Trophodynamic studies on the Condor seamount (Azores, Portugal, North Atlantic)

Deep-Sea Research II 98 (2013) 178–189

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Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2

Trophodynamic studies on the Condor seamount (Azores, Portugal, North Atlantic) A. Colac- o n, E. Giacomello, F. Porteiro, G.M. Menezes Centre of IMAR of the University of the Azores, Department of Oceanography and Fisheries, and LARSyS Associated Laboratory, Rua Prof. Doutor Frederico Machado, 4. 9901-862 Horta, Portugal

a r t i c l e i n f o

a b s t r a c t

Available online 4 February 2013

Compared to the surrounding ocean waters, seamounts are commonly considered habitats where biological productivity is higher and consumers proliferate. Despite their high productivity, studies of seamount trophic webs are still scarce and fragmentary, and little is known about the connections between the different compartments. What are the trophic interactions of seamount fauna? How do the pelagic and benthic environment couple? In order to answer these questions, stable isotopes d15N and d13C were measured in the organisms collected during the course of numerous campaigns at the Condor seamount in the North Atlantic. The Condor seamount food chain is composed of five trophic levels. Mesopelagic organisms are the link between the epipelagic environment and the benthic and benthopelagic organisms, bridging the gap between primary consumers and the 4th and 5th trophic chain levels. Our results demonstrate, through stable isotope analysis, the important role of mesopelagic organisms in the transfer of energy within the seamount food web, as modeling/ theoretical studies have previously suggested. & 2013 Elsevier Ltd. All rights reserved.

Keywords: Stable Isotopes Trophic position Seamount benthopelagic coupling North Atlantic Azores

1. Introduction One of the challenges for organisms living in the deep sea is a general scarcity of food (Gooday and Turley, 1990) reflecting the dependence on photosynthetic primary production concentrated in the upper 100 m of the water column. Consequently, primary and higher-level pelagic consumers are much more abundant in the epipelagic layers than in deeper pelagic waters. Similarly, seabed communities in the photic zone associated with continental and insular land masses are more productive than benthic deep-sea communities (Polis et al., 1997). Traditionally, trophodynamic studies are carried out using gut content analysis; however, this technique assesses diet over very short temporal scales (Hyslop, 1980), it requires high sampling effort, which is a major disadvantage in deep-sea systems, and it may underestimate the extent of generalist and detritus feeding organisms (Carassou et al., 2008). A classical way to trace food sources of aquatic animals is stable isotope analyses (Peterson and Fry, 1987a). The technique provides alternative measures of trophic position and production source and circumvents many of the weaknesses and difficulties inherent in gut content data (Post, 2002).

n

Corresponding author. E-mail address: [email protected] (A. Colac- o).

0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.01.010

Stable isotope analysis utilizes naturally occurring differences in the ratios 15N/14N (d15N) and 13C/12C (d13C) in tissues between consumers and their diet (Peterson and Fry, 1987b). These differences arise due to preferential retention of heavier isotopes and excretion of lighter isotopes, leading to relative enrichment of heavier isotopes in the body tissue of the organisms. Stable isotope ratios of nitrogen may be used to reconstruct food webs and estimate the trophic level of consumers (Cabana and Rasmussen, 1994). Natural stable isotope abundance techniques have been successfully used to define the functional role of marine organisms (Ehleringer et al., 1986; Riera, 1998), carbon sources and trophic links in the deep sea (e.g. Bergmann et al., 2009; Colac- o et al., 2002; Fanelli et al., 2009, 2011; Iken et al., 2001). The number of trophic levels in marine ecosystems average between four and six and appears to be higher in coastal systems, reefs and shelves, and lower in upwelling systems (e.g. Christensen and Pauly, 1993). Seamounts are commonly regarded as habitats where biological productivity is high and consumers proliferate (Fock et al., 2002; Genin et al., 1988; Richer de Forges et al., 2000). Production is supported by a variety of energy inputs, most likely in the form of zooplankton and micronekton horizontally advected or trapped over the seamount during diel vertical migrations (reviewed in Rowden et al. (2010)). Persistent vertical nutrient fluxes and retention above seamounts with consequent enhancement and maintenance of autochthonous productivity and trophic uplift

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

have not been observed. Over the Seine and Sedlo seamounts (Northeast Atlantic) no evidence was found of any significant permanent increase in primary production, casting doubt on the role of Taylor columns in this process. These features are normally non-permanent and are present in a lesser degree when compared with changes caused by temporal or regional variability (Arı´stegui et al., 2009). This is consistent with the results of Santos et al. (2013) and Carmo et al. (2013) that show evidence of higher seasonal than spatial variability of phytoplankton and zooplankton species composition and abundance on the Condor seamount as has been observed on other seamounts in the NE Atlantic (Martin and Christiansen, 2009). Isaacs and Schwartzlose (1965) showed that the food supplied to the seamount community via topographic trapping of vertical migrating species can be as much as 40 times greater than local productivity (‘‘trophic blockage hypothesis’’). Concurrently, lateral advection of pelagic organisms to the seamount summits and slopes is a form of trophic subsidy, importing allochthonous food to the local community (Genin and Dower, 2007). The evidence of seamount communities energy dependence from allochthonous sources is growing (McClain, 2007; Schlacher et al., 2010). The increased productivity in these isolated oceanic systems is thought to provide a unique deep-sea environment to support dense aggregations of sessile (e.g. corals and sponges) and vagile (e.g. crustaceans) epibenthic organisms as well as benthopelagic fishes (Clark, 2001; Dower and Perry, 2001; Koslow, 1997; Koslow et al., 2000; Morato et al., 2009; Rogers, 1994) that are not found in the open ocean or in the adjacent bathyal and abyssal plains (Boehlert and Mundy, 1993; Koslow, 1997; Richer de Forges et al., 2000). Moreover, it has been shown that seamounts often attract epipelagic organisms, such as large tunas, seabirds and cetaceans that rely on the enhanced concentration of pelagic biomass over these structures to feed (Morato et al., 2008, 2010b). Seamount food webs can be quite complex. The primary producers in a seamount food chain are phytoplankton, but bacteria and organic detritus (from dead and dying organisms, for example) are thought to play an important role at the base of these food webs (e.g. Haury et al. (1995)). Primary consumers (zooplankton) link the first trophic level to subsequent levels. Epibenthic macro- and megafauna such as cold-water corals and sponges are mainly suspension feeders. Most of these species require an enhanced water flow that provides a steady supply of organic particles, including zooplankton (Rogers, 1994; Wilson and Kaufmann, 1987), but feeding behavior and preferences are not well known (Roberts et al., 2006; Rogers et al., 2007). Relatively little research has been conducted on seamounts at the ecosystem level. However, recent advances have been made through science programs like OASIS ‘‘Oceanic Seamounts: an Integrated Study’’ (2002–2005) (Christiansen and Wolff, 2009), the International Census of Marine Life program on seamounts ‘‘CenSeam’’ (2005–2010) and CONDOR EEA grants program. In the past few decades, considerable research was devoted to seamount ecology, including the reviews of Keating et al. (1987), Rogers (1994), Pitcher et al. (2007) and Clark et al. (2010). Although several papers have already focused on the different compartments of the seamounts, i.e. residents and aggregators versus visitors; benthic structuring organisms and benthic fauna; zooplankton; predators and detritivores (Morato et al., 2009, 2008; Pusch et al., 2004a, 2004b; Samadi et al., 2007), little is known about how all these compartments are interconnected. The main goals of this work are to: (i) identify the trophic interactions on the Condor seamount; (ii) and understand the coupling between pelagic and benthic organisms.

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2. Materials and methods 2.1. Study site The Condor seamount, located about 18.5 km (10 nautical miles) southwest of Faial Island in the Azores archipelago, has been used for about three decades as a fishing ground by local bottom longline commercial fleet. However since 2009 it has been temporarily closed to demersal commercial fishing to allow for the installation of a scientific underwater seamount observatory (Giacomello et al., 2013; Morato et al., 2010a). The seamount is about 1 km high, 26 km long and 7.4 km wide, and rises to a minimum depth of 180 m (Tempera et al., 2012). It has an elongated shape, almost flat on top with two major peaks, and lies in an approximately east–west orientation. It supports rich assemblages of cold-water alcyonacean corals, sponges, sea urchins, crabs and fishes, some of which are of commercial interest (Tempera et al., 2012; and see papers in this volume). 2.2. Sample collection The different seamount faunistic compartments were sampled during numerous surveys, mostly conducted by the R/V Arquipe´lago. Several surveys sampled decapods with baited traps (Nagib et al., 2004). Demersal bathyal fishes were collected by bottom long-lines. Zooplankton species were caught by a Bongo net. Mesopelagic fauna were surveyed with a 100 Isaacs Kidd Midwater Trawl (IKMT 100 ) operated from the R/V Noruega, in July 2010. Sessile megafauna, such as corals and sponges, were collected from the by catch of bottom fishery surveys. A few samples were obtained by the ROV Luso on board the R/V Gago Coutinho, during visual survey transects for habitat mapping. A total of 397 samples of macro- and megafauna from 65 different taxa and 9 particulate organic matter (POM) samples were collected. The zooplankton was divided into five major groups: large copepods; small copepods; decapods larvae; euphausiids; mysids and ‘‘gelatinous organisms’’ (which include tunicates, ctenophores and scyphozoans). Fish, crustaceans and sessile invertebrates were identified to the lowest taxonomic level as possible. In order to understand the trophic interactions and the benthic–pelagic coupling, stable isotopes analyses were performed for all the collected material. 2.3. Sample preparation Samples were immediately frozen after collection. At the shore laboratory, plankton samples were thawed, sieved and sorted into major groups. The muscle or soft tissues were freeze-dried and homogenized with a mortar and pestle. Where available, invertebrate and fish samples comprised 3 replicates per species and generally included one individual per sample. For the small copepods, euphausiids and chaetognaths, the individuals were pooled to obtain the dry weight necessary for analysis, and several pools were obtained (See Table 1). Samples with carbonate structures were subsampled. The subsample used for carbon isotope analysis was acidified by adding 1 M HCl, drop by drop, to remove inorganic carbonates. This is necessary, since inorganic carbon gives a much stronger signal compared to organic carbon. The other subsample used for nitrogen analysis was not acidified since acidification alters the nitrogen signal (Serrano et al., 2008). Particulate organic matter (POM) was sampled by filtering  5 l seawater collected at 50 m below the surface and at the maximum depth around the Condor seamount (just above the seafloor, see Table 1). Each POM sample was recovered on 1 single pre-combusted (450 1C; 4 h) 47 mm Whatman GF/F filters.

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Table 1 d13C and d15N values (%) of food web components that were collected at the Condor seamount. (a) Mean d13C and d15N values (%) of the particulate organic matter (POM) the Condor seamount. SD ¼ standard deviation; n¼ number of individuals measured Sampling depth (m) d15N mean 7SD d13C mean7 SD 4.23 72.49 7.8 70.97 6.84 70.12

50 250 500

 25.51 7 1.49  23.71 7 1.54  25.17 7 0.30

n 4 3 2

Trophic type

Phylum Porifera Porifera

10.6 7 2.16

 19.6 71.25

5.07 0.77

 18.07 0.86

3.9

17

Mesobenthic

Suspension feeders

Sestonivores

Antenella secundaria Lytocarpia myriophyllum Polyplumaria flabellata

7.7 7 0.14 9.3 7 0.03 8.3 7 0.07

 20.97 0.17  19.2 70.04  19.8 70.29

3.8 70.06 3.3 70.09 3.8 70.10

 20.57 0.11  19.3 70.13  19.4 70.39

3.1 3.5 3.2

2 2 3

Mesobenthic Mesobenthic Mesobenthic

Suspension feeders Suspension feeders Suspension feeders

Sestonivores Sestonivores Sestonivores

Various scyphozoa

6.2 7 0.91

 19.8 70.52

2.9 70.53

 20.27 0.42

2.6

8

Mesopelagic

Predators

Zooplanktivores

Actinaria

8.7 7 1.00

 18.7 70.44

3.07 0.45

 19.1 70.66

3.4

4

Mesobenthic

Suspension feeders

Sestonivores

Acanella arbuscula Candidella imbricata Dentomuricea cf. meteori Viminella flagellum

8.8 9 8.1 7 1.23 6.9

 21.3  21.2  20.97 0.48  21.4

4.7 4.3 3.9 70.59 3.3

 19.9  20.2  20.47 0.86  21.4

3.4 3.4 3.2 2.8

1 1 15 1

Mesobenthic Mesobenthic Mesobenthic mesobenthic

Suspension feeders Suspension feeders Suspension feeders suspension feeders

Sestonivores Sestonivores Sestonivores sestonivores

Ctenophora

6.8

 19.5

3

 19.8

2.8

1

Mesopelagic

Predators

Zooplanktivores

Bryozoa

8.4

 19.2

3.9

 18.7

3.3

1

Mesobenthic

Suspension feeders

Sestonivores

Gastropoda Pteropoda

8.9 7 0.03 5.2

 18.4 70.14  21.9

3.8 70.08 4.6

 18.07 0.06  20.6

3.4 2.3

2 1

Mesobenthic Epipelagic

Predators Suspension feeders

Benthivores Herbivores/omnivores

Copepoda (large) Copepoda (small)

5.7 7 0.31 4.7 7 0.48

 21.7 70.46  21.9 70.40

4.7 70.43 4.8 70.37

 20.47 0.35  20.57 0.29

2.5 2.2

24 28

Epipelagic Epipelagic

Filter feeders Filter feeders

Omnivores/zooplanktivores Herbivores/omnivores

Euphasiacea Euphasiacea

6.3 7 0.32 6.9 7 1.3

 20.47 0.40  20.057 0.07

3.9 70.30 3.3 70.14

 19.9 70.47  20.15 70.21

2.7 2.8

23 4

Epipelagic Mesopelagic

Filter feeders Filter feeders

Herbivores/omnivores Omnivores/zooplanktivores

Phylum Cnidaria Class Hydrozoa

Class Scyphozoa Class Anthozoa Order Actinaria Order Alcyonacea

Phylum Ctenophora Phylum Bryozoa Phylum Mollusca Class Gastropoda

Phylum Arthropoda Subphylum Crustacea Class Maxillopoda Subclass Copepoda

Class Malacostraca Order Euphausiacea

Order Decapoda

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

(b) Mean d13C and d15N values (%) of food web components that were collected at the Condor seamount. SD ¼standard deviation; n¼ number of individuals measured Phylum/Class/Order Lowest taxonomic level C/N mean 7 SD d13C lipid corrected Trophic n Habitat Feeding mode d15N mean d13C mean Position 7SD 7 SD mean 7 SD

Decapoda Decapoda Nematocarcinus sp. Decapod larvae Heterocarpus ensifer Ligur ensiferus Oplophorus sp. Plesionika edwardsii Plesionika martia Plesionika williamsi

7.1 7 1.35 5.6 6.2 6.4 7 0.21 9.0 7 0.28 10.4 7 0.31 8.04 7 0.55 7.9 7 0.44 8.2 7 0.17 10.2 7 0.49

 19.9 70.41  20.8  19.2  20.17 0.05  18.5 70.23  17.7 70.06  19.83 7 0.38  18.1 70.16  18.2 70.11  17.9 70.29

3.4 70.10 3.1 3.1 3.8 70.05 3.2 70.03 3.2 70.05 3.3 70.08 3.1 70.04 3.07 0.03 3.1 70.05

 19.9 70.32  21  19.4  19.6 70.05  18.7 70.21  17.9 70.11  19.8 70.36  18.4 70.15  18.5 70.11  18.2 70.34

2.9 2.4 2.6 2.7 3.4 3.9 3.2 3.1 3.2 3.8

3 1 3 4 3 4 9 28 12 3

Gnathophausia sp.

7.6 7 0.44

 20.47 0.30

3.8 70.16

 20.07 0.27

3.1

Polychaeta

9.5 7

 19.9 7

3.9 7

 19.4

11.6 7 0.31

 21.2 70.23

6.3 70.18

6.5 7 1.74

 20.67 0.60

1.3 7 0.10

Mesopelagic Mesopelagic Mesopelagic Epipelagic Mesobenthopelagic Mesobenthopelagic Mesopelagic Mesobenthopelagic Mesobenthopelagic Mesobenthopelagic

Predators Predators Predators Filter feeders Predators Predators Predators Predators Predators Predators

Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores

9

Mesopelagic

Filter feeders

Zooplanktivores

3.6

1

Mesobenthic

Predators

Benthivores

 18.3 70.41

4.2

2

Mesobenthic

Scavengers

Scavengers

3.3 70.28

 20.67 0.41

2.7

7

Mesopelagic

Predators

Zooplanktivores

 23.1 70.08

4.6 70.24

 21.8 70.22

1.2

3

Epipelagic

Filter feeders

Herbivores/omnivores

12.2 7 0.51 11.9 7 0.29 11.2 7 0.28 10.4 7 0.48 10.6 7 0.24

 17.5 70.13  17.4 70.19  18.2 70.12  19.07 0.48  18.5 70.21

2.7 70.02 2.6 70.09 2.5 70.09 2.7 70.14 2.5 70.11

 18.1 70.11  18.2 70.27  19.07 0.15  19.6 70.40  19.3 70.11

4.5 4.3 4.1 3.9 3.9

3 3 6 8 6

Bathybenthopelagic Bathybenthopelagic Mesobenthic Mesobenthic Mesobenthopelagic

Predators Predators Predators Predators Predators

Mixed Mixed Mixed Mixed Mixed

10.7 7 0.19 12.9 7 0.36 7.8 7 0.63 11.4 7 0.24 10.7 7 1.27 10.1 7 0.61 8.7 7 0.56 8.2 7 1.07 6.0 7 0.23 8.6 7 0.54 10.6 7 0.59 10.5 7 0.21 7.9 7 0.43 7.6 10.4 7 0.21 9.5 7 0.32 9.0 7 0.44 11.9 7 0.36 11.6 7 0.37 9.0 7 1.08 10.3 7 0.81 12.3 7 0.33 11.6 7 0.46 11.7 7 0.44 10.6 7 0.55 9.7 7 0.58

 18.4 70.15  18.7 70.33  19.5 70.45  18.8 70.15  19.5 71.03  19.1 70.19  19.8 70.79  20.07 0.37  20.77 0.16  20.67 0.78  18.9 70.22  18.7 70.20  21.1 70.03  21.3  19.7 70.21  20.47 0.16  22.4 70.79  18.2 70.14  18.5 70.36  20.47 0.36  19.2 70.72  18.2 70.16  18.4 70.29  18.5 70.20  18.7 70.17  20.27 1.12

3.1 70.02 3.2 70.22 3.1 70.35 3.2 70.01 3.6 71.26 3.1 70.11 3.3 70.21 3.3 70.13 3.5 70.05 3.7 70.48 3.1 70.04 3.1 70.08 3.8 70.14 4.5 3.4 70.15 3.4 70.09 5.1 70.74 3.07 0.04 3.2 70.09 3.3 70.11 3.5 70.63 3.07 0.05 3.07 0.05 3.2 70.01 3.07 0.08 3.8 70.76

 18.7 70.15  18.8 70.22  19.8 70.10  18.9 70.16  19.2 70.33  19.4 70.11  19.8 70.58  20.17 0.26  20.67 0.12  20.27 0.35  19.1 70.20  19.07 0.24  20.67 0.11  20.2  19.7 70.25  20.37 0.15  20.77 0.10  18.5 70.14  18.7 70.30  20.47 0.47  19.1 70.30  18.5 70.14  18.8 70.27  18.6 70.19  19.07 0.21  19.7 70.37

3.9 4.6 3.1 4.2 4.0 3.8 3.4 3.1 2.6 3.3 3.9 3.9 3.1 3.1 3.9 3.6 3.5 4.3 4.2 3.5 3.8 4.4 4.2 4.3 3.9 3.7

3 4 3 2 6 6 2 3 3 3 3 7 3 1 5 5 3 6 3 2 18 5 6 2 7 7

Epibenthic Bathypelagic Mesopelagic Mesobenthopelagic Mesobenthopelagic Mesobenthopelagic Epipelagic Mesopelagic Mesopelagic Mesopelagic Mesobenthopelagic Mesobenthic Mesopelagic Mesopelagic Mesobenthopelagic Mesopelagic Epipelagic Mesobenthic Epibenthic Mesopelagic Mesobenthopelagic Mesobenthopelagic Mesobenthic Mesobenthopelagic Mesobenthic Epipelagic

Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators Predators predators Predators Predators predators Predators

Benthivores Micronektivores Zooplanktivores Benthivores Micronektivores Micronektivores Zooplanktivores Zooplanktivores Zooplanktivores Zooplanktivores Mixed diet Mixed diet Zooplanktivores Zooplanktivores Micronektivores Zooplanktivores Zooplanktivores Micronektivores Mixed diet Zooplanktivores Mixed diet Mixed diet Mixed diet Mixed diet Mixed diet Micronektivores

Order Lophogastrida Phylum Annelida Class Polychaeta Phylum Echinodermata Class Asteroidea Asteroidea Chaetognatha Phylum Chordata Subphylum Tunicata Class Thaliacea

diet diet diet diet diet

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Pyrosoma sp. Subphylum Vertebrata Class Chondrichthyes Centroscymnus cryptacanthus Centroscymnus crepidater Deania profundorum Etmopterus pusillus Etmopterus spinax Class Actinopterygii Acantholabrus palloni Aphanopus spp. Argyropelecus aculeatus Benthocometes robustus Beryx decadactylus Beryx splendens Capros aper Chauliodus sloani Cyclothone sp. Diaphus rafinesquii Gadella maraldi Helicolenus dactylopterus Lampanyctus pusillus Lepidophanes guentheri Lepidopus caudatus Lobianchia gemellarii Macroramphosus scolopax Mora moro Muraena helena Notoscopelus bolini Pagellus bogaraveo Phycis blennoides Phycis phycis Polyprion americanus Pontinus kuhlii Scomber colias

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Phylum Chaetognatha

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

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Zooplanktivores Micronektivores Mixed diet Zooplanktivores Zooplanktivores Zooplanktivores

Carbon and nitrogen stable isotope analyses were carried out using a Thermo Finnigan Delta Plus XP IRMS coupled to a Costech 4010 Elemental Analyzer. The isotope ratios of the different samples were calculated according to the following equation:

d13 C or d15 Nð%Þ ¼ ½ðR sample=R standardÞ1  1000 13

12

15

ð1Þ

14

2.9 3.6 4.0 3.7 3.3 3.5

7 1 4 8 1 2

Mesopelagic Mesopelagic Bathybenthopelagic Mesobenthopelagic Mesopelagic Mesopelagic

Predators Predators Scavenger Predators Predators Predators

where R ¼ C/ C or N/ N. Lipids are depleted in 13C and typically have d13C values that are more negative than those for proteins and carbohydrates within an individual organism (DeNiro and Epstein, 1977). This fact has the potential to influence stable isotope analyses using d13C. Some authors suggest extracting lipids from samples prior to stable isotope analysis. Chemical extraction methods typically use a methanol–chloroform solution to physically remove lipids from samples (eg. Bligh and Dyer 1959; White et al., 1979), reducing lipid concentrations to a uniformly low level. These techniques are advantageous because they remove the majority of lipids, creating uniform samples for comparison. However, they may cause fractionation in d15N (Hoffman and Sutton, 2010) and they are time-consuming. Here we used the mathematical normalization technique proposed by Post et al. (2007), which has been used by several authors working with deep-sea organisms (Carlier et al., 2009; Fanelli et al., 2009) since it reduces biases in d13C and better preserves the integrity of samples for d 15N analysis. The correction of d13C for lipid content according to Post et al. (2007) is

d13 C0 ¼ d13 C23:32 þ ð0:99  C : NÞ  20.37 0.28  19.2  19.07 0.18  19.2 70.09  20.5  20.27 0.00

where d13C0 represents lipid-corrected d13C values, d13C the carbon isotope value of the sample, and C:N is the carbon-tonitrogen ratio by mass of each sample. As a number of authors have previously published data for the deep sea without the lipid correction proposed by Post et al. (2007), uncorrected d13C is also reported here. However, only the lipid corrected values were analyzed and discussed further.

3.4 70.53 3.2 3.2 70.07 3.1 70.06 3.3 3.2 70.02

2.5. Trophic position

SD stands for standard deviation; n stands for number of individuals measured.

 20.47 0.38  19  18.9 70.23  18.9 70.07  20.5  20.07 0.02 7.1 7 0.97 9.5 10.8 7 0.23 9.9 7 0.38 8.6 9.2 7 0.62 Stomias boa ferox Stomias longibarbatus Synaphobranchus kaupii Trachurus picturatus Valencienellus tripunctulatus Xenodermichthys copei

(b) Mean d13C and d15N values (%) of food web components that were collected at the Condor seamount. SD ¼standard deviation; n¼ number of individuals measured Phylum/Class/Order Lowest taxonomic level C/N mean 7 SD d13C lipid corrected Trophic n Habitat Feeding mode d15N mean d13C mean Position 7SD 7 SD mean 7 SD

Table 1 (continued )

Trophic type

2.4. Stable isotope analyses

Trophic position of the studied organisms was calculated following Post (2002), where d15N values were converted to trophic position, based on the assumption of a 3.4% fractionation per trophic level and the baseline (Primary consumers¼ herbivores copepods) equal to trophic position 2: 15

15

TPi ¼ ðd Ni2d NPC=3:4Þ þ 2; where TPi represents the trophic position of organism i, d15Ni is the mean d15N of organism i, and d15NPC is the mean d15N of the baseline of the food web (Primary consumers¼2). The maximum trophic position (MTP) is the highest trophic position calculated. 2.6. Statistics Each sample/taxon was also classified by the main habitat type where it lives according to Kukuev (2004) (epibenthic, epipelagic, epibenthopelagic [0–200 m], mesobenthic, mesopelagic, mesobenthopelagic [200–1000 m], bathypelagic, bathybenthopelagic [41000 m]), by its known feeding mode (predators, scavengers, filter feeders and suspension feeders) and by its known trophic type (herbivores/omnivores; omnivores/zooplanktivores; zooplanktivores; micronektivores; mixed diet; sestonivores; benthivores; scavengers), based on information from Nybakken (1997) and Fishbase (Froese and Pauly, 2012). Principal Coordinates Analysis (PCO) was used to identify groups of samples and patterns

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

of isotopic composition. Differences in isotope d15N and d13C0 signatures between habitats and feeding types of the sampled organisms were also examined using permutational analysis of variance (PERMANOVA; Andersen, 2001; Andersen et al., 2008). Resemblance matrices were obtained using Euclidean distance. The Type III SS and permutation of residuals under a reduced model were applied. All these tests were performed using the PRIMER-E software (Clarke and Gorley, 2006) with the add-on package PERMANOVAþ (Andersen et al., 2008).

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obtained from the 65 taxa analyzed fits within a range of 4% (  21 to 18%; Table 1), with some outliers belonging to the Tunicate and Porifera phyla, increasing the range to 6%. All the organisms analyzed showed d15N values consistent with consumers, with the exception of the Pyrosoma sp., which presented a value resembling that of an autotroph (Table 1). Primary consumers (trophic position o2.5) are represented by phytoplankton feeders copepods, and pteropods, the latter feeding mainly through large mucus webs acting as filters (Tsurumi et al., 2005). Large copepods, euphausiids, mysids and some decapod larvae (which are omnivorous, feeding on phytoplankton, dinoflagellates and zooplankton) are at the same position but with a higher score of trophic level. While the majority of filter feeders (crustaceans) occupy the 2nd and 3rd trophic positions, the suspension feeders (corals and sponges), were classified at the 3rd and 4th trophic positions and the predators/scavengers at the 4th and 5th. The mesopelagic organisms occupy the 3rd and 4th trophic positions.

3. Results The d13C and d15N average values obtained for the faunistic components of the food web collected at the Condor Seamount ranged from 25.51% to  17.4% and from 1.3% to 12.9%, (Table 1 and Fig. 1). A 5-position trophic chain characterizes the Condor seamount (Table 1). The majority of the d13C values Bathyal

13

12

11 Mesobenthic

δ15N ‰

10

9

8 Mesobenthopelagic

7 Mesopelagic

6

5 Epipelagic

-22

-21.5

-21

-20.5

-20

-19.5

-19

-18.5

-18

-17.5

4 -17

δ13C ‰ Actinaria, mesobenthic Bryozoa, mesobenthic Ctenophora, mesopelagic Decapoda, mesobenthopelagic Gastropoda, mesobenthic Vertebrata, epipelagic Vertebrata, mesobenthopelagic Vertebrata, bathypelagic

Alcyonacea, mesobenthic Chaetognatha, mesopelagic Decapoda, epipelagic Euphauseacea, epipelagic Hydrozoa, mesobenthic Vertebrata, epibenthic Vertebrata, mesobenthic Polychaeta, mesobenthic

Asteroidea, mesobenthic Copepoda, epipelagic Decapoda, mesopelagic Euphauseacea, mesopelagic Lophogastrida, mesopelagic Vertebrata, mesopelagic Vertebrata, bathybenthopelagic Porifera, mesobenthic

Fig. 1. d13C and d15N of food web components that were collected at the Condor seamount by taxon and habitat. For a better reading the Tunicate value which presents a d15N of 1.3 is not showed in the graph.

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

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Nearly all the benthic crustaceans and corals were found to occupy trophic position 3 (secondary consumers), with different carbon sources in their diet. The trophic positions of the benthic communities (sponges, corals, anemones) ranged from position 3 to 5.

Within the suspension feeders two different signal groups were distinguishable: Alcyonacea and some sponges being at trophic position 3; and sponges at a very high trophic position, close to that of the bathybenthopelagic top predators and scavengers.

Resemblance: D1 Euclidean distance

PCO2 (7,6% of total variation)

5

Habitat epipelagic epibenthic mesopelagic mesobenthopelagic mesobenthic bathypelagic bathybenthopelagic

0

-5 -10

-5

0 PCO1 (92,4% of total variation)

5

10

Resemblance: D1 Euclidean distance

PCO2 (7,6% of total variation)

5

Trophic type herbivores/omnivores omnivores/zooplanktivores zooplanktivores sestonivores micronektivores mixed diet benthivores scavengers

0

-5 -10

-5

0 PCO1 (92,4% of total variation)

5

10

Resemblance: D1 Euclidean distance

PCO2 (7,6% of total variation)

5

Feeding mode filter feeders suspension feeders scavengers predators

0

-5 -9

-4

1 PCO1 (92,4% of total variation)

6

11

Fig. 2. Principal coordinates analysis (PCO) plot based on Euclidian distance of isotopic (d13C and d15N) composition of the sampled organisms, grouped by habitat (A), trophic type (B), and feeding mode (C).

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

The bathybenthopelagic fishes are all grouped at positions 3 and 4 and have more or less the same carbon sources in their diet. The bathypelagic micronektivore black scabbard fish (Aphanopus spp.) and the mixed diet greater forkbeard (Phycis blennoides) are at the top of the food web. About 92% of the isotopic signature variability is explained by the first PCO axis (Fig. 2), which separates relatively well the shallower from the deeper organisms, and also the herbivores and filter feeders from the predators and scavengers, which presented the higher d15N isotope signatures. Predators, mainly the mesopelagic, showed a broad distribution along the first axis at intermediate trophic positions, accordingly with their occurrence along the depth gradient. The second axis explains about 8% of the total variability, separating the samples according to the d13C composition. Suspension feeders are in an intermediate trophic position but showed high variability on their isotopic signature, mainly due to the higher values of d13C of some suspension feeder species, namely the Alcyonacea and some sponges The PERMANOVA analysis (Table 2) showed significant differences in isotope d15N and d13C0 signatures between habitats and feeding types but also a significant interaction between these two factors, meaning that the effect of habitat on isotopic composition depends on the feeding type categories. Pair-wise comparison results of interaction terms for the habitat factor within each trophic type guild are summarized in Table 3. The zooplanktivores/omnivores showed significant differences between those living in the epi- and mesopelagic layers, showing different diets and trophic positions. For the zooplanktivores, significant differences on trophic positions were found between meso- and epipelagic organisms and the mesobenthopelagic. Within micronektivores the main differences were between the mesobenthic

185

organisms and those living in the pelagic environment. Among the pelagic species differences were between those from the bathypelagic layers and those from the upper water column. This means, in general, that shallow and midwater benthic micronektivores have similar isotopic signals. The mixed diet species just differ between mesobenthic and bathybenthopelagic ones, indicating that these species share the same trophic position, being segregated just by the habitat they live in. The maximum trophic position (MTP) of the epipelagic and mesopelagic community is 3.8 and 4.1, respectively, while the bathypelagic fishes have an MTP of 4.6. The MTP of seamount benthos suspension feeders shows the widest range, varying between 2.8 and 5.1, with the highest values being achieved by sponges. The mesobenthopelagic and bathybenthopelagic MTPs are both 4.5. The overall MTP of the studied organisms is 5.1. Regression analysis revealed that TPs (based on the d15N signatures) increased with increasing water depth (Fig. 3). Analyses of different feeding types indicate that the trophic signatures of the suspension feeders increase with increasing depth (TL¼3.05þ0.0011  Depth, n ¼47, r2 ¼0.20 r ¼0.45 p o0.001), as do those of the predators/scavengers (TL¼3.40þ0.0003  Depth, n¼ 47, r2 ¼0.05 r ¼0.23 p o0.0005). However, the low r2 values indicate a poor regression fit.

4. Discussion Stable nitrogen isotopes that occur naturally have been widely used as tracers in marine food webs as they estimate the trophic position and capture trophic interactions within communities (Hobson and Wassenaar, 1999). Although considerable research

Table 2 Results of PERMANOVA for the Euclidean distance Resemblance matrices. Fixed factors tested were Habitat ((epibenthic, epipelagic, epibenthopelagic [0-200 m], mesobenthic, mesopelagic, mesobenthopelagic [200-1000 m], bathypelagic, bathybenthopelagic [ 41000 m]), and Trophic type (herbivores/omnivores; omnivores/ zooplanktivores; zooplanktivores; micronektivores; mixed diet; sestonivores; benthivores; scavengers). Source

df

SS

MS

Pseudo-F

P(perm)

Unique perms

P(MC)

Habitat Trophic type Habitat  Trophic typenn Res Total

6 7 6 377 396

54.832 224.88 27.796 650.86 2474.5

9.1387 32.125 4.6326 1.7264

5.2934 18.608 2.6834

0.001 0.001 0.018

999 998 999

0.001 0.001 0.006

Table 3 Results of PERMANOVA pair-wise test comparisons among isotopic ratios of postulated habitats within factor ‘‘Trophic type’’. Test based on 9999 permutations. Significant Monte Carlo permutations are in bold (P-value o 0.001).

Omnivores/zooplanktivores Mesopelagic vs. epipelagic

0.002

Zooplanktivores Mesopelagic Mesobenthopelagic

Epipelagic 0.589 0.001

Mesopelagic

Micronektivores Mesopelagic Mesobenthopelagic Mesobenthic Bathypelagic

Epipelagic 0.603 0.051 0.001 0.001

Mesopelagic

Mesobenthopelagic

Mesobenthic

0.357 0.001 0.003

0.001 0.001

0.003

Mixed diet Mesobenthopelagic Mesobenthic Bathybenthopelagic

Epibenthic 0.133 0.034 0.82

Mesobenthopelagic

Mesobenthic

0.616 0.011

0.001

Benthivores Mesobenthic Mesobenthopelagic

Epibenthic 0.017 0.033

Mesobenthopelagic

0.001

Mesobenthic 0.021

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

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06 05 05

Trophic level

04 04 03 03 02 02 01 01

0

200

400

600

800

1000

1200

Depth (m) Fig. 3. Relationship between Trophic level and water depth for all the organisms sampled (TL¼ 2.87 þ0.01  Depth, n ¼397, r2 ¼0.27, r¼ 0.52, p o 0.0001).

effort in food web ecology used this method, in the last few years, few studies have focused on seamount ecosystems (Samadi et al., 2007). The species studied at the Condor seamount overall had a narrow range of d13C values that matched those of pelagic prey items, suggesting a common pelagic food source at the base of the food chain, irrespective of the feeding mode and habitat of the consumers. Seamount food webs are assumed to be structured by the habitat background created by bottom geomorphology and physics, and in particular by the various mechanisms that are thought to retain and locally enhance plankton production and/or abundance (Pitcher and Bulman, 2007). The ‘‘trophic blockage hypothesis’’ proposed by Isaacs and Schwartzlose (1965) predicts enhanced food supply to consumers on seamounts due to topographic blockage of diel vertical migrators of the sound-scattering layer during their descent. It predicts that this effect will be highest for seamounts at intermediate depths, where the summit is just below the photic layer (Genin, 2004). The summit plateau of Condor seamount at about 185 m depth is situated just at the lower limit of the photic layer (Tempera et al., 2012) and the resident benthopelagic and benthic faunas are expected to receive food supply from the epipelagic layer and through trapping of epi- mesopelagic diel vertical migrants. There is little doubt that the midwater fish community, cephalopods and gelatinous organisms occurring in the adjacent ocean are also key community components in food-webs of seamounts (Porteiro and Sutton, 2007). The relative significance of different mechanisms providing the connection between ocean and seamount communities is however not so well understood. Studies on the summit plateau of the Great Meteor Seamount (at 280 m depth), situated south of the Azores, showed vertically migrating zooplankton species close to the seafloor during daytime (Martin and Nellen, 2004). Some acoustic data indicate that the Condor seamount may contribute to aggregation of the micronekton community in near-surface waters at night and to retaining part of this community during the day (Casca~ o and Silva, 2011). The work of Hirch and Christiansen (2010) on the Seine Seamount showed no unequivocal support for the ‘‘trophic blockage hypothesis’’. Our interpretation of the Condor results is compatible with both, the trophic blockage and the trophic subsidy hypotheses. From the d13C and d15N values, we show that in Condor seamount food web, mesopelagic organisms link the primary consumers (TP¼2) (which are mainly from the epipelagic habitat) to the other trophic positions (TP43), which

include deeper benthic or benthopelagic animals. It is not surprising to observe that some suspension feeders are in the same TP as the scavengers, and that epibenthic and mesobenthic organisms share the same trophic positions. Most of the mesobenthopelagic fishes at the Condor seamount depend on mesopelagic organisms such as fishes, mysids, euphausiids and cephalopods (Morato et al., 1998). Gelatinous animals might also be an important source of food; however, they are rarely seen in the stomachs of fishes mainly due to their lack of hard structures. The primary prey of open-ocean mesopelagic zooplanktivorous fishes are calanoid copepods (Denda and Christiansen, 2011), but gelatinous prey are also important for deep meso- and bathypelagic fishes around mid-ocean ridges and seamount systems (Sutton et al., 2008). A discrete benthopelagic boundary assemblage, formed by some pelagic micronektonic organisms (fishes, decapod crustaceans and cephalopods), that also live in the adjacent mesopelagic environment, was described at insular and seamounts slopes, in some regions, such as the Hawaii (Benoit-Bird et al., 2001; Cartes et al., 2004; Lammers et al., 2004). The degree of pelagictopographic association appears to be site specific; in the Canary Islands and on the Meteor and Atlantis seamounts, for example, the midwater assemblages interact with the neritic and benthopelagic domains, but specialized boundary communities were not detected (Pusch et al., 2004a; Wienerroither et al., 2009). Our data show that the epi- and mesopelagic invertebrates constitute the trophic linkages to the mesopelagic and mesobenthopelagic environments, indicating their importance in the transfer of energy within the seamount food web. This is the first time that this has been confirmed through stable isotope analysis, although modeling (Morato et al., 2009; Williams and Koslow, 1997) had already predicted that advection of mesopelagic fish and crustaceans is essential to support aggregations of seamount fishes like the orange roughy, alfonsinos, and oreostomatids. Haury et al. (1995) also showed that pelagic food webs associated with seamounts play pivotal roles in channeling energy to fish species on seamounts. Feeding ecology studies of myctophiids near seamounts also show the preference of these migrant fishes for epipelagic invertebrates (e.g. Pusch et al., 2004b), confirming the trophic linkage between the epi-mesopelagic components and the benthos. However, it is expected that lateral advection of nonmigrating organisms (both meso- and bathypelagic) are potential source of energy to seamount fauna. Suspension feeders usually dominate the biomass of the megabenthos on seamounts. Currents are amplified and intensified around seamounts (Genin and Dower, 2007; White et al., 2007) and this is thought to be the main factor that favours their presence, since it transports organic particles consumed by the sessile suspensivores. Taxonomic composition varies between and within seamounts: assemblages may be dominated by sponges and/or corals like stylasterids or gorgonians. These large suspension feeders provide an important habitat for smaller invertebrates and fishes. At the Condor seamount, suspension feeders, such as sponges and gorgonians, generally dominate the benthic invertebrate assemblages (Tempera et al., 2012). According to Samadi et al. (2007) this observation suggests that benthic food chains are short and that their structure is simple, which is confirmed here for the Condor benthic chain. The high variability of the carbon and nitrogen stable isotopes from the Condor seamount suspension feeders might be related to feeding flexibility since it enhances trophic heterogeneity; for example, sponges are highly efficient at capturing ultraplankton (Pile and Young, 2006) but there are also carnivorous forms that prey on copepods (Watling, 2007). Migrating midwater fish cannot be used as food (at least directly) by the epibenthic megafauna such as corals and sponges. It is the increased available organic matter in the form of particles

A. Colac- o et al. / Deep-Sea Research II 98 (2013) 178–189

that this migration might cause (feces, molts) that could be used by that functional group. The less depleted d15N values obtained from the deeper POM samples seem to support this possibility. The increase in trophic position of the suspension feeders as a function of depth has also been reported by other authors (Bergmann et al., 2009; Mintenbeck et al., 2007). Bergmann et al. (2009) hypothesize that: (1) benthic organisms also utilize down slope or re-suspended sediments that might carry different d15N signatures compared with the less-degraded POM from the surface; or (2) the bottom fauna may be increasingly exposed to food scarcity and starvation, and the increase in d15N with depth might reflect nutritional stress due to low particle availability. The first hypothesis was considered more suitable to explain the patterns observed due to the increased abundance of suspension feeders with depth. Mintenbeck et al. (2007) hypothesized that the d15N signatures of POM in the Weddell Sea increase with increasing depth because of biodegradation in the water column, which is also observed in the POM d15N signatures measured. The densities of suspension feeders at different depths were not considered in this study. According to the present data, the trend can be explained by the increase in refractory material at greater depths, with the higher 15N isotope signal being due to the microbial mineralization. The d15N levels of some sponges were unexpectedly high for a group classified as suspension feeders, similar to those of predators/ scavengers. Over recent years some sponges have been classified as carnivorous (Vacelet, 2006; Vacelet and Boury-Esnault, 1995) which might explain the high values measured for some sponges at the Condor seamount. The similar values found in sponges and bathypelagic predators/scavengers can be explained by the fact that macrophagy may be a more effective feeding strategy than microphagous suspension-feeding in food-limited deep-sea environments (Vacelet and Boury-Esnault, 1995). Some authors state that, alternatively, high d15N values in sponges could be due to symbiotic bacteria (Bergmann et al., 2009; Iken et al., 2001). Like Bergmann et al. (2009), we also believe that both carnivory and symbiotic bacteria may explain the unexpectedly high d15N signatures recorded in sponges. The MTP 5.1 obtained for the benthic invertebrates is comparable to that reported also for benthic invertebrates from seamounts on the Norfolk Ridge (MTP: 4–5; depth range: 200–900 m) and to those reported for other shallow and deep marine ecosystems (MTP: 3.5–4.5; Samadi et al., 2007). In our study, all fishes occupied a narrow range of trophic positions. Most species feed at intermediate ones, which could be explained by significant omnivory (Clark et al., 2010). The fishes’ maximum trophic position (MTP) of 4.8 in this study was occupied by the black scabbard fish Aphanopus spp., a bathypelagic fish, while Phycis blennoides showed the highest MTP (4.5) among the mesobenthopelagic fishes. The MTP of the Condor seamount is higher than that of the Seine Seamount (3.8) (Hirch and Christiansen, 2010). However, according to the authors, they only sampled by bottom trawling on the summit plateau and collected a limited number of species (16) (Martin and Christiansen, 2009). Catches from longline surveys within a wider depth range from summit to 2000 m on the Seine Seamount consisted of 41 fish species (Menezes et al., 2009) and contained higher proportions of large predatory species compared to the fishes analyzed by Hirch and Christiansen (2010). Thus, it is plausible that the MTP of the Seine seamount would have been higher if they had analyzed top predators like those in the present study at the Condor seamount, since they share most of the species.

5. Conclusions It is assumed that there are three major energy processes supporting the enhanced biomass of seamount consumers: (a) autochthonous phytoplankton production, (b) topographic

187

trapping, and (c) trophic subsidy (Clark et al., 2010). This study presents isotopic data showing that the pelagic food web associated with the Condor seamount channeled energy to fish species and invertebrates inhabiting the benthopelagic and benthic environment. The summit of the Condor seamount, which lies at the beginning of the disphotic zone (Tempera et al., 2012), probably permits topographic blockage of diel vertical migrators during their descent (Genin, 2004) and strong currents (Bashmachnikov et al., in this issue) allow trophic subsidy by lateral advection (Polis et al., 1997). These processes increase the carbon supply to the Condor seamount, which on its own increases the POM available to the filter and suspension feeders.

Acknowledgments The research leading to these results has received funding from the CONDOR project EEA Grants (PT0040/2008), the European Community’s Seventh Framework Programme (FP7/2007–2013) under the HERMIONE project (grant agreement no. 226354) and the CORAZON project (FCT PTDC/MAR/72169/2006). We thank the ´lago RV Noruega, NRP Alm. Gago Coutinho crews of the RV Arquipe and the ROV Luso team. We would also like to thank Se´rgio Gomes and Clara Loureiro for collecting water samples for the POM analyses, and Paolo Lombardi for collecting the zooplankton samples. A. Colac- o’s work is funded under the Ciˆencia 2007 framework (FCT-PT). IMAR-DOP/UAz is funded by the Research and Development Unit no. 531 and LARSyS Associated Laboratory funded by the Portuguese Foundation for Science and Technology (FCT) through multiannual and programmatic funding schemes (OE, FEDER, POCI2001, FSE, COMPETE) and by the Azores Directorate for Science and Technology. References Andersen, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26, 32–46. Andersen, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA for PRIMER: Guide to Software and Statistical Methods. PRIMER-E Ltd., Plymouth, United Kingdom. Arı´stegui, J., Mendonc- a, A., Vilas, J.C., Espino, M., Polo, I., Montero, M.F., 2009. Plankton metabolic balance at two North Atlantic seamounts. Deep-Sea Res. II 56, 2646–2655. Bashmachnikov, I., Loureiro, C., Martins, A., 2013. Topographically induced circulation patterns and mixing over Condor seamount 98 (PA), 38–51. Benoit-Bird, K.J., Brainard, W.W.L., Lammers, M.O., R.E., 2001. Diel horizontal migration of the Hawaiian mesopelagic boundary community observed acoustically. Mar. Ecol. Prog. Ser. 217, 1–14. Bergmann, M., Dannheim, J., Bauerfeind, E., Klages, M., 2009. Trophic relationships along a bathymetric gradient at the deep-sea observatory HAUSGARTEN. Deep-Sea Res. I 56, 408–424. Bligh, E.G., Dyer, W.J., 1959. A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917. Boehlert, G.W., Mundy, B.C., 1993. Ichthyoplankton assemblages at seamounts and oceanic islands. Bull. Mar. Sci. 53 (2), 336–361. Cabana, G., Rasmussen, J.B., 1994. Modeling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature (London) 372, 255–257. Carassou, L., Kulbicki, M., Nicola, T.J.R., Polunin, N.V.C., 2008. Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, southwest Pacific. Aquat. Living Resour. 21, 1–12. Carlier, A., Le Guilloux, E., Olu, K., Sarrazin, J., Mastrototaro, F., Taviani, M., Clavier, J., 2009. Trophic relationships in a deep Mediterranean cold-water coral bank (Santa Maria di Leuca, Ionian Sea). Mar. Ecol. Prog. Ser. 397, 125–137. Carmo, V., Santos, M., Menezes, G.M., Loureiro, C., Lambardi, P., Martins, A., 2013. Space and time variability of zooplankton communities at Condor seamount, Azores (NE Atlantic) 98 (PA), 63–74. Cartes, J.E., Maynou, F., Moranta, J., Massuti, E., Lloris, D., Morales-Nin, B., 2004. Patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas. Prog. Oceanogr. 60, 29–45. Casca~ o, I., Silva, M., 2011. Acoustic estimation of sound-scattering layer. In: Giacomello, E., Menezes, G. (Eds.). CONDOR Observatory for long-term study and monitoring of Azorean seamount ecosystems. Final Project Report. Arquivos do DOP. Se´rie Estudos 1/2012, pp.71–80. Christensen, V., Pauly, D., 1993. Trophic models of aquatic ecosystems. ICLARM Conference Proceedings, vol. 26, 390 p.

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