Progress in Oceanography 79 (2008) 37–54

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Progress in Oceanography

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The feeding and diet of the deep-sea shrimp Aristeus antennatus off theBalearic Islands (Western Mediterranean): Influence of environmental factorsand relationship with the biological cycle

Joan E. Cartes a,*, Vanesa Papiol a, Beatriz Guijarro b

a Institut de Ciències del Mar (CMIMA-CSIC), Psg. Marı́tim de la Barceloneta 37–49, Spainb IEO-Centre Oceanogràfic de les Balears, P.O. Box 291, 07080 Mallorca, Spain

a r t i c l e i n f o a b s t r a c t

Article history:Received 14 February 2008Received in revised form 25 July 2008Accepted 25 July 2008Available online 6 August 2008

Keywords:Feeding intensityTrophic dynamicsDeep SeaDecapodaBenthic-Planktonic couplingReproductive cycleWater massesDaily migrations

0079-6611/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.pocean.2008.07.003

* Corresponding author.E-mail address: jcartes@icm.csic.es (J.E. Cartes).

Spatio-temporal variation of feeding intensity and diet in the red shrimp Aristeus antennatus was studiedat two locations around the island of Mallorca (Balearic Islands, Western Mediterraean) in August,September, and November 2003, and in February, April and June 2004 at depths between 550 and750 m. The two areas, with different oceanographic conditions, were respectively located in the north-west (Sóller) and the south (Cabrera) of Mallorca. Off Sóller, feeding intensity of A. antennatus showeda significant increase from February to April and June 2004 in all the three size-classes studied (smallshrimps: CL < 30 mm; medium: CL between 30 and 40 mm; large: CL P 40 mm). Off Cabrera, the highestfullness was recorded in November 2003 among small and medium shrimp, while only large specimensshowed patterns similar to that found off Sóller. Off Sóller, the diet of both small (CL < 34 mm) and large(CL P 34 mm) A. antennatus was mainly influenced by season, with three dietary groups corresponding toAugust–September 2003, to November 2003/February 2004, and to hauls from April to June 2004. OffCabrera, hauls (representing diets) were grouped by depth, never by season. The most remarkable sea-sonal shift in the diet of A. antennatus off Sóller was the increase of mesopelagic prey in April–June rel-ative to other months. In all size categories there was an increase off Sóller in the energy intake of preyingested from February to June 2004, an increase not found off Cabrera. Degree of digestion of mesope-lagic prey indicated nocturnal feeding on mesopelagic fauna. These prey probably have a shallower depthdistribution at night than found in our daylight sampling, and possible migratory movements among preyand A. antennatus at night would explain the lack of correlation between prey abundance in guts and inthe environment found during daylight periods for most micronekton mesopelagic prey (euphausiids,myctophids and sergestids). Off Sóller, fullness and diet were significantly linked to temporal changesin water column productivity (e.g., Chl a readings, fluorescence) and to changes in the shrimp biology(lipid content of hepatopancreas, Gonado-somatic Index, GSI). Off Cabrera, we found a higher dependenceof fullness and diet with T and S, both variables in turn related to depth. The increase of stomach fullnessand dietary energy intake in pre-reproductive females from February to April–June 2004 found off Sóller,coupled with the consumption of mesopelagic prey, was parallel to a significant increase of the gonadweight (GSI, fecundity) in June. Most individuals attain gonad development in the period May–June, aftertwo months of the peak of primary production at the surface. The strong link found between pelagicresources and reproductive processes in a deep-sea species such as the shrimp Aristeus antennatus, situ-ated near the top of the trophic web, suggests a rapid energy flow via mesopelagic fauna between surfaceprimary production and bathyal megabenthic communities at oligotrophic insular areas. In contrast tomainland areas off the Catalan coasts submitted to the influence of submarine canyons, around the islandof Mallorca the empoverishment of benthos biomass may enhance consumption of micronektonic preyand a possible accumulation of pre-reproductive females of A. antennatus in areas (e.g., steep slopesand persistent frontal systems found off Sóller) with high zooplankton aggregations.

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1. Introduction

Aristeus antennatus (Risso, 1816) is a demersal deep-sea shrimpdistributed in the subtropical Atlantic from Cape Verde in thesouth into Mediterranean waters (Crosnier and Forest, 1973;

38 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

Lagardère, 1977). It is a dominant species in Mediterraneanmegafaunal assemblages, occupying the middle and lower partsof the slope between 450 and 2261 m (Cartes and Sardà, 1992;Cartes, 1993a), with a few specimens caught deeper, to 3300 m(Sardà et al., 2004). Other species in the genus Aristeus are also dis-tributed at mid-bathyal depths (e.g., Aristeus varidens) in tropicaland subtropical waters (Crosnier and Forest, 1973). Aristeinae alsoincludes a number of large, often red-coloured shrimp such as Ple-siopenaeus spp. and Aristaeaomorpha spp., all of them abundant indeep waters and of high ecological and fisheries interest.

The trophic role of A. antennatus has been studied both in theAtlantic (Lagardère, 1971) and in Mediterranean waters(Relini-Orsiand Wúrtz, 1977; Cartes, 1994; Chartosia et al., 2005). Aristeusantennatus has a highly diverse diet (H0 of 5.58: Cartes, 1994),and together with some Macrouridae (Madurell and Cartes, 2006)and other decapods (e.g., Crangonidae: Lagardère, 1977) it isamong the megabenthic predators whose diet is mainly based onbenthos in the deep Mediterranean (Cartes, 1994; Cartes and Car-rassón, 2004). However, A. antennatus preys on a wide variety ofbenthic and benthopelagic organisms with ontogenic changes inthe diet (Cartes and Sardà, 1989). Small juveniles prey on smallcrustaceans (amphipods, euphausiids and mysids), while amongadults there is an increasing importance of large prey (small fish,the burrowing decapod Calocaris macandreae, mesopelagic deca-pods such as Pasiphaeidae and Sergestidae) in the diet. Size-relateddietary changes have largely been described among fishes, but lessso for decapod crustaceans (Fanelli and Cartes, 2004). The diet of A.antennatus also changes with depth and season (Cartes, 1994).Although this has been attributed to changes in prey availability,the simultaneous sampling of prey has rarely been accomplished.Large specimens prey on infauna and epifauna (e.g., polychaetes,ophiuroids) at the head of submarine canyons, where the biomassof infauna and the stomach fullness (feeding intensity) of A.antennatus increase, probably as a consequence of high local pro-ductivity in canyons (e.g., higher organic matter – OM - content:Cartes, 1994). In addition, A. antennatus occupies a high trophic le-vel (elucidated by their isotopic composition: Polunin et al., 2001)in deep-sea food webs, and it shows diel feeding rhythms and a rel-atively high food consumption rate (deduced from daily rationmodels: Maynou and Cartes, 1997) linked to possible nocturnalmovements upward along the slope canyons (Cartes et al., 1993).

After 21 yrs of studies on the biology of this species, especiallyoff the coasts of Catalonia (Balearic Basin), important knowledgegaps still remain. Aristeus antennatus shows a smaller-deeper trend(Sardà and Cartes, 1993), with smallest recruits (individuals be-tween 7 and 16 mm CL) distributed below 1400 m (Cartes andDemestre, 2003) in both the Balearic Basin (Sardà and Cartes,1993) and the Algerian Basin (Morales-Nin et al., 2003). Why theserecruits are linked to deep waters, expected a priori to be of lowproductivity, is unknown. Relatively high levels of fresh OM havebeen recorded below 1000 m in the Balearic Basin (Cartes et al.,2002), At these depths, there is still a relatively high abundanceof suprabenthic crustaceans (e.g., amphipods, cumaceans), whichcan exploit detritus (Madurell et al., 2008). These small crustaceansare the prey of the smallest A. antennatus recruits (Cartes data inSardà and Cartes, 1997). As the smallest recruits of A. antennatusare practically absent from upper and mid-slope depths above1000 m, possible coupling between potential prey availabilityand shifts in the abundance of A. antennatus above 1000 m depthmust be related with the aggregation of reproductive specimens,not with recruitment of juveniles.

The biological cycles of deep-sea macrofauna have been repeat-edly suggested to derive from cyclic food availability, often linkedto periodic phytodetritus deposition (vertical flux), and to advec-tive fluxes in areas with mainland influence (e.g. via submarinecanyons: Palanques et al., 2006). Among megafauna, links with

pulses of food also happens among detritivorous echinoderms, par-ticularly holothurians (Ginger et al., 2001; Hudson et al., 2004) andasteroids (Howell et al., 2004). Among deep-water predators,including decapods (Cartes et al., 2007) occupying higher trophiclevels than echinoderms, we generally expect a delayed responseto peaks of primary production. Orton’s rule (1920) suggested thatcontinuous (or asynchronous) gametogenesis should be the domi-nant reproductive pattern of deep-living species, permitted by theincreasing environmental stability at great depths. However, con-tinuous and seasonal (or synchronous) reproduction has been doc-umented at mid-slope depths (Gage and Tyler, 1991). In addition,Thorson’s rule (1950) predicted the prevalence of lecitotrophic lar-vae among deep water fauna. However, in the Atlantic Ocean attemperate latitudes, both planktotrophic (e.g., Sergestidae) andlecitotrophic (e.g., Pasiphaeidae) decapods can be found at meso-pelagic levels (Omori, 1974). Lecitotrophic oplophorid shrimp aredominant at bathypelagic depths, whereas at the abyssopelagic le-vel we find planktotrophic species such as Benthysicymus spp. orBentheogenemma spp., species with the same biological strategyfound in Aristeus antennatus. Penaeoidean shrimp are characterizedby shedding eggs into the water, a feature common in ‘r strate-gists’, not attaching them to their pleopods as do the rest of thedecapods. In summary, the data available for deep-water shrimpare not consistent with a single expected pattern of reproduction,probably because the energetic costs of both strategies (plankto-trophy and lecitotrophy) are similar.

Complete understanding of reproductive success among deep-sea invertebrates will require both better knowledge of their lifecycles and simultaneous environmental (physical–chemical) andtrophic data, among the most important probably being food avail-ability and consumption. Recently, the joint study of food and feed-ing and of the reproductive cycle in the pandalid shrimp Plesionikamartia, a species inhabiting the mid-slope of the deep Mediterra-nean, indicates important shifts in the diet of this species depend-ing on season, with a more energy-rich diet (based on theconsumption of energy-rich mesopelagic decapods) in spring coin-ciding with the beginning of gonad development in pre-reproduc-tive females (Fanelli and Cartes, 2008). The congeneric speciesPlesionika heterocarpus, distributed at shallower depths than P.martia and showing a continuous reproductive cycle, did not exhi-bit such substantial changes in the diet as did P. martia. Lipids havean important role in these cycles, and lipid biomarkers indicate dif-ferent biological strategies for mesopelagic fauna (Ju and Harvey,2004) and for deep-sea benthos, depending on the nature of lipidsaccumulated by each species (Ginger et al., 2001). Fluctuations inthe lipid content in muscle, ovary and hepatopancreas have beenreported for A. antennatus (Rosa and Nunes, 2003a,b; Guijarroet al., 2008), with shifts probably linked to its non-continuousreproductive cycle (Arrobas and Ribeiro-Cascalho, 1987; Demestreand Fortuño, 1992). The beginning of gonad development in pre-reproductive females occurs in May with a peak in summer(Demestre and Fortuño, 1992) in the Balearic Basin.

In the present study, the trophic dynamics of Aristeus antenna-tus to the northwest and south of Mallorca (Balearic Islands) weresimultaneously studied in relation to suprabenthos-zooplanktondynamics (see Cartes et al. (2008)) based on bi-monthly sampling.The sampling covered two neighbouring regions (separated by110 km) situated around the island of Mallorca. The areas were ex-pected, before the sampling, to have different oceanographic con-ditions and clear differences in the population dynamics of thered shrimp (Guijarro et al., 2008). The objectives pursued in thisstudy were: (1) to identify the importance of spatial patterns inthe diet and feeding of Aristeus antennatus; (2) to identify seasonalvariations; (3) to establish the main environmental variables con-trolling these trophic aspects; and (4) to establish possible linksbetween the trophic requirements of A. antennatus and its repro-

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 39

ductive cycle. We sought to demonstrate shifts in the diet and pos-sible short-term coupling of general ecological processes with redshrimp reproduction. We worked exclusively with gut contents,excluding other methods used in trophic studies (e.g., isotopicanalyses) that are more focused on demonstrating average charac-teristics of the assimilated food.

2. Material and methods

2.1. Study area and sampling strategy

The study of changes in the feeding and diet of Aristeus antenn-atus was performed in two areas situated to the northwest and tothe south of Mallorca (Balearic Islands, Western Mediterranean:Sòller at 38�980N–2�570E; 39�140N–2�760E and Cabrera at39�680N–2�180E; 39�810N–2�370E, (Fig. 1) The two sites are sepa-rated by ca. 110 km. The Sóller site is in the Balearic Basin (be-tween the coasts of Catalonia – northeast Iberian Peninsula – andthe Balearic Islands). The Cabrera site is close to the Cabrera Archi-pelago in the Algerian Basin. The Balearic and the Algerian basinsare separated by a ridge at ca. 600 m depth in the Mallorca channel.

The two sites have different oceanographic conditions (Millot,1999; López-Jurado et al., 2008), with different surface watermasses. Over the area as a whole there are two main surface watertypes: Modified Atlantic Water (MAW) progressing northwardfrom the Algerian basin and Local Atlantic Water (LAW), a residentwater type in the Balearic basin (López Garcia et al., 1994). OffCabrera, MAW predominates (particularly in spring–summer),and only weak frontal systems are formed. Off both Cabrera andSóller, at mid-slope depths, where A. antennatus is distributed, var-iability is due to the occurrence of the Levantine Intermediatewater (LIW), which is present during the entire year with variableseasonal inflow. LIW seasonal inflow was especially strong offSóller at mid-bathyal depths (350–550 m) in spring–summer, aftercirculating through the northern part of the Western Mediterra-nean from the Eastern Basin (López-Jurado et al., 2008). The Wes-tern Mediterranean Intermediate Waters (WIW), which are formed

Fig. 1. Map of the study area around the Balearic Islands indicating sampling locationMallorca). Profiles constructed after calculating distance of trawls to the nearest coast.

during winter in the Gulf of Lyons (Pinot et al., 2002), can arrive atthe Balearic Islands in early spring (López-Jurado et al., 2008). WIWis found just above the LIW, is not present every year and varies inthickness yearly.

Regarding bottom character, the shelf is narrow and the occur-rence of muddy terrigenous sediment is reduced due to low riverdischarges. Muddy bottoms of biogenic origin dominate deeper,between 350 and 750 m (own data, Cartes et al., 2008). The steep-ness of the slope was greater off Sóller than off Cabrera (Fig. 1),which could enhance differences in the distribution of some foodresources and their availability for red shrimp.

Six surveys were carried out to sample large megafauna, foodresources (macrofauna: suprabenthos and zooplankton) andhydrographic features of the water column in August, September,and November 2003, and in February, April and June 2004. Aristeusantennatus were sampled from F/V Moralti Nou using a commercialotter bottom trawl (Moranta et al., 2008). On each survey and ineach area, three hauls were carried out at 550, 650 and 750 m onred shrimp fishing grounds. All samplings were performed in day-time, comprising sunrise to noon (ca. 05.00–12.30 GMT). Durationof trawlings was 45–60 min. Suprabenthos and meso-macrozoo-plankton were sampled from R/V Francisco de Paula Navarro. A totalof 46 Macer-GIROQ sledge and 461 m2-WP2 plankton net towswere performed corresponding to six cruises (3–7 August 2003;25 September–1 October 2003; 13–21 November 2003; 14–20February 2004; 7–13 April 2004; 23–28 June 2004). During eachcruise, four stations (at depths ca. the 150, 350, 650 and 750 m iso-baths) were sampled off both Sóller and Cabrera (other details inCartes et al. (2008)). Distance between stations along the transectsranged from ca. 6 to 18 km. The sledge sampled suprabenthos be-tween 10–40 and 50–90 cm above the bottom. Macrozooplanktonin the water column was sampled using a WP2 net with a moutharea of 1 m2, in horizontal-oblique hauls performed from between13 and 90 m above the sea bottom to the sea surface. Both WP2and sledges were equipped with 500 lm mesh size nets and weretrawled at ca. 1.5 knots. The durations of sledge hauls over the bot-tom were ca. 10 min; the duration of WP2 tows were 10 min close

s and slope profiles off Sóller (NE of Mallorca) and off Cabrera Archipèlago (S of

40 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

to the bottom (horizontal haul) plus between 3 and 15 min duringthe recovery of the net throughout the entire water column. Thesame depth was maintained during all manoeuvres. Standard2030 flowmeters were attached to the mouth of nets to measurethe amount of filtered water and/or the distance/area covered byeach haul. All samples were collected during daytime.

2.2. Analyses of trends in abundance and in trophic data

Abundance of Aristeus antennatus was standardised to numberk m�2 for each trawl (Guijarro et al., 2008). The centers of gravity(COG: Stefanescu et al., 1992) for total abundance of small andlarge (adult) females collected were calculated for each area andcruise. This population COG is defined as

COG ¼ ðx1 � z1 þ x2 � z2 þ x3 � z3 . . .Þ=X

xi;

where xi is the calculated mean abundance of the species/popula-tion in the depth stratum i and zi is the mean depth of that stratum.Specimens were classified in two/three size classes according toprevious information available on its diet (Cartes and Sardà, 1989;Cartes, 1994) and its biology (Demestre and Fortuño, 1992;Demestre, 1995). To analyze feeding intensity and the energeticcontent of diet we considered three size classes: (i) small with car-apace length (CL) < 30 mm, which comprised all immature speci-mens and small males/females; (ii) mid-sized specimens, with CLbetween 31 and 40 mm, comprising adult females and males, and(iii) large, exclusively adult, females, with CL P 40 mm. For dietonly two groups were considered: (i) individuals smaller than34 mm CL and (ii) individuals larger than or equal to 34 mm CL,in the last case comprising only females. The diets of males and fe-males were not considered separately after it was established thatdiet depends mostly on size, not sex (Cartes and Sardà, 1989), andthis increased the number of specimens analyzed per haul and sizeclasses for MDS analyses.

The following indices were calculated to measure feeding inten-sity and diet:

(1) Stomach fullness, F (stomach content weight/ predatorweight).

(2) W (weight of prey item/total gut content weight � 100, inwet weight).

These are traditional indices employed in the study of fish feed-ing (Hyslop, 1980) and used previously for decapods (e.g., in Cartes(1994)).

Table 1Caloric content (k cal/g DW) of the main prey found in Aristeus antennatus according to li

Species/taxa k cal/g DW Source

PolychaetaCrustacea 2.24 Madurell unp.Gammaridae (Rhachotropis sp.) 2.15 Madurell andBoreomysis arctica 2.16 Madurell andSergestes arcticus 3.16 Madurell andPasiphaea sivado 3.12 Madurell andPlesionika martia 4.88 Madurell andEuphausiacea 5.19 Blaber and BuCephalopoda 5.43 Blaber and BuTeuthoidea 4.06 Madurell andMyctophidae 3.43 Madurell andCyclothone braueri 4.00 Zagami et al. (Argyropelecus hemygymnus 3.51 Zagami et al. (Hygophum benoiti 3.86 Zagami et al. (Maurolicus muelleri 4.11 Zagami et al. (

Data were selected based on studies performed in similar habitats, and on prey sizes si

The abundance of some dominant, broad taxa/species, key preyin the diet of Aristeus antennatus, caught with sledges (e.g. polych-ates, bivalves and Calocaris macandreae among infauna, Boreomysisarctica, and Natatolana borealis among suprabenthos) and WP2nets (e.g., euphausiids, meso-bathypelagic decapods and Mycto-phidae among zooplankton/micronekton) and they were standard-ized to individuals/100 m2.

Degree of digestion was established for some key mesopelagicprey (e.g., natantian decapods, Meganyctiphanes norvegica andmyctophids). Five degrees of digestion of food in stomachs wereconsidered, from undigested to very digested, similar to the scaledescribed by Aloncle and Dalaporte (1970) and adopted by theauthors (e.g., Stefanescu and Cartes, 1992) for deep water fish.We counted prey of the two least digested values on that scaleappearing in stomachs.

Caloric content of the diet was also estimated, based on the val-ues of caloric content of prey found in previous, similar studies(Blaber and Bulman, 1987; Zagami et al., 1991; Madurell andCartes, 2005) performed on deep-sea fauna and summarized inTable 1. Sum of caloric contents of prey found in stomachs was per-formed to estimate the whole caloric content of the diet. Caloriccontent depends, among other variables, on the season, habitat,and size of species and individuals (Hopkins, 1988; Zagami et al.,1991). Therefore, we emphasized the data on caloric content froma study of benthopelagic fish trophodynamics in a bathyal site inthe eastern Mediterranean (Madurell and Cartes, 2005), whereprey consumed by small benthopelagic fish (e.g., Macrouridae)are similar in size to those consumed by A. antennatus.

2.3. Environmental and biological variables

The major part of environmental and biological variables is pub-lished in a monographic issue containing articles related with IDEAproject; however, these data were used in those articles for differ-ent objectives than in the current paper. There we detailed infor-mation as a function of depth and season on granulometry,organic matter and Chl a satellite data (Cartes et al., 2008:Madurell et al., 2008; Moranta et al., 2008), on T and S and fluores-cence (López-Jurado et al., 2008) and on all biological variables(Guijarro et al., 2008; see also Section 4). Only T, S (from 150 to750 m) are again presented with some detail in this paper, thoughonly data from 550 to 750 m, simultaneously taken with redshrimp, were considered for statistical analyses. To avoid, amongother things, duplicity in the publication of environmental/biolog-ical data, the rest of these variables are directly treated in the

terature sources

From polychaetes consumed by C. coelorhynchusCartes (2005) Range size similar to that consumed by A. antennatusCartes (2005) Range size similar to that consumed by A. antennatusCartes (2005) Range size similar to that consumed by A. antennatusCartes (2005) Range size similar to that consumed by A. antennatusCartes (2005)lman (1987)lman (1987)Cartes (2005) Range size similar to that consumed by A. antennatusCartes (2005) Range size similar to that consumed by A. antennatus1991) TL 2.6 cm, similar to that found in WP2 sampling1991) TL 1.6–5.01991) TL 5.3–5.61991) TL 4.4–5.1

milar to those found in A. antennatus.

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 41

respective statistical analyses performed or included in theSection 4.

Environmental variables were collected along the samplingtransects using SBE911 and SBE25 CTD profilers from R/V FP Nav-arro and with an SB37-SM mounted on the mouth of the commer-cial otter trawl (see López-Jurado et al. (2008)). From each profilewe obtained a measure of temperature and salinity at 5 m abovethe bottom (T5 mab; S5 mab). Fluorescence was recorded throughoutthe water column. Maximum fluorescence and depth of that max-imum were obtained from the raw data.

Sediment for granulometric and organic matter analyses werecollected with a Shipeck grab at each station and on each cruise,obtaining the variables: (1) percentage of mud (silt + clay) usingSedigraph techniques (see Cartes et al. (2008) and Moranta et al.(2008) for additional details); and (2) total organic matter (%OM)content, calculated as difference between dry weight (DW: 80 �Cduring 24 h until reaching constant weight) and ash weight(500 �C in a furnace during 2 h).

Phytoplankton pigment concentration (ppc, mg Chl a m�3) ob-tained from satellite imagery (http://reason.gsfc.nasa.gov/Giovanni) was used as an indicator of the productivity in the area.Monthly averages of ppc for the positions of the bottom trawlswere used, considering periods simultaneous with and 1, 2 and 3months before each shrimp sampling.

Biological variables: The following were measured:

(1) red shrimp density (individuals � k m�2);(2) gonadosomatic index (GSI), calculated as GSI = 100 (GW/W),

the gonad wet weight divided by total individual weight;(3) hepatosomatic index (HSI) calculated as HSI = 100 (HW/W),

the weight of hepatopancreas divided by individual weight;(4) condition index (Kn; Le Cren, 1951) calculated as Kn = OW/

EW, the observed weight divided by the expected weightestimated from length-weight relationships based on thewhole data set; and

(5) total lipids from the hepatopancreas, as percentage of dryweight. GSI, HIS, Kn and total lipids, taken from Guijarroet al. (2008).

2.4. Data treatment

Data treatment was based on a total of 1672 Aristeus antennatus,collected in 36 trawls and dissected in the laboratory immediatelyafter capture. The stomach contents of 909 of these individualswere examined (Table 2). Mean stomach fullness (feeding inten-sity) was calculated for 36 hauls (number of specimens per haul:13–23 for small males and females; 9–21 for large males/mid-sizedfemales; 10–23 for large females). Individuals were measured(cephalothorax length – CL– in mm) and weighed to the nearest0.01 g. The stomach content was weighed to the nearest 0.0001 gand prey identified to the lowest possible taxonomic level undera stereomicroscope (�10–�40). When it was not possible to obtaina direct weight for each prey item/type, weight of prey consumed(WW, g) was estimated after the percentage volume occupied byeach prey in stomach contents was estimated using the subjectivepoints methods (Swynnerton and Worthington, 1940). The wholestomach content weight was thereby partitioned for each prey-type.

Data on diet (per haul: all stomachs from a single trawl com-bined) were analyzed by MDS techniques by separate in Cabreraand Sóller. Based on the resemblance matrix obtained by raw ma-trix data, Multi-Dimensional Scaling (MDS) was performed. Thenumber of specimens analyzed for diet per haul ranged between8 and 19 specimens, both for small shrimp and for large females.The similarity index used in MDS ordination was 1 � r (Pearson

correlation coefficient, after log-transformation of the data). Theaggregation algorithm was the UPGMA (Unweighted-paired groupmethod average). PERMANOVA analyses (one factor consisting intime periods off Soller, in depth intervals off Cabrera; 9999 permu-tations) were performed on the resemblance matrix (Bray-Curtisdistance) to test significance of groups formed in MDS analyses.

To relate feeding and diet of the red shrimp with biological andenvironmental variables, we examined possible correlations be-tween diet, and stomach fullness (the dependent variables) andthe following environmental and biological possible explanatoryvariables:

Environmental variables: (1) depth (m); (2) temperature (�C) andsalinity (psu) at 5 m above the bottom (T5 mab; S5 mab); (3) %mud; (4) percentage of organic matter (OM) in sediments; (5)phytoplankton pigment concentration (mg Chl a � m�3)obtained by satellite imagery; (6) Maximum fluorescence and(7) depth of maximum fluoresence taken in IDEA02 and IDEA04.Biological variables: (1) density (individuals � k m�2); (2)Gonadosomatic index (GSI); (3) Hepatosomatic index (HSI);(4) Kn; and (5) Total lipids from the hepatopancreas.

Only T and S are presented in this paper, while the other envi-ronmental variables are already published (Cartes et al., 2008;Guijarro et al., 2008; López-Jurado et al., 2008).

We searched for possible correlations to identify the mainexplanatory variables for feeding intensity and diet at two levels:(1) by simple non-parametric Spearman rank correlations (feedingintensity and diet); and (2) by linear multiple-regression models(MLR; after log transformation of the data), only for feeding inten-sity. All the analyses were performed using PRIMER6 & PERMANO-VA+ (Clarke and Warwick, 1995; Anderson, 2001) and STATISTICA7.0 softwares.

3. Results

3.1. Abundance and size-depth distribution

There were some differences in the depth distribution (COG) oftotal abundance and females between Sóller and Cabrera. The mostremarkable trend was a displacement off Sóller of the COG of fe-males, especially large females, to shallower depths (on averagebetween 50 and 100 m, in a range of 300 m, between 550 and750 m) during February and June (less in August). COGs reachedthe shallowest depths observed in February 2004 (Fig. 2). Differ-ences in COG between Cabrera and Sóller transects increased fromApril to June (Fig. 2), when COG of both females and total abun-dance were displaced to greater depths off Cabrera (Fig. 2).

3.2. Spatio-temporal changes in stomach fullness

The feeding intensity of A. antennatus in the depth interval 550–750 m, showed seasonal fluctuations (Fig. 3), which differeddepending on site (Cabrera and Sóller) and size class. Off Sóller,all size-classes showed significant increases in stomach fullnessfrom February to April 2004 and June 2004 (Fig. 3). Minimum sig-nificant values were always recorded in February 2004 (Fig. 3). OffCabrera, the highest fullness values were recorded in November2003 (significant in comparison to February 2004) among smalland medium shrimp, while only adult specimens showed patternssimilar to that found off Sóller, i.e., an increase in fullness in April–June 2004. In summary, maximum feeding activity of Aristeusantennatus was often found in spring–early summer off Sóller, withlower values in late summer–autumn–winter. Off Cabrera the pat-tern was opposite for small and mid-sized shrimp, with the highestfeeding rates found in autumn (September–November).

Table 2Diet (W: grams wet weight per 100 individuals) of small and large Aristeus antennatus

Small CL <34 mm Large CL P34 mm

Sóller 581–738 m Cabrera 576–752 m Sóller 581–738 m Cabrera 576–752 m

Aug-Sep Nov–Feb Apr–Jun Aug-Sep Nov–Feb Apr–Jun Aug–Sep Nov–Feb Apr–Jun Aug–Sep Nov–Feb Apr–Jun

n 75 84 91 61 86 89 71 72 64 58 92 66

PoriferaHydrozoa

0.045 0.029 0.002 – – – 0.015 0.439 – 0.300 – –

Siphonophora (Chelophyesappendiculata)

0.191 0.073 0.041 0.237 0.125 0.100 0.151 0.006 0.035 0.21 0.14 0.06

Stephanoscyphus sp. 0.022 0.017 0.002 0.048 0.021 0.002 0.002 – – 0.011 0.012 0.006Polychaeta 0.633 0.326 0.755 0.605 1.179 0.892 5.602 4.302 2.462 3.683 4.897 3.474

Glycera spp. 0.030 0.005 0.033 0.029 0.025 0.044 0.01 0.041 0.134 0.059 0.062 0.123Aphroditidae 0.009 – 0.12 0.083 0.266 0.009 0.53 0.515 1.154 0.708 1.286 0.161Eunicida 0.117 0.060 0.128 0.154 0.177 0.193 0.521 – 0.498 0.853 0.899 1.502Nephthydae – – 0.041 – 0.240 0.102 0.932 1.832 0.011 1.054 0.396 0.419Polychaeta (other) 0.477 0.261 0.432 0.339 0.471 0.544 3.608 1.912 0.666 1.009 2.254 1.269

CrustaceaCopepoda Calanoida – � 0.004 0.017 � 0.004 – – – – – –Euphausiacea

Meganyctiphanes non/egica 0.062 0.270 1.529 0.132 0.384 0.547 0.032 0.300 2.129 0.367 0.331 0.763Other (Nematoscelis megalops) 0.092 0.019 0.314 0.056 0.019 0.068 0.009 – 0.207 0.227 0.005 0.193

DecapodaGennadas elegans 0.128 0.050 0.157 0.03 0.003 0.164 2.094 2.021 0.695 0.087 0.607 0.457Aristeus antennatus – 0.020 0.046 0.004 0.105 – 0.227 2.246 1.674 0.311 0.539 –Sergestes arcticus 0.188 0.004 0.183 – 0.259 0.023 0.119 0.034 – 0.708 – 0.546Sergia robusta – 0.022 0.696 – 0.093 0.251 – 0.237 3.903 0.358 0.854 2.232Pasiphaea multidentata 0.219 0.292 0.349 0.024 0.322 0.350 1.339 1.724 0.367 0.822 1.092 0.084Plesionika martia – 0.097 0.112 0.110 0.067 0.216 0.565 0.123 1.526 1.936 0.643 1.256Natantia unid. (Processa sp.) 0.544 0.288 0.202 0.285 0.206 0.271 1.471 0.605 0.283 0.604 0.729 0.663Calocaris macandreae 0.080 0.323 0.159 0.168 0.175 0.012 0.823 0.237 0.017 0.178 0.588 0.241Macrura Reptantia – 0.007 0.01 0.063 0.023 0.052 0.470 0.346 1.229 0.144 1.135 0.894Decapoda (post–larvae) – 0.002 0.154 0.013 – 0.031 – 0.018 0.014 0.04 – 0.017

MysidaceaLophogaster typicus – 0.021 – – – – – – – – 0.025 –Eucopia hanseni 0.036 – – – – 0.044 0.218 – – – – –Boreomysis arctica 0.039 0.100 0.044 0.097 0.015 0.018 0.056 – 0.249 0.056 0.127 0.090Other (Parapseudommacalloplura)

– 0.004 – – – – – – – – 0.027 –

Amphipoda GammarideaRhachotropis spp. 0.033 0.011 0.019 0.015 0.041 0.091 0.079 0.005 0.007 – 0.039 0.011Eusirus longipes 0.013 – – – – 0.019 – – 0.007 – – –Urothoe corsica – – – 0.039 0.035 � 0.007 – – – 0.011 0.013Tryphosites spp. 0.031 0.063 0.080 0.211 0.067 0.098 0.008 – 0.018 0.123 0.028 0.051Other Lysianassidae 0.137 0.038 0.044 0.135 0.074 0.090 0.036 0.005 0.054 0.051 0.092 –Harpinia spp. 0.003 – – 0.005 0.002 – – – – – – –Oedicerotidae 0.024 – 0.038 – 0.008 0.010 0.007 – – – 0.009 0.020Synopiidae (Bruzelia typica) – 0.015 0.011 0.008 0.013 0.038 – 0.005 – – – –Amph.Gammaridea unid. 0.034 0.018 0.019 0.042 0.049 0.023 0.002 0.015 0.007 – 0.042 0.007

42J.E.Cartes

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Amphipoda HyperiideaPhronima sedentaria 0.019 0.026 0.318 0.050 0.080 0.136 0.342 – 1.181 0.050 � 0.395Phrosina semilunata 0.005 0.526 0.734 0.638 0.094 0.045 0.164 0.022 1.998 0.628 0.051 0.481Vibilia armata 0.021 – – 0.057 0.017 – – 0.054 – – 0.013 –Other Hyperiidea 0.066 0.054 0.32 0.056 0.010 0.053 0.008 0.024 0.122 0.053 0.009 0.089

IsopodaAnthuridae 0.004 0.003 – – – 0.001 – – 0.003 – – –Natatolana borealis 0.213 0.270 0.450 1.220 1.188 1.377 2.757 3.704 3.439 5.999 8.309 6.097Eurydice grimaldii 0.003 0.002 – 0.050 0.031 0.076 0.027 – – 0.013 0.005 0.512Gnathia sp. – 0.002 – 0.016 0.011 – – – 0.009 – – –Munnopsurus atlanticus 0.037 – 0.008 0.007 0.005 0.033 0.004 0.002 0.009 0.002 0.021 0.007llyarachna sp. 0.036 0.003 0.009 0.028 0.012 0.015 – – – 0.007 0.002 0.035Other (Desmosomatidae) – – – 0.002 � – – – – – – –

Tanaidacea (Apseudes sp.) 0.032 0.007 0.030 0.096 0.071 0.041 0.103 0.014 0.043 0.055 0.055 0.038Cumacea

Leuconidae – – 0.006 0.017 – 0.006 – – – – – –Cyclaspis longicaudata – – – – 0.012 0.001 – – – – – –Platysympus typicus 0.003 – – – 0.003 – – – – – – –Other Cumacea (Diastylidae) 0.003 – – – 0.002 0.020 – – 0.010 – – –

Ostracoda (Cypridinidae) 0.033 0.010 0.054 0.065 0.077 0.066 0.002 0.009 0.005 0.054 0.029 0.031Pycnogonida (Pallenopsis scoparia) – 0.048 0.038 0.010 – – 0.172 – – – – –Mollusca

Caudofoveata 0.006 – – 0.004 – 0.007 – – 0.013 – 0.008 0.010Escaphopoda 0.030 0.007 0.027 0.012 0.006 0.023 0.064 0.02 0.016 0.030 0.094 0.022Bivalvia Taxodonta 0.115 0.095 0.098 0.048 0.158 0.065 0.252 0.129 0.123 0.345 0.302 0.191Abra longicallus 0.088 0.048 0.073 0.159 0.057 0.140 0.572 0.335 0.309 0.165 0.169 0.418Philine scabra 0.004 0.010 0.043 0.010 0.017 0.286 0.289 0.117 0.019 0.004 0.034Cymbulia peroni 0.023 – – – – – – – – – – –Alvania sp. – 0.002 – 0.010 0.004 0.002 – – – 0.011 – –Benthonella tenella 0.143 0.056 0.009 0.075 0.073 0.012 0.016 0.033 – – 0.005 0.016Gastropoda unid. 0.002 0.008 0.017 0.023 – 0.001 0.079 0.007 0.005 0.010 0.078 0.012Pteropoda 0.013 0.179 0.005 0.013 0.023 0.004 0.014 0.069 0.004 0.060 0.023 –Cephalopoda (Teuthoidea) – 0.086 0.107 0.089 0.007 – 0.216 0.592 2.733 0.078 1.469 0.469

Chaetognatha � 0.004 0.052 – 0.001 0.002 0.010 – – 0.006 0.012Pyrosoma atlanticum – – – – – – 0.318 – – 0.141 – –

Thaliacea – 0.024 0.035 – 0.094 – 0.383 0.022 0.373 0.078 – 0.358Sipunculoidea 0.009 0.026 0.026 0.076 0.019 0.076 0.136 0.023 0.138 0.005 0.029 0.125Echiurida 0.083 0 0.017 0.056 0.012 0.018 0 0 0.011 0 0.083 0.288Echinodermata

Ophiuroidea 0.159 0.075 – 0.072 0.046 0.097 0.158 0.022 0.022 0.013 0.187 0.116Echinoidea 0.051 0.029 0.033 0.002 – 0.008 0.121 0.241 0.055 0.023 0.216 0.231

OsteichthyesMyctophidae 0.077 0.224 0.398 0.011 0.226 0.330 3.345 4.336 2.926 0.515 3.564 2.062Cyclothone braueri 0.189 0.339 0.011 0.061 0.061 0.013 0.564 0.252 0.275 – 0.067 0.143Osteychthyes unid. (remains) 0.606 0.263 0.339 0.348 0.320 0.143 1.433 0.227 1.755 1.265 0.930 1.322

Foraminifera 0.061 0.083 0.013 0.017 0.034 0.055 0.129 0.028 0.051 0.032 0.095 0.102Nylon threats 0.023 0.021 0.003 0.001 0.002 – 0.126 0.004 0.022 0.007 0.002 –Unidentified (gelatinous) 0.296 0.804 0.026 0.167 0.087 0.074 0.532 1.189 0.448 1.408 0.254 0.236Plant remains (Posidonia) 0.027 – – – – – 0.006 – – – – –Unidentifed 0.078 0.030 0.016 0.073 0.003 – 0.027 – 0.277 0.477 – 0.369Other (e.g. Insecta) 0.006 0.008 0.006 – – 0.013 0.015 – – 0.010 – –

Diet is expressed in base of seasonal groups deduced from the MDS analyses. n: number of individuals analyzed; (�): <0.001 g.

J.E.Carteset

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43

SóSóSó

Dep

th (

m)

560

600

640

680

720

Cabrera

Sóller

560

600

640

680

720

Cabrera

Sóller

560

600

640

680

720

Cabrera

Sóller

Total abundance

Small females

Large females

Aug Set Nov Feb Apr Jun2003 2003 2003 2004 2004 2004

Fig. 2. Center of gravity (COG) as a function of season for total abundance and abundance of small and large females of Aristeus antennatus off Cabrera and Sóller.

44 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

3.3. Dietary analyses

A taxonomic range including 157 different prey items was iden-tified in stomach contents of A. antennatus (98 categories identifiedto genus/species level) (Table 2). Among small shrimp(CL < 34 mm) the main prey off Sóller were mesopelagic natantiandecapods (Gennadas elegans, Sergestidae, Pasiphaea multidentata),

fish (Myctophidae, Cyclothone braueri, fish remains) and the isopodNatatolana borealis. Some other prey were important seasonally,e.g., jellyfish remains (probably salps) in Aug–Sep and Nov–Feb,polychaetes and Calocaris macandreae in Nov–Feb and Apr–Jun,and hyperiids and Meganyctiphanes norvegica in Apr–Jun. Mainprey off Cabrera were polychaetes, and N. borealis. Bivalves werealso important prey there in comparison to Sóller. Mesopelagic

0

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F

CL 30 mm

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CL 40 mm

08, 02-06

11 11 11

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04,06 04,06

08, 02-06

1111

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08, 02

02

02

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06

11 11

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CL 30 mm

40 > CL > 30 mm

CL 40 mm

08, 02-06

11 11 11

11, 02

04,06 04,06

08, 02-06

1111

02

08, 02

02

02

11, 02

04,06

11, 04,06

08

06

11 11

04

Fig. 3. Fullness of Aristeus antennatus off Sóller (---------) and Cabrera ( ) as afunction of size (CL, cephalotorax length, mm) and seasonal periods. Numbersabove/behind each point means the periods (months, e.g., 08 = august) for which Fvalues were significantly different in paired comparisons (1-way ANOVA; Tukey’stest; p < 0.05). In dark tone for Cabrera, in light tone for Sóller. Parts of this figureappeared previously in Cartes et al. (2008).

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 45

natantians (in Apr–Jun) and fish (in Nov-Feb, myctophids) wereseasonally important off Cabrera, while siphonophores wereimportant in summer (Aug–Sep).

Both off Cabrera and Sóller dominant prey (in wet weight) inthe diet of large (Cl P 34 mm) females were polychates (mainlyAphroditidae and Nephthydae). In numbers the most abundantpolychate taxon consumed by A. antennatus was Glycera spp. Otherdominant prey by weight in both areas were mesopelagic deca-pods, N. borealis, fish and jellyfish (gelatinous) remains. Moreover,off Sóller euphausiids and hyperiids were important, especially inApr-Jun, while cephalopods were mainly consumed in Apr–Jun/Nov–Feb. In this same period off Cabrera, bivalves and echino-derms were among the dominant prey in the diet, and more Caloc-aris macandreae were consumed there all year round. Themesopelagic decapod Sergia robusta was an especially significantfood off Sóller in Apr-Jun.

MDS analyses summarized trends in diets based on a multipreyanalysis. MDS were performed for small (CL < 34 mm) and largespecimes (CL between 34 and 62 mm) separately. The diet of A.antennatus was primarily influenced by a seasonal component off

Sóller. Three (among small shrimps) and two (among large shrimps)groups corresponding to August–September 2003 and to April–June2004 (both in small and large shrimps) and November 2003–February 2004 (only among small shrimps) were identified inMDS analyses in that area. Hauls from November 2003–February2004 were situated between these two groups (significant differ-ences in the distribution of August–September 2003, April–June2004, and November 2003–February 2004 hauls: PERMANOVA test:Pseudo Fsmall = 7.44, p < 0.001; Pseudo Flarge = 4.74, p < 0.01; all post-hoc tests significant at p < 0.01 between all paired comparisonsexcluding November 2003–February 2004 vs. the two other groupsamong large shrimps). So, a similar seasonal trend was observedboth for small individuals (Fig. 4a) and for adult females (Fig. 4b).Off Sóller we found the most remarkable seasonal shift in the dietof small (CL < 34 mm) A. antennatus in April–June 2004, with a sig-nificant increase (t test, p < 0.05) of mesopelagic prey (e.g. theeuphausiid Meganyctiphanes norvegica, the decapods Gennadas ele-gans, sergestids, and Pasiphaea multidentata, hyperiids and myc-tophids) (Table 2). Other prey hardly varied (e.g., polychaetes, N.borealis, bivalves) or even decreased from August–September/November–February to April–June (e.g., gastropods, siphonophores,jellyfish remains, probably salps). Seasonal changes in the diet oflarge shrimp (CL P 34 mm) were similar to those found in smallones. The most remarkable trend was the increase of Sergia robustaand of euphausiids in gut contents in April–June 2004. However,other mesopelagic prey even decreased in this period (e.g., Gennadaselegans, Pasiphaea multidentata, myctophids) in comparison to Au-gust–September/November–February. Other prey hardly varied(e.g., the whole polychaete groups, N. borealis) or they decreased(e.g., bivalves, gastropods, siphionophores, jellyfish remains).

Off Cabrera, by contrast, the MDS analysis segregated hauls bydepth, never by seasonal groups, again both for juvenile/males(Fig. 4a) and adult females (Fig. 4b). Hauls performed between581 and 662 m were grouped and separated from the deepest sam-ples collected at 745–752 m (significant differences in the distribu-tion of the two depth groups both among large and small shrimps:PERMANOVA test: Pseudo Fsmall = 9.77, p < 0.001; PseudoFlarge = 9.03, p < 0.001). The diet both of small and large specimensat 581–662 m off Cabrera included substantial quantities of theisopod Natatolana borealis (30% of the diet of large; 24.6% in small)and also (in decreasing order) polychaetes (Eunicida, Aphroditida),myctophids and natantian decapods. Sergia robusta and Plesionikamartia were especially consumed by adults. Deeper, at 750 m, dietwas not as dependent on a single prey as at 581–662 m. Meganycti-phanes norvegica was the most important prey for small shrimp(only 7.3% of diet weight), with polychaetes (mainly Nephthydae),natantian decapods and bivalves. Among large shrimp unidentifiedpolychaetes (5.9% of diet) and eunicids were dominant, with signif-icant amounts of brachyurans and myctophids.

Caloric content of the diet, based on values compiled in Table 1,also showed differences between Sóller and Cabrera (Fig. 5). In allsize categories there was an increase in the energy content of preyingested from February to June 2004 off Sóller. Adults showed sim-ilar levels of energy content in their diet in September–November2003 than those found in February and June 2004. Off Cabrerathere was not a sharp increase of energy intake in these same peri-ods, and the highest caloric content was recorded among mediumshrimp in November and among adults in June, while no importantchanges were recorded among small specimens.

3.4. Distribution of prey

The abundance and depth ranges of the main prey consumed byA. antennatus off Sóller and Cabrera (Table 3) overlapped with thedistribution of A. antennatus. However, most prey-species showedhigher abundance in the other area than in the one where prey

C08-751

C08-659

C08-583

C09-752

C09-661

C09-584

C11-745

C11-659

C11-583

C02-750

C02-650C02-580

C04-752

C04-657

C04-586

C06-662C06-584

C06-750

-1.0 -0.4 0.2 0.8 1.4

Dim 1

-2.0

-0.5

1.0

Dim

2

S = 0.171

Cabrera

S08-734

S08-659

S08-581

S09-738

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S09-600

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S11-655

S02-735

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S04-605

S04-726S04-657

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S06-601

-1.4 -0.8 -0.2 0.4 1.0 1.6

Dim 1

-1.4

-0.8

-0.2

0.4

1.0

Dim

2

S = 0.192

Sóller

S08-734

S08-659

S08-581

S09-738

S09-653

S09-600

S11-593

S11-734

S11-655

S02-735

S02-655

S02-593

S04-605

S04-726S04-657

S06-730

S06-659

S06-601

-1.4 -0.8 -0.2 0.4 1.0 1.6

Dim 1

-1.4

-0.8

-0.2

0.4

1.0

Dim

2

S = 0.192

Sóller

C08-751

C08-659

C08-583

C09-752

C09-661

C09-584

C11-745

C11-659C11-583

C02-750

C02-650

C02-580

C04-752

C04-657

C04-586

C06-662

C06-584C06-750

-1.2 -0.6 0.0 0.6 1.2 1.8

Dim 1

-2.0

-0.5

1.0

Dim

2

Cabrera

S = 0.131

C08-751

C08-659

C08-583

C09-752

C09-661

C09-584

C11-745

C11-659C11-583

C02-750

C02-650

C02-580

C04-752

C04-657

C04-586

C06-662

C06-584C06-750

-1.2 -0.6 0.0 0.6 1.2 1.8

Dim 1

-2.0

-0.5

1.0

Dim

2

Cabrera

S = 0.131S08-734

S08-659

S08-581

S09-738

S09-653

S09-600

S11-593

S11-734

S11-655

S02-655

S02-593

S04-605

S04-726

S04-657

S06-730

S06-659

S06-601

-1.2 -0.6 0.0 0.6 1.2

Dim 1

-1.4

-0.8

-0.2

0.4

1.0

Dim

2

S = 0.221

Sóller

S08-734

S08-659

S08-581

S09-738

S09-653

S09-600

S11-593

S11-734

S11-655

S02-655

S02-593

S04-605

S04-726

S04-657

S06-730

S06-659

S06-601

-1.2 -0.6 0.0 0.6 1.2

Dim 1

-1.4

-0.8

-0.2

0.4

1.0

Dim

2

S = 0.221

Sóller

Fig. 4. MDS analyses performed for (a) small (CL < 34 mm) and (b) large (CL P 34 mm) A. antennatus off Cabrera and off Sóller. In haul codes C = Cabrera; S = Sóller; numbersbefore dashes are month, numbers after dashes are depth of haul. S is stress.

46 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

were mainly consumed. In fact only Natatolana borealis and Serges-tes articus, mainly consumed by A. antennatus off Cabrera, and Gen-nadas elegans, more significantly consumed off Sóller, showedcoincidence between their abundance in stomach contents and inthe environment. Some prey were not well sampled with our gear(sledges and WP2 net), the case of Sergia robusta with only twospecimens caught on all cruises.

The maximum size of some prey found in stomachs was higherthan that of specimens collected with the sledge-WP2. This wasthe case of Natatolana borealis, Meganyctiphanes norvegica, Sergestesarcticus and especially Sergia robusta, Pasiphaea multidentata andMyctophidae (main species found in guts: Lampanyctus crocodilus,Notoscopelus elongatus and Ceratoscopelus maderensis). This sug-gests net avoidance by large specimens of these prey consumedby Aristeus antennatus.

Between 16% and 23% (in number) of identified prey amongundigested mesopelagic prey (e.g., decapods, myctophids) musthave been eaten by A. antennatus before (0–1 h) sunrise and to 4 hafter sunrise Fig. 6. The occurrence of somewhat digested and verydigested prey at these periods indirectly indicated nocturnal feedingon these mesopelagic fauna by the red shrimp. The large proportionof myctophids eaten at midday, 8–10 h after sunrise (appearing inFig. 6) was based in a low number (n = 5) of ingested fish.

3.5. Trends in environmental variables

Temperature (T) 5 m above bottom, varied with depth and siteand ranged between 12.94 �C at 650 m to 13.47 �C at 150 m. On

average, close to the bottom, there was an increase in T of 0.2–0.3 �C from the shelf slope break (150 m) to 650–750 m on theslope. The seasonal pattern was determined by depth. On theshelf slope break (the level of Winter Intermediate Water,WIW) maximum T was recorded in February decreasing inApril–June to around 13 �C. This decrease was recorded earlieroff Sóller (April) than off Cabrera (Fig. 7a). Deeper at 550–750 m (a level including the lower depth distribution of Levan-tine Intermediate Water, LIW) there was a decrease of T fromNovember 2003 to April 2004 off Sóller, with a further sharp in-crease in June 2004, more obvious toward 550–650 m. Over thedeepest part of the slope (550–750 m), more regular conditionsof T through the year were recorded off Cabrera in comparisonto Sóller.

Salinity (S) 5 m above bottom ranged from 38.28 ppm at 150 m(November 2003) to 38.51 ppm at 350 m (June 2004). In general Sincreased from the shelf-slope break to bathyal depths to 550 m(Fig. 8), then slightly decreasing. The seasonal pattern was differentdepending on depth. S increased (above 38.4 psu) from February toApril–June at 350 m, and later (June) deeper (550–750 m). Maxi-mum S was regularly recorded in June 2004 both at 150 m andon the slope. However, at 150 m maximum values were also re-corded in November 2004. S was in general higher off Cabrera, ex-cept at 350 m depth where values were rather similar at both sites(Fig. 7). In general T and S values decreased with depth (excluding Sat between 150 and 350 m), especially off Cabrera below 550 m.Also both variables exhibited higher seasonal fluctuations of Sóllerthan off Cabrera (Fig. 7).

0.0

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<

>CL 40 mm

Fig. 5. Trends in the caloric content (in k cal/g WW) in the diet of Aristeusantennatus off Sóller (---------) and Cabrera ( ) as a function of size and annualperiod. CL = cephalotorax length (mm). Parts of this figure appeared previously inCartes et al. (2008).

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 47

3.6. Relationships between feeding/diet and biological/environmentalvariables

Relationships were treated separately for Cabrera and Sóller bymeans of univariante (Spearman r) and multivariate (MLR models)statistical methods. Off Cabrera, fullness (F) was positively corre-

Table 3Abundance (ind./100 m2) and depth ranges of main prey (in g wet weight, W/100 ind.) co

Prey-species Depth range m COG m

Sóller Cabrera

Boreomysis arctica Suprabenthos 335–760 699 682Natatolana borealis Suprabenthos 134–748 465 590Meganyctiphanes norvegica Zooplankton 363–752 713 692Euphausia krohni Zooplankton 150–753 569 599Nematoscelis megalops Zooplankton 156–760 661 657Sergestes arcticus Zooplankton 666–760 728 676Gennadas elegans Zooplankton 347–760 660 698Sergia robusta Micronekton 749 – 749Pasiphaea multidentata Micronekton 670–752 727 732Calocaris macandreae Infauna 365–752 613 715Myctophidae Micronekton 650–753 711 703

(n): number of specimens used to calculate size range. Suprabenthos/infauna collected

lated (non-parametric Spearman rank; p < 0.05) with T close tothe bottom for small and large shrimp (Table 4). Other variableswere correlated with F depending on shrimp size. Among smallshrimp, F was positively correlated with fluorescence and nega-tively with shrimp density (higher F with lower density). Amongmedium-sized shrimp, there were negative correlations betweenF and Chl a readings 2 months before sampling (Table 4). In addi-tion to the variables cited, depth was negatively correlated with Famong large shrimp.

Among small sizes off Sóller, F was positively correlated withChl a readings taken simultaneously and 1–2 months before, alsowith gonadosomatic index (GSI), and with shrimp biomass (Table4). Among mid-sized shrimp, only a negative r between F and Chla 1 month before was found, while no variable was correlated withF in large shrimp.

Regarding changes in the diet of A. antennatus (MDS dimen-sions: DIM1, DIM2), r was significant between DIM1, DIM2 and anumber of environmental variables, though these correlations var-ied depending on the area and size of shrimp (Table 4). Amongsmall (CL < 34 mm) shrimp, DM1 off Cabrera was significantly cor-related with fullness (F), depth and T close to the bottom, whereasDIM2 was only correlated with lipid content (n = 9; r = 0.717;p = 0.03). Among large (CL P 34 mm) shrimp, DIM1 of diet wascorrelated with F, depth and with T and S close to the bottom, with-out any significant r in DIM2.

Off Sóller the diet of small shrimp was significantly correlatedwith F, fluoresence and Chl a (1–2 months before) and also withdensity, while DIM2 was correlated with HSI (n = 12; r = �0.783;p = 0.003). Among large females, DIM1 was significantly correlatedwith F, with Chl a (1–2 months) and with the hepatosomatic (HSI)and Kn indexes, while DIM2 was related with depth (n = 17;r = �0.520; p = 0.03), mean S (n = 17; r = 0.576; p = 0.02), and thegonadosomatic index (GSI) (n = 11; r = �0.630; p = 0.007).

From MLR models, Chl a in surface waters off Cabrera taken 2months before sampling was the main explanatory variable of full-ness for small Aristeus antennatus (Table 5), together with shrimpsdensity and GSI. All these variables showed, however, significantnegative correlations. Salinity and mean size (W) explained full-ness for mid-size shrimp (positive r) as did depth (negative r) forlarge shrimp. Off Sóller higher fullness was found among smallshrimp with decreasing density, and with increasing surface Chla taken 2 moths before. Among mid-sized Aristeus, higher F camewith increasing depth and decreasing surface Chl a taken simulta-neously, whereas no variable significantly explained fullness forlarge specimens. The variance accumulated by MLR models rangedbetween r2 = 0.418 and 0.549.

In summary we found a higher dependence of fullness and dietwith T and S off Cabrera than off Sóller, and that is related to depth.

nsumed by Aristeus antennatus off Sóller and Cabrera

N ind./100 m2 W g/100 ind. Size (n) mm Guts

Sóller Cabrera Sóller Cabrera Water column

18.2 22.4 0.21 0.13 1.3–7.4(1025) 4.2–7.3(14)0.11 0.28 3.61 8.06 1.8–21.2(48) 4.0–24.5 (139)0.24 0.89 1.44 0.84 3.6–9.2(113) 3.2–10.6 (61)2.03 1.96 0.20 0.12 1.1–6.4(330) 4.8–5.3 (8)4.74 6.14 0.25 0.19 0.8–8.9 (693) 2.6–6.9 (8)0.06 0.21 0.20 0.77 3.4–11.1 (27) 5.9–12.9 (7)0.57 0.51 1.72 0.45 1.5–10.0(112) 9.9(1)– 0.08 2.43 1.32 6.3–9.3 (3) 6.6–18.5 (19)0.01 0.04 1.43 0.90 2.6–13.8(13) 5.0–18.0 (13)0.28 0.69 0.55 0.45 2.3–9.8 (57) 5.3–8.7(13)0.07 0.11 3.77 2.24 10.6–45.4(12) 15.0–52.6 (20)

with sledges, zooplankton/micronekton with WP2 nets.

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Fig. 6. Percentage undigested prey (by number) in gut contents of Aristeusantennatus in hauls performed around sunrise and to 10 h after sunrise. E1and E2 indicating two steps of undigested prey from fresh (E1) to slightlydigested (E2); numbers above bars indicate the total number of prey counted ineach period.

48 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

Depth was an important factor affecting diet off Cabrera (seetrends in MDS analyses), and in this area depth was in turn corre-lated with F among large females (higher fullness shallower:r = �0.571; p = 0.02; n = 16) and T (lower T deeper: r = �0.825;p = 2 � 10�5; n = 18). Off Sóller, where seasonal forces were moreimportant in shifting the diet, variables explaining changes in full-ness and diet were more strongly linked to temporal changes inwater column productivity (e.g., positive r with Chl a readingsand fluorescence) and with shrimp biology (GSI, HSI, and kn).

4. Discussion

Aristeus antennatus has the most diverse diet found amongdeep-sea megafauna in the Mediterranean (H0 = 5.58: Cartes,1994), based on the large variety of small benthic/suprabenthicand pelagic macrofauna and micronekton. Compared with otherdecapods and fish cohabiting with it, this is the species in whichbenthos (e.g., polychaetes, ophiuroids) contributes the most to itsdiet (Lagardère, 1971; Relini-Orsi and Wúrtz, 1977; Cartes,1994). However, when comparing diets over the slope off theCatalan coast with those around the Balearic Islands, euphausiids,

small meso-bathypelagic decapods and myctophids were moreimportant in the diet of the insular areas. Off the coasts ofCatalonia, benthic prey are particularly important around submar-ine canyon heads, where higher foregut fullness (more food con-sumption) was also recorded (Cartes, 1994; Fig. 8). Aristeusantennatus, therefore, can eat such a wide variety of taxa that itcan exploit prey of distinct ecological habitats depending on localavailability. Both around the Catalan canyons and the Balearic is-lands, micronekton (euphausiids and small decapods) marked theseasonal changes found in the diet of the red shrimp, to 1200 m(Cartes, 1994), which is the assumed boundary of distribution ofmesopelagic fauna (Goodyear et al., 1972; Stefanescu and Cartes,1992). Below this depth the influence of the mesopelagic assem-blages on the diet of A. antennatus and other demersal species islow (Cartes, 1998).

4.1. Spatio-temporal changes in the diet and prey availability:influence of environmental factors

Off the Balearic Islands dependence upon mesopelagic prey wasmore important off Sóller than off Cabrera. This must be associatedwith higher abundance of (meso)zooplankton off Sóller (Carteset al., 2008) that is linked in turn to higher occurrence of oceano-graphic frontal systems and eddy formation to north of Mallorca(López-Jurado et al., 2008). Some differences between Sóller andCabrera in the sources of food for suprabenthos (prey of small A.antennatus) were evidenced based on the isotopic composition ofsuprabenthos (Fanelli, 2007; Madurell et al., 2008). Correlationsbetween d13C and d15N of suprabenthos increased form Februaryto June 2004 off Sóller, pointing to exploitation of a unique foodsource after the main peak of primary production in surface occur-ring in February–March (Cartes et al., 2008). Off Cabrera, by con-trast, d13C vs. d15N did not follow the same pattern, d13C–d15Ncorrelations were lower than those recorded off Sóller and thehighest d13C–d15N correlation were found in September–November2003 (Fanelli, 2007). This dependence upon mesopelagic preyseems consistent with a longer duration for Chl a peaks (an indirectindicator of surface production) off Sóller in comparison to Cabrera,which may probably favor higher coupling between primary pro-duction and zooplankton/suprabenthos in this area. Finally, a par-allel increase in %OM (total organic matter) in sediments wasfound in April–June 2004, also higher off Sóller (Cartes et al.,2008). All these factors explain the significant correlations foundin MLR models between fullness/diet vs. Chl a in this area.

Oceanographic differences between Cabrera and Sóller includeda higher flux and thickness of Levantine Intermediate Water (LIWwith salinity > 38.45 psu) off Sóller at depths of 300 to 500 m(López-Jurado et al., 2008) and of Winter Intermediate Water(WIW with temperature 613 �C) distributed above LIW between�150–350 m. WIW is formed during winter to the north of BalearicIslands, in the Gulf of Lyons (Pinot et al., 2002). Winter water hasbeen recently linked to cascading events generated in the Gulf ofLyons (Palanques et al., 2006), by which submarine canyons actsnot only as channels for discharges of short-torrential rivers foundalong the coasts of Catalonia but for water masses down the slope.As a consequence, both LIW and WIW flow was particularly strongto the north of Balearic Islands (Sóller) in late winter–spring(López-Jurado et al., 2008), both increasing from February to Apriland especially in June. These water masses can carry nutrientsfrom most productive areas in the Gulf of Lyons, enhancing phyto-plankton and zooplankton production. LIW was also present offCabrera, and maximum influx (September–November 2003:López-Jurado et al., 2008) again coincided with maximum changesin the isotopic signal of suprabenthos there (Fanelli, 2007), henceprobably inducing changes in trophic web dynamics. Water massesconditions (T and S) showed higher variability at shallower (150–

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Fig. 7. Temperature (T) and salinity (S) of the water close to the bottom (5 m above bottom) at the three depth ranges studied off Sóller (—–s—–) and Cabrera (—-�—-). At150–350 m (a) and at 550–750 m (b). In general both T and S decreased with depth at 550–750 m, therefore, lines at the top of plots represent the shallowest depth sampled,and at the bottom the deepest. Redrawn from Cartes et al. (2008).

0

0.02

0.04

Mar AprJu

lDec

F

La BerengueraCanyon (450 m)

600-650 m

Mar AprJu

lDec

F

La BerengueraCanyon (450 m)

600-650 m

Fig. 8. Temporal changes of fullness (F ± CI 95%) in A. antennatus off the Catalancoasts close to Barcelona during 1991 (April/December samples) � 1992 (March/July) at two stations situated in a submarine canyon (average depth, 450 m) and at600–650 m on the slope. Each point is the mean fullness calculated for >30individuals/haul.

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 49

350 m) than at deeper (650–750 m) depths. Variability was higheroff Sóller and the strongest decrease of T found at 150 m occurredearlier (in April) there than off Cabrera (see Fig. 7a). As mainchanges in stomach fullness and diet of A. antennatus occurredfrom February to April 2004, possible influence of oceanographicprocesses in the trophodynamics of red shrimp seems more likelylinked to flow of surficial water masses (WIW) than to deep waters(LIW). Off Sóller the COG of females was shallower than off Cabre-ra, closer to a possible influence of water masses flow coincidingwith the period (April–June) of WIW and LIW occurrence in thearea (López-Jurado et al., 2008). Deep mesopelagic prey consumedby A. antennatus (on average distributed > 400 m depth: see below)

must trophically exploit zooplankton distributed at shallowerdepths (150–350 m) by means of daily migratory movements. Inany case, both WIW and LIW are found above the daylight distribu-tion of A. antennatus (550–750 m) on the Balearic slope, so hypo-thetical upward nocturnal migration by A. antennatus (discussedbelow and suggested by Cartes et al., 1993 off Catalan canyons)in search of prey could also explain a spatial coincidence betweenthe distribution of A. antennatus and zooplankton associated withthe seasonal influx of LIW and WIW.

Aristeus antennatus preferently consumed micronektonic prey(e.g., Myctophidae, Sergia robusta, Meganyctiphanes norvegica. . .)off Sóller. However, most of these species were more abundantin WP2 samplings off Cabrera. This lack of correlation betweenprey in guts and in the environment could be explained by (i) A.antennatus and their prey were not distributed at the same depthrange at the time of samplings (performed in daylight); (ii) possiblenet avoidance by micronekton. Feeding rhythms have been re-ported in A. antennatus, consisting of a higher consumption of prey,mainly suprabenthos, at night (Cartes, 1993b; Maynou and Cartes,1997). Off the Balearic Islands Aristeus antennatus could also preyon micronekton in synchrony with day–night movements of thisfauna. Only 3 of the 98 species identified in gut contents of A.antennatus (two mysids: Boreomysis megalops, Lophogaster typicusand one amphipod, Hippomedon massiliensis) showed a shallowerdistribution than that of the red shrimp during daytime (unpub-lished data), and only one (L. typicus) was a relatively importantprey. However, most mesopelagic prey had a shallower maximumpeak of abundance in the environment than in the depth intervalwhere A. antennatus were caught. Thus, M. norvegica showed aver-age weighted mean depths (abundance peaks) at 440–500 m in theNW Mediterranean (Sardou et al., 1996; Cartes, 1998), whereas wesampled offshore, over bottoms of 576–752 m. Myctophids proba-bly followed a similar pattern. Because most mesopelagic species

Table 4Relationships (Spearman rank correlation: r) between stomach fullness (F) and first dietary dimension (DIM1) of Aristeus antennatus and environmental/biological variables

F Cabrera Sóller

Small Medium Large Small Medium Large

n r P n r P n r P n r P n r P n r P

Depth 18 �0.401 ns 18 �0.402 ns 16 �0.571 0.021 17 0.456 ns 17 0.142 ns 17 0.446 nsT 17 0.495 0.043 17 0.455 ns 15 0.670 0.006 18 �0.147 ns 18 �0.022 ns 17 �0.412 nsS 17 0.233 ns 17 0.104 ns 15 0.488 ns 18 �0.285 ns 18 0.116 ns 17 �0.409 nsOM(%) 11 �0.455 ns 11 �0.627 0.039 11 �0.373 ns 11 0.167 ns 11 0.257 ns 10 0.042 ns% Mud 10 �0.297 ns 10 �0.624 ns 10 �0.467 ns 11 0.539 ns 11 �0.021 ns 10 �0.297 nsRedox 11 �0.627 0.039 11 �0.700 0.016 11 �0.818 0.002 10 0.239 ns 10 �0.453 ns 9 �0.250 nsDepth fluorescence 7 0.546 ns 7 0.400 ns 7 0.036 ns 10 �0.313 ns 10 0.485 ns 5 0.462 nsFluorescence 7 0.764 0.046 7 0.691 ns 7 0.327 ns 10 �0.129 ns 10 0.541 ns 5 0.564 nsChl a (2 months) 18 �0.384 ns 18 �0.489 0.040 16 0.217 ns 6 �0.905 0.013 6 0.000 ns 16 0.244 nsChl a (1 month) 18 �0.271 ns 18 �0.393 ns 16 0.160 ns 17 0.850 0.00002 17 �0.543 0.024 16 0.339 nsChl a sim 18 �0.086 ns 18 �0.148 ns 16 0.171 ns 17 0.762 0.0004 17 �0.241 ns 16 0.373 nsGSI 17 �0.319 ns 17 �0.270 ns 16 �0.168 ns 17 0.750 0.001 17 0.170 ns 17 �0.025 nsHSI 12 0.007 ns 12 �0.175 ns 11 0.245 ns 18 0.129 ns 17 �0.459 ns 11 0.309 nsKn 18 �0.059 ns 18 �0.096 ns 14 0.389 ns 18 �0.084 ns 18 0.028 ns 17 0.456 nsLipids 9 0.200 ns 13 �0.516 ns 9 0.017 ns 9 �0.350 ns 13 0.582 0.037 13 0.148 nsD (ind./km2) 18 �0.558 0.016 18 �0.218 ns 16 �0.347 ns 12 0.345 ns 18 0.370 ns 17 �0.130 nsB (gl/k m�2) 18 �0.515 0.029 18 �0.218 ns 16 �0.347 ns 11 0.717 0.013 18 0.295 ns 17 �0.100 ns

DIM1 Small Large

Cabrera Sóller Cabrera Sóller

n r P n r P n r P n r P

F 18 �0.515 0.029 18 0.480 0.044 16 �0.535 0.033 17 0.686 0.002Depth 18 0.661 0.003 18 0.125 ns 18 0.669 0.002 17 0.074 nsT 17 �0.514 0.035 18 �0.238 ns 17 �0.573 0.016 17 �0.086 nsS 17 �0.320 ns 18 �0.418 ns 17 �0.520 0.032 17 �0.230 nsOM(%) 11 0.291 ns 10 0.176 ns 11 0.309 ns 10 0.455 ns% mud 10 0.455 ns 10 �0.103 ns 10 0.467 ns 10 0.055 nsRedox 11 0.536 ns 9 0.467 ns 11 0.582 ns 9 0.517 nsDepth fluorescence 7 �0.600 ns 6 0.618 ns 7 �0.655 ns 5 0.821 NsFluorescence 7 �0.709 ns 6 0.971 0.001 7 �0.655 ns 5 0.718 NsChl a (2 months) 18 0.068 ns 17 0.585 0.014 18 �0.318 ns 16 0.602 0.014Chl a (1 month) 18 0.085 ns 17 0.566 0.018 18 �0.114 ns 16 0.595 0.015Chl a sim 18 0.211 ns 17 0.341 ns 18 0.220 ns 16 0.324 nsGSI 17 0.027 ns 18 0.273 ns 16 �0.235 ns 17 0.147 nsHSI 12 �0.182 ns 12 0.301 ns 11 �0.336 ns 13 0.808 0.0008Kn 18 0.344 ns 18 0.294 ns 14 �0.213 ns 17 0.608 0.010Lipids 9 0.050 ns 9 0.533 ns 10 �0.248 ns 13 0.451 nsD (ind./k m�2) 18 0.141 ns 18 �0.496 0.036 18 0.253 ns 17 �0.216 nsB (gl/k m�2) 18 0.148 ns 18 �0.350 ns 18 0.358 ns 17 �0.380 ns

Table 5MLR models deduced for stomach fullness (F) of Aristeus antenntus as a function of environmental/biological explanatory variables

n r2 Var. B p-level T

SmallMLR1 Cabrera 17 0.508 Int 2.5E-04

Chl a (2 months) �0.0147 0.018 0.85D �0.0008 0.033 0.96GSI �0.0808 0.038 0.82

MLR2 Sóller 18 0.647 Int 3.1E-04D �0.0005 0.018 1.00Chl a (2 months) 0.0078 0.046 1.00

MediumMLR1 Cabrera 12 0.546 Int 0.022

S 3.420 0.022 0.67W 0.041 0.031 0.62

MLR2 Sóller 17 0.325 Int 0.337Chl a (2 months) 0.023 0.047 0.63

LargeMLR1 Cabrera 16 0.375 Int 0.012

Depth �0.013 0.021 1.00MLR2 Sóller 17 0.374 Int 0.069

Kn 0.037 0.018 0.98

Models built for 3 size categories (small, medium, and large) and for the two areas (Sóller, Cabrera) separately. GSI: gonoadosomatic-index; Kn: condition index; D: density;W: mean size (B/D). n: number of cases; r2: explained variance; int: intersect; B: beta coefficient.; T: tolerance (inverse to redundancy among explanatory variables).

50 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

often show a bigger-deeper size-with-depth relation (e.g., deca-pods: Hargreaves et al., 1984; fish: Stefanescu and Cartes, 1992)

small specimens found in guts of A. antennatus (TL between 2.2and 4.8 cm) may have a shallower, more inshore distribution than

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 51

specimens of TL > 5–6 cm, which in the case of Lampanyctuscrocodilus are distributed over depths of 550–750 m (Stefanescuand Cartes, 1992). Other prey, by contrast, had similar depth distri-butions to that A. antennatus, as was the case of Gennadas eleganswith maximum concentrations at 660–698 m and higher con-sumption and abundance off Sóller. Net avoidance must be size-dependent (i.e. only smaller individuals of prey species are caughtwith the 1 m2 WP2), and most mesopelagic species (e.g., M. norveg-ica, Sergestidae and Pasiphaeidae) found in gut contents were lar-ger than specimens collected with nets. Therefore, it is possiblethat the lack of coincidence between prey found in stomach con-tents of A. antennatus and their distribution in the environmentcould be caused by a shallower distribution of prey sizes consumedby the red shrimp during daylight when plankton sampling wasperformed.

Off the Catalan coasts, it has been suggested that A. antennatusmigrates upward and inshore at night (Cartes et al., 1993). Thesemigrations would take place preferentially through canyon valleys,especially among small shrimp and, suggested by the higher stom-ach fullness found within canyons (Cartes, 1994; Fig. 8). It is wellknown the role of canyons enhancing secondary production espe-cially at canyon heads (Vetter and Dayton, 1998) even favouringrecruitment success of demersal species (e.g. Vetter and Dayton,1999). Hence, upward nocturnal movements by A. antennatuswould be done to feed in more productive depths. A. antennatusis caught by trawling at night at only 100–150 m off Calabriancoasts (Matarresse et al., 1995). Off the Balearic Islands, thesemigrations could point to the capture of mesopelagic prey, coincid-ing with upward-inshore migrations at night by mesopelagic faunaas evidenced by Reid et al. (1991) off Hawaii. An important propor-tion of undigested mesopelagic prey (e.g., decapods, myctophids)were mainly found in guts of A. antennatus before/close to sunrise,and the occurrence at sunrise of digested decapods, euphausiidsand myctophids suggests feeding (previous to our sampling) onthese same prey at night. However, these migratory movementsby A. antennatus which are probably in search of food are only sup-ported by indirect evidence and remain hypothetical.

4.2. Interactions between trophic requirements and the reproductivecycle

Higher consumption of mesopelagic prey with a large energeticcontent occurred off Sóller and this might favour conditions forreproduction in the red shrimp. Rosa and Nunes (2003b) evidencedhigher lipid, and probably energy content in muscle of Aristeusantennatus females in May–June off Portuguesse coasts. At mid-slope depths interactions between food availability and trophicrequirements may only influence the reproductive cycling of A.antennatus, and not recruitment, because early juveniles(CL < 14 mm) are practically restricted to depths below 1400 m(Cartes and Demestre, 2003). A common trend found in both areaswas a sharp increase in stomach fullness during April–June 2004,after a decrease from November 2003 to February 2004. This trendwas more evident off Sóller, where diet was based on mesopelagicprey with a higher energy content also in April–June 2004. Thiscould have led to the significant increase of the GSI (fecundity) ob-served off Sóller in June and higher density of small females of A.antennatus (Guijarro et al., 2008; Fig. 9). In addition, HSI, lipids inhepatopancreas and Kn among females were higher off Sóller fromFebruary to April–June 2003 (Guijarro et al., 2008; Fig. 8), previousto and simultaneously with the period of gonad development. A lastconsequence was the occurrence of smaller mature females off Sól-ler (24.9–26.5 mm CL contrasting to 27.3–29.8 CL off Cabrera) inthis same period. Most individuals attain their first gonad develop-ment in May off the Catalan coasts, when the previtellogenesisphase begins (Demestre and Fortuño, 1992). However, in the NW

Mediterranean variability in the onset and the duration of thereproductive cycle has been recorded between years (Carbonellet al., 2006), which was attributable to environmental (maybe food)variability. The phase of rapid oocyte growth must be incur highmetabolic costs. At the end of the reproductive period (Augustand September), and coinciding with a decrease in the caloric con-tent of the diet, GSI for females was similar both off Sóller and Cab-rera, while Kn, HSI and the percentage of lipids from thehepatopancreas reached minimum values, indicating that the or-ganic reserves stored in the hepatopancreas are used for ovariandevelopment in the later part of the spawning period (Guijarroet al., 2008). The beginning of gonad development occurs twomonths after the peak of primary production in surface layers(February–March: Cartes et al., 2008). In this way, off Sóller, wefound a positive relationship (in small shrimp) between fullness/diet and temporal changes in water column productivity (e.g., Chla readings taken two months before sampling and fluorescence).

Control of populations among abyssal detritivorous fauna mustbe coupled with quality of organic matter arriving at the bottomand to the ability of benthic fauna for selective feeding (Gingeret al., 2001; Witbaard et al., 2001). The link between reproductivestrategy and temporal variations in food availability have been dis-cussed for bathyal species, and synchrony between the release ofjuveniles in peracarids and maximum food availability derivingfrom spring phytoplankton blooms has been suggested for instanceamong peracarids (Cartes et al., 2002; Richoux et al., 2004). Com-parison of species with continuous and non-continuous reproduc-tion is particularly interesting. It has been suggested that shifts inthe food consumption of some slope dwelling fishes are strongeramong fishes with peaks of gonad development (Madurell andCartes, 2005), and during pre-reproductive periods these speciesbase their diet on the consumption of mesopelagic prey. At abyssaland at bathyal depths, macrofauna and detritivorous megabenthoscouple their biological cycles with phytodetritus deposition(Hudson et al., 2004; Richoux et al., 2004). In the case of holothu-rians, the biological cycle types (continuous, synchronous) are re-lated with changes in the food ingested, deduced by changes inthe amount of fatty acid biomarkers (Hudson et al., 2004) depos-ited under conditions before and after the spring phytoplanktonblooms at the surface. We suggest, in the case of the deep shrimpAristeus antennatus, that a highly energetic diet provided by highprey availability can stimulate fecundity and/or allow an earliermaturity. A similar trend has been found comparing the energy in-take and the reproductive cycle of pandalids off the Balearic Islands(Fanelli and Cartes, 2008).

In general, energy reserves (e.g., lipids) strongly affect fecundityand reproduction among fish (e.g., Lloret et al., 2005; Adams,1999), and also in deep water decapods (Rosa and Nunes,2003b). The storage of lipids in the hepatopancreas of A. antennatusbegins before reproduction (Fig. 9), and storage must in turn be en-hanced by a more energetic diet. Aggregation of micronektonic, pe-lagic prey in particular areas, hotspots (e.g., canyons, slope breaks)for zooplankton biomass (Genin, 2004), as likely occurs over thesteep slope off Sóller, can in turn favour aggregation of predatorsfor feeding. In the case of A. antennatus we hypothesize that pre-reproductive females may search for areas with accumulations ofhighly energetic prey.

Reproductive aggregations of the red shrimp have been sug-gested to occur around submarine canyons off the Cataloniancoasts (Sardà et al., 1994). Secondary production of macrofauna lo-cally increases at canyon heads (Vetter and Dayton, 1998). InCatalan canyons, there was also an increase of gut fullness in A.antennatus females in March–April (Fig. 8: Cartes et al., 2006), priorto the beginning of the reproductive period (May: Demestre, 1995).In a pattern that is different from that observed in the BalearicIslands, the increase of fullness off the Catalonian coast was not

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Fig. 9. GSI (left), and Kn , HIS and % lipids (right) of Aristeus antennatus as a function of time off Sóller ( (---------); sh) and Cabrera (( ); �). Individual data was consideredfor GSI, mean monthly data for Kn , HIS and % lipids. Plots of Kn , HIS and % lipids re-drawn by Guijarro et al. (2008). GSI was significantly higher in Soller in June 2004 (MannWithney test, p < 0.05) Part of this figure revised from a published figure in Guijarro et al. (2008).

52 J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54

synchronized with a higher consumption of mesopelagic prey, butwith higher consumption of benthic prey (e.g., large polychaetesand especially the macruran Calocaris macandreae) that are moreabundant in canyons in that area (Cartes, 1994). Calocaris macan-dreae is a key prey in trophic webs around submarine canyons,and some of their potential predators (e.g., Trachyrhynchus scabrusin the insular part of the Balearic Basin: Stefanescu et al., 1993),can decrease or even disappear coinciding with its absence. Thiseven induces local differences in assemblage composition and spe-

cies distribution between mainland and insular areas (Stefanescu,1991; Cartes et al., 2004).

Local differences in the source of energy exploited by A. antenn-atus in pre-reproductive periods should also be considered forlong-term fluctuations of red shrimp populations. Based on resultsfrom the Balearic Islands (Cartes et al., 2008), it has been suggestedthat landings of A. antennatus increase off the Catalan coasts (amainland area) in years of higher secondary production by zoo-plankton ‘blooms’, which are in turn correlated with years of posi-

J.E. Cartes et al. / Progress in Oceanography 79 (2008) 37–54 53

tive NAO (North Atlantic oscillation) index, (Maynou, 2008). How-ever, patterns are different around the Balearic Islands and in Cata-lonian canyons. While zooplankton is important in the diet of pre-reproductive A. antennatus females in the insular area, the benthicpathway covers the energetic requirements of red shrimps in themainland area.

4.3. Conclusions

The increase of food consumption by A. antennatus in pre-repro-ductive periods can derive from different prey, depending onchanges in local prey availability. Around the island of Mallorcathe expected impoverishment of benthic biomass in comparisonto canyon heads off the mainland area of the Catalan coasts ledto enhanced consumption of micronektonic prey and possibly toaccumulation of pre-reproductive females of A. antennatus in areas(e.g., steep slopes, persistent frontal systems) likely to be home todense zooplankton aggregations (Genin, 2004). The occurrence ofzooplankton/micronekton in stomach contents of deep-sea fishand decapods has been widely documented (e.g., Mauchline andGordon, 1991; Cartes, 1993a,b). Also, coupling between reproduc-tive processes and inputs of organic matter originating in surfacewaters has been documented for deep-sea detritivorous mega-fauna (Hudson et al., 2004). However, in the case of the deep-seashrimp Aristeus antennatus, we found a strong link in a predatorat a high trophic level between pelagic resources and reproductiveprocesses. This suggests, together to some other similar cases(Fanelli and Cartes, 2008), a rapid link via mesopelagic fauna be-tween surface primary production and gonad development thatis available to much of the megabenthic, bathyal community.

Acknowledgements

The authors thank to all participants in the F/V Moralti Noucrews and to López Jurado (IEO) who provided some oceanographicdata and conducted oceanographic surveys. We especially thankthe help of Drs. Joan Moranta and E. Massutı́, the last main re-searcher of IDEA project.

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