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Gelatinous Plankton As a Source of Food for Anchovies

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Gelatinous Plankton As a Source of Food for Anchovies Hydrobiologia 451: 45–53, 2001. 45 © 2001 Kluwer Academic Publishers. Printed in the Netherlands. Feeding on survival-food: gelatinous plankton as a source of food for anchovies H. Mianzan1,2,M.Pajaro´ 2, G. Alvarez Colombo2 & A. Madirolas2 1CONICET; 2INIDEP; P.O. Box 175, 7600 Mar del Plata, Argentina E-mail: [email protected] Key words: Engraulis anchoita, gut contents, predation, Iasis zonaria, acoustics, south-western Atlantic Ocean Abstract The gelatinous zooplankton, composed by members of different phyla (Cnidaria, Ctenophora, Tunicata), are usu- ally neglected in most studies about energy transfer in the marine trophic web, and often it is assumed that such soft-bodied fauna are trophic ‘dead ends’ in the food webs. In recent years, however, it has been shown that many fish species feed extensively on gelatinous zooplankton, while other species may feed on them occasionally when other food is scarce. We found that anchovies, Engraulis anchoita Hubbs & Marini, 1935, shoaled close to the Río de la Plata surface salinity front, where dense aggregations of the salp, Iasis zonaria (Pallas, 1774), were detected acoustically in May, 1994. Densities of non-gelatinous zooplankton were low at this interface, and anchovies fed on the salps. In this paper, we describe the environmental and biological conditions that led a normally planktivorous filter feeder E. anchoita to prey on gelatinous plankton. Introduction reasons why those fish species should accept gelatin- ous organisms as food are not clearly understood, but The gelatinous zooplankton, composed by members of it is hypothesized that this happens when nothing bet- different phyla (Cnidaria, Ctenophora, Tunicata), are ter is available to fill fish stomachs. Kashkina (1986) usually neglected in most of the studies about energy described this behaviour as feeding on survival food. transfer in marine trophic webs, principally because To test this hypothesis, a multidisciplinary invest- these animals are usually damaged beyond recogni- igation that included acoustical monitoring, plankton tion when sampled with conventional plankton nets. net sampling and analysis of fish stomach contents As a consequence, their distribution and abundance was performed in order to obtain a synoptic picture. patterns are poorly known. Furthermore, even though In this paper, we describe the environmental and bio- many papers have focused on their role as consumers logical conditions that led a normally planktivorous (Alvariño, 1985; Madin & Kremer, 1995; Madin et al., filter feeder (Engraulis anchoita) to prey on gelatinous 1997; Purcell, 1997), there are relatively few reports plankton. that document the predators of gelatinous zooplankton (Purcell, 1991). These discrepancies have fostered a belief that such soft-bodied fauna are trophic ‘dead Materials and methods ends’ in marine food webs. This leads to the assump- tion that some jelly species that can reach enormous Day and night sampling was conducted on the Argen- biomass merely die, sink and decompose. tine Continental shelf (Fig. 1), with the R/V Eduardo In recent years, it has been shown that many fishes Holmberg (INIDEP) from 15th to 28th May, 1994, fo- feed on gelatinous zooplankton (Ates, 1988; Arai, cused on acoustical estimation of Engraulis anchoita 1988; Mianzan et al., 1996; Mianzan et al., 1997; Pur- biomass. Zooplankton was sampled using a CalVET cell & Arai, 2001). Although some fish species may net (200 µm), 25 cm diameter. Sixty five plankton depend heavily and be specialized to feed on gelatin- stations were performed from Río de la Plata up to the ous species, others utilize them only occasionally. The slope front (Fig. 1). The net was towed vertically from 46 Figure 1. Cruise design: CTD (conductivity-temperature-depth profiler) and plankton (CalVET net) stations (), fishing stations (Nichimo Midwater trawl) () and acoustic sampling (solid line) along parallel transects (SIMRAD EK500 echosounder operating at 38 kHz), performed during Autum, 1994 by the R/V Dr E. Holmberg (INIDEP). the bottom to the surface or from 70 m up the sur- processed to achieve a one-meter vertical resolution. face. The average volume of water filtered was 1.4 m3 Salinity data are reported with a precision of 0.05. (range 0.4–3.2 m3). Standing stocks were estimated Nineteen fishing stations (Fig. 1) were sampled by converting wet weight (ww) or number of indi- with a Nichimo midwater trawl, with an inner mesh viduals to dry weight (dw) and then to organic carbon of 10 mm at the cod end. One hundred and twenty using conversion factors (Omori, 1969; Madin et al., anchovies were sub-sampled from ten stations for 1981; Larson, 1986; Fernandez Araoz, 1994). Results analyses. Length and weight of each specimen was are expressed as mg carbon m−3. Conductivity and recorded. Gut contents were identified from preserved temperature were measured with a SeaBird 19 CTD collected specimens either macroscopically or using a at a sampling rate of 2 scans per second. Data were dissecting microscope (Wild M8). Salps were recog- 47 nized by their muscle bands and stomachs or by the range: 0–3406) and 112 cladocerans m−3 (stand- whole body of the animal. Salps were identified ac- ard deviation: 338.3; range: 0–2291). Many other cording to Esnal (1981) and Esnal & Daponte (1999). taxa were collected: chaetognaths, appendicularians, Each stomach was weighed with and without the stom- meroplankton including bivalve, decapod and poly- ach content in order to determine the weight of the chaete larvae, ichthyoplankton (Engraulis anchoita ingested prey, expressed as the difference between eggs and larvae), ctenophores (Mnemiopsis sp. L. both weights. The ‘Stomach Repletion Index’ (SRI) Agassiz, 1860), and hydromedusae (Liriope tetra- was calculated following the scale proposed by Ange- phylla (Chamisso & Eysenhardt, 1821) and Turritop- lescu (1982). This index indicates the state of satiety sis nutricola McCradyi, 1859). Copepod and clado- from 1 (an empty stomach: <0.5% of the anchovy ceran biomasses reached maxima of 3.8 and 4.4 mg weight) to 4 (full stomach: >6% of the anchovy Cm−3, respectively. These maximum values were weight). found along the surface salinity front. However, less Acoustic sampling was performed along parallel than 30% of the samples showed values higher than transects (Fig. 1). A Simrad EK500 echosounder op- 1mgCm−3. Of the rest, most of 40% showed values erating with a 38 kHz split-beam transducer was em- less than 0.1 mg C m−3. When present, salps (Iasis ployed. The processing method was echo-integration zonaria) largely dominated zooplankton biomass with (Forbes & Nakken, 1972). The averaging interval was aggregations up to 277 mg C m−3, several orders 1 nm. Echograms as well as integrated area scattering of magnitude greater than non-gelatinous zooplankton coefficient values (sa, in units of m2 nm−2), were re- biomass. Except for the stations at which salps were corded with a color printer. Nine surface-referenced abundant, the biomass of total zooplankton was very layers starting at 3 m from the transducer face, i.e. low during the survey (Fig. 3). 6.5 m below sea surface, were programmed. The echo- Stomach contents of anchovies reflected what was sounder was calibrated during the cruise, according observed in plankton samples. Fifty five percent of the to the centered sphere method with standard targets stomachs studied were empty or with very little iden- (Foote et al., 1987). Echograms were analyzed in or- tifiable food. No regurgitated material was observed. der to determine the sa fraction corresponding to the Stomach contents of the rest (45%) included a few concentrations of salps. copepods (calanoids and harpacticoids, 22.5%), clado- cerans(2.5%), appendicularians (2%), anchovy eggs (2%) and salps (oozooids and blastozooids, 11.7%). Results Almost 90% of the stomachs analyzed showed SRI values of 1–2 (corresponding to up to 1% of the The surface salinity contour of the Río de la Plata body weight), implying very little or no food in them showed a typical autumn NNE drainage, parallel to (Fig. 4A). Salps were found in the remaining 11.7% the Uruguayan coast as a low salinity wedge 30–35 of the stomachs reaching the maximum SRI values nautical miles off the coastline (Fig. 2). The central found (SRI= 3) (corresponding to up to 6% of the body and southern sections of the water column were highly weight) (Fig. 4B). More than 50 specimens of salps stratified. The central section had more than 200 km of (mostly aggregated zooids: Fig. 5B) were found in estuarine surface waters. The southern one was shorter one anchovy stomach. In one single haul, 40% of the and the stratified region occupied a small portion, up to specimens analyzed showed salps in their stomachs 60 km in length. Here, vertically homogeneous waters (Fig. 5), the rest being empty. were observed at the outer sector of the section. The At the working frequency (38 kHz, widely used northern section was weakly stratified due to a Con- for fish biomass estimations) large planktonic aggreg- tinental shelf marine waters intrusion lying over the ations were detected, some of them covering areas of coast. more than 1000 square nautical miles between tran- Mesozooplankton was dominated by copepods sects. Vertical profiles of the echotraces showed dif- (Acartia tonsa Dana, 1848, Paracalanus parvus ferences along the acoustic transects, either occupying (Claus, 1863), Labidocera fluviatilis F. Dahl, 1894, most part of the water column or forming well-defined Corycaeus sp. Dana, 1849, Euterpina acutifrons scattering layers with marked diurnal migrations. Ag- (Dana, 1852)) and cladocerans (Evadne sp. Lovén, gregations of zooplankton were often close to anchovy 1836, Podon sp. Lilljeborg, 1853), with mean densit- shoals. The highest numbers of salps observed in ies of 466 copepods m−3 (standard deviation: 710.5; plankton samples, fishing mid-water trawls and stom- 48 Figure 2. Surface salinity contours in the R´ıo de la Plata area.
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