Appendicularians: an important food supply for the Argentine anchovy Engraulis anchoita in coastal waters

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1 J. Appl. Ichthyol. 21 (200), 1 1 Ó 200 Blackwell Verlag, Berlin ISSN 01 Received: May 1, 200 Accepted: December 22, 200 Appendicularians: an important food supply for the Argentine anchovy Engraulis anchoita in coastal waters By F. L. Capitanio 1,M.Pa jaro 2 and G. B. Esnal 1 1 CONICET, Departamento de Ciencias Biolo gicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires; 2 Instituto Nacional de Investigacio n y Desarrollo Pesquero (INIDEP), Mar del Plata, Argentina Summary The stomach contents of 2 adult specimens of the Argentine anchovy, Engraulis anchoita, caught in coastal waters of the Argentine Sea from 1 to 1, were analyzed. Larger amounts of food were found in the stomachs of anchovies collected in the northern surveys ( 0 S), with the highest values attained in 1. Main diet items were copepods, appendicularians, cladocerans, fish eggs, and pteropods. Anchovies caught in the southern surveys (0 S) ingested less food, whereby the main items were copepods and appendicularians. Plankton samples collected simultaneously with the fishing trawls were also analyzed. Except for Fritillaria borealis, which occurred only in plankton samples, the same appendicularian species (Oikopleura dioica and O. fusiformis) were found in both stomach contents and in plankton samples. The Ivlev selectivity index calculated for O. dioica and O. fusiformis and for the different maturity stages of both species were in all cases 0, supporting the hypothesis of a non-selective feeding. Introduction In the last decades researchers have increasingly studied appendicularians because they are among the few metazoans capable of efficiently filtering picoplankton and nanoplanktonsize particles and even colloidal materials (Flood et al., 12; Hopcroft et al., 1). This ability, in combination with high grazing rates (Paffenho fer, 1, 1; Alldredge, 1a, 11), indicates that appendicularians may exert significant grazing pressures on the pelagic environment. The significant contribution of small phytoplankton (< lm) to total primary production and the grazing of these small cells by microphages (e.g. ciliates, appendicularians, marine cladocerans, and cyclopoid copepods) suggests that this fraction of primary production may be partially transferred to fish larvae through the microbial food web. This pathway may be as important as the traditional herbivorous food web: spring diatom bloom fi herbivorous calanoid copepods fi fish (Mousseau et al., 1; Ramírez and Sabatini, 2000; Sabatini et al., 2000; Pomeroy, 2001), and appendicularians might play an important role in this transfer of energy. Several fish species and larvae from the North Atlantic and Pacific oceans such as sole, sprat, flounder, salmon, and herring, frequently consume appendicularians in coastal areas (Davis, 1; Balanov et al., 1; Huse and Toresen, 1; Mochioka and Iwamizu, 1; Tadokoro et al., 1; Davis et al., 1; Grover, 1; Woehrling and Le Fe` vre-lehoërff, 1). In the Argentine Sea (SW Atlantic Ocean), the overall ichthyoplankton composition of the continental shelf ( S) is dominated by the South-west Atlantic anchovy (Engraulis anchoita Hubbs & Marini 1). This anchovy is the forage species of several commercially exploited fish stocks such as hake, Merluccius hubbsi (Sa nchez and Ciechomski, 1; Hansen et al., 1, 2001). At least two reproductive populations inhabit the study area in spring and summer; one is located north of 1 S, whereas the other thrives in the Patagonian region from 1 to S (Hansen et al., 1). The study by Capitanio et al. (1) on material collected during two cruises carried out in the Argentine Sea is the first to report predation of appendicularians by the anchovy, E. anchoita. These organisms have not been mentioned in previous works on the diet of this fish (Angelescu, 12). Capitanio et al. (1) found only mature specimens of Oikopleura dioica in the stomachs of E. anchoita, whereas in simultaneously taken plankton samples only 0% of the animals were mature (the remaining 0% included both immature and intermediate stages). We assumed that anchovies filtered breeding aggregations of mature ÔhouselessÕ appendicularians grouped near surface waters to spawn. Appendicularians build and live within a small balloon of mucus called a ÔhouseÕ equipped with filters for feeding. When these animals reach sexual maturity, they abandon their houses and swim freely prior to spawning. The present research reports new observations on the feeding behavior of E. anchoita, also introducing the hypothesis of a non-selective ingestion strategy. The importance of appendicularians in the diet of the anchovy during the spawning season is herein confirmed on the basis of a -year sampling program carried out in coastal waters of the Argentine Sea. Materials and methods Stomach contents of 2 adult E. anchoita were analyzed. The anchovies were caught during surveys carried out by the research vessels BIP Capita n Oca Balda and Eduardo Holmberg in a broad section of the Argentine Sea between and S. The northern surveys (OB-0/, OB-/, EH-0/ and EH-1/) were performed in the coastal area of Buenos Aires Province ( 0 S), mainly in October 1, 1 and 1, whereas the southern surveys (OB-/, OB-1/ and OB-1/) took place in Patagonian coastal waters (0 S) in December of the same years. Twenty-five fishing trawls were performed with a mm mesh size mid-water Nichimo net (Fig. 1), and 1 to 2 adult anchovies were separated from each catch for stomach content analyses. Stomach contents U.S. Copyright Clearance Centre Code Statement: 01 /200/2 01$1.00/0

2 Appendicularians in the diet of anchovies 1 ARGENTINA Latitude (s) Fig. 1. Geographic location of the 2 trawling stations during the Buenos Aires and Patagonian surveys from 1 in the Argentine Sea. Black circles: northern Buenos Aires surveys; white circles: southern Patagonian surveys Longitude (w) Study area Atlantic Ocean 2 Table 1 Food items found in the stomach contents of adults of Engraulis anchoita during surveys carried out in the Buenos Aires (northern) and Patagonian (southern) areas. Average number of organisms per fishing trawl of each food item is indicated. TP: total prey items ingested per catch, SD; standard deviation Appendicularia Fish O.dioica O. fusiformis Copepoda Cladocera eggs Pteropoda Amphipoda Bivalve Larvae Postlarva Crustacea Euphausiacea TP/catch SD Buenos Aires cruises 1 catch catch catch catch catch catch TP/group s catch catch catch TP/group s catch catch catch catch catch catch catch catch catch TP/group s Patagonian cruises 1 catch catch TP/group s catch catch , TP/group s catch catch catch TP/group s

3 1 F. L. Capitanio, M. Pájaro and G. B. Esnal were fixed in % formaldehyde all at the same time (0 min after the catch). Paired plankton samples, collected simultaneously with each fishing trawl at the same depth, were also analyzed. They were collected with 200 lm mesh size Bongo and Pairovet nets, except for survey EH-0/ where a 00 lm mesh size Calvet net was used. Oblique (Bongo net) and vertical (Pairovet and Calvet nets) trawls were performed from bottom to surface. Surface water temperature and salinity were recorded in each sampling station using a Conductivity Temperature Depth profiler (CTD). Plankton samples were fixed in 2% formaldehyde. Appendicularians were identified to the specific level both in plankton samples and stomach contents and classified according to their gonadal maturity as immature, intermediately mature and mature. Appendicularian density in plankton samples was calculated, discriminating species and maturity stages; their trunk lengths were also measured. The degree of selection of the appendicularian species by the anchovy was quantitative studied using a modified Ivlev selectivity index (D) (Jacobs, 1; Samaeoto et al., 1). This index was calculated for each catch and species as D ¼ (r ) p)/(r + p ) 2rp), where r is the proportion of one species in the stomachs and p is the proportion of that species in the paired plankton sample. The value of D varies from )1 to 0 for negative selection and from 0 to +1 for positive selection. For each species, the same index was calculated to test the degree of selection of the different maturity stages by the anchovy. Results Main items found in the stomach contents of adult E. anchoita collected in both coastal regions are shown in Table 1. The mean total length of anchovies was similar in both regions (northern surveys: 1.±1. mm; southern surveys: 12.±1. mm). Larger amounts of ingested food were found in the stomachs of the anchovies caught in the northern region;.% of the ingested organisms were mesozooplankters. The main items found in the stomach contents included copepods, appendicularians (O. dioica Fol 12 and O. fusiformis Fol 12), cladocerans, fish eggs (mainly anchovy eggs), and pteropods. Amphipods, euphausids, bivalve larvae, and crustacean postlarvae were rarely represented. In the southern region, the ingested organisms were also principally mesozooplankters (%), but the amount of food was less than in the northern surveys. The main items found in the stomachs were copepods and appendicularians (only O. dioica), whereas other taxa were rarely represented. Figure 2 shows availability of appendicularians in the plankton during the years analyzed. Total density (Fig. 2a) was somewhat higher in the northern surveys than in the southern (a) Density (ind. m ) < >200 1 Río de La Plata estuary 1 (b) Río de La Plata estuary st. st. st. st. st. st. st. st. Río de La Plata estuary Frequencies (%) Fig. 2. (a) Total density of appendicularians (specimens per m ) in the plankton samples obtained during the -year sampling period. (b) Relative frequencies of Oikopleura dioica, O. fusiformis and Fritillaria borealis in the different stations. See Fig. 1 for position of station numbers

4 Appendicularians in the diet of anchovies 1 Stomachs 1 Plankton Catches 1 Stations % 0% 0% 0% 0% 0% 1 Catches Stations 0% 0% 0% 0% 0% 0% Fig.. Relative proportion of the three maturity stages of Oikopleura dioica and O. fusiformis, both in the stomachs of anchovies and in the plankton. I, immature; II, intermediate; III, mature; N, total sample size Catches % 0% 0% 0% 0% 0% I II III Maturity stages Stations 2 2 ones, especially in 1 and 1. In the southern surveys the total density attained its maximum in 1. Three species were identified: O. dioica, O. fusiformis and Fritillaria borealis Lohmann 1. The most abundant species was O. dioica, which appeared in all stations during 1. The two remaining species appeared only in the northern surveys at the same stations (except in st. /1) always with O. dioica but at much lower densities, in particular F. borealis (Fig. 2b). In the southern region only O. dioica was found. A higher density of these three species was found in front of the discharge of the Rı o de la Plata estuary, with temperatures between and 1 C. Mean temperature was 1.2 C (SD ¼ 1.) in the northern region and 1. C (SD ¼ 1.1) in the southern region. The proportion of maturity stages of O. dioica and O. fusiformis recorded in the stomach contents and in the paired plankton sample are indicated in Fig.. In the northern surveys, mature specimens were dominant in 1, while in 1 all three maturity stages were equally represented. In 1, immature and intermediate specimens were dominant in the Río de la Plata estuary stations (no.,,, and ; Fig. 1), while mature appendicularians were mostly observed in stations further south. In the southern surveys, immature and intermediate stages were dominant. Trunk length of each maturity stage of both species was determined only in the plankton samples. Mature animals of O. dioica reached 1. mm trunk length and 1.0 mm in the case of O. fusiformis. The rare F. borealis found in the northern surveys were all mature specimens. The Ivlev selectivity index (D) calculated for O. dioica and O. fusiformis and for the three maturity stages of both species was in all cases 0, indicating a nonselective feeding (Table 2). Discussion The same appendicularian species were found both in plankton samples and in the stomachs of E. anchoita, with the exception of F. borealis, whose presence was not detected in the stomachs, probably owing to its low density in the plankton. Anchovies with the largest amounts of appendicularians in their stomachs corresponded to a greater availability of these organisms in plankton samples and, conversely, anchovies having rare animals in their stomachs corresponded to low appendicularian densities in paired plankton samples. The Argentine anchovy is an opportunistic predator with two modes of ingestion (Angelescu, 12). Organisms < mm long are trapped in the gill chambers by the filtration mechanism, which is a passive mode of feeding. Alternatively, organisms longer than mm are captured as single prey items, one at a

5 1 F. L. Capitanio, M. Pájaro and G. B. Esnal Table 2 Ivlev selectivity index (D) for Oikopleura dioica and O. fusiformis, and for their three maturity stages in each catch Area Year n O. dioica I II III O. fusiformis I II III Buenos Aires ) )0.001 )0.00 ) ) )0.002 ) ) ) ) )0.001 )0.001 )0.001 ) )0.002 ) ) ) ) ) ) )0.001 )0.00 ) ) ) ) ) ) ) ) )0.002 )0.001 ) ) ) ) )0.00 ) ) Patagonia )0.00 ) ) )0.001 ) ) ) ) )0.00 ) time, through active feeding. Engraulis anchoita alternates between both feeding modes depending on prey size and their relative abundance in the eupelagic layer (Angelescu, 12; Pájaro, 1). For example, Mianzan et al. (2001) found that anchovies shoaled in surface waters of the Río de la Plata salinity front actively feed on dense aggregations of salp blooms. In addition, Huse and Toresen (1) detected that the feeding modes of the capelin Mallotus villosus from the Barents Sea are usually variable. This capelin frequently consumed copepods and appendicularians (Oikopleura sp. and Fritillaria sp.) by passive filtration but sometimes ingested euphausids by active feeding. Differing from a previous observation by Capitanio et al. (1), we have now found similar proportions of maturity stages of O. dioica and O. fusiformis in plankton samples and in stomach contents, thus indicating a non-selective ingestion. As most of the time appendicularians remain inside their houses, fish predators may consume them together with their houses. Therefore, O. dioica and O. fusiformis were filtered passively by E. anchoita, destroying their houses and ingesting their fragments together with their dwellers. The mucous nature of these fragments makes them rare among food items found in the stomach contents. It is worth noting that the energetic value of the consumption of appendicularians and their houses is also enriched by particles that appendicularians remove from the water but which are not ingested (Alldredge, 1b; Gorsky et al., 1; Bedo et al., 1). Consumption of the discarded houses may also be important as they constitute a substratum on which a rich community of associated organisms develops (Davoll and Silver, 1; Fortier et al., 1; Steinberg et al., 1). The present results indicate that mesozooplankters represented a high percentage of the food ingested by anchovies both in northern and southern surveys of the Argentine Sea, copepods and appendicularians being the most representative taxonomic groups during three consecutive study years. In terms of production, appendicularians make a significant contribution in comparison with copepods, as their higher growth rates compensate for their lower biomass (Hopcroft and Roff, 1; Nakamura, 1). Appendicularians may not have been detected as prey of the anchovy before the study by Capitanio et al. (1), probably owing to their rapid decomposition in the fish stomach. As copepod densities in coastal and inner-shelf waters of the Argentine Sea during the northern anchovy spawning season are low as compared with those of the outer shelf during the summer season (Pájaro, 1), appendicularians probably become an important alternative food supply for the reproductive schools of E. anchoita. Acknowledgements We wish to thank C. Bertelo and P. Quiroga for their assistance with the sampling surveys and data collection. This research was supported by research grants from CONICET and UBACYT provided to Dr G.B. Esnal. This paper was improved as a result of the advice of the reviewers. References Alldredge, A. L., 1a: Field behavior and adaptative strategies of Appendicularians (Chordata: Tunicata). Mar. Biol., 2 1. Alldredge, A. L., 1b: Discarded appendicularians houses as sources of food, surface habitats, and particulate organic matter in planktonic environments. Limnol. Oceanogr. 21, 1 2. Alldredge, A. L., 11: The impact of appendicularian grazing on natural food concentrations in situ. Limnol. Oceanogr. 2, 2 2. Angelescu, V., 12: Ecología tro fica de la anchoíta del Mar Argentino (Engraulidae, Engraulis anchoita). Parte II. Alimentacio n, comportamiento y relaciones tro ficas en el ecosistema. Rev. Invest. Des. Pesq. (INIDEP) 0, 1. Balanov, A. A.; Gorbatenko, K. M.; Efimkin, A. Ya., 1: Diel dynamics of feeding of mesopelagic fishes of the Bering Sea during autumn. Russ. J. Mar. Biol. 21, 1. Bedo, A. W.; Acuña, J. L.; Robins, D.; Harris, R. P., 1: Grazing in the micron and sub-micron particle size range: the case of Oikopleura dioica (Appendicularia). Bull. Mar. Sci., 2 1.

6 Appendicularians in the diet of anchovies 1 Capitanio, F. L.; Pájaro, M.; Esnal, G. B., 1: Appendicularians (Chordata, Tunicata) in the diet of anchovy (Engraulis anchoita) in the Argentine Sea. Sci. Mar. 1, 1. Davis, N. D., 1: Caloric content of oceanic zooplankton and fishes for studies of salmonid food habits and their ecologically related species. (NPAFC Doc.) FRI-UW-. Fisheries Research Institute, University of Washington, Seattle, WA. pp. Davis, N. D.; Myers, K. W.; Ishida, Y., 1: Caloric value of highseas salmon prey organisms and simulated salmon ocean growth and prey consumption. N. Pac. Anadr. Fish. Comm. Bull. 1, 1. Davoll, P. J.; Silver, M. W., 1: Marine snow aggregates: life history sequence and microbial community of abandoned larvaceans houses from Monterey Bay, California. Mar. Ecol. Prog. Ser., 1 0. Flood, P. R.; Deibel, D.; Morris, C. C., 12: Filtration of colloidal melanin from sea water by planktonic tunicates. Nature,, 0 2. Fortier, L.; Le Fèvre, J.; Legendre, L., 1: Export of biogenic carbon to fish and to the deep ocean: the role of large planktonic microphages. J. Plankton Res. 1, 0. Gorsky, G.; Fisher, N. S.; Fowler, S. W., 1: Biogenic debris from the pelagic tunicate Oikopleura dioica, and its role in the vertical transport of a transuranium element. Estuar. Coast. Shelf Sci. 1, 1 2. Grover, J. J., 1: Feeding habits of pelagic summer flounder, Paralichthys dentatus, larvae in oceanic and estuarine habitats. Fish. Bull., 2 2. Hansen, J. E.; Cousseau, M. B.; Gru, D. L., 1: Características poblacionales de la anchoíta (Engraulis anchoita) del mar argentino. Parte I. El largo medio al primer an o de vida, crecimiento y mortalidad. Rev. Invest. Des. Pesq. (INIDEP), 21. Hansen, J. E.; Madirolas, A.; Perrota, R. G., 1: Evaluación del efectivo bonaerense de anchoíta (Engraulis anchoita) entre las latitudes de y S en el oton o de 1. Rev. Invest. Des. Pesq. (INIDEP), 1. Hansen, J. E.; Martos, P.; Madirolas, A., 2001: Relationship between spatial distribution of the Patagonian stock of Argentine anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish. Oceanogr., Hopcroft, R. R.; Roff, J. C., 1: Production of tropical larvaceans in Kingston Harbour, Jamaica: are we ignoring an important secondary producer? J. Plankton Res. 20,. Hopcroft, R. R.; Roff, J. C.; Bouman, H. A., 1: Zooplankton growth rates: the larvaceans Appendicularia, Fritillaria and Oikopleura in tropical waters. J. Plankton Res. 20,. Huse, G.; Toresen, R., 1: A comparative study of the feeding habits of herring (Clupea harengus, clupeidae) and capelin (Mallotus villosus, Osmeridae) in the Barents Sea. Sarsia 1, 1 1. Jacobs, J., 1: Quantitative measurement of food selection. A modification of the forage ratio and Ivlev s selectivity index. Oecologia, 1, 1 1. Mianzan, H.; Pájaro, M.; Alvarez Colombo, G.; Madirolas, A., 2001: Feeding on survival-food: gelatinous plankton as a source of food for anchovies. Hydrobiologia 1,. Mochioka, N.; Iwamizu, M., 1: Diet of anguilloid larvae: leptocephali feed selectively on larvacean houses and fecal pellets. Mar. Biol., 2. Mousseau, L.; Fortier, L.; Legendre, L., 1: Annual production of fish larvae and their prey in relation to size-fractionated primary production (Scotian Shelf, NW Atlantic). ICES J. Mar. Sci.,. Nakamura, Y., 1: Blooms of tunicates Oikopleura spp. and Dolioletta gegenbauri in the Seto Inland Sea, Japan, during summer. Hydrobiologia, Paffenhöfer, G. A., 1: The cultivation of an appendicularian through numerous generations. Mar. Biol. 22, 1 1. Paffenhöfer, G. A., 1: On the biology of appendicularia of the southeastern North Sea. In: th European Symposium in Marine Biology, Ostende, Belgium, September 1 2, 1, 2,. Pájaro, M., 1: El canibalismo como mecanismo regulador densodependiente de mortalidad natural en la anchoíta argentina (Engraulis anchoita). Su relacio n con las estrategias reproductivas de la especie. Tesis Doctoral, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata. 2 pp. Pomeroy, L. R., 2001: Caught in the food web: complexity made simple? Sci. Mar., 1 0. Ramírez, F. C.; Sabatini, M. E., 2000: The occurrence of Calanidae species in waters off Argentina. Hydrobiologia, Sabatini, M. E.; Ramírez, F. C.; Martos, P., 2000: Distribution pattern and population structure of Calanus australis Brodsky, 1 over the southern Patagonian Shelf off Argentina in summer. ICES J. Mar. Sci., 1 1. Samaeoto, D.; Neilson, J.; Waldron, D., 1: Zooplankton prey selection by juvenile fish in Nova Scotian Shelf basins. J. Plankton Res. 1, 0 1. Sa nchez, R. P.; Ciechomski, J. D., 1: Spawning and nursery grounds of pelagic fish species in the sea-shelf off Argentina and adjacent areas. Sci. Mar.,. Steinberg, D. K.; Silver, M. W.; Pilskaln, C. H.; Coale, S.; Paduan, J. B., 1: Midwater zooplankton communities on pelagic detritus (giant larvacean houses) in Monterey Bay, California. Limnol. Oceanogr., 0. Tadokoro, K.; Ishida, Y.; Davis, N.; Ueyanagi, S.; Sugimoto, T., 1: Change in chum salmon (Oncorhynchus keta) stomach contents associated with fluctuation of pink salmon (O. gorbuscha) abundance in the central subarctic Pacific and Bering Sea. Fish. Oceanogr. 2,. Woehrling, D.; Le Fèvre-Lehoërff, G., 1: Long-term series in ichthyoplankton: sole and sprat at French coast of the North Sea from 1 to 1. Oceanol. Acta. 21, 1. Author s address: Fabiana L. Capitanio, Departamento de Ciencias Biolo gicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C12EHA Buenos Aires, Argentina. capitani@bg.fcen.uba.ar

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