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Feeding habits of amphipods (Crustacea: Malacostraca) from shallow soft bottom communities: Comparison between marine caves and open habitats
Journal of Sea Research 78 (2013) 1–7
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Feeding habits of amphipods (Crustacea: Malacostraca) from shallow soft bottom communities: Comparison between marine caves and open habitats Carlos Navarro-Barranco a, c,⁎, José Manuel Tierno-de-Figueroa b, c, José Manuel Guerra-García a, c, Luis Sánchez-Tocino b, José Carlos García-Gómez a a b c
Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Campus Fuentenueva s/n, 18071 Granada, Spain Jun Zoological Research Center, C/Los Jazmines n° 15, 18213 Jun, Granada, Spain
a r t i c l e
i n f o
Article history: Received 20 August 2012 Received in revised form 22 December 2012 Accepted 30 December 2012 Available online 17 January 2013 Keywords: Feeding Habits Marine Caves Soft-bottom Amphipods Gut Contents Trophic Dynamics
a b s t r a c t Marine caves are environments of great interest since the organisms that inhabit them are forced to develop specific adaptations to high constraint conditions. Because of some of these particular conditions, such as light absence or oligotrophy, it can be expected that feeding strategies into caves differ from that present outside them. Nevertheless, no studies have been done to compare the trophic structure of marine caves and open habitats, at least for amphipod communities, considering their importance both inside and outside of the caves. In this study, the diet of the dominant amphipod species living on shallow sediments, both inside and outside of six marine caves in western Mediterranean, was characterized. Thereby, the gut content of 17 amphipod species was studied, being this study the first attempt to establish the feeding habit of most of these species. Analysis of digestive contents of the species showed that amphipod diet is less diverse in sediments than in other environments, such as algae and seagrasses. No herbivorous species were found in the sediment and carnivorous amphipods showed a little variety of prey, feeding mainly on crustaceans. Differences in the trophic structure were also found between marine caves and open habitats sediments: while outside the caves detritivorous was the dominant group (both in number of species and number of individuals), amphipods mainly play the role of carnivorous inside the caves. No detritivorous species were found into the caves, where carnivorous represents almost 60% of amphipods species and more than 80% of amphipod individuals. This pattern obtained in amphipods differ from the general trend observed in marine cave organisms, for which a generalist diet, such as omnivory, usually is an advantage in these oligotrophic conditions. The possible causes of this pattern are discussed. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved.
1. Introduction Submarine caves constitute interesting ecosystems characterized by distinctive biological and ecological peculiarities (Gili et al., 1986). Despite the increased interest of the last decades in the study of these habitats (Benedetti-Cechi et al., 1996), many aspects remain almost unknown. Marine caves can be inhabited by specialized taxa, many of them restricted to live in caves (sometimes exhibiting extreme adaptations), or by more generalist taxa than can find temporal or permanent refuge there (e.g. Bussotti and Guidetti, 2009; Harmelin et al., 1985; Vacelet et al., 1994). In any case, from the feeding point of view, caves are usually poor environments that greatly condition their trophic webs, at a global scale, and the particular diet of the species present, at a low scale. Thus, the absence of light in marine caves (common fact to ⁎ Corresponding author at: Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain. Tel.: +34 954556229. E-mail address: [email protected] (C. Navarro-Barranco).
freshwater and terrestrial caves) avoids the presence of primary producers (except in some cases chemosynthetic bacteria) (e.g. Airoldi and Cinelli, 1996; Pohlman et al., 1997). Parravicini et al. (2010) pointed out that, because of the differences in water confinement and trophic depletion among different sectors inside marine caves, consistent variations in the trophic guild of sessile species can be found. Additionally for soft bottom communities, the existence of a lower hydrodynamism influences their habitat structure, usually offering a finer sediment substrate than the surrounding seabed (Bamber et al., 2008). Iliffe and Bishop (2007) note, at community levels, that the scarcity of food in anchialine caves drives organisms toward a generalist diet, being expected that detritus feeders, together with omnivorous, dominate in these environments. Nevertheless, the role of a particular taxon needs to be evaluated to really categorize it inside the trophic web. In fact, it is amazing how little is known about the ecology of caves in general, particularly when it comes to their trophic structure (Romero, 2009). In soft-bottom marine substrates, amphipod crustaceans are one of the most important and diverse components of the fauna (Dauvin et al., 1994; Fincham, 1974; Lourido et al., 2008; Prato and Biandolino, 2005)
1385-1101/$ – see front matter. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.seares.2012.12.011
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structuring benthic assemblages (Duffy and Hay, 2000). Amphipods are frequent both inside and outside caves (Bamber et al., 2008; Iliffe, 2005; Navarro-Barranco et al., 2012). In relation with all the previously noted, the study of the feeding habits of amphipods can constitute an interesting tool to understand the trophic webs in the benthos of marine caves and their surroundings. Thus, the aim of the present study is to describe the feeding habits of the most abundant species of amphipods inhabiting inside and outside of some marine caves in western Mediterranean, to compare the obtained results and to test the hypothesis that species and/or populations living inside the caves are more detritivorous or omnivorous than those living outside of the caves. 2. Material and methods Six karstic marine caves were selected for this study (Fig. 1 and Table 1). All the caves presented similar length (10–25 m) and morphology, with a single submerged entrance followed by a rectilinear blind-ending tunnel without air chambers. The sampling was conducted during July and August of 2011. Two sampling stations were selected in each cave: one in the exterior area (outside the cave) and another inside the cave (each one approximately 10 m from the cave mouth). Samples were collected in each station using a hand-held rectangular core of 0.025 m2 to a depth of 10 cm by SCUBA diving. Samples were washed using a 0.5 mm mesh sieve, fixed with ethanol (70%) stained with rose Bengal. Amphipods were sorted under binocular microscope. Additional samples were collected at each station for physicochemical analyses of the sediment. All samples were immediately stored frozen until the laboratory analyses. Granulometry was determined following the method proposed by Guitián and Carballas (1976). Organic matter was analyzed by dichromate oxidation and titration with ferrous ammonium sulfate (Walkley and Black, 1934). To characterize the feeding habits of the amphipod community, we selected the species which contributed with at least 1% to the total abundance. In total, we studied 137 specimens of 7 species of amphipods living inside caves and 351 specimens of 13 species living outside caves. The whole list of analyzed material and details of provenance is included in Table 1, and the mean abundance of the amphipod species inside and outside the caves is included in Fig. 2. For the diet study, individuals were analyzed following the methodology proposed by Bello and Cabrera (1999) with slight variations. This method has been successfully used to study the gut contents of different
Table 1 Cave localities where amphipods were collected. Amb: Ampelisca brevicornis (Costa, 1853); Bag: Bathyporeia guilliamsoniana (Bate, 1857); Gaf: Gammarella fucicola (Leach, 1814); Haa: Harpinia antennaria Meinert, 1890; Hac: Harpinia crenulata (Boeck, 1871); Hap: Harpinia pectinata Sars, 1891; Him: Hippomedon massiliensis Bellan-Santini, 1965; Leh: Leptocheirus hirsutimanus (Bate, 1862); Mem: Megaluropus monasteriensis Ledoyer, 1976; Mef: Metaphoxus fultoni (Scott, 1890); Mog: Monoculodes griseus Della Valle, 1893; Pat: Pariambus typicus (Krøyer, 1884); Pel: Perioculodes longimanus (Bate & Westwood, 1868); Phl: Photis longipes (Della Valle, 1893); Phm: Phtisica marina Slabber, 1769; Sis: Siphonoecetes sabatieri De Rouville, 1894; Ure: Urothoe elegans (Bate, 1857). Caves
Coordinates
Depth (m)
Amphipod species Outside
Inside
Gorgonias (GR) Cantarriján (CN) Treinta Metros (TM) Raja de la Mona (RM) Punta del Vapor (PV)
36° 44′ 17″ N, 3° 46′ 42″ W 36° 44′ 16″ N, 3° 46′ 41″ W 36° 43′ 12″ N, 3° 44′ 9″ W
6 8 30
Bag, Mem Sis, Ure Hac
Hap, Pel Hap, Pel Haa, Hac
36° 43′ 10″ N, 3° 44′ 6″ W
30
Leh, Phl
Gaf, Phm
36° 43′ 22″ N, 3° 42′ 35″ W
12
Hac
Calahonda (CL)
36° 42′ 46″ N, 3° 22′ 18″ W
19
Amb, Him, Mem, Pat, Pel, Phl, Sis Hap, Him, Mem, Mef, Phl, Pat, Sis, Ure
Hac, Hap, Mog
arthropod groups and other animals, both aquatic and terrestrial forms and both ethanol and formalin preserved samples, revealing that it is a very appropriate method for gut content analysis (e.g. Bo et al., 2012; Fenoglio et al., 2008; Tierno de Figueroa et al., 2006). Particularly, this method has been used previously in Amphipoda (Alarcón-Ortega et al., 2012; Guerra-García and Tierno de Figueroa, 2009; Vázquez-Luis et al., 2012). Each individual was introduced in a vial with Hertwig's liquid (consisting of 270 g of chloral hydrate, 19 ml of chloridric acid 1 N, 150 ml of distillated water and 60 ml of glycerin) and heated in an oven at 65 °C for approximately 3 h. After this, they were mounted on slides for its study under the microscope. The percentage of the absolute gut content (at 100×), as the total area occupied by the content in the whole digestive tract, and the relative gut content (at 400×), as the area occupied for each component within the total gut content, were estimated using the microscope equipped with an ocular micrometer. Mean and standard error of the mean were calculated. Amphipod species were assigned to their feeding group (detritivorous, carnivorous, and omnivorous) according to the diet. When the gut content included more
N La Herradura
Salobreña
Motril
Almuñecar Castell de Ferro
GR CN TM RMPV
CL
5 km
MEDITERRANEAN SEA Fig. 1. Map of the study showing the location of marine caves where amphipods were collected. GR: Gorgonians, CN: Cantarriján, TM: Treinta Metros, RM: Raja Mona, PV: Punta Vapor, CL: Calahonda.
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Siphonoecetes sabatieri Metaphoxus fultoni Photis longipes Leptocheirus hirsutimanus Pariambus typicus Perioculodes longimanus Urothoe elegans Hippomedon massiliensis Harpinia pectinata Harpinia crenulata Bathyporeia guilliamsoniana Megaluropus monasteriensis
A
Ampelisca brevicornis 0
100 200 300 400 500 600 700 800 900
5000
6000
7000
8000
Harpinia pectinata Harpinia crenulata Perioculodes longimanus Harpinia antennaria Gammarella fucicola Monoculodes griseus
B
Phtisica marina 0
100 200 300 400 500 600 700 800 900 100
1000
1500
2000
Abundance (individuals/m2) Fig. 2. Abundance (ind/m2) of the dominant amphipod species (>1%) both outside (A) and inside (B) of the studied caves.
than 50% of prey, we cataloged the species as a carnivorous, considering that other materials can appear as the prey gut content or accidentally ingested when preying. The affinities among species according to the dietary analysis were explored by cluster analysis using UPGMA (unweighted pair group method using arithmetic averages) and Bray Curtis similarity index. This multivariate analysis was carried out using the PRIMER package (Clarke and Gorley, 2001). For the three species inhabiting both inside and outside of the caves (Harpinia crenulata, Harpinia pectinata and Perioculodes longimanus), we used an analysis of variance (ANOVA) with the following factors: ‘Position’, a fixed factor with two levels: outside and inside the caves; ‘Species’ a fixed factor and orthogonal, with three levels (the three species). The number of specimens with detected digestive contents was different among species. Consequently, to properly conduct a balanced ANOVA design, we chose the species with the lowest values (n=8 for P. longimanus) and we selected randomly 8 specimens of the remaining species. Additional ANOVA was used to test whether the organic matter and silt and clay percentage in the sediment changes between positions. Prior to ANOVA, heterogeneity of variance was tested with Cochran's C-test. Univariate analyses were conducted with GMAV5 (Underwood et al., 2002). 3. Results In total, we studied 488 specimens of 17 species of amphipods. Digestive contents were found in 238 of the 351 specimens outside the
caves (67.8%) and 82 of the 137 specimens inside the caves (59.9%) (Table 2). The average of the total area occupied by the content in the whole digestive tract ranged from 11.1 to 73.3% outside the caves and from 9.4 to 58.2% inside the caves. Gut contents of the studied amphipod species included mainly detritus and crustaceans, and secondly microalgae and polychaetes. According to the diet, species were included in three different feeding groups: detritivorous (6 species), carnivorous (5 species) and omnivorous (6 species) (Table 2). This classification was supported when the cluster analysis was conducted (Fig. 3). Carnivorous and detritivorous constituted well defined groups, while omnivorous species were in an intermediate position, with most of species closer to detritivorous, and one species, Hippomedon massiliensis, closer to carnivorous. We found species belonging to the three feeding groups outside the caves, while inside the caves the detritivorous were absent. Carnivorous dominated the caves, both in number of species and abundances, while detritivorous were dominant outside the caves (Fig. 4). The three studied species which were found inside and outside the caves, H. crenulata, H. pectinata, and P. longimanus, were carnivorous. There were no significant differences in digestive contents (measured as percentage of detritus) among the three species. Furthermore, each species showed the same feeding pattern inside and outside the caves (Table 3, Fig. 5). In connection with physicochemical parameters, organic matter was higher inside the caves, although values were always low (b 1%) both inside and outside the caves (Fig. 6). The studied caves showed a dominance of very fine and fine sands and this pattern was obtained inside
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Table 2 Gut contents of the studied amphipod species inside and outside of the caves. N: number of specimens of each species examined; n: number of specimens with detected gut content. %abs: total area occupied by the content in the whole digestive tract. Values: mean values±standard errors of the mean and, in parenthesis, minimum–maximum. FG (feeding group): D: detritivorous; O: omnivorous; C: carnivorous. Components (100%) %detritus Outside Ampelisca brevicornis Bathyporeia gilliamsoniana Harpinia crenulata Harpinia pectinata Hippomedon massiliensis Leptocheirus hirsutimanus Megaluropus monasteriensis Metaphoxus fultoni Pariambus typicus Perioculodes longimanus Photis longipes Siphonoecetes sabatieri Urothoe elegans
12/12 14/13 12/9 17/14 30/17 25/17 6/6 49/5 24/18 25/16 41/30 70/60 26/21
60.8 ± 8.5 (10–90) 46.5 ± 8.7 (5–90) 11.1 ± 2.9 (5–30) 28.6 ± 5.5 (5–70) 69.4 ± 6.0 (20–100) 43.5 ± 8.3 (5–100) 73.3 ± 11.1 (20–90) 28.0 ± 3.7 (20–40) 44.4 ± 7.1 (5–100) 16.9 ± 3.1 (5–50) 29.2 ± 5.2 (5–100) 41.7 ± 4.0 (5–100) 21.0 ± 2.5 (10–50)
Inside Gammarella fucicola Harpinia antennaria Harpinia crenulata Harpinia pectinata Monoculodes griseus Perioculodes longimanus Phtisica marina
8/7 8/6 20/12 66/34 7/4 17/8 11/11
40.0 ± 10.5 (10–80) 14.2 ± 2.7 (5–20) 15.4 ± 3.2 (5–40) 13.8 ± 1.5 (5–40) 12.5 ± 2.5 (10–20) 9.4 ± 1.8 (5–20) 58.2 ± 8.2 (20–90)
92.5 ± 4.5 (50–100) 100 ± 0 (0–100) 41.1 ± 7.7 (0–70) 35.4 ± 7.6 (0–100) 58.2 ± 9.9 (0–100) 100 ± 0 (100–100) 100 ± 0 (100–100) 14.0 ± 7.5 (0–40) 100 ± 0 (100–100) 29.4 ± 7.3 (0–80) 100 ± 0 (100–100) 100 ± 0 (100–100) 73.3 ± 5.4 (0–10)
85.7 ± 7.2 (60–100) 80.0 ± 16.3 (0–100) 42.5 ± 9.1 (0–90) 39.1 ± 5.6 (0–100) 32.5 ± 11.8 (0–50) 26.3 ± 9.6 (0–70) 91.8 ± 7.2 (20–100)
FG %microalgae
%crustacea
%polychaeta
– – – 0.5 ± 0.4 (0–5) 0.3 ± 0.3 (0–5) – – – – – – – 1.4 ± 1.0 (0–20)
4.2 ± 4.2 (0–50) – 58.9 ± 7.7 (30–100) 60.6 ± 8.8 (0–100) 41.5 ± 9.9 (0–100) – – 86.0 ± 7.5 (60–100) – 70.6 ± 7.3 (20–100) – – 25.2 ± 5.6 (0–100)
3.3 ± 2.3 (0–20) – – 3.6 ± 3.6 (0–50) – – – – – – – – –
O D C C O D D C D C D D O
– – – – – – 0.5 ± 0.5 (0–5)
14.3 ± 7.2 (0–40) 20.0 ± 16.3 (0–100) 57.5 ± 9.1 (10–100) 60.1 ± 5.6 (0–100) 67.5 ± 11.8 (50–100) 73.8 ± 9.6 (30–100) 7.7 ± 7.3 (0–80)
– – – – – – –
O O C C C C O
there are not always clear relationships among these characters and the digestive contents. Only the diet of 2 of the 17 species considered had previously been studied based in the gut contents. The data obtained in the present study for these two species, Pariambus typicus and Phtisica marina, agree with those obtained by Guerra-García and Tierno de Figueroa (2009). On the other hand, the knowledge about feeding habits in amphipods is limited, in some cases, to family level. In this sense, our results usually agree with the previous literature. According to our data, Siphonocetes sabatieri is a strictly detritivorous species, which agree with the previously recorded for the Corophidae family (Bellan-Santini and Ruffo, 1998). Studying the crop contents of some phoxocephalid species, Oliver et al. (1982) concluded that this group acts as a key taxon in soft bottom communities, playing an important functional role as carnivorous. Other studies using stable isotope analyses also showed
and outside. However, the percentage of silt and clay was significantly higher inside the caves (Fig. 6). 4. Discussion The present work is the first comprehensive study on the feeding habits of amphipod species inhabiting soft bottom communities. There are very few studies dealing with the diet of amphipod species and this biological aspect is unknown for many of them (Scipione, 1989). Moreover, the knowledge about the feeding of many species was based on assumptions from fecal pellet composition or morphological characters, but these assumptions must be taken carefully since they are not always fulfilled. For example, the feeding habit of caprellids has been traditionally inferred from mouthparts or antennae morphology (Caine 1974, 1977); however, Guerra-García and Tierno de Figueroa (2009) showed that
Harpinia crenulata IN Harpinia crenulata OUT Harpinia pectinata IN Harpinia pectinata OUT Perioculodes longimanus OUT Monoculodes griseus IN Perioculodes longimanus IN Metaphoxus fultoni OUT Hippomedon massiliensis OUT Harpinia antennaria IN Gammarella fucicola IN Urothoe elegans OUT Phtisica marina IN Ampelisca brevicornis OUT Pariambus typicus OUT Megaluropus monasteriensis OUT Leptocheirus hirsutimanus OUT Bathyporeia guilliamsoniana OUT Siphonoecetes sabatieri OUT Photis longipes OUT
40
60
80
100
Bray Curtis Similarity (%) Fig. 3. Dendrogram based on the digestive contents of the studied amphipod species inside and outside the caves.
CARNIVOROUS
% abs
DETRITIVOROUS OMNIVOROUS
N/n
C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7
100%
5
OUT IN
OUT IN
OUT IN
ABUNDANCE
Harpinia crenulata
Harpinia pectinata
Perioculodes longimanus
Detritivorous
Microalgae
100%
80%
80%
60%
60%
40%
40%
20% 20%
0% Outside
Inside
Outside
NUMBER OF SPECIES Omnivorous
Carnivorous
0%
Inside
Prey
Detritus
Fig. 4. Contribution in percentage of each feeding group to the total number of species and abundance.
Fig. 5. Contribution of each feeding component for the three species inhabiting both inside and outside of the caves. See also Table 3.
the carnivorous behavior of Harpinia species (Fanelli et al., 2009). Our data support this assertion, since almost all the phoxocephalid species studied (H. pectinata, H. crenulata and Metaphoxus fultoni) had a diet mainly composed by crustaceans. Nevertheless, in some cases, species belonging to the same family or even genus showed different feeding habits. For example, Harpinia antennaria had an omnivorous diet in the present study. Urothoe elegans was omnivorous while Bathyporeia guilliamsoniana (both of them belonging to Haustoridae family) fed exclusively on detritus. These results show that the feeding habits of an unstudied species cannot be inferred from studies of congeners, as it has been noted for other aquatic invertebrates (e. g. Stewart and Stark, 2002), and consequently gut content analyses are needed to correctly assign each taxon to each feeding group. Within the same species, variations in the trophic preferences can also be found when studying different environments. In a comparative work carried out in the Mediterranean to study the variations in the gut contents of some amphipod species living in native and invasive seaweeds, Vázquez-Luis et al. (2012) found that some species (such as Ampithoe ramondi or Dexamine spiniventris) had different feeding modes depending on the habitat they live on. In the same way, Alarcón-Ortega et al. (2012) reported variations in the feeding behavior of the caprellids Aciconula acanthosoma and Caprella equilibra when they live in algae, hydroids or gorgonians. In our study, the three species found both inside and outside the caves did not show significant changes in their gut components between both habitats. The absence of differences in the feeding modes for H. crenulata, H. pectinata, and
P. longimanus (all of them carnivorous) between habitats could be due to the availability of this food source inside and outside the caves. Strong differences between habitats can also been found when all amphipod assemblages are considered. Our data reflects that amphipod diet in sediments is less diverse than in other environments such as algae and seagrasses (Guerra-García and Tierno de Figueroa, 2009; Vázquez-Luis et al., 2012). The percentage of algae in the gut contents was zero or very low in all cases. Obviously, that pattern was expected inside the caves, where no primary producer is present, but it is remarkable that no herbivorous species could be found in the external sediments. The variety of prey in carnivorous species was also lower, composed mainly (and often exclusively) by crustaceans. Diet diversity in soft bottom amphipod assemblage was even less diverse inside the caves. No detritivorous species was present inside the caves and, while this feeding group was the dominant group (both number of species and number of individuals) in the external sediments, cave community was dominated by carnivorous species. This pattern in amphipod species is highly unexpected since the general pattern in cave communities drives organisms toward a generalist diet (with a dominance of omnivorous and detritivorous species). However, as in such case, some particular groups can follow a different trend. Bianchi (1985) found a high percentage of carnivorous species in polychaete assemblages of marine cave. According to Romero (2009), cave amphipods feed mostly on detritus but our data show that they occupy mainly the role of carnivorous. The reason of the absence of detritivorous amphipods into these caves remains still uncertain. A potential factor could be the limited food supply, since marine caves are usually considered as oligotrophic habitats. Experimental studies on vegetated habitats reveal that species richness and abundance of amphipods were highly and positively related with the detritus content (Vázquez-Luis et al., 2009). However, our chemical data showed significant higher concentrations of organic matter inside the caves, although it has been suggested that the quality of organic matter in marine caves may decrease toward the inner parts (Fichez, 1991). The feeding behavior, not only the feeding group, should be also an important factor to consider. Because of the low hidrodinamism inside caves, strong differences between habitats can be expected in the way in which such organic matter is available to organisms. Thereby, while inside the caves the organic matter percentage in the sediment is higher, the suspended detritus is much less abundant.
Table 3 Results of the two-factor ANOVA for percentage of detritus in the amphipod species inhabiting outside and inside of the caves: Harpinia crenulata, H. pectinata and Perioculodes longimanus. MS=mean square; df=degrees of freedom. Source of variation
Position (Po) Species (Sp) Po × Sp Residual Cochran's C-test Transformation
%detritus df
MS
F
P
1 2 2 42
75.00 506.25 1406.25 921.43
0.08 0.55 1.53
0.78 0.58 0.23
C = 0.22 None
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ORGANIC MATTER
colonize such habitats, among others, which can act like a limiting factor for the presence of detritivorous. Further studies about the ecological conditions in marine caves and the feeding habit and behavior of all the soft-bottom community are necessary to understand the trophic dynamic of such environments.
1,5
Acknowledgments
1
Financial support of this work was provided by the Ministerio de Educación y Ciencia (Project CGL 2011-22474/BOS). This work forms part of C.N-B's Ph.D. Thesis, supported by the Universidad de Sevilla (PIF Grant).
%
References
0,5
0
Outside
Inside
GRANULOMETRY 100
75
% 50
25
0
Outside
Inside
Gross-very gross sands and gravels Very fine and fine sands
Medium sands
Silt and clay
Fig. 6. Organic matter and granulometry in the studied caves. Data are mean values of the six caves (for organic matter standard error of the mean is also included).
In that way, gatherer–collectors find abundant settle detritus to feed inside caves while filter feeders should have more problems to colonize cave environments, since they need more exposed habitats, with a greater degree of turbulence. Nevertheless, little is known about the feeding behavior of detritivorous species present inside our caves and about amphipods in general. Moreover, Shillaker and Moore (1987) pointed out that some detritivorous species can even change its feeding methods, using alternative techniques in poor feeding conditions. So, we cannot relate assertively the absence of detritivorous species inside the caves with their feeding behavior. The finer sediment inside the caves neither seems to be the problem, since many of the detritivorous species present outside the caves usually inhabit muddy sediments (Bellan-Santini et al., 1982, 1989, 1993). There are many other physical gradients (light, salinity or oxygen) and the low capacity of the larvae to
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C. Navarro-Barranco et al. / Journal of Sea Research 78 (2013) 1–7 Harmelin, J.G., Vacelet, J., Vasseur, P., 1985. Les grottes sous-marines obscures: un milieu extrème et un remarquable biotope refuge. Tethys 11, 214–229. Iliffe, T.M., 2005. Biodiversity in anchialine caves. In: Culver, D.C., White, W.B. (Eds.), Encyclopedia of Caves. Elsevier Academic Press, London, pp. 24–30. Iliffe, T.M., Bishop, R.E., 2007. Adaptations to life in marine caves. In: Safran, Patrick (Ed.), Fisheries and Aquaculture, Encyclopedia of Life Support Systems (EOLSS). Eolss Publishers, Oxford. Lourido, A., Moreira, J., Troncoso, J.S., 2008. Assemblages of peracarid crustaceans in subtidal sediments from the Ría de Aldán (Galicia, NW Spain). Helgoland Marine Research 62, 289–301. Navarro-Barranco, C., Guerra-García, J.M., Sánchez-Tocino, L., García-Gómez, J.C., 2012. Soft-bottom crustacean assemblages in Mediterranean marine caves: the cave of Cerro Gordo (Granada, Spain) as case study. Helgoland Marine Research 66, 567–576. Oliver, J.S., Oakden, J.M., Slattery, P.N., 1982. Phoxocephalid amphipod crustaceans as predators on larvae and juveniles in marine soft-bottom communities. Marine Ecology Progress Series 7, 179–184. Parravicini, V., Guidetti, P., Morri, C., Montefalcone, M., Donato, M., Bianchi, C.N., 2010. Consequences of sea water temperature anomalies on a Mediterranean submarine cave ecosystem. Estuarine, Coastal and Shelf Science 86 (2), 276–282. Pohlman, J.W., Iliffe, T.M., Cifuentes, L.A., 1997. A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Marine Ecology Progress Series 155, 17–27. Prato, E., Biandolino, F., 2005. Amphipod biodiversity of shallow water in the Taranto seas (north-western Ionian Sea). Journal of the Marine Biological Association of the UK 85, 333–338. Romero, A., 2009. Cave Biology, Life in Darkness. Cambridge University Press, Cambridge.
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Scipione, M.B., 1989. Comportamento trofico dei Crostacei Anfipodi in alcuni sistemi bentonici costieri. Oebalia 15 (1), 249–260. Shillaker, R.O., Moore, P.G., 1987. The feeding habits of the amphipods Lembos websteri Bate and Corophium bonellii Milne Edwards. Journal of Experimental Marine Biology and Ecology 110, 93–112. Stewart, K.W., Stark, B.P., 2002. Nymphs of North American Stonefly Genera (Plecoptera), Second ed. Caddis press, Columbus, Ohio. Tierno de Figueroa, J.M., Vera, A., López-Rodríguez, M.J., 2006. Adult and nymphal feeding in the stonefly species Antarctoperla michaelseni and Limnoperla jaffueli from Central Chile (Plecoptera, Gripopterygidae). Entomologia Generalis 29 (1), 39–45. Underwood, A.J., Chapman, M.G., Richards, S.A., 2002. GMAV-5 for Windows. An Analysis of Variance Programme.Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories, University of Sydney, Australia. Vacelet, J., Boury-Esnault, N., Harmelin, J.G., 1994. Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep Sea Research 41 (7), 965–973. Vázquez-Luis, M., Borg, J.A., Sanchez-Jerez, P., Png, L., Carvallo, M., Bayle-Sempere, J.T., 2009. Why amphipods prefer the new available habitat built by C. recemosa?: a field experiment in Mediterranean Sea. International Symposium on Marine Sciences, University of Alicante. Vázquez-Luis, M., Sanchez-Jerez, P., Bayle-Sempere, J.T., 2012. Does the invasion of Caulerpa racemosa var. cylindracea affect the feeding habits of amphipods (Crustacea: Amphipoda)? Journal of the Marine Biological Association of the UK 93 (1), 87–94. Walkley, A., Black, I.A., 1934. An examination of Degtjareff method for determine soil organic matter and a proposed modification of the chromic acid titration method. Soil Science 37, 29–37.
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Feeding habits of amphipods (Crustacea: Malacostraca) from shallow soft bottom communities: Comparison between marine caves and open habitats Carlos Navarro-Barranco a, c,⁎, José Manuel Tierno-de-Figueroa b, c, José Manuel Guerra-García a, c, Luis Sánchez-Tocino b, José Carlos García-Gómez a a b c
Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Campus Fuentenueva s/n, 18071 Granada, Spain Jun Zoological Research Center, C/Los Jazmines n° 15, 18213 Jun, Granada, Spain
a r t i c l e
i n f o
Article history: Received 20 August 2012 Received in revised form 22 December 2012 Accepted 30 December 2012 Available online 17 January 2013 Keywords: Feeding Habits Marine Caves Soft-bottom Amphipods Gut Contents Trophic Dynamics
a b s t r a c t Marine caves are environments of great interest since the organisms that inhabit them are forced to develop specific adaptations to high constraint conditions. Because of some of these particular conditions, such as light absence or oligotrophy, it can be expected that feeding strategies into caves differ from that present outside them. Nevertheless, no studies have been done to compare the trophic structure of marine caves and open habitats, at least for amphipod communities, considering their importance both inside and outside of the caves. In this study, the diet of the dominant amphipod species living on shallow sediments, both inside and outside of six marine caves in western Mediterranean, was characterized. Thereby, the gut content of 17 amphipod species was studied, being this study the first attempt to establish the feeding habit of most of these species. Analysis of digestive contents of the species showed that amphipod diet is less diverse in sediments than in other environments, such as algae and seagrasses. No herbivorous species were found in the sediment and carnivorous amphipods showed a little variety of prey, feeding mainly on crustaceans. Differences in the trophic structure were also found between marine caves and open habitats sediments: while outside the caves detritivorous was the dominant group (both in number of species and number of individuals), amphipods mainly play the role of carnivorous inside the caves. No detritivorous species were found into the caves, where carnivorous represents almost 60% of amphipods species and more than 80% of amphipod individuals. This pattern obtained in amphipods differ from the general trend observed in marine cave organisms, for which a generalist diet, such as omnivory, usually is an advantage in these oligotrophic conditions. The possible causes of this pattern are discussed. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved.
1. Introduction Submarine caves constitute interesting ecosystems characterized by distinctive biological and ecological peculiarities (Gili et al., 1986). Despite the increased interest of the last decades in the study of these habitats (Benedetti-Cechi et al., 1996), many aspects remain almost unknown. Marine caves can be inhabited by specialized taxa, many of them restricted to live in caves (sometimes exhibiting extreme adaptations), or by more generalist taxa than can find temporal or permanent refuge there (e.g. Bussotti and Guidetti, 2009; Harmelin et al., 1985; Vacelet et al., 1994). In any case, from the feeding point of view, caves are usually poor environments that greatly condition their trophic webs, at a global scale, and the particular diet of the species present, at a low scale. Thus, the absence of light in marine caves (common fact to ⁎ Corresponding author at: Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain. Tel.: +34 954556229. E-mail address: [email protected] (C. Navarro-Barranco).
freshwater and terrestrial caves) avoids the presence of primary producers (except in some cases chemosynthetic bacteria) (e.g. Airoldi and Cinelli, 1996; Pohlman et al., 1997). Parravicini et al. (2010) pointed out that, because of the differences in water confinement and trophic depletion among different sectors inside marine caves, consistent variations in the trophic guild of sessile species can be found. Additionally for soft bottom communities, the existence of a lower hydrodynamism influences their habitat structure, usually offering a finer sediment substrate than the surrounding seabed (Bamber et al., 2008). Iliffe and Bishop (2007) note, at community levels, that the scarcity of food in anchialine caves drives organisms toward a generalist diet, being expected that detritus feeders, together with omnivorous, dominate in these environments. Nevertheless, the role of a particular taxon needs to be evaluated to really categorize it inside the trophic web. In fact, it is amazing how little is known about the ecology of caves in general, particularly when it comes to their trophic structure (Romero, 2009). In soft-bottom marine substrates, amphipod crustaceans are one of the most important and diverse components of the fauna (Dauvin et al., 1994; Fincham, 1974; Lourido et al., 2008; Prato and Biandolino, 2005)
1385-1101/$ – see front matter. Crown Copyright © 2013 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.seares.2012.12.011
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structuring benthic assemblages (Duffy and Hay, 2000). Amphipods are frequent both inside and outside caves (Bamber et al., 2008; Iliffe, 2005; Navarro-Barranco et al., 2012). In relation with all the previously noted, the study of the feeding habits of amphipods can constitute an interesting tool to understand the trophic webs in the benthos of marine caves and their surroundings. Thus, the aim of the present study is to describe the feeding habits of the most abundant species of amphipods inhabiting inside and outside of some marine caves in western Mediterranean, to compare the obtained results and to test the hypothesis that species and/or populations living inside the caves are more detritivorous or omnivorous than those living outside of the caves. 2. Material and methods Six karstic marine caves were selected for this study (Fig. 1 and Table 1). All the caves presented similar length (10–25 m) and morphology, with a single submerged entrance followed by a rectilinear blind-ending tunnel without air chambers. The sampling was conducted during July and August of 2011. Two sampling stations were selected in each cave: one in the exterior area (outside the cave) and another inside the cave (each one approximately 10 m from the cave mouth). Samples were collected in each station using a hand-held rectangular core of 0.025 m2 to a depth of 10 cm by SCUBA diving. Samples were washed using a 0.5 mm mesh sieve, fixed with ethanol (70%) stained with rose Bengal. Amphipods were sorted under binocular microscope. Additional samples were collected at each station for physicochemical analyses of the sediment. All samples were immediately stored frozen until the laboratory analyses. Granulometry was determined following the method proposed by Guitián and Carballas (1976). Organic matter was analyzed by dichromate oxidation and titration with ferrous ammonium sulfate (Walkley and Black, 1934). To characterize the feeding habits of the amphipod community, we selected the species which contributed with at least 1% to the total abundance. In total, we studied 137 specimens of 7 species of amphipods living inside caves and 351 specimens of 13 species living outside caves. The whole list of analyzed material and details of provenance is included in Table 1, and the mean abundance of the amphipod species inside and outside the caves is included in Fig. 2. For the diet study, individuals were analyzed following the methodology proposed by Bello and Cabrera (1999) with slight variations. This method has been successfully used to study the gut contents of different
Table 1 Cave localities where amphipods were collected. Amb: Ampelisca brevicornis (Costa, 1853); Bag: Bathyporeia guilliamsoniana (Bate, 1857); Gaf: Gammarella fucicola (Leach, 1814); Haa: Harpinia antennaria Meinert, 1890; Hac: Harpinia crenulata (Boeck, 1871); Hap: Harpinia pectinata Sars, 1891; Him: Hippomedon massiliensis Bellan-Santini, 1965; Leh: Leptocheirus hirsutimanus (Bate, 1862); Mem: Megaluropus monasteriensis Ledoyer, 1976; Mef: Metaphoxus fultoni (Scott, 1890); Mog: Monoculodes griseus Della Valle, 1893; Pat: Pariambus typicus (Krøyer, 1884); Pel: Perioculodes longimanus (Bate & Westwood, 1868); Phl: Photis longipes (Della Valle, 1893); Phm: Phtisica marina Slabber, 1769; Sis: Siphonoecetes sabatieri De Rouville, 1894; Ure: Urothoe elegans (Bate, 1857). Caves
Coordinates
Depth (m)
Amphipod species Outside
Inside
Gorgonias (GR) Cantarriján (CN) Treinta Metros (TM) Raja de la Mona (RM) Punta del Vapor (PV)
36° 44′ 17″ N, 3° 46′ 42″ W 36° 44′ 16″ N, 3° 46′ 41″ W 36° 43′ 12″ N, 3° 44′ 9″ W
6 8 30
Bag, Mem Sis, Ure Hac
Hap, Pel Hap, Pel Haa, Hac
36° 43′ 10″ N, 3° 44′ 6″ W
30
Leh, Phl
Gaf, Phm
36° 43′ 22″ N, 3° 42′ 35″ W
12
Hac
Calahonda (CL)
36° 42′ 46″ N, 3° 22′ 18″ W
19
Amb, Him, Mem, Pat, Pel, Phl, Sis Hap, Him, Mem, Mef, Phl, Pat, Sis, Ure
Hac, Hap, Mog
arthropod groups and other animals, both aquatic and terrestrial forms and both ethanol and formalin preserved samples, revealing that it is a very appropriate method for gut content analysis (e.g. Bo et al., 2012; Fenoglio et al., 2008; Tierno de Figueroa et al., 2006). Particularly, this method has been used previously in Amphipoda (Alarcón-Ortega et al., 2012; Guerra-García and Tierno de Figueroa, 2009; Vázquez-Luis et al., 2012). Each individual was introduced in a vial with Hertwig's liquid (consisting of 270 g of chloral hydrate, 19 ml of chloridric acid 1 N, 150 ml of distillated water and 60 ml of glycerin) and heated in an oven at 65 °C for approximately 3 h. After this, they were mounted on slides for its study under the microscope. The percentage of the absolute gut content (at 100×), as the total area occupied by the content in the whole digestive tract, and the relative gut content (at 400×), as the area occupied for each component within the total gut content, were estimated using the microscope equipped with an ocular micrometer. Mean and standard error of the mean were calculated. Amphipod species were assigned to their feeding group (detritivorous, carnivorous, and omnivorous) according to the diet. When the gut content included more
N La Herradura
Salobreña
Motril
Almuñecar Castell de Ferro
GR CN TM RMPV
CL
5 km
MEDITERRANEAN SEA Fig. 1. Map of the study showing the location of marine caves where amphipods were collected. GR: Gorgonians, CN: Cantarriján, TM: Treinta Metros, RM: Raja Mona, PV: Punta Vapor, CL: Calahonda.
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Siphonoecetes sabatieri Metaphoxus fultoni Photis longipes Leptocheirus hirsutimanus Pariambus typicus Perioculodes longimanus Urothoe elegans Hippomedon massiliensis Harpinia pectinata Harpinia crenulata Bathyporeia guilliamsoniana Megaluropus monasteriensis
A
Ampelisca brevicornis 0
100 200 300 400 500 600 700 800 900
5000
6000
7000
8000
Harpinia pectinata Harpinia crenulata Perioculodes longimanus Harpinia antennaria Gammarella fucicola Monoculodes griseus
B
Phtisica marina 0
100 200 300 400 500 600 700 800 900 100
1000
1500
2000
Abundance (individuals/m2) Fig. 2. Abundance (ind/m2) of the dominant amphipod species (>1%) both outside (A) and inside (B) of the studied caves.
than 50% of prey, we cataloged the species as a carnivorous, considering that other materials can appear as the prey gut content or accidentally ingested when preying. The affinities among species according to the dietary analysis were explored by cluster analysis using UPGMA (unweighted pair group method using arithmetic averages) and Bray Curtis similarity index. This multivariate analysis was carried out using the PRIMER package (Clarke and Gorley, 2001). For the three species inhabiting both inside and outside of the caves (Harpinia crenulata, Harpinia pectinata and Perioculodes longimanus), we used an analysis of variance (ANOVA) with the following factors: ‘Position’, a fixed factor with two levels: outside and inside the caves; ‘Species’ a fixed factor and orthogonal, with three levels (the three species). The number of specimens with detected digestive contents was different among species. Consequently, to properly conduct a balanced ANOVA design, we chose the species with the lowest values (n=8 for P. longimanus) and we selected randomly 8 specimens of the remaining species. Additional ANOVA was used to test whether the organic matter and silt and clay percentage in the sediment changes between positions. Prior to ANOVA, heterogeneity of variance was tested with Cochran's C-test. Univariate analyses were conducted with GMAV5 (Underwood et al., 2002). 3. Results In total, we studied 488 specimens of 17 species of amphipods. Digestive contents were found in 238 of the 351 specimens outside the
caves (67.8%) and 82 of the 137 specimens inside the caves (59.9%) (Table 2). The average of the total area occupied by the content in the whole digestive tract ranged from 11.1 to 73.3% outside the caves and from 9.4 to 58.2% inside the caves. Gut contents of the studied amphipod species included mainly detritus and crustaceans, and secondly microalgae and polychaetes. According to the diet, species were included in three different feeding groups: detritivorous (6 species), carnivorous (5 species) and omnivorous (6 species) (Table 2). This classification was supported when the cluster analysis was conducted (Fig. 3). Carnivorous and detritivorous constituted well defined groups, while omnivorous species were in an intermediate position, with most of species closer to detritivorous, and one species, Hippomedon massiliensis, closer to carnivorous. We found species belonging to the three feeding groups outside the caves, while inside the caves the detritivorous were absent. Carnivorous dominated the caves, both in number of species and abundances, while detritivorous were dominant outside the caves (Fig. 4). The three studied species which were found inside and outside the caves, H. crenulata, H. pectinata, and P. longimanus, were carnivorous. There were no significant differences in digestive contents (measured as percentage of detritus) among the three species. Furthermore, each species showed the same feeding pattern inside and outside the caves (Table 3, Fig. 5). In connection with physicochemical parameters, organic matter was higher inside the caves, although values were always low (b 1%) both inside and outside the caves (Fig. 6). The studied caves showed a dominance of very fine and fine sands and this pattern was obtained inside
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Table 2 Gut contents of the studied amphipod species inside and outside of the caves. N: number of specimens of each species examined; n: number of specimens with detected gut content. %abs: total area occupied by the content in the whole digestive tract. Values: mean values±standard errors of the mean and, in parenthesis, minimum–maximum. FG (feeding group): D: detritivorous; O: omnivorous; C: carnivorous. Components (100%) %detritus Outside Ampelisca brevicornis Bathyporeia gilliamsoniana Harpinia crenulata Harpinia pectinata Hippomedon massiliensis Leptocheirus hirsutimanus Megaluropus monasteriensis Metaphoxus fultoni Pariambus typicus Perioculodes longimanus Photis longipes Siphonoecetes sabatieri Urothoe elegans
12/12 14/13 12/9 17/14 30/17 25/17 6/6 49/5 24/18 25/16 41/30 70/60 26/21
60.8 ± 8.5 (10–90) 46.5 ± 8.7 (5–90) 11.1 ± 2.9 (5–30) 28.6 ± 5.5 (5–70) 69.4 ± 6.0 (20–100) 43.5 ± 8.3 (5–100) 73.3 ± 11.1 (20–90) 28.0 ± 3.7 (20–40) 44.4 ± 7.1 (5–100) 16.9 ± 3.1 (5–50) 29.2 ± 5.2 (5–100) 41.7 ± 4.0 (5–100) 21.0 ± 2.5 (10–50)
Inside Gammarella fucicola Harpinia antennaria Harpinia crenulata Harpinia pectinata Monoculodes griseus Perioculodes longimanus Phtisica marina
8/7 8/6 20/12 66/34 7/4 17/8 11/11
40.0 ± 10.5 (10–80) 14.2 ± 2.7 (5–20) 15.4 ± 3.2 (5–40) 13.8 ± 1.5 (5–40) 12.5 ± 2.5 (10–20) 9.4 ± 1.8 (5–20) 58.2 ± 8.2 (20–90)
92.5 ± 4.5 (50–100) 100 ± 0 (0–100) 41.1 ± 7.7 (0–70) 35.4 ± 7.6 (0–100) 58.2 ± 9.9 (0–100) 100 ± 0 (100–100) 100 ± 0 (100–100) 14.0 ± 7.5 (0–40) 100 ± 0 (100–100) 29.4 ± 7.3 (0–80) 100 ± 0 (100–100) 100 ± 0 (100–100) 73.3 ± 5.4 (0–10)
85.7 ± 7.2 (60–100) 80.0 ± 16.3 (0–100) 42.5 ± 9.1 (0–90) 39.1 ± 5.6 (0–100) 32.5 ± 11.8 (0–50) 26.3 ± 9.6 (0–70) 91.8 ± 7.2 (20–100)
FG %microalgae
%crustacea
%polychaeta
– – – 0.5 ± 0.4 (0–5) 0.3 ± 0.3 (0–5) – – – – – – – 1.4 ± 1.0 (0–20)
4.2 ± 4.2 (0–50) – 58.9 ± 7.7 (30–100) 60.6 ± 8.8 (0–100) 41.5 ± 9.9 (0–100) – – 86.0 ± 7.5 (60–100) – 70.6 ± 7.3 (20–100) – – 25.2 ± 5.6 (0–100)
3.3 ± 2.3 (0–20) – – 3.6 ± 3.6 (0–50) – – – – – – – – –
O D C C O D D C D C D D O
– – – – – – 0.5 ± 0.5 (0–5)
14.3 ± 7.2 (0–40) 20.0 ± 16.3 (0–100) 57.5 ± 9.1 (10–100) 60.1 ± 5.6 (0–100) 67.5 ± 11.8 (50–100) 73.8 ± 9.6 (30–100) 7.7 ± 7.3 (0–80)
– – – – – – –
O O C C C C O
there are not always clear relationships among these characters and the digestive contents. Only the diet of 2 of the 17 species considered had previously been studied based in the gut contents. The data obtained in the present study for these two species, Pariambus typicus and Phtisica marina, agree with those obtained by Guerra-García and Tierno de Figueroa (2009). On the other hand, the knowledge about feeding habits in amphipods is limited, in some cases, to family level. In this sense, our results usually agree with the previous literature. According to our data, Siphonocetes sabatieri is a strictly detritivorous species, which agree with the previously recorded for the Corophidae family (Bellan-Santini and Ruffo, 1998). Studying the crop contents of some phoxocephalid species, Oliver et al. (1982) concluded that this group acts as a key taxon in soft bottom communities, playing an important functional role as carnivorous. Other studies using stable isotope analyses also showed
and outside. However, the percentage of silt and clay was significantly higher inside the caves (Fig. 6). 4. Discussion The present work is the first comprehensive study on the feeding habits of amphipod species inhabiting soft bottom communities. There are very few studies dealing with the diet of amphipod species and this biological aspect is unknown for many of them (Scipione, 1989). Moreover, the knowledge about the feeding of many species was based on assumptions from fecal pellet composition or morphological characters, but these assumptions must be taken carefully since they are not always fulfilled. For example, the feeding habit of caprellids has been traditionally inferred from mouthparts or antennae morphology (Caine 1974, 1977); however, Guerra-García and Tierno de Figueroa (2009) showed that
Harpinia crenulata IN Harpinia crenulata OUT Harpinia pectinata IN Harpinia pectinata OUT Perioculodes longimanus OUT Monoculodes griseus IN Perioculodes longimanus IN Metaphoxus fultoni OUT Hippomedon massiliensis OUT Harpinia antennaria IN Gammarella fucicola IN Urothoe elegans OUT Phtisica marina IN Ampelisca brevicornis OUT Pariambus typicus OUT Megaluropus monasteriensis OUT Leptocheirus hirsutimanus OUT Bathyporeia guilliamsoniana OUT Siphonoecetes sabatieri OUT Photis longipes OUT
40
60
80
100
Bray Curtis Similarity (%) Fig. 3. Dendrogram based on the digestive contents of the studied amphipod species inside and outside the caves.
CARNIVOROUS
% abs
DETRITIVOROUS OMNIVOROUS
N/n
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100%
5
OUT IN
OUT IN
OUT IN
ABUNDANCE
Harpinia crenulata
Harpinia pectinata
Perioculodes longimanus
Detritivorous
Microalgae
100%
80%
80%
60%
60%
40%
40%
20% 20%
0% Outside
Inside
Outside
NUMBER OF SPECIES Omnivorous
Carnivorous
0%
Inside
Prey
Detritus
Fig. 4. Contribution in percentage of each feeding group to the total number of species and abundance.
Fig. 5. Contribution of each feeding component for the three species inhabiting both inside and outside of the caves. See also Table 3.
the carnivorous behavior of Harpinia species (Fanelli et al., 2009). Our data support this assertion, since almost all the phoxocephalid species studied (H. pectinata, H. crenulata and Metaphoxus fultoni) had a diet mainly composed by crustaceans. Nevertheless, in some cases, species belonging to the same family or even genus showed different feeding habits. For example, Harpinia antennaria had an omnivorous diet in the present study. Urothoe elegans was omnivorous while Bathyporeia guilliamsoniana (both of them belonging to Haustoridae family) fed exclusively on detritus. These results show that the feeding habits of an unstudied species cannot be inferred from studies of congeners, as it has been noted for other aquatic invertebrates (e. g. Stewart and Stark, 2002), and consequently gut content analyses are needed to correctly assign each taxon to each feeding group. Within the same species, variations in the trophic preferences can also be found when studying different environments. In a comparative work carried out in the Mediterranean to study the variations in the gut contents of some amphipod species living in native and invasive seaweeds, Vázquez-Luis et al. (2012) found that some species (such as Ampithoe ramondi or Dexamine spiniventris) had different feeding modes depending on the habitat they live on. In the same way, Alarcón-Ortega et al. (2012) reported variations in the feeding behavior of the caprellids Aciconula acanthosoma and Caprella equilibra when they live in algae, hydroids or gorgonians. In our study, the three species found both inside and outside the caves did not show significant changes in their gut components between both habitats. The absence of differences in the feeding modes for H. crenulata, H. pectinata, and
P. longimanus (all of them carnivorous) between habitats could be due to the availability of this food source inside and outside the caves. Strong differences between habitats can also been found when all amphipod assemblages are considered. Our data reflects that amphipod diet in sediments is less diverse than in other environments such as algae and seagrasses (Guerra-García and Tierno de Figueroa, 2009; Vázquez-Luis et al., 2012). The percentage of algae in the gut contents was zero or very low in all cases. Obviously, that pattern was expected inside the caves, where no primary producer is present, but it is remarkable that no herbivorous species could be found in the external sediments. The variety of prey in carnivorous species was also lower, composed mainly (and often exclusively) by crustaceans. Diet diversity in soft bottom amphipod assemblage was even less diverse inside the caves. No detritivorous species was present inside the caves and, while this feeding group was the dominant group (both number of species and number of individuals) in the external sediments, cave community was dominated by carnivorous species. This pattern in amphipod species is highly unexpected since the general pattern in cave communities drives organisms toward a generalist diet (with a dominance of omnivorous and detritivorous species). However, as in such case, some particular groups can follow a different trend. Bianchi (1985) found a high percentage of carnivorous species in polychaete assemblages of marine cave. According to Romero (2009), cave amphipods feed mostly on detritus but our data show that they occupy mainly the role of carnivorous. The reason of the absence of detritivorous amphipods into these caves remains still uncertain. A potential factor could be the limited food supply, since marine caves are usually considered as oligotrophic habitats. Experimental studies on vegetated habitats reveal that species richness and abundance of amphipods were highly and positively related with the detritus content (Vázquez-Luis et al., 2009). However, our chemical data showed significant higher concentrations of organic matter inside the caves, although it has been suggested that the quality of organic matter in marine caves may decrease toward the inner parts (Fichez, 1991). The feeding behavior, not only the feeding group, should be also an important factor to consider. Because of the low hidrodinamism inside caves, strong differences between habitats can be expected in the way in which such organic matter is available to organisms. Thereby, while inside the caves the organic matter percentage in the sediment is higher, the suspended detritus is much less abundant.
Table 3 Results of the two-factor ANOVA for percentage of detritus in the amphipod species inhabiting outside and inside of the caves: Harpinia crenulata, H. pectinata and Perioculodes longimanus. MS=mean square; df=degrees of freedom. Source of variation
Position (Po) Species (Sp) Po × Sp Residual Cochran's C-test Transformation
%detritus df
MS
F
P
1 2 2 42
75.00 506.25 1406.25 921.43
0.08 0.55 1.53
0.78 0.58 0.23
C = 0.22 None
6
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ORGANIC MATTER
colonize such habitats, among others, which can act like a limiting factor for the presence of detritivorous. Further studies about the ecological conditions in marine caves and the feeding habit and behavior of all the soft-bottom community are necessary to understand the trophic dynamic of such environments.
1,5
Acknowledgments
1
Financial support of this work was provided by the Ministerio de Educación y Ciencia (Project CGL 2011-22474/BOS). This work forms part of C.N-B's Ph.D. Thesis, supported by the Universidad de Sevilla (PIF Grant).
%
References
0,5
0
Outside
Inside
GRANULOMETRY 100
75
% 50
25
0
Outside
Inside
Gross-very gross sands and gravels Very fine and fine sands
Medium sands
Silt and clay
Fig. 6. Organic matter and granulometry in the studied caves. Data are mean values of the six caves (for organic matter standard error of the mean is also included).
In that way, gatherer–collectors find abundant settle detritus to feed inside caves while filter feeders should have more problems to colonize cave environments, since they need more exposed habitats, with a greater degree of turbulence. Nevertheless, little is known about the feeding behavior of detritivorous species present inside our caves and about amphipods in general. Moreover, Shillaker and Moore (1987) pointed out that some detritivorous species can even change its feeding methods, using alternative techniques in poor feeding conditions. So, we cannot relate assertively the absence of detritivorous species inside the caves with their feeding behavior. The finer sediment inside the caves neither seems to be the problem, since many of the detritivorous species present outside the caves usually inhabit muddy sediments (Bellan-Santini et al., 1982, 1989, 1993). There are many other physical gradients (light, salinity or oxygen) and the low capacity of the larvae to
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