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Feeding habits of caprellids (Crustacea: Amphipoda) from the west coast of Mexico. Do they feed on their hosting substrates

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Feeding habits of caprellids (Crustacea: Amphipoda) from the west coast of Mexico. Do they feed on their hosting substrates
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  Zool. baetica, 23:   11-20,   2012 Feeding habits of caprellids (Crustacea: Amphipoda) from the west coast of Mexico. Do they feed on their hosting substrates? Alimentación de los caprélidos (Crustacea: Amphipoda) de la costa oeste de Méjico. ¿Se alimentan de los sustratos en los que viven? L. C. A LARCÓN -O RTEGA 1 , J. M. G UERRA -G ARCÍA 2, *, J. E. S ÁNCHEZ -M OYANO 2  &F. G. C UPUL -M AGAÑA 1  1. Laboratorio de Ecología Marina del Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad de Guadalajara, Avda. Universidad de Guadalajara 203, Puerto Vallarta, C.P. 48280, México. 2. Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012, Sevilla (Spain). * Corresponding author. Fax: 0034 954233480; E-mail: jmguerra@us.esRecibido el 17 de julio de 2012. Aceptado el 26 de julio de 2012.ISSN: 1130-4251 (2012), vol. 23, 11-20 Key words:  Caprellids, feeding, Mexico, Pacific Ocean, hydroids, gorgonians. Palabras clave:  Caprélidos, alimentación, Méjico, Océano Pacífico, hidrozoos, gorgonias. ABSTRACT  We studied the gut contents of the dominant species of the West coast of Mexico to explore if caprellids can use their host substrates (mainly hydroids and gorgonians) as food resource or just as a place to cling on. Two hundred and forty two specimens of four species of caprellids were examined:  Aciconula acanthosoma  Chess, 1989, Caprella equilibra Say, 1818, Caprella aff.  penantis  Leach, 1814 and  Paracaprella  sp. Detritus was the dominant component in all the species, although hydroids were also abundant in C. equilibra and  Paracaprella  sp. Crustaceans were present in the digestive tracts of the four species, being an important component in  Aciconula acanthosoma  and  Paracaprella  sp. Caprella aff.  penantis  and C. equilibra  collected from gorgonians did not show any trace of gorgonian sclerites in their guts. Therefore, the present study reveals that caprellids from the Pacific coast of Mexico are able to feed on hydroids but not on gorgonians. Furthermore,  Paracaprella  sp. associated to hydroids also showed a significant amount of harpacticoid copepods in the digestive tract, supporting the idea of cleptocomensalism. Further experimental studies are needed to explore the complex relationships between hydroids and caprellids.  Zool. baetica, 23:   11-20,   2012 ALARCÓN-ORTEGA, GUERRA-GARCÍA, SÁNCHEZ-MOYANO & CUPUL-MAGAÑA 12 RESUMEN  Se estudió el contenido del digestivo de las especies dominantes de la costa oeste de Méjico para explorar si los caprélidos pueden usar los sustratos en los que viven (principalmente hidrozoos y gorgonias) como fuente de alimento o solamente como sustrato al que anclarse. Se examinaron doscientos cuarenta y dos ejemplares de cuatro especies de caprélidos:  Aciconula acanthosoma  Chess, 1989, Caprella equilibra Say, 1818, Caprella aff.  penantis  Leach, 1814 y  Pa-racaprella  sp. El componente dominante en todas las especies fue el detritus, aunque los hidrozoos también fueron abundantes en C. equilibra y  Paracaprella  sp. Se encontraron restos de crustáceos en los tractos digestivos de las cuatro especies, siendo un componente importante en  Aciconula acanthosoma  y  Para-caprella  sp. Caprella  aff.  penantis  y C. equilibra  recolectadas en gorgonias no mostraron ningún resto de escleritos en sus digestivos. Por tanto, el presente estudio revela que los caprélidos de la costa pacífica de Méjico son capaces de alimentarse de hidrozoos pero no de gorgonias. Además,  Paracaprella  sp. asociada a hidrozoos también mostró una cantidad importante de copépodos harpacticoides en el tracto digestivo, lo que apoya la idea de cleptocomensa-lismo. Para el futuro, sería interesante desarrollar estudios experimentales para explorar las complejas relaciones entre hidrozoos y caprélidos. INTRODUCTION Caprellids are small crustaceans which constitute an important trophic link between primary producers and higher trophic levels in marine ecosys-tems (Woods, 2009). They have been proposed as useful marine bioindicators (Guerra-García & García-Gomez, 2001; Ohji et al. , 2002; Guerra-García et al  ., 2009) and as potential marine finfish aquaculture resource (Woods, 2009). A recent study based on 62 species in 31 genera has shown that caprellids feed mainly on detritus (Guerra-García & Tierno de Figueroa, 2009) and, secondarily, on microalgae, dinoflagellates, hydroids, sponges, polychaetes and crustaceans (copepods and amphipods). Although this study reveals the main components of the general diet of a wide variety of species, little is known yet about the trophic relationships among caprellids and their substrates.Caprellids usually live as epibionts on a variety of substrates from the littoral zone to a depth of 4790 m (Laubitz & Mills, 1972). The majority of species occur on a variety of organisms, clinging to algae, hydroids,  bryozoans, sponges, seagrasses (McCain, 1968; Laubitz, 1972; Caine, 1989; Guerra-García, 2001). Several caprellid species, however, live in more specific associations with invertebrates such as gorgonians, sea anemones, mollusks, medusae, large crustaceans and echinoderms (see references in Guerra-García, 2001). Species with specific habitats have morphological adaptations to their substrate, and even those species occurring on different  Zool. baetica, 23:   11-20,   2012 FEEDING HABITS OF CAPRELLIDS FROM MEXICO 13 substrates may exhibit some substrate-specific morphological adaptations (Caine, 1978, McCain, 1968). Caprellids use their substrates mainly as a place to cling on, but it is not still clear if they can also feed on their own substrates. It is evident that caprellids can receive food from the substrates in the form of attached diatoms and entrapped detritus (Caine, 1998), and that the substrates can also provide refuge from predators (Guerra-García, 2006) but little has been explored about the possibility of caprellids feeding directly on the substra-tes where they are clinging on. In this sense, Mayer (1882) suggested that caprellids might feed on polyps of hydroids and bryozoans. Guerra-García & Tierno de Figueroa (2009) did not find trace of bryozoans in the gut contents of the 62 studied species, but they found abundant hydroid cnido-cysts in three caprellid species. However, other authors (Bavestrello et al  ., 1996; Di Camillo et al. , 2008) point out that caprellids do not feed directly on hydroid polyps but the food collected by these polyps (e.g. copepods) can be exploited by caprellids in a cleptocommensalistic relationship. Caine (1998) reported the first case of caprellid-hydroid mutualism:  Paracaprella tenuis  Mayer, 1903 aggressively displaces Tenellia pallida  (Alder & Han-cock, 1845), a nudibranch predator of the hydroid. The caprellid receives a substrate of suitable diameter to be grasped by the pereiopods and access to food items (detritus, diatoms, nematodes and harpacticoid copepods) from the epibiotic community, but it does not feed directly on hydroid polyps. This caprellid aggressively defends its location on the hydroid, causing the nudibranch to move away. A similar relationship has also been proposed for  Paracaprella pusilla  and the hydroid  Eudendrium racemosum in Southern Spain (Ros & Guerra-García, 2012). Regarding with corals, Scinto et al  . (2008) pointed out the importance of cnidarians as a trophic source for ca- prellids and suggested that these predator/prey interactions are very fragile and that disequilibrium towards predators can occur, dramatically affecting  prey survivorship and gorgonian population stability. These authors reported a gorgonian mortality related to a massive attack by the caprellid  Metapro-tella sandalensis  in North Sulawesi, Indonesia; finding numerous sclerites in the digestive tract. Lewbel (1978) also reported that Caprella gorgonia feed on gorgonian tissue and polyp mucus secretions. However, Guerra-García & Tierno de Figueroa (2009) did not find any trace of gorgonian sclerites in the gut contents of any of the 62 species studied. Therefore, it remains unclear if caprellids effectively feed on polyps of hydroids and gorgonians or if the consumption is only accidental.Although in temperate ecosystems the highest densities of caprellids can  be found in algae (Guerra-García, 2001), in the tropical region caprellids are mainly associated to hydroids and secondarily to gorgonians and other  Zool. baetica, 23:   11-20,   2012 ALARCÓN-ORTEGA, GUERRA-GARCÍA, SÁNCHEZ-MOYANO & CUPUL-MAGAÑA 14 corals (Guerra-García, 2006; Scinto et al  ., 2008). In fact, in the Pacific coast of Mexico, hydroids and gorgonians are clearly the substrates containing highest abundances of caprellids (Sánchez-Moyano, in prep.). Consequently, the main objective of the present study was to explore if caprellids feed on  polyps of hydroids and gorgonians, based on the study of digestive contents of material collected from the West Coast of Mexico. MATERIAL AND METHODS We studied 242 specimens of 4 species of caprellids:  Aciconula acanthosoma  Chess, 1989, Caprella equilibra Say, 1818, Caprella aff.  penantis  Leach, 1814 and an undescribed species of  Paracaprella  (Table 1). These are the most common species inhabiting shallow waters of the West coast of Mexico. Caprellids were collected from June 2011 to February 2012 at 3 to 25 m deep. To explore if substrates could influence the feeding habitats of each species, caprellids were collected, whenever possible, from different substrates.  Aciconula acanthosoma  were collected from algae (I. Pájaros) and hydroids (C. Pelón), Caprella equilibra from gorgonians (I. Pájaros) and hydroids (B. Tiburón and B. Viudas), Caprella  aff.  penantis  from gorgonians of different stations (I. Pájaros, C. Pelón and Las Monas) and  Paracaprella  sp from hydroids (I. Pájaros) and coral rubble (I. Marietas) (Fig. 1, Table 1). The substrates were collected by snorkelling or SCUBA and samples were fixed in 70% ethanol. In the laboratory, the caprellids were sorted and identified. For the diet study, individuals were analyzed following the methodology of Bello & Cabrera (1999) used previously for caprellids by Guerra-García & Tierno de Figueroa (2009). Each individual was introduced in a vial with Hertwig’s liquid (consisting on 270 g of chloral hydrate, 19 ml of chloridric acid 1 N, 150 ml of distilled water and 60 ml of glycerine) and heaten in an oven at 65% for 3 to 10 hours depending on the size of specimens. After this, they were mounted on slides for its study under the microscope. The percentage of the absolute gut content (100x), as the total area occupied by the content in the whole digestive tract, and the relative gut content (400 and 1,000x), as the area occupied for each component within the total gut content, were estimated using a microscope equipped with an ocular micrometer. Mean and standard error of the mean were calculated. RESULTS AND DISCUSSION Two hundred and forty two specimens were examined (Table 2). The  percentage of empty guts were very high (63% in  Paracaprella sp., 61% in  Zool. baetica, 23:   11-20,   2012 FEEDING HABITS OF CAPRELLIDS FROM MEXICO 15 Fig. 1.—Map of the study area where caprellids were collected.Fig. 1.—Mapa del area de estudio donde se recolectaron los caprélidos.  A. acanthosoma , 55% in C. equilibra , 44% in Caprella aff.  penantis ). The mean value of the total area occupied by the content in the whole digesti-ve tract ranged from 21% (  A. acanthosoma ) and 37% in C.  aff.  penantis ). Gut contents of the studied caprellid species included detritus, crustaceans (mainly harpacticoid copepods), hydroids, microalgae (mainly diatoms) and dinoflagellates. Detritus was the dominant component in all the species, although hydroids were also abundant in C. equilibra and  Paracaprella  sp. Crustaceans were present in the digestive tracts of the four species, although they represented an important component in  Aciconula acanthosoma  and  Paracaprella  sp. When the gut contents were graphically compared among substrates (Fig. 2), a clear pattern was observed. The three species which were collected from hydroids (  A. acanthosoma , C. equilibra  and  Paracaprella  sp.) showed a significant amount of polyp tissue in the stomachs. This indicates that hydroid can constitute effectively an important part of the diet. However, Caprella aff. p enantis  collected from gorgonians of different localities, and
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