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Mar Biol (2009) 156:1881–1890 DOI 10.1007/s00227-009-1220-3

ORIGINAL PAPER

What do caprellids (Crustacea: Amphipoda) feed on? José Manuel Guerra-García · José Manuel Tierno de Figueroa

Received: 26 January 2009 / Accepted: 5 May 2009 / Published online: 24 May 2009 © Springer-Verlag 2009

Abstract The present study represents the Wrst comprehensive work dealing with the dietary analysis of Caprellidea. We studied 743 specimens of 31 genera and 62 species from all around the world. Analysis of digestive contents revealed that caprellids are mainly detritivores (detritus represented the 86% of the caprellid diet), but a small percentage of species, those lacking molars belonging to the Phtisicinae, can be considered as obligate predators and feed mainly on small crustaceans (copepods and other amphipods) and polychaetes. The contribution of sponges, hydroids, macroalgae, diatoms and dinoXagellates to the caprellid diet was very low (80%) for both species, based on the gut examination of abundant material (79 specimens of C. penantis and 13 of C. mutica). Diatoms have been frequently found in the gut of diVerent species studied with the methodology proposed by Bello and Cabrera (1999) (López-Rodríguez and Tierno de Figueroa 2008). In fact, diatoms suppose one of main components of the diet of many species (Tierno de Figueroa et al. 2006; López-Rodríguez et al. 2009a), even of some species previously though to be predators, such as the insects Isoperla curtata or Guadlagenus franzi (López-Rodríguez et al. 2009b). Thus, if in our study we have not found diatoms frequently this is not a consequence of the employed method but of their real absence or low presence. Our study showed that crustaceans, mainly amphipods, represent the second component in abundance percentage after detritus. Although most of the amphipod components (basically rests of mouthparts and broken gnathopods) belonged to gammarideans, some of them could probably belong to caprellid themselves. In fact, where food is inadequate, caprellid may even display cannibalism (Takeuchi 1998; Guerra-García et al. 2002). In the species Caprella equilibra, C. liparotensis and Pseudoprotella phasma digestive contents also included a signiWcant contribution of hydroids. Caprellids clinging on hydroids have been reported as cleptocommensalists, exploiting the food collected by polyps, mainly plankton (see Camillo et al. 2008). However, this study shows that some caprellids can feed on the hydroids themselves. On the other hand, caprellids have been also reported as one of the most important prey captured by polyps of some hydroids (Genzano 2005) (hydroids were generally assumed to be passive predators that capture zooplanktonic prey by means of nematocysts on tentacles). Interestingly, we found a great amount of demosponge spicules in two species, Caprella dubia and Paracaprella tenuis, indicating an active feeding on sponges by these two species. Although caprellids have been reported living on sponges (Guerra-García 2001), to our knowledge, this is the Wrst evidence of caprellids feeding on sponges. On the other

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hand, we did not Wnd gorgonian sclerites in any of the studied species, while Scinto et al. (2008) found numerous sclerites in the stomach contents of Metaprotella sandalensis. Digestive contents and mouthparts morphology Traditionally, feeding mechanisms of caprellids have been considered a function of the mouthpart morphology. Caine (1974, 1977) considered Wve feeding strategies (Wlter-feeding, scraping, browsing, scavenging and predation). Based on the presence/absence of swimming setae, mandibular palp and molar process he established six categories (Table 2) and indicated that species in the Category 3 (with mandibular palp and molar process but without swimming setae) were predators, in category 4 (with molar and swimming setae but without mandibular palp) Wlter feeders and scrapers, and in category 5 (with molar process but without swimming setae nor mandibular palp) without feeding preferences. However, the present study revealed that a predatory way of life is directly related with the absence of molar process. Apart from this, the present study did not show other relationships between digestive contents and other features of the mouthparts structure. Caine (1974) also pointed out that the relative length of the Wrst antennae was a reXection of the emphasis on predatory habits. Nevertheless, in our study, species belonging to the genera Protella, Proaeginina, Parvipalpus, Aeginina, Aeginella, which are provided with very long Wrst antennae, fed exclusively on detritus. The mandibular palp is not necessarily a feeding structure and its gradual loss may represent a trend within the caprellids away from a shift from a predatory type of existence to a Wltering one, so that the presence of a mandibular palp would be indicative of a form morphologically more similar to the ancestral stock and not a necessity for a predatory existence (Caine 1974). In fact, in the present work, the presence/absence of mandibular palp was not related with the digestive contents. Two functions have been attributed to swimming setae: locomotion and particle capture during Wlter-feeding; Caine (1979) reported that, although the importance of them to the ability to swim is not absolute, caprellids with swimming setae gathered food primarily by Wltration. According to this author, only a few genera of caprellids have swimming setae (Caprella, Heterocaprella, Metacaprella and Tritella). Metacaprella has been recently considered a synonymous of Caprella (Mori 1999) but we could also add the genera Caprogammarus and Chaka as having swimming setae. Curiously, the genus Caprella, one of the Wve genera provided with swimming setae, includes around 50% (190 species of 400) of described species so far in the Caprellidea excluding the whale lice Cyamidea (GuerraGarcía unpublished). Furthermore, we found Caprella specimens in most of the categories separated by the cluster

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(detritivores, detritivores/predators and opportunistic). Indeed, all the species included in the opportunistic subgroup, except for Phtisica marina, belong to the genus Caprella. Consequently, although the presence of swimming setae cannot be assigned exclusively to a particular kind of digestive contents, it seems that the presence of these setae opens a feeding niche for caprellids and this could lead to the species explosion. Probably, swimming setae have some impact on the species proliferation of the genus Caprella (Caine 1979; present study). Caine (1976) described in detail the cleansing mechanisms in caprellids. Behaviorally, he found that Wlter feeders groom and feed approximately as much as predators, but Wlter feeders cleanse their entire body, whereas predators primarily cleanse only both pairs of antennae. The possibility that Wlter-feeding was evolutionarily derived from cleaning activities is proposed by this author. Phylogenetic implications All the species forming the group of obligate predators (see cluster of Fig. 1), characterized by absence of molar process, belong to the subfamily Phtisicinae (according to the classiWcation of Myers and Lowry 2003). This could have phylogenetic implications: a line formed by the Pthisicinae would have evolved from ancestors with predatory habits, while the line Caprogammaridae-Caprellinae would have derived from ancestors that fed on material suspended in the water column. In fact, Myers and Lowry (2003) established a new phylogeny and high-level classiWcation for the suborder Corophiidea, based on the hypothesis of the evolution of diVerent feeding strategies. According to these authors, members of the Corophiida infraorder are derived from bottom-feeding detritivores, whereas members of the Caprellida infraorder are derived from Wlter-feeding ancestors. However, it would be possible that not all the members of Caprellidae derived from Wlter-feeding ancestors, and that a diVerent line of caprellids lacking molar process and having six-articulate pereopods 3 and 4 derived from a carnivorous ancestor that used these pereopods to manipulate the prey. This would support the hypothesis of polyphyly for the Caprellidea. Caprellids have evolved fascinating morphological characters distinct from those of other malacostracan crustaceans (Ito et al. 2008). It remains to be a mystery how and why Caprellidea developed such unique morphologies. Moreover, Caprogammaridae and Phtisicidae add further mystery, because Caprogammaridae have a Wve-segmented abdomen with appendages and Phtisicidae have six-articulated pereopods 3 and 4. Based on these morphological distinctions, Takeuchi (1993) suggested that the taxon Caprellidea may be a polyphyletic group. Laubitz (1993) also proposed two distinct evolutionary lines based on the mouthpart structure and regarded

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Phtisicidae as being derived from a diVerent evolutionary process than that of the corophioid–caprogammarid–caprellid lineage. However, molecular analyses conducted by Ito et al. (2008) based on the 18S rRNA gene strongly support the phylogenetic aYnity of the Wve caprellid families including Phtisicidae and, consequently, indicated the monophyly of Caprellidea. Future molecular, morphological and behavioral studies are necessary to clarify if the taxon Caprellidea is a monophyletic group or not. Acknowledgments Financial support of this work was provided by the Ministerio de Educación y Ciencia (Project CGL2007-60044/ BOS) co-Wnanced by FEDER funds, and by the Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía (Project P07-RNM02524). Special thanks to Dr. Manuel Jesús López-Rodríguez for his help during the processing of the samples and for the English revision of the manuscript.

Appendix List of the 62 caprellid species used for the study. Whenever possible, data of substrate, depth, location and date of collection are provided (for some species some of these data were not available). Aeginella spinosa Boeck, 1861: Sand, 160 m, Island, 12/ 07/1993. Aeginina longicornis (Kroyer, 1843): Silty sand, 489 m, Island, 15/07/1993. Caprella acanthifera Leach, 1814: Seaweeds intertidal pools, Tarifa (Spain), 1991 and 2008; seaweed Cystoseira usneoides, 5–10 m, Ceuta (Spain), 1999. Caprella acanthogaster Mayer, 1890: Filamentous algae, 2–6 m, Tasmania (Australia), 16/04/1993. Caprella acanthopoda Guiler, 1954: Victoria (Australia). Caprella andreae Mayer, 1890: caparace turtle of Caretta caretta, Algeciras Bay, Cádiz (Spain), May 1999. Caprella californica Stimpson, 1856: Vancouver (Canada). Caprella cf dubia Hansen, 1887: Buoys and ropes, BamWeld (Canada), March 2005. Caprella danilevskii Czerniavskii, 1868: Hydroid Cnidoscyphus imarginatus, 0–10 m, Bahía Concha (Colombia), 08/07/1985; seaweeds Cystoseira usneoides, C. tamariscifolia and Asparagopsis armata, 0–10 m, Ceuta and Alboran Island (Spain), 1999; seaweed Gracilaria verrucosa, intertidal, Mindelo (Portugal); Caprella decipiens Mayer, 1890: Sargassum spp., 0–10 m, Japan, April 2007. Caprella dilatata Kroyer, 1843: Mussels, intertidal, Uruguay, 2005; Fish farms, 0–2 m, Alicante (Spain), 05/12/ 2006; buoys, 0–1 m, Algeciras and Huelva (Spain), 2004. Caprella equilibra Say, 1818: Seaweeds Gelidium spp., 0–5 m, Huelva (Spain), January 1999; buoys, Japan, October 1999; hydroids under boulders, Coquimbo (Chile),

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14/12/2000; on farms of Cassostrea gigas, 15 m, Cádiz (Spain), 12/08/2007. Caprella erethizon Mayer, 1901: Hydroids, 30–40 m, Ceuta (Spain), August 1999. Caprella grandimana (Mayer, 1882): Seaweed Corallina elongata, intertidal, Tarifa (Spain), 2008. Caprella hirsuta Mayer, 1890: Seaweeds Jania spp., Cystoseira tamariscifolia and Corallina elongata, 0–3 m, Cádiz, Málaga and Alborán Island (Spain), 1992, 2006 and 2008. Caprella horrida Sars, 1877: Artic, 24/08/1978. Caprella kernnerlyi (Stimpson, 1864): Vancouver (Canada). Caprella linearis (Linnaeus, 1767): On hydroids attached to the surface of seaweed Fucus serratus, Clachan Seil (Scotland), 28/5/2000. Caprella liparotensis Haller, 1879: Seaweed Cystoseira tamariscifolia and hydroids, 0–2 m, Málaga and Alborán Island (Spain), 2004 and 2006. Caprella monoceros Mayer, 1890: Sargassum spp., 0–10 m, Japan, April 2007. Caprella mutica Schurin, 1935: Pontoons out of the Helgoland harbour, Helgoland (Germany), 2006. Caprella penantis Leach, 1814: Seaweeds Gelidium spp, Asparagopsis armata, Cystoseira tamariscifolia, Pterocladia capillacea, intertidal, Cádiz, Ceuta (Spain), Castelejo (Portugal), SaW and Grottes d’Hercule (Morocco), 2006– 2008; hydroid Cnidosciphus, Bahía Concha (Colombia), 1985. Caprella sabulensis Guerra-García, Sánchez-Moyano and García-Gómez, 2001: Sediments, biodetritic, 15 m, Ceuta (Spain), 18/08/2000. Caprella santosrosai Sánchez-Moyano, Jiménez-Martín and García-Gómez, 1995: Hydroids, 30–40 m. Ceuta (Spain), August 1999. Caprella scaura Templeton, 1836: Red algae, 0–3 m, Mauritius, 24/06/2002; seagrass Heterozostera, 2 m, South Australia; ephiphytic algae, 1 m, Koronissia (Greece), 03/ 08/2002; buoys, Coquimbo (Chile), 30/10/2006 Caprella subinermis Mayer, 1890: Sargassum spp., 0– 10 m, Japan, April 2007. Caprella tuberculata Guérin, 1836: Seaweed Dilophus spiralis and hydroid Sertularella gayi, 20–30 m, Ceuta (Spain), July 1999. Caprella verrucosa Boeck, 1871: On Xoating buoys, Coquimbo (Chile), October 2006. Caprellaporema subantarctica Guerra-García, 2003: 103 m, Antipodes Islands (New Zealand), 03/01/1967. Caprellina longicollis Nicolet, 1849: Seaweeds and seagrasses, 2–3 m, Tongoy Bay (Chile), 16/12/2000. Deutella vemae (McCain and Gray, 1971): Canal Tuamapu (Chile), 15/11/2002.

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Deutella venenosa Mayer, 1890: On Xoating buoys, Coquimbo (Chile), December 2000. Dodecas tasmaniensis Guiler, 1954: 5 m, Tasmania (Australia), 17/06/1992. Hemiaegina minuta Mayer, 1890: Mixed algae, Andaman Islands (India), 31/12/1978. Liriarchus perplexus Mayer, 1912: Red algae with epiphitic hydroids and bryozoans, 24 m, King George Sound (Australia), 17/12/1983. Liropus africanus Mayer, 1920: Sediments?, Senegal. Mayerella magellanica McCain and Gray, 1971: Muddy bottoms, 50 m, Huasco (Chile), August 1996. Metaprotella mauritiensis Guerra-García, 2003: Fine sediments among soft corals of the genus Dendronephthya, 2–3 m, Cap Malheureux (Mauritius). July 2002. Metaprotella sandalensis Mayer, 1898: Seaweed Turbinaria ornata, 3 m, Baie du Tombeau (Mauritius), 9/07/ 2002. Metaproto novaehollandiae (Haswell, 1880): Sand, 5–25 m, Lizard Island (Australia), 16/10/2001. Monoliropus agilis Mayer, 1903: Persian Gulf. Orthoprotella australis (Haswell, 1880): Hydroids, 2–3 m, Bali (Indonesia), 19/05/1994. Orthoprotella pearce Guerra-García, 2006: Hydroids, 5–10 m, Lizard Island (Australia), October, 2001. Paracaprella pusilla Mayer, 1890: Hydroids, 0–1 m. Sta Marta (Colombia), 16/05/1985. Paracaprella tenuis Mayer, 1903: Intertidal, under boulders, clinging on sponges, Mauritius, 13/02/2002. Paradeutella bidentata Mayer, 1890: Data not available. Pariambus typicus (Kroyer, 1884): Gross sand, 3 m, Ceuta (Spain), August 2000. Parvipalpus onubensis Guerra-García, García-Asencio and Sánchez-Moyano, 2001: Gross sand, 20 m, Huelva (Spain), August 2000. Pedoculina garciagomezi Sánchez-Moyano, Carballo and Estacio, 1995: Seaweeds Halopteris spp., 10 m, Algeciras Bay, Cádiz (Spain), March 1992. Perotripus keablei Guerra-García, 2006: Sand, 1.5 m, Lizard Island (Australia), 30/09/1978. Phtisica marina Slabber, 1769: Seaweeds Halopteris scoparia and Zonaria sp., anthozoan Anemonia sulcata, ascidian Synoicum blochmanni and coarse sediments, 3–25 m, Ceuta (Spain), 1999 and 2000; hydroid Eudendrium armatum 35 m, Ceuta (Spain), 1999; bryozoan Bugula neritina, 2 m, May 2008. Proaeginina norvegica (Stephensen, 1931): Silty sand, 1085 m, Island, 27/08/1995. Protella similis Mayer, 1903: Hydroids, 10–12 m, Bali (Indonesia), 24/05/1994. Protellina ingolW Stephensen, 1944: Gravely sand, 746 m, Island, 13/07/1993.

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Pseudaeginella colombensis Guerra-García, Müller and Krapp-Schickel, 2006: Algae, hydroids and bryozoan, 6–10 m, Punta El Diamante (Colombia), 25/02/1986. Pseudaeginella inae Krapp-Schickel and Guerra-García, 2005, rocks, 0–0.5 m, Bali Desa Antita (Indonesia), 22/09/ 1987 Pseudocaprellina pambanensis Sundara Rej, 1927: Algae and sediment, 0–1 m, Cape Range National Park (Australia), 31/12/1983. Pseudolirius kroyeri (Haller, 1897): Fine sediments, 12 m, Algeciras Bay, Cádiz (Spain), 22/08/1991. Pseudoprotella inermis Chevreaux, 1927: Seaweed Dilophus spiralis and hydroid Sertularella gayi, 30–40 m, Ceuta (Spain), August 1999. Pseudoprotella phasma Montagu, 1804: Hydroid Aglaophenia pluma, 1 m, Huelva (Spain), 1989; seaweed Cystoseira usneoides, 5–20 m, Tarifa and Ceuta (Spain), 1999; gorgonian Paramuricea clavata and hydroids Sertularella gayi and Eudendrium armatum 35–40 m, Ceuta (Spain), 1999. Quadrisegmentum triangulum Hirayama, 1988: Gorgonians, 25 m, Lizard Island (Australia), 14/10/2001. Thorina elongata Laubitz and Mills, 1972: Silty sand, 1681 m, Island, 31/08/1995.

References Barnes RD (1968) Invertebrate zoology. WB Saunders Company, Philadelphia Bello CL, Cabrera MI (1999) Uso de la técnica microhistológica de Cavender y Hansen en la identiWcación de insectos acuáticos. Bol Entom Venez 14:77–79 Bo T, Fenoglio S, López-Rodríguez MJ, Tierno de Figueroa JM (2008) Trophic behavior of two Perlidae species (Insecta, Plecoptera) in a river in southern Spain. Int Rev Hydrobiol 93(2):167–174. doi:10.1002/iroh.200711034 Caine EA (1974) Comparative functional morphology of feeding in three species of caprellids (Crustacea: Amphipoda) from the North western Florida Gulf Coast. J Exp Mar Biol Ecol 15:81–96. doi:10.1016/0022-0981(74)90065-3 Caine EA (1976) Cleansing mechanisms of caprellid amphipods (Crustacea) from North America. Mar Behav Physiol 4:161–169. doi:10.1080/10236247609386948 Caine EA (1977) Feeding mechanisms and possible resource partitioning of the Caprellidae (Crustacea: Amphipoda) from Puget Sound, USA. Mar Biol (Berl) 42:331–336. doi:10.1007/BF00 402195 Caine EA (1979) Functions of swimming setae within caprellid amphipods (Crustacea). Biol Bull 156:169–178. doi:10.2307/1541041 Camillo CD, Bo M, Lavorato A, Morigi C, Segre-Reinach M, Puce S, Bavestrello G (2008) Foraminifers epibiontic on Eudendrium (Cnidaria: Hydrozoa) from the Mediterranean Sea. J Mar Biol Assoc UK 88:485–489 Clarke KR, Gorley RN (2001) Primer (Plymouth Routines in Multivariate Ecological Research) v5: User Manual/Tutorial. PRIMER-E Ltd, Plymouth Cook E, Willis KJ, Lozano-Fernandez M (2007) Survivorship, growth and reproduction of the non-native Caprella mutica Schurin,

123

1890 1935 (Crustacea: Amphipoda). Hydrobiologia 590:55–64. doi:10.1007/s10750-007-0757-8 Corbari L, Sorbe JC, Massabuau JC (2005) Video study of the caprellid amphipod Parvipalpus major: morpho-functional and behavioural adaptations to deep-sea bottoms. Mar Biol (Berl) 146:363– 371. doi:10.1007/s00227-004-1433-4 Costa S (1960) Note préliminaire sur l’éthologie alimentaire de deux Caprellidés de la rade de Villefranche-sur-Mer. Trav Sta Zool Villefranche 19:103–105 Daugherty EC (1960) Caprellidae. In: McGraw-Hill encyclopedia of science and technology. McGraw–Hill, New York Dewey RA (1970) The feeding of Caprella equilibra Say, 1818 (Amphipoda: Crustacea). Thesis, Faculty of San Diego State College, San Diego DuVy JE (1990) Amphipods on seaweeds: partners or pests? Oecologia 83:267–276. doi:10.1007/BF00317764 Fenoglio S, Bo T, Tierno de Figueroa JM, Cucco M (2008) Nymphal growth, life cycle, and feeding habits of Potamanthus luteus (Linnaeus, 1767) (Insecta: Ephemeroptera) in the Bormida River, Northwestern Italy. Zool Stud 47(2):185–190 Genzano GN (2005) Trophic ecology of a benthic intertidal hydroid, Tubularia crocea, at Mar del Plata, Argentina. J Mar Biol Assoc UK 85:307–312. doi:10.1017/S0025315405011197h Gosse PH (1853) A naturalist’s rambles on the Devonshire coast. J Van Voorst, London Green J (1963) A biology of Crustacea. Quadrangle Books, Chicago Guerra-García JM (2001) Habitat use of the Caprellidea (Crustace: Amphipoda) from Ceuta, North Africa. Ophelia 55:27–38 Guerra-García JM, Corzo J, García-Gómez JC (2002) Clinging behaviour of the Caprellidea (Amphipoda) from the Strait of Gibraltar. Crustaceana 75:41–50. doi:10.1163/156854002317373500 Guerra-García JM, Martínez-Pita I, Pita ML (2004) Fatty acid composition of the Caprellidea (Crustacea: Amphipoda) from the Strait of Gibraltar. Sci Mar 68:501–510. doi:10.3989/scimar.2004. 68n4501 Ito A, Wada H, Aoki MN (2008) Phylogenetic analysis of caprellid and corophioid amphipods (Crustacea) based on the 18S rRNA gen, with special emphasis on the phylogenetic position of the Phtisicidae. Biol Bull 214:176–183 Keith DE (1969) Aspects of feeding in Caprella californica Stimpson and Caprella equilibra Say (Amphipoda). Crustaceana 16:119– 124. doi:10.1163/156854069X00367 Laubitz D (1993) Caprellidea (Crustacea: Amphipoda): towards a new síntesis. J Nat Hist 27:965–976. doi:10.1080/0022293930077 0591 Lockington WN (1875) Observations on the genus Caprella, and description of a new species. Proc Calif Acad Sci 5:405–406 López-Rodríguez MJ, Tierno de Figueroa JM (2006) Life cycle and nymphal feeding of Rhabdiopteryx christinae Theischinger, 1975 (Plecoptera, Taeniopterygidae). Ann Soc Entomol Fr 42:57–61 López-Rodríguez MJ, Tierno de Figueroa JM (2008) Feeding Habits of Two Capniidae (Plecoptera) Species from Southern Iberian Peninsula. J Entomol Sci 43(1):141–142 López-Rodríguez MJ, Tierno de Figueroa JM, Alba-Tercedor J (2009a) The life history of Serratella ignita (Poda, 1761) (Insecta: Ephemeroptera) in a temporary and permanent Mediterranean stream. Aquat Sci. doi:10.1007/s00027-009-9211-5

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Mar Biol (2009) 156:1881–1890 López-Rodríguez MJ, Tierno de Figueroa JM, Fenoglio S, Bo T, AlbaTercedor J (2009b) Life strategies of three Perlodidae species (Plecoptera, Insecta) in a Mediterranean seasonal stream of Southern Europe. J N Am Benthol Soc MacGinitie GE, MacGinitie N (1968) Natural history of marine animals. McGraw–Hill, New York Mayer P (1882) Die Caprelliden des Golfes von Neapel. Fauna Flora Golf Neapel 6:1–201 Mori A (1999) Caprella kuroshio, a new species (Crustacea: Caprellidae), with a redescription of Caprella cicur Mayer, 1903, and an evaluation of the genus Metacaprella Mayer, 1903. Proc Biol Soc Wash 112:722–738 Myers AA, Lowry JK (2003) A phylogeny and a new classiWcation of the Corophiidea Leach, 1814 (Amphipoda). J Crustac Biol 23:443–485. doi:10.1651/0278-0372(2003)023[0443:APAANC] 2.0.CO;2 Nakajima K, Takeuchi I (2008) Rearing method for Caprella mutica (Malacostraca: Amphipoda) in an exhibition tank in the port of Nagoya public aquarium, with notes on reproductive biology. J Crustac Biol 28:171–174. doi:10.1651/06-2811R.1 Navarro-Martínez D, López-Rodríguez MJ, Tierno de Figueroa JM (2007) The life cycle and nymphal feeding of Capnioneura petitpierreae Aubert, 1961 (Plecoptera, Capniidae). Illiesia 3(8):65– 69 Patton WK (1968) Feeding habitats, behaviour and host speciWty of Caprella grahami, an amphipod commensal with the starWsh Asterias forbesi. Biol Bull 134:148–153. doi:10.2307/1539973 Sano M, Omori M, Taniguchi K (2003) Predator-prey systems of drifting seaweed communities oV the Tohoku coast, northern Japan, as determined by feeding habitat analysis of phytal animals. Fish Sci 69:260–268. doi:10.1046/j.1444-2906.2003.00616.x Saunders CG (1966) Dietary analysis of caprellids (Amphipoda). Crustaceana 10:314–316. doi:10.1163/156854066X00243 Scinto A, Bavestrello G, Boyer M, Previati M, Cerrano C (2008) Gorgonian mortality related to a massive attack by caprellis in the Bunaken Marine Park (Noth Sulawesi, Indonesia). J Mar Biol Assoc UK 88:723–727. doi:10.1017/S002531540800129X Takeuchi I (1993) Is the Caprellidea a monophyletic group? J Nat Hist 27:947–964. doi:10.1080/00222939300770581 Takeuchi I (1998) Dry weitht, carbon and nitrogen components of caprellid amphipods (Crustacea) inhabiting Sargassum yezoense community of Otsuchi Bay, northeastern Japan. Mar Biol (Berl) 130:417–423. doi:10.1007/s002270050262 Takeuchi I, Hirano R (1991) Growth and reproduction of Caprella danilevskii (Crustacea: Amphipoda) reared in the laboratory. Mar Biol (Berl) 110:391–397. doi:10.1007/BF01344358 Takeuchi I, Hirano R (1992) Growth and reproduction of the epifaunal amphipod Caprella okadai (Crustacea: Amphipoda: Caprellidea). J Exp Mar Biol Ecol 161:201–212. doi:10.1016/0022-0981 (92)90097-T Tierno de Figueroa JM, Vera A, López-Rodríguez MJ (2006) Adult and nymphal feeding in the stoneXy species Antarctoperla michaelseni and Limnoperla jaVueli from Central Chile (Plecoptera: Gripopterygidae). Entomol Gen 29(1):39–45 Wirtz P (1998) Caprellid (Crustacea)-Holothurian (Echinodermata) associations in the Azores. Arquipelago 16:53–55