Ontogenetic shifts and temporal changes in the ... - Wiley Online Library

Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE

Ontogenetic shifts and temporal changes in the trophic patterns of the deep-sea red shrimp, Aristaeomorpha foliacea (Decapods: Aristeidae), in the Eastern Ionian Sea (Eastern Mediterranean) Kostas Kapiris1, Maria Thessalou-Legaki2, George Petrakis1 & Alexis Conides1 1 Hellenic Centre for Marine Research, Institute of Marine Biological Resources, Anavissos, Attica, Greece 2 Department of Zoology-Marine Biology, School of Biology, University of Athens, Panepistimioupolis, Athens, Greece

Keywords Aristaeomorpha foliacea; deep sea; Eastern Mediterranean; feeding habits; giant red shrimp; Ionian Sea. Correspondence Kostas Kapiris, Hellenic Centre for Marine Research, Institute of Marine Biological Resources, 47o km Athens-Sounio, Mavro Lithari PO Box 712, 19013, Anavissos, Attica, Greece. E-mail: [email protected] Accepted: 3 October 2009 doi:10.1111/j.1439-0485.2009.00344.x

Abstract The purpose of this paper is to provide the first detailed data concerning the diet and feeding activity of the giant red shrimp, Aristaeomorpha foliacea, in the Eastern Ionian Sea (Eastern Mediterranean), in relation to season, size class and sex. Feeding activity in A. foliacea was intense, based on its low vacuity index and high prey diversity, with a diet dominated by mesopelagic prey and less frequent occurrence of benthic taxa. Giant red shrimp displayed a highly diversified diet that exhibited slight seasonal fluctuations. The diets of both sexes consisted of 60 different prey categories belonging chiefly to three groups: crustaceans (e.g. decapods, such as Plesionika spp. and Pasiphaeidae, amphipods), cephalopods (mainly Enoploteuthidae) and fishes (Myctophidae, Macrouridae). These three prey categories accounted for 72–82% of the relative abundance and total occurrence for males and 70–88% for females, respectively. Variation in food availability, as well as increased energy demands related to gonad development and breeding activity, appear to be critical factors driving temporal changes in feeding strategy. Feeding activity increased during spring and summer, which coincides with reproductive activities (mating, gonad maturation, egg-laying). Females seem to be more active predators than males, consuming prey with greater swimming ability. However, ontogenetic shifts in diet were also apparent, despite high dietary overlap among small, medium and large females. Large individuals, which are more efficient predators, selected highly mobile prey (e.g. fishes), whereas small individuals consumed low-mobility prey (e.g. copepods, ostracods, tanaids and sipunculans).

Problem The giant deep water red shrimp (Aristaeomorpha foliacea Risso, 1827) is, with Aristeus antennatus (Decapoda: Aristeidae), the most economically and ecologically important deep water crustacean resource in the West and Central Mediterranean Sea, after the Norway lobster (Nephrops norvegicus). Because of its importance on the bathyal fishery grounds of the Mediterranean, numerous Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH

papers have addressed the biology, ecology and fishery of this decapod in the whole Mediterranean (e.g. Cau et al. 1994; Sarda` & Cartes 1994; Ragonese 1995; D’Onghia et al. 1998; Politou et al. 2004). In the past decade, this decapod has also become a potentially viable fishery in the Greek Eastern Ionian Sea (Eastern Mediterranean) (Papaconstantinou & Kapiris 2001, 2003). The unexploited high abundance of this shrimp in Greek waters, in relation to other regions of the Mediterranean, seems to 341

Feeding pattern of the deep-sea red shrimp

Kapiris, Thessalou-Legaki, Petrakis & Conides

be related to the particular ecological conditions of this area (e.g. temperature and salinity), which satisfy its niche demands (Papaconstantinou & Kapiris 2003). The abundance and the population dynamics of this species suggests that the population of the giant red shrimp in the Ionian Sea could provide a new target species for the deep-trawl fishery of the area (Papaconstantinou & Kapiris 2003). Due to the increased commercial importance of A. foliacea, many aspects of its biology and fishery have been studied recently in Greek waters (e.g. Papaconstantinou & Kapiris 2003; Kapiris & Thessalou-Legaki 2006, 2009; Mytilineou et al. 2006). Very few published papers describe the alimentary habits of this shrimp and only limited data concerning the quantitative composition of its diet are available (e.g. Gristina et al. 1992; Cartes 1995; Kapiris et al. 1999; Chartosia et al. 2005). Aristaeomorpha foliacea, in general, has a highly diverse diet, and is a fast and active predator of large and mobile organisms (e.g. Lagarde`re 1972; Cartes 1995). The object of this paper is to provide a detailed description of the feeding habits of the giant deep water red shrimp in the Eastern Mediterranean (especially in

the Eastern Ionian), in relation to season, size and sex. New information concerning its feeding patterns provides greater insight concerning the population ecology of this important and unexploited resource of the Greek seas. In addition, such data could serve in the comparison of its life history traits along the Mediterranean.

Material and Methods Study area

Exploratory sampling of Aristaeomorpha foliacea took place along the south coast of the Greek Ionian Sea, between Zakinthos Island and Peloponnisos Peninsula (Fig. 1), within the framework of the research project ‘Deep Water Fisheries’ (FAIR 95-0655). A total of 92 hauls were taken during 12 experimental trawl survey cruises on a monthly basis (December 1996–November 1997) during the daytime, to avoid the possible effect of diel movements. Samples were collected by the commercial trawler Panagia Faneromeni II (26 m in length, 450 HP) using a net with a cod-end mesh size of 18 mm from knot to knot.

0m

80

Epirus

0m

80

A

A

nS

nia

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21˚05′

Zakinthos

80 0m Pe

nissos

Pelopo

20˚32′

lo

po

ni

ea

nS nia Io

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ss

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Zakinthos

200 m

B 500 m

Mediterrannean Sea

800 m

37˚32′

20˚32′

342

20˚48′

21˚05′

37˚32′

Fig. 1. Map of the research area (A = isobath of 800 m in the whole area of the Eastern Ionian Sea, B = sampling area with sampling stations).

Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH


Feeding activity

To study the quantitative parameters (stomach fullness, food quality) of the shrimp’s diet, samples of A. foliacea collected from trawls were preserved at +4 C on the boat and at )30 C in the lab. Carapace length (CL) (±1 mm) and wet body weight (BW) (±0.1 g) were measured. The vacuity index (VI) [(number of empty stomachs per number of stomachs examined) * 100] (Hyslop 1980) was estimated. Feeding activity, the quantitative and qualitative study of the diet of both sexes, was analyzed among seasons. Stomach contents were weighed as wet (stomach wet weight, SWW, g), dry (stomach dry weight, SWD, g; after 24 h of oven drying at 70 C) and ash-free dry weight (AFDW; as loss on ignition at 450 C for 3 h). All the weights were measured to an accuracy of 0.0001 g. The stomach fullness was calculated in two different ways: (i) wet food weight (g) per 100 g shrimp wet weight [% body weight (BW) Wet = (SWW ⁄ BW) * 100] and (ii) dry food weight (g) per 100 g wet weight [%BW Dry = (SWD ⁄ BW) * 100] (He´roux & Magnan 1996). To approach the food quality aspects of the species, two expressions of food quality were taken into account: 1 % dry weight (DW) = (SWD ⁄ SWW) · 100 and 2 % ash free dry weight (AFDW) = (AFDW ⁄ SWD) · 100 Dietary overlap among the sexes, the size groups and seasons was measured by applying the percentage of similarity proposed by Schoener (1970): Cxy = 1 ) 0.5 P jpxi pyij , where Cxy is the similarity between diets of the specimens belonging in the size group or season or sex x and y, pxi is the proportion of food category i (in terms of the relative abundance, %N) in the diet of specimens or species x, and, pyi is the proportion of food category i (relative abundance, %N) in the diet of specimens or species y. The diet overlap index ranges from 0 to 1 and is biologically significant when it exceeds 0.60 (Macpherson 1981). Shannon–Wiener diversity (H’) (Shannon & Weaver 1963) was used to estimate the diversity in the diet at different size classes and seasons as established, based on the relative abundance (%N). Diet composition

For the study of dietary composition, some individuals of Aristaeomorpha foliacea, taken from the same haul in which the quantitative parameters of the diet were estimated, were fixed immediately after capture in 10% formaldehyde solution for subsequent processing in the laboratory. In the laboratory, the diets of a total of 1416 individuals of A. foliacea (710 males, 706 females) were studied. Stomach contents were sorted and prey identifiMarine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH


cation was carried out under a dissecting microscope to the lowest possible taxon. Fish, polychaetes and echinoderms were counted as a single prey item per stomach because it was not possible to distinguish the exact number of these prey items. Unidentified crustaceans, natantian decapods, euphausiids, cephalopods and fishes were referred to separately. Fragments of larger crustaceans, such as decapods, were often found broken into small pieces and the taxa of origin could not be identified, but some fragments (e.g. rostra, mandibles) were identified because they were characteristic of certain taxonomic groups. Most of the cephalopod remains were identified by the flesh, beaks, suckers and hooks. Seeds and macrophytes were reported under the term ‘plant detritus’. The presence of scales was not taken as proof that fish had been eaten because ingestion of scales has been assumed to occur in the net during capture (Cartes & Sarda` 1989). The identification of fish prey species was based on scales, pigment abundance and, rarely, otoliths. Soft amorphous portions of prey that could not be identified to a taxon were called ‘soft tissue’. They most likely came from natantian crustaceans. Euphausiids, mysids, amphipods, isopods, cumaceans, tanaidaceans and copepods were together called ‘other crustaceans’, and ‘other’ included mud, plastics, plants, chaetognaths, foraminifera, sipunculans and unknown. We used the term ‘unknown’ prey for any amorphous soft portion that could not be identified as a taxon. Two indices, the frequency of occurrence (%F) and the relative abundance (%N) (Hyslop 1980), were used to describe the diets of shrimp. Thus, for each prey taxon, we calculated %F as (the number of stomachs containing the taxon ⁄ total number of non-empty stomachs examined) · 100, and %N as (the number of prey items of a given taxon in all non-empty stomachs in a sample ⁄ total number of food items in all stomachs) · 100. Graphically, the feeding strategy of the decapod studied by season and sex is given by a two-dimensional representation of preyspecific abundance (Pi) and frequency of occurrence (%F) of the different prey types in the seasonal diet of the species. This method (Amundsen et al. 1996) allows prey importance, feeding strategy and the inter- and intra-individual components of niche width to be explored together. Prey-specific abundance is defined as the percentage a prey taxon comprises all prey items in only those predators in which the actual prey occurs, or, in mathematical terms: Pi = (RSi ⁄ RSti) * 100, where Pi is the prey-specific abundance of prey i, Si the stomach content comprising prey i, and RSti the total stomach contents in only those predators with prey i in their stomach. A non-metric multidimensional scaling analysis (MDS) was applied for the ordination of months based on the relative abundance of prey in the diet of both sexes. 343



Feeding activities in relation to size

Results Feeding intensity

Spring

18

Summer Autumn

16 14

Vacuity index

To detect possible variations in feeding habits related to size, the females were separated into three size groups and the males into two, according to known maturity data: ‘small size’ group (CL < 30 mm), ‘medium size’ (30 > CL > 40 mm), for males and females, and, only for females, ‘large size’ (CL > 40 mm). As the minimum size of mature male and female specimens of both sexes and species was approximately 30 mm total length (TL) (Kapiris 2004), the ‘small size’ individuals can be considered immature, whereas those of the ‘medium size’ and ‘large size’ group included the mature individuals. All size groups were captured in all months. To explain in more detail the prey importance in the diet of the several size groups of the giant red shrimp, the authors used the Costello method (Costello 1990). This graphical method makes it possible to visually compare the diet of different age groups or population of a predator. Statistical differences in diet compositions and stomach fullness values by size and season were tested by ANOVA. The assumption of normality was tested using the Kolmogorov–Smirnov test, and the non-parametric tests Kruskal–Wallis and Mann–Whitney test were performed to test the significant differences. All the above statistics were applied using PRIMER 5.2.4., STATISTICA v5 and STATGRAPHICS Plus software. Statistical significance was indicated by P < 0.05.

Winter 20

12 10 8 6 4 2 0

A. foliacea

A. foliacea

Fig. 2. Seasonal values of vacuity index of Aristaeomorpha foliacea, by sex, in the Eastern Ionian Sea in the period December 1996– November 1997.

Wet in both sexes occurred in winter and the minimum in spring (Table 1). On the other hand, the lowest medians of %BW Dry for both sexes were found in winter and the maximum values in autumn (Table 1). Diet quality (%BW Dry and %AFDW) also differed significantly among seasons for both sexes of A. foliacea. (Kruskal–Wallis test, P < 0.05) (Table 1). In general, few significant differences in food quality were detected between males and females for each season (Mann–Whitney test, P < 0.05). Males and females of A. foliacea presented the highest values of both quality indices in spring and the minimum in winter (Table 1) (Kruskal–Wallis test, P < 0.05).

Vacuity index, fullness and food quality indices

Dietary overlap, trophic diversity

The occurrence of empty stomachs in both sexes is shown in Fig. 2. The vacuity index (VI) ranged between 4.5% and 18.1% of all stomachs for males and females, respectively implying a high feeding rate or slow digestion rate, or both. In general, the VI values varied significantly among seasons for both sexes (ANOVA, P < 0.05). The lowest proportion of empty stomachs of Aristaeomorpha foliacea was found in spring for both sexes, followed by summer (Fig. 2). In contrast, the highest number of empty stomachs was found in autumn for females and summer for males (Fig. 2). The carapace length (CL) of A. foliacea males with empty stomachs ranged from 23.68 to 38.58 mm and those of females from 21.79 to 52.56 mm. No pronounced differences existed between the sexes (Kolmogorov–Smirnov test, P > 0.05, in all cases). The stomach fullness of A. foliacea varied seasonally in both sexes (Kruskal–Wallis, P < 0.05) (Table 1). Both fullness indices (%BW Wet, %BW Dry) were significantly higher in females than in males for each season (Mann– Whitney test, P < 0.05). The maximum values of %BW

Dietary overlap was high (>0.60) in all seasons, for both sexes (Table 1). Trophic diversity varied slightly among seasons in both sexes (Fig. 3) and no statistically significant differences were established between sexes (Mann– Whitney, P > 0.05). The maximum diversity (3.00 and 3.04 for males and females, respectively) and mean number of prey items (2.9 and 3.1 for males and females, respectively) were found in summer for both sexes of A. foliacea.

344

Diet composition General food habits

The diets of both sexes of Aristaeomorpha foliacea consisted of 60 different prey categories (most as species-level prey categories). In total, 1697 food items were identified for males and 1724 for females, belonging chiefly to three major groups: (i) crustaceans – particularly decapods, reptantia (anomurans, brachyurans), amphipods, euphausiids, ostracods, copepods, mysids, tanaidaceans, cumaceans, (ii) cephalopods and (iii) fishes. These




Table 1. Mean seasonal values of fullness (%BW Wet. %BW Dry), food quality (%DW. %AFDW), overlap index values and mean number of prey items (no. of ind. examined per total number of prey consumed) of both sexes of Aristaeomorpha foliacea. Significant values are in bold. Males

Females

Males

three prey categories constituted 72–82% of the relative abundance and total occurrence for males and 70–88% of the relative abundance and the total occurrence in females (Table 2). The most dominant natantians found were the nektobenthic Plesionika martia, Plesionika heterocarpus and Plesionika giglioli, followed by Pasiphaea sp., Sergestes sp. and Solenocera sp. Some appendages from Aristeus antennatus were also found mainly in female A. foliacea. Among cephalopods, the dominant species were Abraliopsis pfefferi, Pyroteuthis margarifera and Abralia veranyi. For fishes, specimens of Myctophidae and Macrouridae were the most abundant in the foreguts.

Females

Season

%BW Wet

%DW

Winter Spring Summer Autumn

0.18 0.14 0.16 0.15 %BW Dry

0.48 0.29 0.29 0.27

26.18 36.42 33.65 32.87 %AFDW

21.76 37.85 32.25 31.07

Winter Spring Summer Autumn Winter

0.02 0.04 0.05 0.06 0.02

0.01 0.07 0.08 0.09 0.01

51.34 61.61 57 53.85 51.34

56.91 60.72 53.60 59.59 56.91

Winter 1

Spring 0.71 1

Summer 0.81 0.83 1

Autumn 0.62 0.79 0.77 1

Winter 1

Spring 0.80 1

Summer 0.85 0.88 1

Autumn 0.60 0.79 0.78 1

Seasonal variation in diet composition

Only slight differences were found in the relative abundance of prey (%N) among months for both sexes (Kruskal–Wallis test, P > 0.05) (Fig. 4). The lowest similarities were observed among the winter months (December, January and February) in males and in the autumn months (September, October, November) in females. In Fig. 5 the feeding strategy diagram of A. foliacea, by sex and season, according to Amundsen et al. (1996) is given. In most seasons, A. foliacea had a generalized feeding strategy (Fig. 5). In general, both sexes fed upon natantian decapods, particularly Plesionika spp., Sergestes sp., Pasiphaea sp., and fishes throughout the year, while ‘other crustaceans’ and polychaetes were ingested on a secondary basis. These prey were consumed by most A. foliacea, with some variation in relative abundance among seasons (Fig. 5). Feeding strategies differed among sexes only in autumn and winter. In autumn, males specialized on fishes, which represented the only dominant prey (Fig. 5). In winter, a wide variety of prey types (except echinoderms and sipunculans) were consumed, but in low abundance, by a few A. foliacea (Fig. 5). Females had a more generalized feeding strategy in all seasons. It is worth noting that the mean seasonal number of prey

Overlap index Males Winter Spring Summer Autumn Females Winter Spring Summer Autumn

Mean Seasonal number of prey items Males Winter Spring Summer Autumn

2.28 2.79 2.95 2.47

Females 2.66 3.01 3.10 2.08

Shannon diversity

Season

Autumn Summer Spring Winter 1.6 Fig. 3. Diversity index (H’, Shannon–Wiener index) values of Aristaeomorpha foliacea per sex and season.


1.8

2.0

2.2

A. foliacea, males

2.4

2.6

2.8

3.0

3.2

A. foliacea, females

345



Table 2. Seasonal dietary composition of Aristaeomorpha foliacea males (a) and females (b). Winter Taxa (a) Crustacea Decapoda Gennadas sp. Pasiphaea sp. Sergestes sp. Plesionika spp. Processa sp. Solenocera sp. Aristeus antennatus Acanthephyra sp. Crangonidae Unidentified Natantia Calocaris sp. Alpheus sp. Polycheles sp. Unidentified Reptantia Anomura Brachyoura Xanthidae Portunidae Unidentified Brachyoura Euphausiacea Isopoda Anthuridae Unidentified isopods Amphipoda Gammaridea Hyperiidea Caprellidea Unidentified Amphipods Cumacea Tanaidacea Apseudomorpha Tanaiidomorpha Unidentified Tanaids Ostracoda Copepoda Mysidacea Unidentified Crustacea Mollusca Bivalvia Gastropoda Scaphopoda Unidentified Molluscs Pteropoda Cephalopoda Pyroteuthis margarifera Abraliopsis pfefferi Enoploteuthinae Teutothidea Abralia veranyi Todarodes sagittatus Octopus salutii

346

Spring

%N

%F

1.35 0.54 2.43 9.46 0.54 1.08 0.54 0.27 1.08 11.08

1.39 0.55 2.49 9.14 0.55 1.11 0.55 0.28 1.11 11.08

0.27 0.54

0.28 0.55

Summer

%N

%F

3.17

3.37

7.72

8.21

0.40 0.59 0.00 0.40 9.11

0.42 0.63 0.00 0.42 9.68

0.20 0.59

0.21 0.63

%N

Autumn %F

0.18 3.38

0.19 3.61

7.30 0.36 0.18 0.18 0.18 0.18 10.85 0.18

7.79 0.38 0.19 0.19 0.19 0.19 11.41 0.19

%N

%F

1.92 1.54 5.77 0.38

1.97 1.57 5.91 0.39

0.38 1.15 11.92

0.39 0.39 12.20

0.38

0.39

0.38 0.77 1.15 0.38

0.39 0.79 1.18 0.39

0.38

0.39

1.54

1.57

0.27 0.27 1.62 0.81

0.28 0.28 1.66 0.83

0.20 1.19 1.98 1.19

0.21 1.26 2.11 1.26

0.53 2.31 0.53

0.57 2.47 0.57

0.27

0.28

2.18

2.11

0.36

0.38

1.98

1.05

4.75 0.79

5.05 0.42

1.96 0.18

2.09 0.19

0.20 0.20

0.21 0.21

0.18

0.19

2.28 0.57 0.95 5.51

4.23

3.94

0.77 4.23

0.79 4.33

1.54 0.38 0.38 1.54

1.57 0.39 0.39 1.57

0.38

0.39

0.38

0.39

1.89

1.94

1.08

1.11

5.15

2.74

0.54 2.43

0.55 2.49

0.99 4.75

1.05 4.84

2.49 0.71 0.89 5.87

0.54

0.55

0.20 0.59 0.20 0.20

0.21 0.63 0.21 0.21

0.18 1.25 3.02 1.07

0.19 1.14 1.33 1.14

0.54

0.55 0.18 0.18

0.19 0.19

0.27 0.27

0.28 0.28




Table 2. Continued. Winter Taxa Histioteuthis bommellii Onychoteuthidae Eggs Unidentified Cephalopoda Echinodermata Ophiuroideas Echinoidea Holothuroidea Osteichthyes Myctophidae Hymenocephalus italicus Macruridae Unidentified Fishes Polychaeta Aphroditidae Nereididae Spionidae Serpulidae Eunicidae Unidentified Polychaetes Sipunculoidea Chaetognatha Foraminifera Mud Soft tissues Plastics Plant Unknown No. of individuals (b) Crustacea Decapoda Gennadas sp. Pasiphaea sp. Sergestes sp. Plesionika spp. Processa sp. Solenocera sp. Aristeus antennatus Acanthephyra sp. Crangonidae Unidentified Natantia Calocaris sp. Alpheus sp. Polycheles sp. Unidentified Reptantia Anomura Brachyoura Xanthidae Portunidae Unidentified Brachyoura Euphausiacea Isopoda Anthuridae Unidentified isopods

Spring

%N

%F

0.27 1.89

0.28 1.94

0.27

Summer

%N

%F

%F

0.38 2.66

0.27

0.36

0.38

0.54 0.27 1.08 27.84

0.55 0.28 1.11 27.70

0.53

0.57

1.25 23.67

1.33 23.19

0.58

0.88

0.53

0.57

9.13 0.38 0.55 0.28 0.55 3.60 0.96 9.97 1.39

19.41

20.63

0.59 0.20 0.99 1.58 5.54 0.59 0.70 0.20 0.69 5.74

0.63 0.21 0.84 1.68 5.89 0.54 0.62 0.21 0.65 6.11

9.31 1.58

9.89 1.68

162

0.99 0.99 10.74 0.80 0.40 0.40

2.64 0.42

%N

0.36 2.67

8.92 0.37 0.54 0.27 0.54 4.05 0.97 10.27 1.35

3.56 0.40

Autumn

0.20

0.40 0.20 1.39 3.78

0.76 6.84 0.19

1.60 0.49 4.98 0.18 9.45 1.25

1.52 0.73 5.32 0.19 9.76 1.33

181

1.04 1.04 10.83 0.83 0.42

12.29 0.21 0.21

%F

1.92 3.08

1.57 2.36

1.54 33.84

1.57 33.46

0.38 1.54 0.77 3.46 0.38

0.39 1.57 0.79 3.54 0.39

0.77

0.79

3.08

3.15

6.92 0.77

7.09 0.79

190

105

0.25 1.52 1.52 11.14

0.26 1.56 1.56 11.43

0.85 0.85 0.17 10.24

0.90 0.90 0.18 10.39

0.51 1.52

0.52 1.56

0.25 9.11 0.25

0.26 9.35 0.26

0.34 0.34 0.17 0.34 11.77 0.17 0.17

0.36 0.36 0.36 0.18 12.01 0.18 0.18

0.42 0.80 12.13 0.20

0.71 6.94 0.18

%N

0.42 4.17 0.83 12.08 1.67 0.42 1.67

0.42 4.24 0.85 12.29 1.69 0.42 1.69

0.83 12.50

0.85 12.29

0.42

0.42

2.08

2.12

0.21

0.42 0.21 1.46 1.46


0.17

0.18

0.51 0.76 2.28 0.76

0.52 0.78 2.34 0.78

0.17 0.51 1.19 1.71

0.18 0.54 1.25 1.61

0.25

0.26

0.17

0.18

347



Table 2. Continued. Winter Taxa Amphipoda Gammaridea Hyperiidea Caprellidea Unidentified Amphipods Cumacea Tanaidacea Apseudomorpha Tanaiidomorpha Unidentified Tanaids Ostracoda Copepoda Mysidacea Unidentified Crustacea Mollusca Bivalvia Gastropoda Scaphopoda Unidentified Molluscs Pteropoda Cephalopoda Pyroteuthis margarifera Abraliopsis pfefferi Enoploteuthinae Teutothidea Abralia veranyi Todarodes sagittatus Octopus salutii Histioteuthis bommellii Onychoteuthidae Eggs Unidentified Cephalopoda Echinodermata Ophiuroidea Echinoidea Holothuroidea Osteichthyes Myctophidae Hymenocephalus italicus Macruridae Unidentified Fishes Polychaeta Aphroditidae Nereididae Spionidae Serpulidae Eunicidae Unidentified Polychaetes Sipunculoidea Chaetognatha Foraminifera Mud Soft tissues Plastics Plant

348

%N

1.77

Spring %F

1.82

1.19

1.25

3.18

%N

1.79

Summer %F

1.88

%N

Autumn %F

0.85 0.17

0.90 0.18

0.17

0.18

%N

%F

0.42

0.42

3.33

0.76 0.25 0.51 5.32

0.78 0.26 0.52 5.45

0.68 0.51 0.17 3.75

0.72 0.54 0.18 3.76

0.42 0.42 0.42 5.42

0.42 0.42 0.42 5.51

1.59 0.20

1.46 1.04

4.30 0.51

0.26 2.60 0.52

0.68 2.05 1.19 0.68

0.72 2.15 0.54 0.72

0.42 0.83

0.42 0.85

0.80 0.60 0.20

0.83 0.63 0.21

0.25 1.01 0.25

0.26 1.04 0.26

0.51 0.34 0.34

0.54 0.36 0.36

1.67 0.42

1.69 0.42

0.40

0.42

0.51

0.52

0.17 0.17

0.18 0.18

0.83

0.85

0.42 0.42

0.42 0.42

1.25 5.00

1.27 4.24

1.67

1.69

0.99 3.38

1.04 3.54

0.25

0.26

0.76

0.78

0.20

0.21

0.20

0.21

1.19 20.28

1.25 21.25

0.51 23.04

1.59

1.67

0.99 0.40 7.95 3.18

1.04 0.42 7.71 2.50

0.40 1.59 2.19 0.60 10.14

0.42 1.67 2.29 0.63 10.00

0.17 3.07

0.18 3.23

0.17

0.18

0.52 23.64

1.54 24.40

1.61 23.48

0.42 0.42 21.25

0.42 0.42 21.61

0.76

0.78

0.51

0.54

0.42

0.42

0.76 0.25 6.08 0.76 0.25

0.78 0.26 5.97 0.78 0.26

0.34 1.54 0.17 5.12 2.56

0.36 1.25 0.18 5.38 2.69

3.33 0.83

3.39 0.85

0.76 4.05 0.51 14.18

0.78 4.16 0.52 13.77

1.02 1.88 4.78 0.51 8.87

1.08 1.97 5.02 0.54 8.60

0.42 0.83 4.58 0.83 7.92

0.42 0.85 4.66 0.85 7.63




Table 2. Continued. Winter Taxa

%N

Unknown No. of individuals

1.39

Spring %F

%N

1.46

1.01

189

Summer

131

items [number of individuals (ind) examined ⁄ total number of prey consumed] was highest in summer and spring (Table 1). During winter, the highest value of the wet weight of the prey (%BW Wet) (Table 1) could be attributed to the highest numerical abundance of natantian decapods and plant debris in males and to the increased presence of cephalopods in the stomachs of female giant red shrimp. The lowest value of %BW Dry also occurred during winter (Table 1), and was linked to an increase in consumption of polychaetes, chaetognaths and sipunculans, which A. foliacea - males Stress: 0.1

JANUARY

AUGUST DECEMBER JULY SEPTEMBER FEBRUARY

OCTOBER

JUNE NOVEMBER

MARCH APRIL MAY

%F

%N

1.04

1.54

Autumn %F

%N

1.61

1.67

189

%F 1.69 115

have high water content (Table 2). In spring, both sexes of the giant red shrimp seemed very well fed, reflected by the lowest observed VI value (Fig. 4). During this season, heavy prey (e.g. decapods and cephalopods) were low in importance compared to other seasons (Table 2). In the same season (spring), the highest abundance of suprabenthos prey (mysids, amphipods and, particularly in males, tanaidaceans, cumaceans) was included in the diets of both sexes of A. foliacea (Table 2). Feeding patterns during summer differed from wintertime diets. In males, a relatively low VI (Fig. 2) and increased values of both fullness and quality indices were found (Table 1). Females also appear to be well fed (max VI, intermediate values of fullness indices, minimum value of feeding quality – %AFDW) (Fig. 2, Table 1). In autumn, the low value of %BW Wet and the highest %BW Dry values, in both sexes of A. foliacea, could be attributed the great abundance of some weighty categories, with a great swimming capacity (natantian decapods, especially Pasiphaea spp., Plesionika spp.; cephalopods, particularly Pyroteuthis margarifera and Abralia veranyi) predominating in their diet (Table 2). Diets during autumn differed from other seasons, implying some heterogeneity in the relative abundance of the prey (Fig. 4). Variations of stomach contents in relation to size

A. foliacea - females Stress: 0.14

NOVEMBER OCTOBER

JULY

DECEMBER

MARCH

AUGUST

MAY FEBRUARY

APRIL

JANUARY

SEPTEMBER

JUNE

Fig. 4. Ordination (MSD) of sampling seasons based on the relevance abundance (%N) of the prey found in the stomachs of Aristaeomorpha foliacea, by sex in the Eastern Ionian Sea in the period December 1996–November 1997.


Fullness and quality indices were lower in the smaller individuals, but only %BW Wet differed statistically among size classes in both sexes of Aristaeomorpha foliacea (Table 3). Trophic overlap between the small and larger (medium size) males was very low, indicating that the size categories of males fed on different resources or on the same prey with different abundance (Table 3). In contrast, dietary overlap between all size classes of females was high. In general, highest overlap values were observed between medium and large females. Prey diversity also varied among sizes, with the highest diversity observed for smaller males and large females. The smallest individuals seem to consume fewer prey items and specimens, but, due to their low abundance in the samples, showed a higher diversity (Table 3). The relationship of prey importance and predator feeding strategy by size is given in Fig. 6, according to the Costello method (1990). The dominant prey 349


A. foliacea, males

Autumn

65 60 55 50 45 40 35 30 25 20 15 10 8 2 5 0 0

7

3

4

5

1

10

15

20

25

30

Spring

25

5

Prey-specific abundance (%)



20

1 5

15 4

10

7

5

0

5

10

7

9 3

4

6



Summer

2

1

5

8

0

5

10

15

20

25

15

30

6 8

4

2

0

3 7

5

10

A. foliacea, females

20

3

15

2 1

4

10

9

5

8

5

6

0 –5

–5

0

5

10

15

20

25

30



7

25

35

20 18 16 14 12 10 8 6 4 2 0 –2

15

20

25

5

30

Spring

9

28

3 1 7

4

5

4

10 16 22 Frequency of abundance (%)

Frequency of abundance (%)

28

Winter

Summer 20

20 9

15 3 2

8

5

4

1

7

10

5 6

0 0

5

10

15

20

25

30

35




1

9


Autumn

30

25

Winter

50 45 40 35 30 25 20 15 10 5 0 –5


35

20



20 18 16 14 12 10 8 6 4 2 0 –5

3

8

0

35

9 2

3 1

5

4 2

7

8

9

10

6

0 –5

0

5

10

15

20

25

30


Fig. 5. Feeding strategy diagram of Aristaeomorpha foliacea, by sex and season in the Eastern Ionian Sea, according to the Amundsen et al. (1996) method (1: Natantian decapods, 2: Reptantian decapods, 3: Other crustaceans, 4: Molluscs, 5: Fishes, 6: Echinoderms, 7: Polychaetes, 8: Sipunculans, 9: Other).

consumed by all sizes of both sexes of A. foliacea was natantian decapods (Fig. 6), although their abundance and occurrence were highest in medium and large individuals. Larger individuals of both sexes seemed to consume more molluscs, fishes and fewer polychaetes than small individuals. In general, the dominant prey items 350

of small individuals (CL < 30 mm) of both sexes were species characterized by low mobility, such as copepods, ostracods, chaetognaths, sipunculans, tanaidaceans (Fig. 6). Highly mobile prey (e.g. fishes) were more abundant in the diets of medium and large A. foliacea (Fig. 6). Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH



Table 3. Mean values of fullness (% BW Wet, % BW Dry), food quality (% DW, % AFDW), overlap and diversity index values of both sexes of Aristaeomorpha foliacea per size (small size: CL < 30 mm, medium size: 30 > CL > 40 mm, large size: CL > 40 mm). Significant values are in bold. Fullness indices Size # – small # – medium $ – small $ – medium $ – large

% BW Wet 0.10 0.15 0.11 0.17 0.35

% BW Dry 0.03 0.05 0.03 0.05 0.09

% DW 35.76 35.00 29.19 32.84 33.73

% AFDW 59.37 58.14 52.60 59.84 58.15

Overlap index values Size # – small # – medium $ – small $ – medium $ – large

1 –

2 0.49 –

3

4

5

–

0.73 –

0.68 0.84 –

Diversity index values Size # – small # – medium $ – small $ – medium $ – large

H’ 2.73 2.12 2.96 2.76 3.07

No. of prey 80 90 101 387 973

No. of specimens 39 599 47 162 414

Discussion Feeding activity

The highly diversified diets observed in Aristaeomorpha foliacea are typical of bathyal penaeoideans in the Western Mediterranean (Cartes 1995). The feeding activity of A. foliacea is generally comparable to those reported in other regions of the Mediterranean, such as in the Catalan Sea (Cartes 1995), Sicilian Channel (Gristina et al. 1992) and Aegean Sea (Chartosia et al. 2005). Any observed differences in its feeding activity and diet among areas in the Mediterranean, such as food diversity, different food categories and mean number of prey, could be due to bottom morphology (Cartes 1995) and to the oligotrophic conditions of the Eastern Mediterranean. This characteristic of the Eastern Mediterranean could also explain the increased number of pelagic prey consumed by A. foliacea compared to the western part of the basin (Cartes 1995). The considerably higher water temperature of the Eastern Mediterranean (Politou et al. 2004) may also play a role, resulting in a higher metabolic rate of this species, in comparison with those from the western part of the basin. The observed low number of empty stomachs in the present study, indicating either a high feeding rate or Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH

slow digestion rate, could be explained by their high metabolic rates, as Company (1995) showed for other deep water shrimp (Aristeus antennatus) in the Western Mediterranean. Since both nektobenthic species, belonging in the same family, have a similar depth distribution, it is expected that they have similar energy values (in terms of wet mass), water body content (K. Kapiris unpublished observations) and oxygen consumption rates (Company & Sarda` 1998). In general, a decrease in diversity and mean prey items with increasing overlap was observed. In the Eastern Ionian Sea, the giant red shrimp fed on a greater proportion of pelagic resources and prey with a good swimming ability, such as the natantian decapods, and to a lesser extent on benthic prey, indicating that this shrimp is an active and effective predator of the bathyal zone in the Eastern Mediterranean. The low presence of the benthic prey taxa could be attributed to the lower benthos availability found in the study area (Madurell & Cartes 2005). The characteristic of its active predation could be also confirmed by the very low abundance of infaunal and epibentic prey (e.g. polychaetes, bivalves and gastropods) in the stomachs of this species. The increased abundance of fishes and cephalopods in their foreguts most probably reflects the great scavenging ability of this species. In any case, this does not exclude the possibility that this species feeds actively upon fishes and cephalopods, as Bello & Pipitone (2002) have pointed out. Some remains of A. antennatus in the stomachs of A. foliacea could be accidental, as they were found in the sampling stations where both species coexisted and, thus, some body appendages could have been destroyed and mixed during the net tow (net feeding). It is also possible that the smaller individuals of each species were consumed by larger adults of the other, due to their voracious character, but further study of this hypothesis is required. Food habits in relation to sex, season and size

Only a partial differentiation in the feeding behaviour, in terms of both diet composition and feeding activity, was observed between sexes of Aristaeomorpha foliacea. The consumption of the same prey items, but in different abundance and occurrence, may be attributed to sexual dimorphism and to size difference between the sexes. From the above results, a slightly higher predatory ability was indicated for females in the Eastern Ionian, as reported for the Sicilian Channel (Gristina et al. 1992). In general, the existence of regular seasonal rhythms in the feeding activity of deep water species is related mainly 351



A. foliacea males, medium

A. foliacea males, small

40

40



DEC. NATANTIA

35 30 DEC. NATANTIA

25

OTHER CRUSTACEA OTHERS

20 15 10 5

POLYCHAETES FISHES MOLLUSCS DEC. REPTANTIA

0 –5 –5

0

5

10

15

20

25

30

35

35 30 FISHES

25

OTHER CRUSTACEA

20 15

OTHERS MOLLUSCS

10 5

DEC. REPTANTIA POLYCHAETES ECHINODERMS

0 –5 –5

40

5

15

Frequency of occurence (%)



35 30 25 OTHER CRUSTACEA OTHERS

15

POLYCHAETES FISHES MOLLUSCS

10 5

ECHINODERMS DEC. REPTANTIA MUD

0 –5 –5

0

5

10

15

20

25

45

55

40 DEC. NATANTI A

20

35

A. foliacea females, medium

A. foliacea females, small

40

25


30

35

40

35

DEC. NATANTIA

30 25 20

OTHERS

15

FISHES POLYCHAETES OTHER CRUSTACEA MOLLUSCS

10 5

DEC. REPTANTIA MUD

0 –5 –5

0

5


10

15

20

25

30

35

40

Frequency of occurence (%) A. foliacea females, large

40


DEC. NATANTIA

35 30 25 20

OTHERS

15

FISHES MOLLUSCS OTHER CRUSTACEA POLYCHAETES

10 5 0 –5 –5

DEC. REPTANTIA MUD ECHINODERMS

0

5

10

15

20

25

30

35

40


Fig. 6. Prey importance by size group and sex of Aristaeomorpha foliacea, by sex in the Eastern Ionian Sea in the period December 1996–November 1997 according to Costello’s 1 theory.

to seasonal fluctuations in various factors including the abundance of their prey, depth, local geographical characteristics, submarine canyons, bottom type, seabed features, seasonal horizontal or diurnal vertical migrations, etc. (Cartes 1993, 1998). In the Eastern Ionian Sea the seasonal feeding habits of the giant red shrimp seem to be related to reproduction, and perhaps to other biological processes, and food availability. High observed values of trophic overlap between seasons for both sexes indicated that season is not the main factor affecting the diet of deep-water shrimps in the Eastern Ionian Sea. In spite of this, most feeding activity values (vacuity index, quality indices, mean number of prey items found into the stomachs, diversity index) support the finding that feeding activity increased during 352

spring–summer for both sexes. This increase could be attributed to the increased reproductive activity (gonad maturity, egg-laying) observed in this period (Papaconstantinou & Kapiris 2001, 2003). In addition, copulation begins at the end of winter and by spring almost all females are inseminated (Kapirs 2004). The minimum value of the stomach fullness in spring, in combination to the highest food quality value and the lowest vacuity index in females in the same season, suggests that egg maturation is connected to the feeding habits of A. foliacea. During winter, A. foliacea had the highest stomach fullness, but with decreased food quality. This increase of food consumption by the giant red shrimp of the Ionian Sea during the pre-reproductive period has also been observed in Aristeus antennatus off the Balearic Islands. Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH


Increased feeding rates could be the main reason for its egg development and could allow earlier gonad maturity (Cartes et al. 2008). Besides the seasonal feeding adaptation to the biological requirements (reproductive process), food availability also plays an important role for these species in the Eastern Ionian Sea. Madurell & Cartes (2005) noted that significant seasonal changes in the diet of the deep-water fish Hoplostethus mediterraneus in North-eastern Ionian Sea could reflect variation in prey availability. Accordingly, we observed the highest densities in the suprabenthic fauna (mysids, cumaceans, amphipods, isopods, tanaidaceans) during spring, but zooplankton (chiefly copepods, ostracods and chaetognaths) were more abundant in summer and autumn. Such fluctuations in food availability have also been shown in the diets of both sexes of A. foliacea in this study. Thus, the diet of the giant red shrimp probably reflects localized forage assemblages rather than a preference for specific items. The size-related changes in diet composition are an important factor in determining ecological relationships of marine organisms during their life span. Several studies on the diets of decapods highlight ontogenetic changes as the most important biotic factor in diet variability (e.g. Freire & Gonza´lez-Gurriarań 1995). Comparison of diet composition, dietary diversity, and feeding activity among small, medium and (only for females) large individuals reveals that this decapod undergoes slight changes in feeding habits with increasing body size, as well as gonad maturity, in the Eastern Ionian Sea. Small males and females (immature individuals) consumed fewer prey due to their smaller stomachs, with more frequent occurrence of epibenthic prey in their foreguts. Larger, mature individuals of both sexes are more efficient predators due to their greater swimming ability and larger mandibles. A positive trend of ingesting larger prey with increased size was observed only for females. This is the first time where this gradation, probably due to the population structure and to morphological variation among size classes and sexes (Burukovsky 1972), has been observed for A. foliacea. In general, somatic growth and gonad development induce a change in this species’ feeding behavior as the body grows an increase in the mean weight of prey and a decrease in the mean number of prey items per stomach was obvious. However, almost the same prey occurred in the stomachs of small, medium and large specimens, but in different proportions. Acknowledgements The material was collected during sampling cruises within the research program ‘Deep Water Fisheries’ partly supported by the EU (FAIR 95-0655). The authors wish to Marine Ecology 31 (2010) 341–354 ª 2010 Blackwell Verlag GmbH


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