G. Kehayias, J. Lykakis, and N. Fragopoulu. Introduction. Materials and methods
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1 ICES Journal of Marine Science, 53: The diets of the chaetognaths Sagitta enflata, S. serratodentata atlantica and S. bipunctata at different seasons in Eastern Mediterranean coastal waters G. Kehayias, J. Lykakis, and N. Fragopoulu Kehayias, G., Lykakis, J., and Fragopoulu, N The diets of the chaetognaths Sagitta enflata, S. serratodentata atlantica and S. bipunctata at different seasons in Eastern Mediterranean coastal waters. ICES Journal of Marine Science, 53: The chaetognaths Sagitta enflata, S. serratodentata atlantica and S. bipunctata were caught in six sampling periods from September 1988 until July 1989 during both day and night in Kisamos Gulf (Cretan Sea, Eastern Mediterranean) in the upper layers ( 5 m). Gut content analysis showed that copepods were the predominant food organisms in the diet of these three predators. Positive electivity indices were found for Corycaeus spp. and Oncaea spp. but negative for Clausocalanus spp. copepodites and Clausocalanus furcatus females, which were the most numerous among copepods. Cannibalism was observed mainly in S. bipunctata while S. serratodentata atlantica was found to be less cannibalistic. The size of the predator was reflected in the size of prey. Feeding intensity indicated by Food containing ratio (FCR) and Number of prey per chaetognath (NPC) increased just before the reproductive period of each chaetognath species. Differences between day and night feeding were only found in S. enflata International Council for the Exploration of the Sea Key words: feeding habits, diets, Sagitta enflata, Sagitta serratodentata atlantica, Sagitta bipunctata, Eastern Mediterranean. Received 26 October 1995; accepted 29 February G. Kehayias, J. Lykakis, and N. Fragopoulu: Section of Animal Biology, Department of Biology, University of Patra, 265 Patra, Greece. Introduction Chaetognaths are dominant zooplankton predators and are generally believed to have a considerable influence on their prey populations, especially under conditions of low environmental productivity (Kimmerer, 1984; Øresland, 199). Copepods seem to be the most important prey (Øresland, 1987). Reeve (197) speculated that most of the energy converted to animal biomass by copepods is transferred to higher trophic levels via these predators. Chaetognaths are food for a wide variety of larger organisms, and therefore occupy a central position in the planktonic food webs (Feigenbaum and Maris, 1984). The literature concerning chaetognath feeding has been reviewed by Feigenbaum and Maris (1984) and Feigenbaum (1991). However, data on chaetognaths feeding in Mediterranean waters are available only for the three species Sagitta enflata, S. minima and S. friderici, common in the coastal waters of Spain and the Western Mediterranean (Pearre, 1974, 1976). Sagitta enflata, S. serratodentata atlantica and S. bipunctata are the three more numerically important species in Cretan Sea coastal waters and the Eastern Mediterranean, comprising almost 9% of the total chaetognaths (Kehayias et al., 1992). In the present study, the diel diet and food selection of these three species were estimated during six different sampling periods. We consider prey species abundance in the diet as well as in the environment, and size selection between prey. Materials and methods Five sampling stations were located in the Kisamos Gulf (23 4 E, N) (Cretan Sea, Eastern Mediterranean) (Fig. 1). Zooplankton was sampled from the upper 5 m on 25 September and 2 November 1988, and 22 February, 8 April, 23 May and 29 July During the first three sampling dates, day and night samples were collected while on the other dates only day samples were taken. On each occasion double oblique hauls were conducted with a Bongo net (5 μm mesh size) and a WP-2 net (2 μm mesh size) for the collection of the samples, which were preserved in 4% formaldehyde buffered solution immediately after collection. WP-2 net samples were not taken in September The samples /96/ $18./ 1996 International Council for the Exploration of the Sea Downloaded from on 18 August 218
2 838 G. Kehayias et al. 22 3' ' ' E 23 35' 23 4' 23 45' E 41 N Kisamos Gulf 35 4' N 39 Aegean Sea ' Cretan Sea ' 22 3' ' ' E 23 35' 23 4' 23 45' E Figure 1. The Gulf of Kisamos (Cretan Sea, Eastern Mediterranean) indicating the five stations of sampling. collected with the finer mesh were used to estimate abundances of chaetognath prey in the field. The samples taken with both nets were used for gut analysis in order to examine a wider range of sizes of chaetognaths. In the laboratory, all chaetognaths were extracted from the samples, and they were further sorted by species. The chaetognaths were then classified under a dissecting microscope by maturity stage based on the development of the ovary and the seminal vesicles, using a modification of Ghirardelli s (1961) system, as follows: stage I, young without visible ovaries; stage II, immature with visible ovaries but no visible seminal vesicles; stage III, seminal vesicles present, ova visible, a few large; stage IV, filled seminal vesicles and large ova. All chaetognaths apparently containing food particles were examined to identify the food material. Prey was visible through the body wall. Chaetognaths which had not completely swallowed their prey, or in which the prey was found in the forward third of their gut were not included in the further analysis. Prey was identified to zooplankton taxa while copepods were identified to species or only to genus when there was difficulty in identification owing to partial digestion. Copepods which were in an advanced state of digestion were considered as unidentified copepods. Head width of chaetognaths is considered to be more closely related to prey size than body length (Pearre, 198). Head widths of all chaetognath specimens were therefore measured with the chaeta in the closed position as well as the maximum body width of the food specimens, and a regression equation of head width vs. food width was established for each chaetognath species. Total lengths of chaetognaths and food items were also measured. Food containing ratio (FCR) and number of prey per chaetognath (NPC) (Feigenbaum and Maris, 1984) were estimated. FCR is expressed as the frequency of chaetognaths containing food while NPC is expressed as the frequency of prey in the chaetognaths examined. Selectivity calculations for every species were based on all identifiable prey for a given sampling date, and mean abundances from all plankton samples from that date. Therefore Ivlev s (1961) index of electivity (E) was used: E i =r i n i /r i +n i where E i =the selectivity for prey i, r i =the frequency of prey i in the diet, and n i =frequency of prey i in the 2 μm mesh size net plankton samples. Results Of the 12 chaetognaths examined, 175 contained food. Among these 514 were Sagitta enflata, 345 S. serratodentata atlantica, 172 S. bipunctata and 44 specimens were a mixture of S. lyra, S. hexaptera and S. minima. As the three latter species were too rare for Downloaded from on 18 August 218
3 Chaetognath diet in Eastern Mediterranean coastal waters 839 Table 1. Diet (%), FCR and NPC of Sagitta enflata in the six sampling periods in Kisamos Gulf. Values are means of the five sampling stations. Diet Day Night September November February April May July September November February Neocalanus minor Eucalanus spp Clausocalanus mastigophorus Clausocalanus furcatus Clausocalanus jobei.7 Clausocalanus pergens Clausocalanus paululus 2.1 Clausocalanus spp Clausocalanus spp. juv Euchaeta spp. 1. Temora stylifera Pleurommama gracilis Centropages typicus Calocalanus spp Candacia spp. 1.9 Lucicutia spp. 5.2 Microsetella norvegica Acartia spp Oncaea spp Corycaeus spp Unidentified copepods Total copepods Siphonophores Cladocerans Amphipods 1.4 Euphausiids Decapod larvae Chaetognaths Appendicularians Fish larvae.7 Unidentified organic material Total no. of food items No. of chaetognaths examined No. of fed chaetognaths FCR NPC useful analysis the following data concern the diet of the other three. No statistically significant difference (t-test, p>.5) was recorded between the sizes of chaetognath specimens of each species in the two nets. On each sampling date no statistically significant difference was found in the abundance of the zooplankton taxa between the five sampling stations (ANOVA, p>.5). Mean relative abundance of the total chaetognaths in the zooplankton from the Bongo samples was 11.2% (n=2.1, 1 m 3 ) and from the WP-2 samples.72% (n=269.7, 1 m 3 ). Sagitta enflata Table 1 shows the diet (%), FCR and NPC data for the total Sagitta enflata population in the different seasons by day and night. Night samples were available only for September, November and February. The gut content was dominated by copepods in all sampling periods. Copepods were also the most abundant group in the mesozooplankton (Table 2). Median electivity indices were significantly different from zero and were positive for the copepods Oncaea spp. (+.64), Corycaeus spp. (+.66), chaetognaths (+.43) and decapod larvae (+.47), but negative for the juvenile Clausocalanus spp. (.33) although these were the more numerous specimens among the copepods (Table 3). Similarly, the index for the female Clausocalanus furcatus was negative (.4). Cladocerans, although abundant in the field in May and especially in July, were very rarely found in S. enflata guts, possibly because of the lower numbers of animals caught with food at these periods. Comparison between day and night samples showed that unidentified organic material contributed significantly to the gut contents during the night. Significant differences (t-test, p=.16) between day and night FCR and NPC Downloaded from on 18 August 218
4 84 G. Kehayias et al. Table 2. Mean frequency (%) of mesozooplankton groups, density and biomass of total mesozooplankton in the five sampling periods in Kisamos Gulf Zooplankton taxa November February April May July Siphonophores Polychaetes Pteropods Cladocerans Ostracods Copepods Euphausiids Amphipods Decapod larvae Chaetognaths Appendicularians Salps Doliolids Fish larvae Total specimens (n m 3 ) Total biomass (mg m 3 ) Table 3. Mean frequency (%), density and biomass of copepods in the five sampling periods in Kisamos Gulf Copepod species November February April May July Mesocalanus tenuicornis Neocalanus minor Calanus gracilis Eucalanus attenuatus Eucalanus spp Clausocalanus lividus (f) Claus. mastigophorus (f) Clausocalanus furcatus (f) Clausocalanus jobei (f) Clausocalanus spp. (m) Clausocalanus spp. (juv) Euchaeta spp Temora stylifera Pleurommama gracilis Centropages typicus Centropages violaceus Mecynocera clausi Calocalanus spp Heterorabdus papilliger..... Candacia spp Haloptilus spp Acartia spp Oithona spp Oncaea spp Corycaeus spp Total specimens (n m 3 ) Total biomass (mg m 3 ) values showed a preference for feeding at night. In the day samples FCR varied between.25 and.1 and NPC between.29 and.114, while at night FCR varied between.161 and.263 and NPC between.182 and.37 (Table 1). FCR was higher for older developmental stages. The high percentage of empty S. enflata specimens should be noted. Multiple prey were found in 14.6% of the predators; most of them contained two Downloaded from on 18 August 218
5 Chaetognath diet in Eastern Mediterranean coastal waters 841 (a) Sagitta enflata Stage I NPC (b) Sagitta serratodentata atlantica.7 NPC (c) Sagitta bipunctata.7 NPC Sept. Sept. Sept. Nov. Feb. Apr. May Nov. Feb. Apr. May Nov. Feb. Apr. May Jul. Jul. Jul. Figure 2. Seasonal variation of NPC for the four developmental stages of (a) Sagitta enflata, (b) S. serratodentata atlantica and (c) S. bipunctata ( I, II, III, IV). Values are means of the five sampling stations during day. Percentage of prey items in the total diet Stage II Stage III Stage IV prey but some had as many as six. NPC for stages III and IV increased towards summer while a peak was also found in February for all the developmental stages (Fig. 2). The size of the predator (total length mm) was reflected in the size of prey (total length mainly.5 1. mm). As the developmental stage increased the length of the prey also increased (Fig. 3). Stage I consumed only small copepods while later stages of development consumed larger prey as well. The largest food item found was 11.6 mm. Positive correlation was found between the width of the chaetognath s head and the width of the food items (regression analysis, r=.58, p<.5) (Fig. 5). Sagitta serratodentata atlantica and Sagitta bipunctata Tables 4 and 5 show the diet (%), FCR and NPC data for S. serratodentata atlantica and S. bipunctata >3.5 Size class of prey items Figure 3. Size classes of prey items in the diet of the four developmental stages of Sagitta enflata. respectively. The contribution of the unidentified organic material to the gut content of both species was significant. Mean electivity indices were, as found for S. enflata, positive for the copepods Corycaeus spp. (+.57 for S. serratodentata atlantica and +.5 for S. bipunctata) and Oncaea spp. (+.43 and +.32 respectively), but negative for Clausocalanus spp. and Clausocalanus furcatus females (.25 and.35 Downloaded from on 18 August 218
6 842 G. Kehayias et al. Table 4. Diet (%), FCR and NPC of Sagitta serratodentata atlantica in the six sampling periods in Kisamos Gulf. Values are means of the five sampling stations. Diet Day Night September November February April May July September November February Neocalanus minor 1.5 Clausocalanus furcatus 3.7 Clausocalanus spp Clausocalanus spp. juv Pleurommama gracilis 1.5 Microsetella norvegica 7.4 Oncaea spp Corycaeus spp Unidentified copepods Total copepods Decapod larvae 3.7 Chaetognaths 3.7 Unidentified organic material Total no. of food items No. of chaetognaths examined No. of fed chaetognaths FCR NPC Table 5. Diet (%), FCR and NPC of Sagitta bipunctata in the six sampling periods in Kisamos Gulf. Values are means of the five sampling stations. Diet Day Night September November February April May July September November February Neocalanus minor 2.1 Clausocalanus spp. 4.2 Clausocalanus spp. juv Temora stylifera 3.6 Microsetella norvegica Oncaea spp Corycaeus spp Unidentified copepods Total copepods Cladocerans Euphausiids 6.3 Decapod larvae 2.1 Chaetognaths Unidentified organic material Total no. of food items No. of chaetognaths examined No. of fed chaetognaths FCR NPC respectively). S. bipunctata was the most cannibalistic among the three chaetognath species studied. No preference for feeding at night was found for either species. Comparison between day and night FCR and NPC values showed no statistically significant difference (t-test, p>.5). Only one food item was found in the gut of 98% of both predators. NPC values for S. serratodentata atlantica increased in April, in February for stage IV S. bipunctata and in May for the other stages of development (Fig. 2). As for S. enflata, the size of the predator was reflected in the size of prey for both S. serratodentata atlantica (total length mm) and S. bipunctata (total length mm) (Fig. 4). The largest food item found for the former species was 3.2 mm and for the latter 6.4 mm. Positive but small correlations were found between the width of chaetognath head and the width of food items (regression analysis, r=.27, p<.5 for S. serratodentata atlantica Downloaded from on 18 August 218
7 Chaetognath diet in Eastern Mediterranean coastal waters 843 (a) Sagitta serratodenta atlantica (b) Sagitta bipunctata 6 Stage I 6 Stage I Stage II 6 Stage II 8 Percentage of prey items in the total diet Stage III Stage III 1 Stage IV Stage IV > >3.5 Size classes (mm) Figure 4. Size classes of prey items in the diet of the four developmental stages of (a) Sagitta serratodentata atlantica and (b) S. bipunctata. and r=.41, p<.5 for S. bipunctata) (Fig. 5). S. serratodentata atlantica specimens could take prey of a greater width than the unexpanded width of their heads. Discussion Copepods are commonly reported as being the most abundant food item found in chaetognath guts, because Downloaded from on 18 August 218
8 844 G. Kehayias et al. Prey width (mm) (a) (b) (c) Chaetognath head width (mm) Figure 5. Head width prey width relationship for three chaetognaths (a) Sagitta enflata, (b) S. serratodentata atlantica and (c) S. bipunctata. of the abundance of these prey in their ecosystem (Feigenbaum, 1991). Small copepods were the main food for the three chaetognath species studied. Significant amounts of unidentified organic material were found in the gut contents mainly of Sagitta serratodentata atlantica. Pearre (1974) found high proportions of unidentified food items in the gut contents of S. minima in the Western Mediterranean. He suggested that this was due to the small size of this species leading to smaller prey and hence more rapid digestion of the prey. This could be an explanation for the highest proportions of unidentified organic material being found in S. serratodentata atlantica, which was the smallest of the three species studied. Since chaetognaths can utilize prey of a wide range of sizes and developmental stages, the actual diet can be expected to reflect to some extent the relative prey abundance (Øresland, 1987; Pearre, 1974, 1976; Szyper, 1978). However, chaetognaths show selectivity in their feeding behaviour. Selection may be based on size, shape, aggregation behaviour, or may result from differential movement patterns or escapability of prey (Feigenbaum, 1991). Clausocalanus spp. copepodites and Clausocalanus furcatus females were the most abundant copepods in the field, followed by Corycaeus, Oithona, Acartia and Oncaea. Clausocalanus spp. copepodites and Corycaeus were the most common food items in the guts. Corycaeus and Oncaea were selected by the three predators, while Oithona and Acartia were ignored. The evidence for the selection of the two former genera could be an artifact of digesting times. Corycaeus and Oncaea can be found at the end of the digestive tract, or even partially ejected, with very little outward sign of digestion due to their hard body (Pearre, 1974). The same was often found in the present study. This effect may have influenced the results of Stone (1969) who found high selectivity values for Corycaeus, Corycella, Oncaea and Microsetella, although their frequency in the field was low. Alvarez-Cadena (1993) suggested that Acartia clausi females were ignored as a food item of Sagitta elegans because of their morphology. Similarly, Oithona and Acartia were ignored in our samples possibly because of their morphology (spiny processes of the antennae) and/or their swimming behaviour. However, Pearre (1976) noted that S. friderici was heavily dependent on Oithona spp. Electivity indices were negative for Clausocalanus copepodites and C. furcatus females, possibly because of the different position of prey and predator in the water column at the time of sampling, but we cannot relate vertical distribution or migration to diet in this study due to the sampling method used. Another difficulty for the interpretation of the electivity indices obtained from gut contents is the estimation of prey density in the field on a size scale important to the predator with a tow net (Sullivan, 198). Microsetella norvegica was found in the diet while Downloaded from on 18 August 218
9 Chaetognath diet in Eastern Mediterranean coastal waters 845 it was not found in our samples probably due to the small size of this copepod in comparison with the mesh size of the net. Although cladocerans, euphausiids and other meroplankters can be a significant part of the diet in a given locality (Feigenbaum and Maris, 1984), this was not the case in Kisamos Gulf. Fish larvae were also not found in chaetognath guts, perhaps because they are scarce members of the zooplankton. Cannibalism is an important source of carbon in the diet of chaetognaths (Feigenbaum, 1991). Cannibalism, i.e. combination of inter- and intra-specific predation, was observed mainly for S. bipunctata (mean annual value 5.1%) followed by S. enflata and S. serratodentata atlantica (3.2% and.3% respectively). Stone (1969) in South Africa found S. enflata to be more cannibalistic (1.4%) followed by S. bipunctata (6.7%) and S. serratodentata atlantica (1.2%). Larger species and stages of development have been found to contain a variety of larger prey items (Pearre, 1982), which often results in a shift in prey species as the chaetognaths grow. S. enflata, which was the largest among the three studied species, consumed a wider variety of prey than the smaller S. bipunctata and S. serratodentata atlantica. This was also evident for the developmental stages within each population of the three predators. The information on size and species of prey consumed by Sagitta increases our understanding of the predatory impact of chaetognaths on copepod communities (Sullivan, 198). Food availability increased in April when the highest abundance and biomass of zooplankton were observed. This was not coupled with highest FCR or NPC values for the chaetognaths except for S. serratodentata atlantica. FCR and NPC values for S. enflata were lower than those reported by Pearre (1974, 1976), Szyper (1976, 1978), Feigenbaum (1979), Bushing and Feigenbaum (1984) or Kimmerer (1984). This is possibly due to the oligotrophic characteristic of the Eastern Mediterranean. For the same species NPC increased in February for all the developmental stages and towards summer for stages III and IV. The former evidence is possibly a result of the long digestion times in cold waters (Feigenbaum, 1991). Higher NPC values found towards summer for the older stages are probably a result of increasing food intake to satisfy the extra energy requirements of gametogenesis in the summer. Similarly, the increase of NPC for S. serratodentata atlantica and S. bipunctata was noticed just before their reproductive period (Kehayias et al., 1992). Chaetognaths display a diel feeding rhythm, with an increase of feeding during the night. This has also been demonstrated in the laboratory and supported by field studies (Bushing and Feigenbaum, 1984; Nagasawa, 1985). In our samples feeding differences between day and night were found only for S. enflata. Acknowledgement We wish to express our thanks to the Ministry of Agriculture for funding the research programme in Kisamos Gulf. References Alvarez-Cadena, J. N Feeding of the chaetognath Sagitta elegans Verill. Estuarine, Coastal and Shelf Science, 36: Bushing, M. and Feigenbaum, D Feeding by an expatriate population of Sagitta enflata. Bulletin of Marine Science, 34: Feigenbaum, D. L Daily ration and specific daily ration of the chaetognath Sagitta enflata. Marine Biology, 54: Feigenbaum, D. L Food and feeding behaviour. In The Biology of Chaetognaths, pp Ed. by Q. Bone, H. Kapp, and A. C. Pierott-Bults. Oxford University Press, Oxford. 173 pp. Feigenbaum, D. L. and Maris, R. C Feeding in the Chaetognatha. Annual Review of Oceanography and Marine Biology, 22: Ghirardelli, E Istologia e citologia degli stadi di maturita nei Chetognati. Bolletino di Pesca, Piscicoltura e Idrobiologia, 36(15): Ivlev, V. S Experimental ecology of the feeding of fishes. (D. Scott, trans.), Yale University Press, New Haven, CT. 32 pp. Kehayias, G., Lykakis, J., and Fragopoulu, N Temporal variation of the different developmental stages of chaetognaths in the Gulf of Kisamos (Cretan Sea). Rapports et Procès-verbaux des Réunions Commission Internationale pour l Exploration Scientifique de la Mer Mediterranée, 33: 254. Kimmerer, W. J Selective predation and its impact on prey of Sagitta enflata (Chaetognatha). Marine Ecology Progress Series, 15: Nagasawa, S The digestive efficiency of the chaetognath Sagitta crassa Tokioka, with observations on the feeding process. Journal of Experimental Marine Biology and Ecology, 87: Øresland, V Feeding of the chaetognaths Sagitta elegans and Sagitta setosa at different seasons in Gullmarsfjorden, Sweden. Marine Ecology Progress Series, 39: Øresland, V Feeding and predation impact of the chaetognath Eukrohnia hamata in Gerlache Strait, Antarctic Peninsula. Marine Ecology Progress Series, 63: Pearre, S. Jr Ecological studies of three West- Mediterranean chaetognaths. Investigacion Pesquera. Barcelona, 38: Pearre, S. Jr A seasonal study of the diets of three sympatric chaetognaths. Investigacion Pesquera. Barcelona, 4: Pearre, S. Jr Feeding by Chaetognatha: the relation of prey size to predator size in several species. Marine Ecology Progress Series, 3: Pearre, S. Jr Feeding by Chaetognatha: aspects of interand intra-specific predation. Marine Ecology Progress Series, 7: Reeve, M. R The biology of Chaetognatha. I. Quantitative aspects of growth and egg production in Sagitta hispida. In Marine Food Chains, pp Ed. by J. H. Steele. Oliver & Boyd, Edinburgh. Downloaded from on 18 August 218
10 846 G. Kehayias et al. Stone, J. H The Chaetognatha community of the Agulhas Current: its structure and related properties. Ecological Monographs, 39: Sullivan, B In situ feeding behaviour of Sagitta elegans and Eukrohnia hamata (Chaetognatha) in relation to the vertical distribution and abundance of prey at ocean station P. Limnology and Oceanography, 25: Szyper, J. P The role of Sagitta enflata in the southern Kaneohe Bay system. Ph.D. dissertation, University of Hawaii. 147 pp. Szyper, J. P Feeding rate of the chaetognath Sagitta enflata in nature. Estuarine and Coastal Marine Science, 7: Downloaded from on 18 August 218
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