[advances in marine biology] the biology of the penaeidae volume 27 || 11. predation on penaeids

11. Predation on Penaeids

1. Penaeids as Prey

Juvenile and adult penaeids are attractive as food for predators; their energy content (4.6 kJ/g live weight) is higher than that of polychaetes (3.6 kJlg), gastropods (1.4 kJ/g), bivalves (1.6 kJ/g) or echinoderms (2.2 kJ/g) (Thayer et al., 1973). Although fish have an even higher energy content (6.5 kJ/g) (Whitfield, 1980) and would appear to be more attractive as prey, most fish are more active and swim faster than penaeids and so they are probably more difficult to catch. In addition, fish are more wary of predators, and an approach by a predator elicits an escape response more frequently in fish than in penaeids (Minello and Zimmerman, 1984).

Predation is probably the major cause of natural mortality in juvenile and adult penaeids. The extent of natural mortality varies markedly between the three phases of the life cycle (Table 11.1). The highest rates are in the larval stages and the lowest are in the adult stages.

TABLE 11.1. Habitat, length of stage (duration) and rate of mortality of three stages in the life cycle of penaeids.

Stage Habitat Duration Rate of mortality

Larvae Offshore 2-3 weeks Very high, >70%lweek Juvenile Inshore 2-3 months High, 1&25%/week Adult Offshore 8-20 months Moderate, 2-10%/week

A. Predation on Larvae

The rate of mortality of larvae has seldom been estimated but it is probably extremely high. Only about 0.05% of the population of P. duorarum survives the 35 days from hatching to reaching the nursery

357

358 BIOLOGY OF PENAEIDAE

grounds (Munro et al., 1968). Predation is not, however, the sole or even necessarily the major cause. Many never reach the nursery grounds (Rothlisberg et al., 1983a) and, as is the case for fish larvae, many probably starve to death because their food is patchily distributed and they cannot swim far without feeding (see review by McGurk, 1986).

The major predators of penaeid larvae are likely to be ctenophores, scyphozoan and hydrozoan medusae, chaetognaths, crustaceans and fish. Although penaeid larvae are much the same size as many abundant planktonic crustacea (see Chapter 7) and are therefore likely to be preyed upon by planktivores, they are only a very small proportion of the plankton. In the Gulf of Carpentaria for example, penaeid larvae make up only 0.001% of the live volume of plankton (CSIRO, unpublished estimates). They are probably not, therefore, a major component of the diet of planktivores and they may well be missed in dietary analyses. Marichamy (1972) did, however, find that up to 50% of the anchovy Thryssa baelama had planktonic stages of prawns in their guts.

B. Predation on Juveniles

Once postlarvae and juveniles reach inshore nursery areas, they are exposed to several causes of mortality: biotic factors such as predation and disease as well as abiotic factors such as hypoxia and low temperature. The nursery areas inhabited by juvenile prawns are mainly shallow estuaries and intertidal flats. These areas support large populations of fish, cephalopods and birds that feed on benthic animals. The very high incidence of postlarvae and juveniles in the guts of some predatory species is an indicator of the extent of this predation. Late larvae and early postlarvae were found in 10-30% of juvenile (37-120 mm) cutlassfish (Trichiurus lepturus) in Indian waters (Narasimham, 1972). Postlarval P. aztecus (8-16 mm total length) made up 15-25% of the diet of juvenile (70-99 mm total length) red drum (Sciaenops ocellatu) in inshore areas of the Louisiana coast of the Gulf of Mexico (Bass and Avault, 1975). Red drum is one of the most abundant fish in this region and probably exerts considerable predation pressure on postlarval penaeids. Juvenile penaeids contributed 19-32% of the total energy intake of the estuarine stages of four species of juvenile carangids in southern African estuaries (Blaber and Cyrus, 1983). Penaeids were found in the stomachs of 37 out of 77 fish species in a tropical estuary in northern Australia (Salini et al., in press). Edwards (1978) estimated that 90% of juvenile P . vannarnei died in the 6-12 weeks they spent in lagoons in Mexico. He considered that this natural mortality is due to predation.

PREDATION ON PENAEIDS 359

C . Predation on Adults

When penaeids move out of shallow inshore areas into deeper water, the rate of mortality drops. As adults they have the lowest mortality rate of their life cycle. This decline in mortality rate probably reflects a reduction in predation. Most birds that prey on prawns feed in shallow water, not in deep water. Many juvenile fish that feed on penaeids switch to feeding on fish as adults (see below). The predation pressure on penaeids therefore decreases as they move offshore. Nevertheless it is still high. Garcia and Le Reste (1981) calculated from 16 estimates of the natural mortality of eight species of adult Penaeus and Metapenaeus that the rates ranged between 10 and 36% per month. Edwards (1978) reported similar monthly rates (&21%) for three Mexican species (P . californiensis, P . stylirostris, and P. vannamei).

II. Predators of Penaeids

A. Coelenterates

Coelenterate medusae may have a major impact on populations of copepods and fish larvae (Moller, 1980) but the extent to which they prey on planktonic stages of penaeids is not known. Cubomedusae are common in ,estuaries in southeastern Asia and northern Australia and probably come into contact with juvenile penaeids. Barnes (1966) found experimentally that small stings from cubomedusae caused an escape response in P. merguiensis but did not kill them even when repeated. Prawns exposed to a stronger sting were immobilized and took 15-20 min to recover, long enough for a medusa to capture them. However, a review of the diet of seven species of cubomedusae, shows no predation on penaeids, although they do feed on carids and mysids (Larson, 1976).

B. Cephalopods

Nixon (1987), in a review of the diet of cephalopods, pointed out that cephalopods are active carnivores feeding mainly upon crustacea, molluscs and fish. Cephalopods may be significant predators of penaeids, but few studies have been made of the diet of species found in areas supporting large populations of penaeids. Analysis of the gut contents of large samples (>400) of two Sepiodea (Sepia aculeata and Sepiella inermis), and one loliginid (Loligo duvaucili), gives an indication of the


possible extent of predation from this source (Oommen, 1977). Crusta- ceans were the largest food group in Sepia aculeata and the second largest group in the other two species. In all three cephalopods, species of Meta- penaeus and Penaeus were the most common component of the crustaceans. Najai and Ktari (1974, quoted in Nixon 1987) found Penaeus sp. to be one of the major prey items of Sepia officinalis from the Bay of Tunis.

The predatory behaviour of cuttlefish (Sepia officinalis) on carid shrimp (Leander sp.) described by Wilson (1946) and Messenger (1968) is probably also applicable to penaeids. Cuttlefish respond to visual, but not to chemical cues. Regardless of the angle of approach, the cuttlefish oriented itself so that its tentacles and arms faced the prey. When it was within a mantle-length of the prey it shot its long tentacles forward reaching the prey in about 32 ms. These attacks were very accurate; 81% of first strikes were successful. Captured shrimp were bitten on either side of the abdomen and usually died within 5 s from the neurotoxin injected by the cuttlefish. All but the antennae and rostrum was eaten. In captivity, Sepia officinalis (80-120 mm dorsal mantle length) ate five or six shrimp (55-63 mm total length) a day. Squid appear to prey on prawns in a similar manner (Fields, 1965).

C. Crustaceans

Mantis shrimp (stomatopods) and crabs (brachyurans) are known to attack and feed on penaeids. Hamano and Matsuura (1986) established that the mantis shrimp Oratosquilla orutoria preyed on penaeids including Trachypenaeus curvirostris in Hakata Bay, Japan. The mantis shrimp preferred particular sizes of penaeids because of the geometry and size of their raptorial second maxillipeds. When mantis shrimp became aware of a prey animal, they emerged from their burrow and approached the prey. If the prey was within certain size limits, they unfolded the raptorial claws and jumped at the prey, spearing it with the spines on the claw and grasping it. The attack was extremely rapid taking 0.03-0.3 s from jumping to grasping.

Penaeids made up about 5% of the summer diet of the portunid crab Callinectes sapidus in a Florida estuary (Laughlin, 1982). Prawns were rarely preyed upon by small crabs, but made up to 7.6% of the diet by weight of large crabs (>60 mm carapace width) possibly because large crabs are better able to capture mobile fast moving prey. Hill (1976) showed experimentally that adults of another portunid crab, Scylla serrafa, did not feed on live penaeids even if the crabs were starved for up to 15 days.


D. Fish

Fish are probably the most important and best studied predators of penaeids and there are many reports of penaeids being found in the guts of fish. Unlike the case for invertebrate predators, attempts have been made to assess the extent of fish predation on prawns because of their impact on commercially fished prawns. Even in cases where individual fish eat only a few penaeids, a large population of such fish may exert considerable predation pressure. The sea catfish, Galeichthys [ = Arius] felis, is one of the most abundant fish in inshore waters of the northern Gulf of Mexico. Although Harris and Rose (1968) found on average only 0.6 penaeids per catfish gut, they pointed out that the large numbers of catfish would lead to considerable loss of commercial penaeids. Conversely, species of fish that feed heavily on penaeids may be present in only small numbers and consequently not have a major impact on penaeid populations.

Many fish that eat penaeids also feed on other natant decapods. Thus penaeids, mysids and carids may be interchangeable in the diet. Gunn and Milward (1985), for example, found that Sillago sihama, which had been feeding heavily on penaeids, switched to the sergestid Acetes australis when these became abundant in their habitat. The barramundi (Lutes calcarifer) fed on penaeids in salt water but switched to palaemonids in fresh water (Davis, 1985).

1. Species of fish preying on penaeids

Without attempting to compile an exhaustive list of records of fish that eat penaeids, we have identified 19 families containing species in which penaeids were found in at least 25% of the sample examined at some time of the year (Table 11.2). These include sciaenids, pomadasyds, sparids, synodontids, serranids and bothids - all families of bottom fish commonly found in the same areas as penaeids (Sheridan et al., 1984). The carangids, pomadasyds and sciaenids each contain at least four different species that prey heavily on penaeids (Table 11.2). Because of considerable regional differences, no one family of fish can be singled out as the most important predator of penaeids. The sciaenids appear to be the most important predators of prawns in estuaries of the Gulf of Mexico, where penaeids have been identified as a major dietary component of Cynoscion nebulosus and Sciaenops ocellata by numerous authors (see review by Minello and Zimmerman, 1983). In the Gulf of Carpentaria, Brewer et al. (1989), found that a carangid, Caranx bucculentus, was the most important predator of penaeids.

TABLE 11.2. Family, species and age category of fish that feed on penaeids and the frequency with which they occur in their diet. Records are drawn from studies in which a minimum of 25 fish were examined and in which penaeids were found in at least 25% of the sample. Where possible, the size classes (cm total length) and age category, J (Juvenile) or A (Adult) of fish

are given. Scientific names have been altered where necessary to reflect current taxonomy.

Family and species

Fish length Fish stage Frequency of Source (cm> occurrence

(Yo )

Ambassidae (glass perchlets) Ambassis commersoni

Ariidae (catfishes) Arius felis Arius proximus Arius thalassinus Arius thalassinus

Bothidae (flounders) Pseudorhombus arsius

Carangidae (kingfish, jacks) Alepes djedaba Caranx bucculentus Caranx ignobilis Caranx ignobilis Caranx melampygus Caranx papuensis Caranx sem Caranx sexfasciatus Caranx sexfasciatus

15-29 - - -

- 31-120 -

JIA

JIA A A JIA

J J J J J J J J JIA

3-73

2 4 8 main

3 1 4 4

34

40 30 main 42 41 25 43 main 3 1-64

Nair and Nair, 1984

Sheridan et al., 1984 Blaber, 1980 Blaber, 1980 Mojumder, 1969

Euzen, 1987

Blaber and Blaber, 1980 Brewer et al., 1989 Blaber, 1980 Blaber and Cyrus, 1983 Blaber and Cyrus, 1983 Blaber and Cyrus, 1983 Whitfield and Blaber, 1978a Blaber and Cyrus, 1983 Mojumder, 1969

Clupeidae (herring) Harengula abbreviata Illisha elongata

Centropomidae (barramundi) Lates calcarifer Lates calcarifer

Elopidae (ladyfishes) Elops machnata

Engraulidae (anchovies) Thryssa baelama Thryssa hamiltoni

Merlucciidae (hakes) Urophycis floridana

Platycephalidae (flatheads) Grammoplites scaber

Polynemidae (threadfins) Polydactylus multiradiatus

Pomadasydae (grunts) Orthopristis chrysoptera Pomadasys argenteus Pomadasys kaakan Pomadasys olivaceum

Sciaenidae (drums) Argyrosomus hololepidotw Cynoscion arenarius

J/A -

33 main

Blaber and Blaber, 1980 Ahmed and Al-Mukhtar, 1982

4-20 - J/A J

3646 59

Davis, 1985 Russel and Garrett, 1985

A 10-70 Whitfield and Blaber, 1978a

14 -

A A

50 96

Marichamy, 1972 Blaber and Blaber, 1980

10-20 J 55-67 Divita et al., 1983

8-30 J/A 12-90 Kuthalingam, 1970

J 68 Blaber and Blaber, 1980

26-80 -

J/A J/A J A

80 main main 30

Carr and Adams, 1973 Blaber, 1980 Blaber, 1980 Cockroft and Emmerson, 1984

J/A J

10-70 44

Whitfield and Blaber, 1978a Sheridan and Trimm, 1983

TABLE 11.2. continued

Family and species

Fish length Fish stage Frequency of Source (cm> occurrence

(Yo)

Cynoscion arenarius Cynoscion arenarius Cynoscion nebulosus Cynoscion nothus Cynoscion nothus Menticirrhus arnericanus Micropogonias undulatus Micropogonias undulatus Micropogonias undulatus Micropogonias undulatus Nibea soldado Otolithes ruber Otolithes ruber Sciaenops ocellata Sciaenops ocellata Stellifer lanceolatus

Serranidae (seabass) Centropristis philadelphica Diplectrum bivattatum

Sillaginidae (whitings) Sillago siharna Sillago sihama Sillago siharna

13-24 3-3 1

8-22 3-28

11-28 9-12 9-35

12-32

-

-

- - - 7-10

19-78 7-1 1

8-20 9-12

- - -

J JIA J J J/A J J J/A O+/J J/A J J

J JIA

-

-

J J

JIA JIA J/A

77-88 2 4 8

30-77 26-42 0-47

2242 29 17-41 35 0-100 main main main 15-25 3144 35

29-50 50-59

main

44 -

Divita et al., 1983 Sheridan et al., 1984 Pearson, 1929 Divita et al., 1983 Sheridan et al., 1984 Divita et al., 1983 Divita et al., 1983 Overstreet and Heard, 1978b Sheridan and Trimm, 1983 Sheridan et al., 1984 Blaber, 1980 Blaber, 1980 Ahmed and Al-Mukhtar, 1982 Bass and Avault, 1975 Overstreet and Heard, 1978a Divita et al., 1983

Divita et al., 1983 Divita et al., 1983

Blaber, 1980 Radhakrishnan, 1957 Gunn and Milward, 1985

Sparidae (breams) Diplodus sargus - Rhabdosargus globiceps -

J 68 A 54

Synodontidae (lizardfishes) Synodus foetens 15-20 - 38

Cockcroft and Emmerson, 1984 Cockcroft and Emmerson, 1984

Divita et af.. 1983

Teraponidae (tigerfishes) Pelates quadrilineatus - Terapon jarbua -

Trichiurus lepturus - Trichiuridae (cutlassfish)

J 28 Blaber and Blaber, 1980 JIA main BIaber, 1980

10-35 Narasimham, 1972 -


Generalizations about diet should not be made at the family level, however, because there can be large differences between species. Blaber and Cyrus (1983) found that in southern African estuaries, penaeids were a major item of diet of four species of juvenile carangids (Caranx ignobilis, Caranx melampygus, Caranxpapuensis and Caranx sexfasciatus), but that juveniles of two other species of carangid (Lichia amia and Scomberoides lysan) from the same estuarine areas rarely ate penaeids. There may even be differences between species in the same genus. The whitings Sillago sihama and Sillago analis both feed on benthic and planktonic prey, but while the guts of up to 44% of the former contained penaeids, no more than 6% of the latter from the same area in Queensland did (Gunn and Milward, 1985). Stokes (1977) found penaeids in 22% of juvenile (10-150 mm) southern flounder (Paralichthys lethostigma) from the Gulf of Mexico, but in only 1% of juvenile Gulf flounder ( P . albigutta). In this case, the difference in diet may relate to habitat preferences of the two flounder, since P. lethostigma is tolerant of low salinity and fine sediments typical of areas inhabited by penaeids, whereas P. albigutta is not found in salinities below 16%0 and prefers coarse sediments.

Most studies of the diet of fish in areas of high penaeid density have either not included elasmobranchs or analysed very few individuals (e.g. Carr and Adams, 1973; Divita et al., 1983; and Rogers (unpublished but results listed in Sheridan et al., 1984)). Little is known of the diets of sharks living in the same areas as large populations of penaeids. Published reports suggest that in the Gulf of Mexico, penaeids either are not eaten or are only rarely found in shark guts. Branstetter (1981), for example, found no penaeids in the guts of a large collection of sharks from the northern Gulf of Mexico. Snelson et al. (1984) found no penaeids in the guts of Carcharhinus leucas from coastal lagoons in Florida. Young sandbar sharks (Carcharhinus plumbeus), that are commonly found in inshore waters of Florida and the Gulf of Mexico, feed on Crustacea but Medved and Marshall (1981) found penaeid remains in only 1.3% of the guts of 80 C. plumbeus they examined. Medved et al. (1985) found no penaeids at all in the guts of a further 414 C. plumbeus. Schmidt (1986), however, found that juvenile (6-22 mm CL) Penaeus duorarum formed a substantial portion of the diet of 18 young (<1 m TL) lemon sharks (Negaprion brevirostris) caught on seagrass flats in Florida. In southern African waters, Bass et al. (1973) found only five of 16 species of carcharhinid sharks examined had eaten penaeids and the average frequency of occurrence was only 5%. By contrast, in inshore waters of northern Australia, prawns are a major dietary item of Carcharhinus cautus and a frequent item in the diet of


Carcharhinus Jitzroyensis (Lyle, 1987). Predation by sharks may also be significant in the Arabian Gulf; Euzen (1987) found that penaeids made up 14.5% by weight of the diet of small (30-90 cm TL) sharks (Carcharhinus spp.) from this areas. Buried penaeids may be especially vulnerable to predation by rays and also to specialized sharks like the nurse shark (Ginglymostoma cirrutum) that use a strong suction pressure generated in the pharyngeal cavity to feed on benthic invertebrates (Tanaka, 1973). There is evidence that rays feed on penaeids. Truchypenaeus curvirostris is eaten by the ray Raja tengu (Kosaka, 1979). Six rays of three species (Dasyafis sabina, Rhinoptera bonasus and Raja texana) from the Gulf of Mexico were found with “their stomachs crowded with [penaeid] shrimp” (Kruse, 1959). Penaeids are an important part of the diet of the ray Himanfura uarnak in the Gulf of Carpentaria (Salini et ai., in press).

2. Variation in predation by fish on penaeids

Seasonal availability of penaeids is reflected in the diets of their predators. In the estuarine St Lucia system in southern Africa, penaeid prawns comprised less than 10% of the diet of Elops machnata and Argyrosomus hololepidotus in winter when prawns were sparse, but up to 70% of the diet in summer when prawns were abundant (Whitfield and Blaber, 1978a). In Indian waters, seasonal peaks in the frequency of penaeids in the diet of the catfish Arius thaiassinus corresponded to periods of abundance of prawns in trawl catches (Mojumder, 1969). In Japanese waters, Kosaka (1977) found that predation by fish on Metupenaeopsis duiei was heaviest in October-April; for the rest of the year they fed on Crangon afinis, reflecting the seasonal availability of the two prey types. In areas where penaeids are available the whole year round, predation is continuous. Postlarvae, juveniles and adults of P. indicus, Penaeus spp. and Mefupenaeus spp. were found in the guts of Ambassis comrnersoni in Indian waters in most months over a two-year period (Nair and Nair, 1984). In some monthly samples, penaeids were the main food item; as many as 40-50 were found in a single stomach.

3. Size of fish preying on penaeids

Fish size influences the extent to which most species feed on prawns. Very small fish feed on penaeids to only a minor extent. Fish around 10-30 cm total length feed heavily on prawns but larger fish do so to a lesser extent. Consequently medium sized species of fish and the juveniles of large species of fish are the chief predators of prawns. About half of


the fish shown in Table 11.2 preyed on prawns only as juveniles; 34% did so both as juveniles and as adults; only 15% did so as adults. Most of these are small species, for example, Ambassis commersoni, Grammoplites scaber, Sillago sihama, Terapon jarbua, and Thryssa hamiltoni are all less than 30 cm in total length as adults.

This pattern of 10-30 cm (TL) fish being the heaviest predators of prawns has been found in many studies. The flathead (Grammoplites scuber) starts feeding on prawns when the fish are around 8 cm long and consumption increases as it grows; it reaches a maximum in the adult fish (Fig. 11.1) (Kuthalingam, 1970). Juvenile, (1.5-2.0 cm standard length), Truchinotis falcatus eat mysids and small penaeids; larger fish eat fish and crabs (Carr and Adams, 1973). The sciaenid Cynoscion nebulosus when smaller than 10 cm TL, feeds primarily on carids; when larger than 10 cm they mainly eat penaeids but above 30 cm, they feed chiefly on other fish (Moody, 1950). The pomadasyd Haemulon plumieri feeds initially on copepods but switches to mysids and prawns when over 3.6 cm long (Carr and Adams, 1973). Barramundi (Lutes calcarijer) less than 4 cm total length, feed almost exclusively on small crustaceans such as copepods and amphipods (Davis, 1985). Above this size they eat mainly macrocrusta- ceans, including penaeids, which were found in the guts of 3646% of fish between 5 and 20 cm long (Fig. 11.1). The incidence of penaeids declined in larger fish; these were almost exclusively predators of fish. Penaeids made up 30% by weight of the diet of the carangid Caranx bucculentus of less than 120 mm TL but declined to only 10% of the diet of fish larger than 335 mm TL (Brewer et al., 1989). At this size, 70% of their diet was other fish. A consequence of the switch away from prawns by larger fish is that predation on large penaeids is low in the absence of large fish. The low levels of predation by fish on adult commercial penaeids in the northern Gulf of Mexico (Divita et al., 1983) are probably due to a scarcity of large fish in the region.

As shown above, many species of fish that grow to a large size tend to feed less on crustaceans and more on fish as they become adult. This switch to a higher energy fish diet may result from the greater ability of large fish to catch prey having a high mobility. Most predatory fish use a combined biting and sucking action to catch prey. The volume of the buccal cavity and hence the volume of water sucked into the mouth, is a cubic function of length, and so large fish are more effective at sucking in prey. Brewer et al. (1989) found a significant positive relationship between mouth width of the predatory fish Caranx bucculentus and the carapace length of penaeids in their guts. As Caranx bucculentus grows, it switches from smaller species (<110 mm TL) to larger species (>150 mm


9

110

Total length (cm)

FIG. 11.1. Percentage frequency of occurrence of penaeids in the diet of Grammoplites scuber and Lutes calcarifer of different sizes. Data on G. scuber from Kuthalingam, 1970, on L. calcarifer from Davis, 1985.

TL). Many fish swallow their prey whole; this puts an upper limit on the size of prey eaten. When Cynoscion nebulosus were offered a range of P. aztecus, they preferred prawns between half and one third of their own length (Minello and Zimmerman, 1984). Kakuda and Matsumoto (1978) found a direct relationship between the length of white croaker (Argyrosomus argentatus), and the length of their prey (fish and prawns). White croaker generally ate prey that were about a third of their own length. When croaker reached about 20 cm, they fed only on fish; thus prawns larger than about 6-7 cm total length would not be preyed upon by this species. There is a significant correlation between length of the barramundi (Lutes calcarifer) and length of prey in six out of eight families of prey fish (Davis, 1985): most of the prey were about 30% of the length of the predator. Euzen (1987) did not find a significant relationship between the size of penaeids and Acetes eaten and that of either of two of their predators (Saurida spp. and Pseudorhombus arsius) from the Arabian Gulf.

In areas with few large but many medium-sized fish, there could be heavy predation on small species of penaeids and on juveniles of the larger species. This possibility appears to be supported by field data. In the northern Gulf of Mexico, the penaeids found in fish guts are usually species that do not reach a large size (Sheridan and Trimm, 1983). Sheridan et al. (1984) cited an unpublished study by Rogers of the diets of


26 abundant offshore fishes in the Gulf of Mexico: none had eaten prawns of the genus Penaeus but they had eaten species of Sicyonia, Solenocera, Parapenaeus and Trachypenaeus that are smaller than the species of Penaeus. Divita et al. (1983) analysed the gut contents of fish collected from shrimp trawls off the Texas coast in June and July - the period when P. aztecus migrates from estuarine to offshore waters. Fifty of the 81 species of fish examined did not feed on penaeids. The most commonly eaten penaeids were Trachypenaeus spp., Sicyonia spp. and P. aztecus. They found 302 Trachypenaeus spp. in 28 fish species, 52 Sicyonia spp. in 13 fish species and only 13 P. aztecus in six fish species although P. aztecus was the most common penaeid caught in trawls in the survey area. These results indicate a higher level of predation on small penaeids (Trachypenaeus and Sicyonia), confirmed by the observation that the smallest Sicyonia were the most heavily preyed on. Sheridan et al. (1984) reported that Trachypenaeus (weight 4-6 g) were found in 4% (n = 7374) of fish guts examined from the Gulf of Mexico, whereas P. aztecus (weight 10-37 g) were found in only 0.18% of fish guts. Similarly, the penaeids eaten by fish in Japanese estuaries are chiefly the small species; the large commercially exploited prawn species are a minor component of fish diets (Kakuda and Matsumoto, 1978). Euzen (1987) claimed that shrimps eaten by fish in the Arabian Gulf are mainly smaller than 90 mm (TL) and most predation is on shrimp of 30-60 mm TL. A drawback of most of these studies is that fish samples were collected in prawn trawls. This is not an effective way of catching large fish and so their abundance is seriously underestimated.

In regions where there are significant populations of large fish which feed on penaeids, the extent of predation may be massive. In Kuwait waters, fin fish are estimated to eat 6000 t of prawns annually; this is about three times the weight taken by the commercial fishery (Pauly and Palomares, 1987). Because the fishery takes mainly adult prawns of the large species whereas the fish concentrate on small prawns - chiefly of non-commercial species, the difference between the numbers of prawns taken is far larger; fish are estimated to consume about 11 000000 prawns annually, this is 61 times the number taken by the fishery. Pauly and Palomares (1987) appear to assume that all the penaeids taken by fish are commercial species. Euzen (1987), however, has shown that small non- commercial species probably form the bulk of the diet. Consequently the impact of fish predation may not be as large as postulated. Pauly (1982) found a significant negative relationship between the standing stock of fish and the recruitment of penaeids in the Gulf of Thailand. When the biomass of fish was high, the level of predation on penaeids by large fish


and the competition from small fish for food were sufficient to reduce survival in the prawn population. In the eastern Gulf of Carpentaria, an abundant population of large predatory fish appears to consume a similar weight of adult commercial prawns to that taken by the commercial fishery (CSIRO, unpublished information). Thus, even though many fish switch to a diet of fish as they grow, predation by fish can be sufficiently large to make a major impact on prawn populations. This has led to suggestions that commercially fished populations of penaeids could benefit from removal of their predators (Pauly and Palomares, 1987). Edwards (1978) has proposed intensifying the fishery for the predatory catfish Galeichthys caerulescens in lagoons on the Pacific coast of Mexico to reduce the extent of predation on penaeids.

E. Reptiles

None of the many species of marine reptiles appear to be significant predators of penaeids. Juvenile (up to 180 cm total length) salt water crocodiles (Crocodylus porosus) in northern Australia, feed on crustacea and insects, but penaeid remains were found in the stomach of only one individual of the 289 examined by Taylor (1979). Sea snakes are abundant in many areas in the Indo-Pacific region in which penaeids are found but they feed almost exclusively on fish (McCosker, 1975). In a review of information from 1063 gut content analyses from 39 species of sea snakes, Voris and Voris (1983) recorded “shrimps” in the diet of only two species. The incidence was low in both cases: 5% in Aipysurus laevis and 1% in Enhydrina schistosa.

No species of turtle appears to feed to any significant extent on penaeids. The most abundant turtle in inshore areas also inhabited by penaeids is the green turtle Chelonia mydas. This species is almost exclusively herbivorous with animal material (chiefly sponges) making up less than 1.5% of the diet (Mortimer, 1981; Garnett et al . , 1985). Coelenterates and molluscs appear to be the main components of the diet of most other turtle species (Hughes, 1974; Den Hartog, 1980).

F. Birds

Marine birds are important and abundant predators of fish in many regions of the world and they probably also take large quantities of penaeids in some regions. Analysis of the diet of waterbirds in estuaries and mangrove swamps in West Bengal showed heavy predation by herons


on Mefapenaeus brevicornis and M . monoceros (Mukherjee, 1971). He found remains of 267 metapenaeids in 76 grey heron (Ardea cinerea), 46 metapenaeids in 70 purple heron (Ardea purpurea), 28 metapenaeids in 26 little green heron (Butoroides striatus) and 71 in 105 Indian pond heron (Ardeola grayii). All four species of herons hunt in shallow water amongst mangroves and reeds. Mukherjee found the remains of only two metapenaeids in 78 night heron (Nycficorax nycticorax).

The St Lucia estuarine system in southern Africa, which has large populations of penaeids (Forbes and Benfield, 1986b), was the site of a major study of the diet of wading, swimming and diving birds (Whitfield and Blaber, 1978b, 1979a, b). Remains of small crustaceans, mostly penaeids, were found in 75% of 122 regurgitated pellets of the little egret (Egretfa garzeffa). Little egret feed in shallow water where they use a disturb-and-chase foraging strategy. Penaeids are eaten to a lesser extent by great white egret (Egretfa a h ) and grey heron (Ardea cinerea), both of which feed in slightly deeper water and either stand still waiting for prey to come past, or search slowly over the bottom. Goliath heron (Ardea goliafh) feed in even deeper water and do not eat any crustaceans. The swimming birds (cormorants and pelicans) do not take any penaeids. Amongst the diving birds, the fish eagle (Haliaeetus vocifer) and Caspian tern (Hydroprogne fschegruva) do not feed on crustaceans but crustacean remains were present in 10% of 61 pellets of the pied kingfisher (Ceryle rudis). This species feeds mainly in the shallow margins within 50 m of the shore. These studies suggest that penaeids in very shallow water are vulnerable to bird predation, but prawns in deeper water are unlikely to be eaten by birds.

G. Mammals

The distribution of some species of small Cetacea, such as the dolphins, overlaps with that of penaeids. However, little is known of the diet of dolphins; most reports are based upon beach strandings or from accidental deaths, consequently sample sizes are small. Leatherwood (1975) found a strong association between dolphins (Tursiops spp.) and prawn trawlers. The dolphins followed working trawlers and appeared to feed on animals disturbed by the action of the trawls and on material discarded from catches. Since discarded material can include non- commercial species of penaeids as well as damaged or recently moulted commercial species, gut contents of dolphins from areas where trawling takes place cannot be used for deciding whether or not dolphins normally


feed on penaeids. Racek (1959) reported that the stomach of a beach- stranded dolphin in New South Wales was entirely filled with adult king prawns (Penaeus plebejus). Since this record predates the advent of large- scale offshore prawn trawling in the area, it appears that this dolphin had been capturing penaeids. The black porpoise (Neophocaena phocanoides) is found along the southern coasts of Asia in coastal waters, estuaries and rivers. Analyses of the gut contents of Neophocaena from Pakistan (no numbers given) showed they feed mainly on P. merguiensis and P. penicillatus (Pilleri and Gihr, 1975). These authors link an annual inshore migration of these porpoises in Pakistan and the Persian Gulf with the seasonal abundance of prawns, suggesting that prawns may be a significant component of the diet of black porpoise.

The African water mongoose (Atilax paludinosus) is a nocturnal predator that lives along the margins of bodies of water. Penaeids were a common food item of A. paludinosus from estuarine areas (Whitfield and Blaber, 1980)

111. Defence Against Predators

This review has identified three groups of animals as significant predators of penaeids: cephalopods, fish and birds. Cephalopods and birds are chiefly visual predators, although cephalopods may also be able to hear (Hanlon and Budelmann, 1987). Most fish use vision for finding prey, and also have a lateral line system for detecting low-frequency vibrations. Their chemosensory abilities are well developed: distance chemoreception (scent) using the nostrils, and contact chemoreception (taste) by the lips (Norman and Greenwood, 1975). In fish such as catfish, the chemo- receptors extend onto the barbels enabling them to detect benthic prey encountered while swimming even in the dark or in turbid water.

These predators are all larger than their prey, and well equipped to immobilize prey rapidly. The penaeid defence against these three groups of predators appears to lie mainly in reducing their visibility, using escape movements when attacked. In addition it is advantageous to minimize the production of vibrations and chemicals that could be used by predators for locating prey. Visual defence by penaeids has received considerable attention; the production of sound vibrations by penaeids does not appear to have been investigated, and there is little information on chemical detection of penaeids by predators.

The juvenile stages of many penaeids are found in vegetation such as seagrasses or Spartina and this makes them difficult to see. Disruptive


colouring, especially stripes or bars, assist in camouflage. Minello and Zimmerman (1983) found that the presence of artificial Spartina reduced predation by two species of fish (Lagodon rhomboides and Micropogonias undulatus), on juvenile P. aztecus. In another experiment, they found that Micropogonias undulatus fed more frequently on P. setiferus than on P. aztecus when artificial Spartina was present but no preference was seen in the absence of cover (Minello and Zimmerman, 1985). The authors suggested that the fish were not selective in their predation, but preyed on them equally when no cover was available. When cover was present, P. aztecw spent more time in cover than did P. setiferus which reduced its exposure to predation. Experiments with killifish (Fundulus heteroclitus) as predator and a carid (Palaemonetes pugio) as prey, showed that provision of seagrass shelters with high density (674 shoots/m2) reduced predation whereas at lower shoot densities (464 shoots/m2) predation rates were not significantly different from controls with no seagrass shelter (Heck and Thoman, 1981). Bell and Westoby (1986a), however, found no significant difference in the number of P. plebejus in control seagrass (Zostera capricorni) plots and in those in which the cover was reduced by one-third. Bell and Westoby (1986b) claim that higher abundances of prey animals in seagrass beds are due to habitat preference and not to greater survival because of reduced predation, although they recognize that predation pressure may have influenced habitat preference. This would imply that there is selective advantage in seeking cover. Penaeus plebejus is fairly commonly found in habitats without seagrass cover (Young, 1978), and so it is not a good species to test the effect of variations in the degree of seagrass cover.

Main (1987) argued that physical structures such as seagrass do not in themselves protect prawns from visual predators. The potential prey must take avoiding action by hiding behind the structures. An avoidance behaviour is thus an important component of sheltering in structured habitats (Main, 1987). The effectiveness of penaeid defence strategies in seagrass is supported by the finding that only one of 21 species of fish from seagrass beds in Florida fed mainly on penaeids while a further three fed mainly on penaeids and mysids (Carr and Adams, 1973).

Visual predators require light and fairly clear water to see their prey. In captivity, the cuttlefish (Sepia oficinalis) did not capture prey shrimp in total darkness, but did so within 5s of a dim light being switched on (Messenger, 1968). Movement of the prey is also important to many visual predators, as demonstrated in the predatory fish (Lagodon rhomboides) which rarely struck at stationary shrimp (Main, 1987). The behaviour pattern adopted by many penaeids of remaining buried in the


substratum during the day and emerging at night could be a defence against visual predators, since the prawns are active in the dark when they are least visible (Fuss and Ogren, 1966). Burrowing in the substratum removes the prawn from the visual field of predators. This has been tested experimentally with the spotted sea trout Cynoscion nebulosus, a major predator of juvenile penaeids in Texas waters. When given a choice between P. aztecus and juveniles of a prey fish, Cynoscion nebulosus fed exclusively on P. aztecus if there was no substratum into which the prawns could burrow (Minello and Zimmerman, 1984). Predation on the penaeids was reduced if they could burrow. Minello et al. (1987) subsequently showed that predation by southern flounder (Paralichthys lethostigma) and by pinfish (Lagodon rhomboides) on P . aztecus was significantly lowered if sand was available in which the prawns could burrow.

Buried penaeids are vulnerable to predation by some species of fish. Pinfish (Lagodon rhomboides) can successfully attack buried P. aztecus, pulling them out of the substratum by their eyestalks (Minello and Zimmerman, 1983). Fricke (1971) pointed out that cuttlefish (Sepiodea) and some pufferfish (Balistidae, Tetraodontidae and Ostraciodontidae) can blow a jet of water onto the substratum exposing or flushing out prey. Although P. aztecus burrow deeper and more frequently than do P. setiferus, Minello and Zimmerman (1985) found no difference in predation levels by fish on the two species in tanks.

Penaeids can be divided into three groups on the basis of their burrowing response (Penn, 1984). The first group consists of species that live over sandy substrata in clear, brightly lit water. These species would be extremely vulnerable to predation during the day; they are all strongly nocturnal and are always buried during the day and in bright moonlight. Species in this group include P . duorarum, P. latisulcatus and P. plebejus. Prawns in the second group live over more muddy substrata in slightly turbid water. Although this group is also essentially nocturnal, they do occasionally emerge during the day. They have camouflage colouring including vertical stripes. Penn regards this as a more versatile group, able to occupy a wide range of habitats. It includes P. aztecus, P. semisulcatus, P. monodon, P. japonicus and P. esculentus. Minello et al. (1987) showed experimentally that burrowing in one of the members of this group, juvenile P. aztecus, was related to turbidity with a higher proportion burying in clear than in turbid water. The third group is found over muddy substrata. Typical members are P. setiferus, P. indicus, P. merguiensis and P. chinensis [= orientalis]. They seldom burrow during the day and appear to rely upon high turbidity to avoid being


detected by predators. Prawns in this group occasionally show schooling behaviour. able to detect prawns before the latter are aware of them (Minello et al., 1987). Low visibility may allow a predator to approach very close to its prey before being detected. Such predators as fish, which can exert a suction force with the buccal cavity, or cuttlefish that can very rapidly shoot out a pair of tentacles, could possibly approach within striking distance before the penaeid attempts to escape. The backwards jumping response of penaeids is probably their only means of avoiding attacking predators under these circumstances. Penaeus japonicus averaged jumps of 0.8 m at speeds of 172 c d s (KO et al., 1970). The backwards jump is produced by a rapid flexing of the abdomen; this causes it to bend initially down and then the posterior end with the tail fan formed by telson and uropods scoops forward and finally squeezes water out of the space between the abdomen and cephalothorax. As shown by Daniel and Meyhofer (1989), this movement of the abdomen produces a backward movement as well as a strong rotational force that lifts the posterior end of the body and drops the anterior end. The result is that prawns jump backwards and upwards, a movement that may make them more difficult to catch, Prawns are capable of repeated jumps: P. juponicus could make about 40 before exhaustion, and so would be able to move rapidly away from a predator. Thus, provided a prawn becomes aware of a predator in time, jumping could be an effective escape manoeuvre especially in low visibility.

Turbidity reduces predation on prawns by some species of fish. Minello et al. (1987) found that pinfish (Lagodon rhornboides), and Atlantic croaker (Micropogonias undulatus), ate significantly fewer P. aztecus in turbid than in clear water. Neither high turbidity nor darkness guarantees immunity from predation. Minello et al. (1987) found that flounder (Paralichthys lethostigma), caught more P. aztecus in turbid than in clear water, and could catch them in complete darkness. Predatory fish hunting in turbid waters or in the dark, either remain stationary and wait for the prey, or swim more or less at random leading to chance encounters with prey. An important defence against random searching by predators is for the prey species to form schools. Murphy (1980) reviewed the value of schooling to aquatic animals. He pointed out that, because visibility is limited in water, schooling behaviour reduces the probability of contact between predator and prey. The lower the visibility the greater this effect. Penaeus merguiensis can stir up fine sediments by rapidly beating its pleopods while remaining in contact with the bottom. When a school does this, they cause a large cloud of muddy water, reducing visibility and presumably predation. Schooling also confuses a predator by offering a


large number of targets at the same time. Fish and cephalopod predators have less success at capturing schooled than isolated prey (Neil1 and Cullen, 1974).

Most species of fish have well-developed chemosensory abilities and can locate food by detecting amino acids. This ability could be used for finding and recognizing prey in the dark and for locating buried animals. The probability of a potential prey animal being discovered by a fish can be reduced if the prey minimizes excretion of amino acids. Marine decapod crustaceans excrete about 10% of their nitrogenous waste as amino acids (Claybrook, 1983). Penaeids excrete far less than this; in P. esculentus, amino acids represent less than 2% of the total excreted nitrogen (Dall and Smith, 1987). Thus buried prawns release minimal amounts of chemicals that could be a signal to predators.

Fish can be stimulated into feeding behaviour by extracts of penaeids. The stimulus appears to be based on a mixture of amino acids as shown by the response of the pinfish (Lagodon rhomboides) to extracts of P. duorarum (Carr and Chaney, 1976). Rapid closure of wounds through a well-developed blood clotting mechanism is probably of vital importance in reducing predation on damaged crustaceans.

The most prominent passive defences of penaeids are the spines at either end of the body (the rostrum and the telson). However, such spines are not a good defence against some species of fish; Davis (1985) for example, reported finding catfish spines in the gut and inside the body cavity of the barramundi (Lutes calcarifer). Spines do not appear to inhibit cuttlefish or mongoose, both of which discard the rostra when feeding on penaeids.

Penaeids clearly rely upon a wide variety of defence mechanisms against predators. These include hiding in seagrass, burying in the substratum, living in turbid water, restricting active periods to the night, forming schools and having a well-developed jumping response. These mechanisms must contribute to the success of the penaeids in avoiding capture to the extent that numerous species achieve an abundance sufficient to support large commercial fisheries.

[advances in marine biology] the biology of the penaeidae volume 27 || 11. predation on penaeids

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