45 Indian J. Fish., 58(3) : 45-50, 2011 Food and feeding habits of deepsea pandalid prawns Heterocarpus gibbosus, Bate 1888 and Heterocarpus woodmasoni, Alcock off Kerala, south India S. R. RADHIKA RAJASREE AND B. MADHUSOODANA KURUP* Centre for Ocean Research, NIOT-SU Research Centre, Sathyabama University Jeppiaar Nagar, Rajiv Gandhi Road, Chennai - 600 119, Tamil Nadu, India *Kerala University of Fisheries and Ocean Studies, Panangad P. O., Kochi - 682 506, Kerala, India e-mail: radhiin@gmail.com ABSTRACT Food and feeding habits of two deepsea prawns Heterocarpus gibbosus and Heterocarpus woodmasoni were studied from the commercial deepsea prawn landings off Kerala coast (south India). The diet of both the species were examined giving emphasis to variations with regard to months, size groups, sex and maturity stages. Stomach conditions in various maturity stages, length groups and gastrosomatic index were also studied. The diet of both the species were found similar showing presence of euphausids, foraminiferans, sponges and detritus. In both the species, highest numbers of full stomachs were observed in orange-berried females, and spent males, which may be due to their voracious feeding after spawning while highest number of empty stomachs was observed in head roes of females and maturing males. Variations in the gastrosomatic index indicated strong correlation between feeding intensity and breeding periods of both the species. Keywords: Deepsea prawns, Feeding habits, Heterocarpus gibbosus, Heterocarpus woodmasoni, Kerala coast, south India. Introduction Prawns form one of the most economically important constituents in the marine fish landings in India. Kerala is a fertile strip of land lying along the south-west coast of India, which forms, less than 10% of the entire Indian coastline. This state occupies the foremost position in marine fish production, accounting for about 29% of the total all India landings (Rajasree, 2005). With the decrease in traditionally exploited prawn stocks in shallow coastal waters, prawns in deeper water layers increasingly attracted economic interest. Targeted fishery for deepsea prawns off Kerala began for the first time in 1999. However, the rapid developments of fisheries as well as the considerable vulnerability to overfishing often lead to a fast decrease in deep sea prawn stocks off Kerala (Rajasree, 2004). As food being the major factor regulating the abundance, growth and movement of animals, any information in this regard will add to the existing knowledge needed for better management of the prawn stock. Some of the important works on the food and feeding habits of deepsea prawns are those of Turpaeva (1948, 1953), Allen (1959), Butler (1964), Berenboim (1981, 1992) and Weinberg (1980) on the pandalid prawn Pandalus borealis and those of Mistakidis (1957), Allen (1963) and Cartes (1993) on the feeding habits of the deepsea prawns of the western Mediterranean slope. In the Indian Ocean, only very little is known on the food and feeding habits of the deepsea prawns, the pioneer study being the study conducted by Kurian (1965) on the gut contents of Penaeopsis jerryi in comparison with the feeding habits of littoral penaeids. Suseelan (1985) conducted a preliminary study on the gut contents of deepsea prawns collected during the exploratory surveys off south-west coast of India, however, information on their food preference pertaining to season, sex, maturity stage and size class are still lacking. Therefore, the present study was aimed to unravel the seasonal variations, if any, in sex-wise, maturity stage-wise, size group-wise food preference and stomach conditions of males and females of H. gibbosus and H. woodmasoni off Kerala coast. Materials and methods Samples of H. gibbosus and H. woodmasoni were collected at weekly intervals from the landings of commercial deepsea trawls fishing at depths between 300 – 500 m off Kerala coast between September 2000 and August 2002. The specimens collected from Cochin, Munambam and Sakthikulangara harbours of Kerala were pooled for gut content analyses. The specimens obtained 46 S. R. Radhika Rajasree and B. Madhusoodana Kurup from exploratory surveys conducted by FORV Sagar Sampada along Kerala coast were also utilized for the studies. In the laboratory, the specimens so collected were washed, segregated sex-wise and maturity stage-wise and preserved in 5% formalin. Each prawn was measured for its total length (TL) and weight (TW) to the nearest mm and g respectively. After cutting open the carapace wall, the stomach was dissected out, weighed and stomach fullness was recorded. The intensity of feeding was determined by observing the degree of distension of the stomach due to the quantity of food inside the anterior and posterior chambers of the proventriculus and this is further expressed by computing the gastrosomatic index, as the percentage weight of stomach to the total body weight. The condition of feeding was expressed as full, 3/4 full, 1/2 full, ¼ full, trace and empty respectively (Pillay, 1952). A preliminary qualitative analysis of the gut contents showed that H. gibbosus and H. woodmasoni are carnivores and detritus feeders and therefore the index of preponderance method (Natarajan and Jhingran, 1961) suitable for carnivorous animals was adopted in this study. Food items of prawns were identified up to generic level wherever possible, counted and measured volumetrically. All identifiable and partially digested food remains were grouped under semi-digested matter. A total of 407 specimens of H. woodmasoni and 596 specimens of H. gibbosus were used in the present study. Food analysis was done in relation to months, sexes, maturity stages and size groups. The prawns were grouped with a class interval of 10 mm. For maturity stage-wise analysis, three stages in males and seven stages in females were employed following Ceccaldi (1966) and Company and Sardá (1997). Results Euphausids appeared as the most predominant among the food items and could be easily identified by the presence of appendages, broken bright orange coloured shells and antennae. In H. gibbosus, they formed 40% of the diet whereas it was 28% in H. woodmasoni. Detritus formed 16% and 14% to the diets of H. gibbosus and H. woodmasoni respectively, whereas foraminifera constituted 13% and 23% each to the diets of H. gibbosus and H. woodmasoni. Among the foraminifers encountered from the stomachs, Globigerina species showed its predominance. In most cases, this was represented as whole organisms. This was followed by Lagena vulgaris, Proteonina fusiformes, Entosolenia marginata, Rotalina mammalia, Redobolivina mexicana while Cristellaria calcar was found only very occasionally in the diet. Echinoderms and sponge spicules were present as spicules of glass sponges and skeletal rests of echinoderms. Fish scales belonging to species of the family Gadidae were also found in a number of guts of H. gibbosus (4%) and H. woodmasoni (5%). Other crustaceans comprising of mostly amphipods and rarely isopods were encountered in the stomach of H. gibbosus in significant quantities (11%). On the contrary, in H. woodmasoni, it was not regularly represented and if present, was only in traces (3%). Polychaetes consisting of mostly Paramphinome spp. and aphrodites were rarely encountered from the stomach of H. woodmasoni (0.5%). Molluscan shells were present in the stomachs of both the species in quite negligible quantities. Among them, thecostomata (Cavolina trispinosa) and gastropoda (Gapulus ungaricus) were the dominant items. Crushed unidentified items were also often encountered. Preference to food items Monthly variations in the Index of preponderance of various food items encountered from the guts of males and females of H. gibbosus showed euphausids as the most preferred food during most of the months. Detritus turned out to be the major food items during November in females and during September in males. Foraminifers were found aplenty in the female diet during September, May, January and August. Other crustaceans were present as an important diet during February and April in females and during January in males. Monthly variations in the diet preference of H. woodmasoni showed the predominance of euphausids in some of the months in the gut contents of females (September, January, February, March, April, August and March) whereas foraminifers showed preponderance in October, December, January, July, January and February. In males, euphausids and foraminifers were found equally in most of the months. Detritus was found in significant quantities during September, November and February in females but found in less quantity in males. Echinoderms showed regular occurrence during most of the months in both the sexes especially during May. In H. gibbosus, immature females preferred detritus as the major component (50%), however, with the progression of maturity, the presence of euphausids was regular (Fig. 1). In males, the euphausids and detritus showed regular occurrence at all the maturity stages (Fig. 2). The presence of foraminifera was encountered only in maturing males while sand, molluscs and fish remains were preferred by maturing and spent males. In females of H. woodmasoni, the maturity stages viz., immature, maturing, head roes and spent showed a strong preference towards euphausids while in other maturity stages detritus also showed equal preference (Fig. 3). The foraminifera were found in relatively higher quantities in immature, maturing and spent females whereas the diet of orange berries mostly comprised of glass sponges (33.33%). Copepods and fish remnants were observed in 47 Food and feeding habits of deepsea prawns Fig. 1. Index of preponderance of various food items in different maturity stages of female H. gibbosus Fig. 4. Index of preponderance of various food items in different maturity stages of male H. woodmasoni (53.3%) and sponge spicules (66.7%). Euphausids, detritus and foraminifers were the most favored food items in females of H. gibbosus in 70-79 mm length group. From 80 mm onwards females of H. gibbosus fed on sponge spicules, echinoderms and molluscs. Euphausids were the most preferred food items in males of H. gibbosus of 60-139 mm length group. Stomach conditions Fig. 2. Index of preponderance of various food items in different maturity stages of male H. gibbosus Fig. 3. Index of preponderance of various food items in different maturity stages of female H. woodmasoni Percentage occurrence of various stomach conditions in different maturity stages of H. woodmasoni showed that in females, the occurrence of empty stomachs were high in head roes (20%) where as high percentage of ‘¾ full’ stomachs was observed in orange (75%) and grey berries (60%) due to the voracious feeding, while ‘full’ stomachs could be discernible only in black berries (20%) (Fig. 5). Among male maturity stages of H. woodmasoni, highest percentage of ‘¾ full’ stomachs were observed in spent animals (Fig. 6). The presence of ‘empty’ and ‘1/4th’ stomach conditions were predominant in females of different maturity stages of H. gibbosus viz., immature females (50%) and head roes (52%) whereas higher numbers of ‘full’ stomachs were noticed in spent females (21%) as well as in orange berries (19%). In orange, black and grey berries, high occurrence of ‘½ full’ stomach was appreciable quantities in the diets of maturing females (10.19%) and black berries (34.62%). Euphausids and detritus dominated the diets of immature males (50%) whereas mature males showed preference towards foraminifera, detritus and echinoderms (Fig. 4). Results of size-wise index of preponderance showed that in females of H. woodmasoni, besides euphausids, foraminifera, detritus, echinoderms, fish remains, molluscs and semi-digested matter showed regular occurrence up to 80-89 mm length groups. Small males of H. woodmasoni preferred detritus and euphausids as the major food items and with growth, the preference got shifted to detritus Fig. 5. Variations of stomach condition in female maturity stages of H. woodmasoni S. R. Radhika Rajasree and B. Madhusoodana Kurup 48 Active feeding was noticed in 130-139 mm and 140-149 mm length groups, as manifested by the occurrence of ‘¾ full’ and ‘½ full’ stomachs in these prawns. Incidence of empty stomachs was less in 60-69 mm and 70-79 mm length groups in males and females of H. gibbosus. In male H. gibbosus, the number of full stomachs was invariably high from 120-129 mm to 150-159 mm, showing highest percentage in 140-149 mm (50%) length group. Gastrosomatic index (GSI) Fig. 6. Variations of stomach condition in male maturity stages of H. woodmasoni GSI observed which would manifest their voracious feeding habits after the gonadal maturation process (Fig. 7). In males of H. gibbosus, high percentage of ‘full’ stomachs was observed in spent males (17%) in contrast to the high percentage of ‘empty’ stomachs seen in mature males (33%) (Fig. 8). Variations in the gastrosomatic index observed in males and females of H. woodmasoni commensurating with ovarian maturation process are depicted in Fig. 9 and 10. The feeding intensity was high in immature females (1.59), while it was low in head roes (1.00) Among the three maturity stages of males of H. woodmasoni, the lowest GSI values were recorded in immature males (1.20) in contrast to the high GSI values observed in spent males (3.5). Among various maturity stages of H. gibbosus, the highest GSI values were observed in immature and spent specimens of both females and males while it was lowest in matured males and head roe females. 4 3.5 3 2.5 2 1.5 1 0.5 0 H. woodmasoni H. igibbosus Immature Headroe Grey berry Spent Maturity stages Fig. 7. Variations of stomach condition in female maturity stages of H. gibbosus Fig. 9. Variation of gastrosomatic index in female maturity stages of H. woodmasoni and H. gibbosus 5 GSI 4 3 H. woodmasoni 2 H. igibbosus 1 0 Immature Maturing Spent Maturity stages Fig. 10.Variation of gastrosomatic index in male maturity stages of H. woodmasoni and H. gibbosus Discussion Fig. 8. Variations of stomach condition in male maturity stages of H. gibbosus In males of H. woodmasoni, empty stomachs were noticed in the length groups 80-89 mm, 90-99 mm, 110-119 mm and 120-129 mm while in female H. woodmasoni, the empty stomachs were more in 80-89 mm, 90-99 mm and 100-109 mm length groups. The results of stomach content analysis have shown that the food of pandalid shrimp H. woodmasoni consisted of two major groups viz., euphausids and foraminifera whereas H. gibbosus feeds mainly on euphausids. Belogrudov (1973) stated that the most preferable food components of pandalids were crustaceans whereas polychaetes and molluscs formed the least preferred food items. The presence of detritus, euphausids and mixture of 49 Food and feeding habits of deepsea prawns bottom and planktonic organisms in the food of H. woodmasoni and H. gibbosus suggests their greater inclination for bottom feeding habits. Similar observations have been reported by a number of workers in other pandalids. Turpaeva (1948, 1953) reported dominance of flake like detritus mainly composed of fragments of crustacean chitin, foraminifera, polychaetes and planktonic copepods in the gut contents of P. borealis from Barents Sea. Though there exists inter-specific dietary overlap between two species, H. woodmasoni exhibits highly diverse preference for diets. On the contrary, H. gibbosus has a restricted dietary preference as the number of taxa observed in their diet is lesser than that of H. woodmasoni. Though H. woodmasoni and H. gibbosus exhibit nektobenthic behaviour, the depths of inhabitance of both the species differ significantly and this may be attributed to the variation in the dietary preference. H. woodmasoni inhabits comparatively shallower depth zones in the range 200 and 300 m while the distribution of H. gibbosus has been recorded from 300 to 600 m (Suseelan, 1985). As a result of inhabitance in deeper waters and less productive zones, the animals exhibit scavenging behaviour and become more detritophagus (Mary and Ioannis, 1999). The diet of H. gibbosus is predominated by high concentration of euphausids, detritus, other crustacean carcasses and semidigested matter. Sporadic presence of carapace remnants and chewed muscle tissue of pandalid shrimps indicate its cannibalistic behaviour due to lack of food items in its place of inhabitance (Turpaeva, 1953). From the presence of copepods, polychaetes and nematodes in H. woodmasoni and their total absence in the diets of H. gibbosus, it can reasonably be inferred that H. woodmasoni prefers shallower depth zones. This is further confirmed by the presence of trace quantities of euphausids and detritus and predominance of shallow water foraminifers in the gut contents. Mary and Ioannis (1999) reported that there exist strong differences in the dietary behaviour of Plesionika ensis and Polycheles typhlops inhabiting at greater depths than Parapenaeus longirostris and Plesionika heterocarpus from Eastern Mediterranean Sea. The qualitative analysis of food in relation to size showed that there exists significant variation in the diet composition of juveniles and adults of both the species. In H. gibbosus, immature male and female devoured more actively on other crustaceans, sponges and echinoderms, the former up to 80-89 mm and latter up to 100-109 mm where as in adults of both the sexes, a glaring shift in the diet composition was observed towards molluscs, fish scales and nematodes. The percentage composition of foraminifers declined steadily with the increase of length groups and in adults, foraminifera was rarely observed in males and females of H. gibbosus. In H. woodmasoni, juveniles devoured less detritus and more foraminifers than adults and with progression of length groups, the amount of detritus in the diet also showed an increase thus exhibiting more and more detritophagus behaviour with increasing stages of growth. Ivanova (2000) also reported similar findings in the diets of P. borealis from Flemish Cap in north Atlantic. Sex-wise analysis of food preference in various length groups showed that in females of H. gibbosus and H. woodmasoni the higher length groups showed more selectivity in comparison with their males. Females of H. woodmasoni showed preference to detritus, euphausids and other crustaceans where as males preferred euphausids, detritus, foraminifers and other crustaceans. In H. gibbosus, females preferred euphausids, nematodes and sand particles whereas non-selective feeding was observed in males by the occurrence of diverse number of diets than females. Ivanova (2000) noticed slight difference in the diets of both the sexes of P. borealis where males showed rich diversity of dietary preference. In contrast, females exhibited only a narrow range of dietary variation. Maturity stage-wise feeding intensity of H. gibbosus and H. woodmasoni indicated that in both the species, highest number of empty stomachs was observed in head roes of females and matured males. Voracious feeding habit in females after oviposition was observed as evidenced by the occurrence of highest number of ‘full stomachs’ and ‘3/4full’ stomachs in the orange berry to black berry stages. This finding strongly corroborates with that of Suseelan (1985) who reported highest frequency of empty stomachs in ovigerous females. The feeding intensity studies also showed that occurrence of ‘trace’ stomachs were high in all the months. This might be due to the faster digestive rates of carnivores (Qasim, 1972) or may be due to regurgitation while removing from deeper waters (Job, 1940). Low feeding intensity of head roes and matured males are further explained on the basis of their lower gastrosomatic index. In H. woodmasoni and H. gibbosus, higher GSI values were observed in spent males whereas in females, the GSI values were maximum in orange berries and spent females. The lowest values recorded in head roe females have been attributed to less space in the cephalic region due to the fully developed ovaries thus affecting food intake (Weinberg, 1980). Acknowledgements The authors are grateful to the Director, School of Industrial Fisheries, Cochin University of Science and Technology for providing necessary facilities to carry out the work. S. R. Radhika Rajasree and B. Madhusoodana Kurup References Allen, J. A. 1959. On the biology of Pandalus borealis Kroyer, with reference to a population off the Northumberland coast, J. Mar. Biol. Ass. U. K., 38 (1): 189-220. Allen, J. A. 1963. Observations on the biology of Pandalus montagui (Crustacea: Decapoda). J. Mar. Biol. Ass. U. K., 43 (3): 665-682. Belogrudov, E. A. 1973. On feeding of commercial shrimps in different regions of the Far Eastern seas. Fish. Res. Board Can. Transl. Ser., 9. Berenboim, B. I. 1981. Feeding of northern shrimp in Barents Sea. Biol. Morya, 5: 28-32. Berenboim, B. I. 1992. 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