaunal caprellids
Guerra-García JM, Martínez-Pita I, Luisa-Pita M (2004) Fatty acid com- (Amphipoda) inhabiting the Sargassum zone on the Pacific coast of
position of the Caprellidae (Crustacea: Amphipoda) from the strait Japan, with its evolutionary implications. J Crust Biol 15(3):481–
of Gibraltar. Sci Mar 68(4):501–510 492
Guerra-García JM, Sánchez JA, Macarena R (2009) Distributional and Vader W (1983) Associations between amphipods (Crustancea:
ecological patterns of caprellids (Crustacea: Amphipoda) associated Amphipoda) and sea anemones (Anthozoa, Actiniaria). In: Lowry
with the seaweed Stypocaulon scoparium in the Iberian peninsula. JK (ed) Papers from the conference on the biology and evolution of
Mar Biodiv Rec 2:1–8 crustacean. Australian Museum Memoir, Australia, pp. 141–153
Jordan DS, Stark EC (1895) 195. Scorpaena mystes. In: Jordan DS (ed)
Vázquez-Luis M, Guerra-García JM, Sanchez-Jerez P, Bayle-Sempere JT
The fishes of Sinaloa, Proceedings of the California Academy of
(2009) Caprellid assemblages (Crustacea: Amphipoda) in shallow
Sciences (Series 2), vol 5, pp 491–492
waters invaded by Caulerpa racemosa Var. cylindracea from south-
Lacerda MB, Masunari S (2011) Substrate selection of the caprellid
eastern Spain. Helgol Mar Res 63:107–117
Caprella dilatata (Crustacea, Amphipoda). Rev Biol Mar Ocean
46(2):207–218 Volbehr U, Rachor E (1997) The association between the caprellid
Lindsay DJ, Takeuchi I (2008) Associations in the deep-sea Pariambus typicus Krøyer (Crustacea, Amphipoda) and ophiuroids.
benthopelagic zone: the amphipod crustacean Caprella subtilis Hydrobiologia 355:71–76
(Amphipoda: Caprellidae) and the holothurian Ellipinion kumai Wirtz P (1998) Caprellid (Crustacea)-holothurian (Echinodermata) asso-
(Elasipodidad: Elpidiidae). Sci Mar 72(3):519–526 ciations in the Azores. Arquipelago 16:53–55
Mori A, Yamato S (1993) Caprella simia Mayer, 1903 (Crustacea: Woods C (2009) Caprellid amphipods: an overlooked marine finfish
Amphipoda) collected from the body surface of a frogfish aquaculture resource? Aquaculture 289(3):199–211

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