[advances in marine biology] the biology of the penaeidae volume 27 || 10. behavioural responses to...

10. Behavioural Responses to the Environment

The behaviour of penaeids can be divided into activities related to such physiological functions as feeding, moulting or reproduction, and activities that are responses to such environmental factors as light, tide or temperature. The physiological behaviours are dealt with separately in this book; moulting behaviour is covered in Chapter 6, reproductive behaviour in Chapter 7, and feeding behaviour in Chapter 9. This chapter deals with behavioural responses to environmental factors and with endogenous rhythms. A major manifestation of behaviours are migrations by larvae, postlarvae, juveniles and adults; these are covered in Chapter 8 (Life History).

1. Burrowing, Emergence and Activity

A. Burrowing

Field observations of changes in the catchability of penaeids suggested that most of them burrow in the substratum during the day and emerge at night (Idyll, 1950; Le Guen and Crosnier, 1968; Le Reste, 1970). This behaviour has been confirmed by laboratory observations of P. duorurum (Wickham, 1967; Hughes, 1968; Wickham and Minkler, 1975; Bishop and Herrnkind, 1976) P. esculentus (Hill, 1985), P. juponicus (Miura and Yamaguchi, 1955), P. semisufcutus (Kutty and Murugapoopathy, 1968; Moller and Jones, 1975), and P. vunnumei (Moctezuma and Blake, 1981). In the case of P. duorurum, laboratory studies have been confirmed by direct observations in the field (Fuss, 1964; Fuss and Ogren, 1966).

The two obvious advantages of burrowing are a reduction in energy requirements and defence from predators. Buried penaeids are less active than when they are emerged but stationary (Dall, 1986). Since oxygen demand is related to activity, burrowing reduces the total energy demand. Buried penaeids are also less likely to be preyed upon and so burrowing

333

334 BIOLOGY OF PENAEIDAE

during the day is an important form of defence (see Chapter 11). Because penaeids do not occupy permanent burrows or burrow in the

same place each night, they are not territorial. The method of burrowing has been described for Metupenaeus bennettue (Dall, 1958), M. mucleuyi (Ruello, 1973a), P. duorurum (Fuss, 1964) and P. juponicus (Miura and Yamaguchi, 1955; Otazu-Abrill and Ceccaldi, 1981). Metupenueus mucleuyi and P. duorarum start burrowing by generating a strong current with their pleopods to scour a furrow into which the animals settle. They use their pereopods to hold onto the substratum, to push material away from the body and to pull the body forwards. As they move downwards, the substratum is displaced laterally and upward around the body, which gradually becomes covered. Finally the antennal scales and uropods are used to move and flick sediment over the body to conceal it completely. Penueus duorurum forces its body into the substratum by pulling and pushing with its pereopods whereas M. mucleuyi and P. juponicus also spread and close the antennal scales and uropods to assist in burrowing and covering the body. Williams (1958) reported that P. setiferus tended to leave its long antennae above the surface of the substratum when buried, whereas P. uztecus and P. duorurum usually buried their antennae.

The depth to which penaeids burrow varies with the species; for example Penueus duorurum burrows deeper than either P. setiferus or P. aztecus (Williams, 1958). Metapenueus macleuyi buries itself completely, with its body about 1 cm below the surface of the substratum (Ruello, 1973a). Penueus juponicus lies about 3 cm below the surface with its abdomen nearly horizontal and the cephalothorax inclined upwards, its eyes completely buried and the tip of the respiratory siphon as much as 1 cm below the the surface (Egusa and Yamamoto, 1961). The depth of burrowing by P. duorarum is related to size; at a total length of 110- 120 mm, animals burrowed 27 mm below the surface, whereas at 130- 140 mm TL, they burrowed 40 mm deep (Fuss, 1964).

B . Emergence and Activity

Most prawns emerge at night. While emerged they may move around or remain stationary. Movement is not continuous and P. esculentus, for example, moves for only about 75% of the time that it is emerged (Hill, 1985). In many experimental studies movement or activity rather than emergence is measured. The patterns for activity and emergence may be different. In P. uztecus, emergence shows a unimodal pattern whereas activity is clearly bimodal (Fig. 10.1) (Wickham and Minkler, 1975).

B E H A V I O U R A L RESPONSES TO THE ENVIRONMENT 335

Light Dark Light

0 > ‘& u B 80-

60 -

1 200 1800 1200

FIG. 10.1. A . Pattern of emergence; B. Pattern of activity of Penaeus azfecus under laboratory conditions. Summarized and redrawn from Wickham and Minkler (1975)

Penaeus duorarum (Wickham, 1967), P. esculentus (Hill, 1985) and P. semisulcatus (Moller and Jones, 1975) emerge shortly after dusk; the number that are emerged is highest at this time and then gradually declines over the night. According to Hughes (1969d), emergence in P . duorarum follows a bimodal crepuscular pattern with a peak after dusk and another before dawn. Penaeus azfecus (Wickham and Minkler, 1975), P. duorarum (Reynolds and Casterlin, 1979a) and P. semisulcatus (Moller and Jones, 1975) are most active a few hours after dusk and again near dawn.

The nocturnal emergence of P. duorarum and P. attecus is reported to be the same in “dim” light (3 x lux), but the prawns were more active in dim light (Wickham and Minkler, 1975). This suggests light may inhibit movement and that emergence and activity responses may be triggered by different light intensities.

lux) and “bright” light (3 X


I I . Light

Penn (1984) divided penaeids into three groups on the basis of their burrowing behaviour. Members of the first group live in clear water; they are always burrowed in the day or in bright moonlight and emerge only at night. The group includes P. duorarum, P. latisulcatus, P. plebejus and probably P. brasiliensis and P. notialis. Prawns in the second group live in slightly turbid water; they are nocturnal but occasionally emerge during the day. Species in this group include P. aztecus, P. esculentus, P. monodon, P. japonicus and P. semisulcatus. The third group is found in turbid water and seldom if ever burrows. It includes P. indicus, P. merguiensis, P. chinensis [= orientalis], P. setiferus and probably P. occidentalis and P. schmitti.

The prawns in Penn’s groups are clearly responding to light and to factors that affect light intensity. Three factors can be regarded as the major ones influencing light intensity and thus prawn behaviour; these are diel changes, moonlight and turbidity.

A, Die1 Responses

A diel cycle of emergence and movement is seen even in deepwater penaeids. The catchability of Parapenaeus longirostris from depths around 200 m in the Mediterranean, declines from dawn to midday and then rises again towards dusk (Ghidalia and Bourgois, 1961). Light is the environmental controlling factor in prawns’ burrowing during the day and emerging at night. Moller and Jones (1975), for example, found that although adult (50-100 mm TL) P. semisulcatus follow this pattern, they immediately burrow if illuminated with white light at night. If light is excluded during the day they emerge.

A drop in light intensity during the day can trigger emergence in some species, even amongst those in Penn’s (1984) first group. Fuss (1964) noted that, although P. duorarum was usually buried during the day, it was occasionally taken in trawls in daylight in muddy water or on cloudy days. Carothers and Chittenden (1985) similarly related unusually high catch rates of P. aztecus during the day to high turbidity after storms.

Small changes in the length of day or night do not affect the pattern of emergence. Hill (1985) found no correlation between duration of emergence of adult P. esculentus and the length of the night in the range 10-13 h. Experiments with exceptional lengths of night or day do result in changes of the pattern of emergence. Bishop and Herrnkind (1976), for example, found that the duration of emergence of juvenile (55-60 mm

BEHAVIOURAL RESPONSES TO THE ENVIRONMENT 337

TL) P . duorarum was directly related to the length of darkness in a 24-h cycle which included continuous light and continuous dark as two of the three conditions tested. The average amount of movement in darkness of adult P. semisulcatus and P. monodon kept in a 6 h light:6 h darkness cycle was 50 to 100% greater than when in a 12 h light : 12 h dark or an 18 h light:6 h dark cycle (Moller and Jones, 1975). Moller and Jones suggest this may be a response to forced inactivity during long periods of illumination.

Juvenile penaeids in Penn’s first two groups do not show as strong a burrowing response to light as do adults and so they are more likely to be caught during the day. This has been found for P. aztecus (Joyce, 1965), P. duorarum (Aaron and Wisby, 1964; Fuss and Ogren, 1966), P. esculentus (White, 1975a) and P. vannamei (Moctezuma and Blake, 1981).

B . Moonlight

Racek (1959) found that the catch rates of M. macleayi and P. plebejus were lower around the time of full moon and suggested that this was because they emerged less at this time. As moonlight would not, he thought, penetrate to the depths at which they lived, he argued that the burrowing-emergence cycle had a lunar rhythm. Moonlight can, however, penetrate a considerable distance into the sea (White, 1975a). Ghidalia and Bourgois (1961) found the catch rates of Parapenaeus Eongirostris in the Mediterranean at depths of 156255 m varied over a two-month period; catches were greatest at the time of full moon and lowest at new moon. The authors suggested the prawns move inshore between new and full moon, and offshore between full and new moon.

Juvenile penaeids also show responses to moonlight but these may not be the same as those of adults of the same species. Fuss and Ogren (1966) found that fewer P. duorarum (80-175 mm TL) emerge on bright moonlight nights than on dark nights. This is probably a negative response to bright light. When juvenile P. duorarum are emigrating from estuaries on ebb tides however, they move towards the surface in moonlight (Beardsley, 1970). Juveniles of some species do not show any clear response to moonlight; moon phase does not affect catchability of juvenile P. merguiensis (Staples and Vance, 1979). This species lives in very turbid water where moonlight may provide insufficient light on the bottom for the prawns to respond.

BIOLOGY OF PENAEIDAE

C. Turbidity

Even where the water is clear on the surface, water currents may stir up fine particles, faeces and pseudofaeces causing a zone of high turbidity near the bottom (Rhoads, 1974). Turbidity affects light penetration and, in very turbid waters, the light levels on the bottom may be sufficiently low during the day to induce prawns to emerge. Penaeus duorarum normally burrows during the day (King, 1971) but in very turbid water, there was no difference in day and night catch rates of P. duorarum (Clark and Caillouet, 1975), suggesting that the prawns were continually emerged. Garcia and Le Reste (1981) point out that seasonal changes in turbidity can give rise to apparent rhythms of activity; in the Gulf of Guinea, when turbidity is high, catches of P. notiulis are at a maximum in the day. When turbidities are low and the water is clear, maximum catches are at night.

It is not clear whether penaeids respond directly to turbidity. On the Texas coast, Stokes (1974) found P. aztecus and P. setiferus in turbid water and Penaeus duorarum in clear water. The prawns may have been responding to the muddiness of the bottom and this in turn affected the turbidity of the water. Population densities of P. aztecus are highest in turbidity plumes off the coast of the Gulf of Mexico (Lindner and Bailey, 1968). Although these plumes are not formed by river discharge but by converging longshore currents, they orginate inshore and so could have characteristics other than turbidity to which the prawns are responding.

111. Tides, Currents and Water Depth

A. Tides

Although juveniles of many species of penaeids are found in intertidal areas, there appear to have been no studies of their behaviour in such conditions. Studies of the behaviour of subtidal populations show that some species respond to tides. In an estuary in the Gulf of Carpentaria, juvenile P. rnerguiensis show a strong tidally based pattern of movement that is independent of current (Staples and Vance, 1979). Even in the wet season when there is a continuous unidirectional outgoing current, the prawns still respond to tidal fluctuations. Coles (1979), however, found no difference in catches of juvenile P . plebejus made at ebbing, flooding or slack tides and concluded that there was no significant current- or tide- related change in behaviour in this species.

Under experimental conditions, juvenile P. rnerguiensis and


P. duorarum both respond to raised water level by increased movement and, in the case of P. duorarum, by emerging from the substratum even during the day (Wickham, 1967; Hindley, 1975a). Prawns are sensitive to small changes in pressure: P. duorarum responded when water depth was changed from 10 cm to 40 cm (Wickham, 1967). Postlarval P. japonicus responded to pressure changes of 1-2 kPa by swimming up into the water (Forbes and Benfield, 1986a). Beardsley (1970) found that tidal amplitude did not affect the number of juvenile P. duorarum captured in the water column. The importance of change in water level rather than absolute depth is illustrated by observations of juvenile P. merguiensis. Although they became more active when the water depth was increased by 2 m, there was no difference in activity between prawns kept at constant high pressure (220 cm depth) and those kept at constant low pressure (20 cm depth) (Hindley, 1975a).

B. Currents

Water currents can affect the distribution of prawns indirectly and directly. One indirect effect is that water currents determine the distribution of particles in the substratum. The transition from gravel to sand is associated with currents around 100 c d s and from sand to silt with speeds around 50 c d s (Johnson et al., 1982).

Moderate and strong water currents can affect behaviour directly. Buried P. duorarum show no definite orientation when currents are below 20 c d s , but in faster currents they burrow facing the current (Fuss and Ogren, 1966). Penaeus duorarum exhibit positive rheotaxis in water currents above 20 cm/s and can maintain their position in currents of up to 26 cm/s by swimming against them (Fuss and Ogren, 1966) although they cannot move against a current of approximately 30 c d s (Wickham, 1967). They occasionally swim vertically and are swept along with the current. When stationary on the substratum in a current, P. duorurum lowers the anterior end of its body, lifts its abdomen and spreads its uropods, which help to generate a downward force to prevent it from being swept away. Metapenaeus bennettae and M. macleuyi respond to fast currents (mean 37 c d s ) by burrowing in the substratum (Coles, 1979). Both species spend most of their life in estuaries, and apparently cope with strong tidal currents by avoiding them.

Animals swimming in the water column with no fixed point of reference cannot orient themselves with respect to current direction. Hughes (1969a) noted that juvenile P. duorurum swim against the current in a series of short hops close to the bottom allowing frequent orientation by


contact with the bottom. Individuals swimming with the current tended to remain swimming for long periods or sometimes drifted passively for hours.

C. Water Depth

The most comprehensive study of the depth preference of penaeids is that by Somers (1987), working in the Gulf of Carpentaria. He reported that the highest catch rates for M . endeavouri were in the depth range 20-40 m, for M . ensis in 30-50 m, and for P. longistylus in 45-50 m. Depth accounts for 56% of the variation in the catch rate of P. esculentus. It accounts for 41% of the variation with P. merguiensis and 34% with M . ensis but only 17% with P. semisulcatus, 16% with P. longistylus and 5% with P. latisulcatus.

Adult penaeids from the Gulf of Mexico are also associated with distinct depth ranges. Penaeus aztecus are found over a large depth range - from 18-128 m, P. duorarum from 2446 m, and P. setiferus in water less than 35 m deep (Rulifson, 1981). Not all penaeids show such a restricted depth range. Parapenaeus longirostris is caught from 25 m down to 550 m in the Mediterranean and eastern Atlantic (Ghidalia and Bourgois, 1961).

In some species, the depth range with the highest catch rates is different for juveniles. Juvenile (<20 mm CL) P. esculentus and P. semisulcatus are caught mainly in water shallower than 20 m whereas adult P. esculentus are found down to 30 m and adult P. semisulcatus between 30 and 40 m (Somers, 1987b).

Some penaeids make extensive nocturnal vertical migrations and a few appear to live permanently in the water column, but most species appear to remain near the bottom even when swimming. Coles (1982) found that P. plebejus and M. bennettae are equally distributed at heights of 0-16 cm, 17-33 cm and 34-50 cm above the bottom. He found that M . macleayi is more likely to swim up into the water column when the water is flowing. The height that P. japonicus swim above the bottom is related to size (KO et al., 1970): prawns of 120-150 mm TL were captured at an average height of 160 mm above the bottom; larger sizes (210-240 mm TL) were captured at an average height of 540 mm. Beardsley (1970) found no differences in the vertical distribution by size or sex of juvenile P. duorarum. A few penaeids spend most of the time in the water column; Macropetasma africanus, for example, lives in the water column in the surf zone in southern Africa (Cockcroft and McLachlan, 1986).


IV. Substratum

A. Characteristics of Substrata

Penaeids spend most of their life in contact with the sea bottom. This is a complex environment with many features that may be of importance to penaeids. Bottom structures such as seagrass play a significant role in in defence from predation (see Chapter 11) and in habitat selection.

Juveniles of some species of penaeids are found in association with seagrasses or algae whereas other appear to avoid them. Staples et al. (1985) found P. esculentus and P. semisulcatus almost only in seagrass and algae in an estuary in the Gulf of Carpentaria. Metapenaeus ensis and M. endeavouri were found both in seagrass and on mud banks devoid of vegetation. Penaeus merguiensis was found only on mudbanks. De Freitas (1986) and Hughes (1966) found a similar relationship between juvenile penaeids and habitat in Mozambique. Juvenile P. semisulcatus were found only in association with submerged vegetation whereas P. japonicus was on bare intertidal flats and P. indicus and P. monodon appeared to prefer muddy areas in mangrove swamps. Metapenaeus monoceros was found in a variety of habitats including seagrass and bare mud banks. Little is known about these associations and they require investigation. For example, are all species of seagrass equally attractive or not attractive? Although some species do appear to differentiate between seagrass and algae, others do not. Metapenaeus ensis for example was found on seagrass but almost never on algae whereas M. endeavouri was found on both (Staples et al., 1985).

The substratum itself has several properties that may influence penaeids that burrow into it and feed on it: particle size distribution, pore space and porosity, water content, thixotropy and shear strength, as well as organic content and the presence of other organisms. Although porosity is important in the distribution of other burrowing animals (Webb, 1958, 1969), its possible effect on penaeids has not been investigated. Grain size and to a lesser extent organic content are the only substratum characteristics that have been investigated as factors influencing the distribution of penaeids.

Grain sizes are usually classified on the Wentworth Scale. The particle diameter in each grade is double that of particles in the grade below it. Sand covers the range between 2 mm and 63 ym; silt includes particles between 63 ym and 4 ym; particles smaller than 4 ym are classified as clay. Mud is a mixture of silt and clay, i.e. particles smaller than 63 pm. In this review, the class names defined in Table 10.1 will be used even where this has required the changing of names used by other authors.


TABLE 10.1. Classification of particle sizes according to diameter. (From

various sources).

Particle size

2-65 mm 1-2 mm

0.5-1 mm 250-500 pm 125-250 pm 63-125 pm 31-63 pm 16-31 pm 8-15 pm 4-8 pm <4 pm

Class

Gravels Very coarse sand Coarse sand Medium sand Fine sand Very fine sand Coarse silt Medium silt Fine silt Very fine silt Clay

Substrata are almost always a mixture of particles; the composition of the mixture determines many of its physical properties. Particle size composition is measured by sieving, usually of dried samples. Rhoads (1974) showed that the upper 1-2 cm of marine sediments is extensively modified by benthic animals. These modifications include an increase in organic content, a reduction in shear strength and a rise in effective grain size by aggregation. Drying of the particles before sieving destroys this secondary structure. Morgans (1956) described a wet sieving technique for marine sediments to overcome this problem, but most workers still use dry sieving for particles larger than 63 pm. Particles below 63 pm are analysed by pipetting techniques based upon Stokes’ Law.

Sands, especially the finer grades, that have a high clay and water content are thixotropic - they become more fluid when a shear stress is applied. When a prawn thrusts its appendages into a thixotropic substratum, the substratum is softened, making it easier for them to burrow. Fine sediments are not necessarily the softest, because clay has high cohesion and can form a hard substratum. The softness of mud is related to its water content: as the water content increases, the sediment becomes softer (Biggs, 1978).

B. Natural Distribution of Penaeids Relative to Particle Sizes

Penaeids, unlike many sessile benthic animals, can make a choice of burrowing site at least once each day or night and so their choice is not


final and unlikely to be critical. In addition adult penaeids migrate from inshore to offshore areas, travelling over substrata that may not be optimal for burrowing. Thus penaeids may be captured over substrata that are not the most preferred type. Some species of penaeids appear to have no particular substratum preference and are found over a wide range of substrata. Parapenaeus longirostris from the Mediterranean and eastern Atlantic, for example, lives over all types of sediments from mud to clean sand (Ghidalia and Bourgois, 1961). Nevertheless, penaeids generally favour fine sediments and most species prefer substrata with a high mud content, probably because they are easier to burrow in. For example, the greatest catches of prawns on two grounds in the Gulf of Mexico were made over bottoms with fine substrata, either sand-silt or sand-silt-clay (Grady, 1971). Penaeids burrow by forcing the body into the substratum which is difficult if the substratum is firm. Fuss and Ogren (1966) found that, although Penaeus duorarum could burrow in all substrata including hard sand, the type of bottom type affected the rate of burrowing: the,softer the bottom the more rapidly the prawns could burrow.

Rulifson (1981) used the results of preference experiments and field records to categorize the distributions of adults of the major commercial penaeid species of the Gulf of Mexico with respect to substratum. Juvenile P. aztecus and P. duorarum are found mainly on sediments containing over 50% mud, whereas juvenile P. setiferus occur more frequently on sediments with a lower mud content. In the adult phase, P. aztecus and P. setiferus both prefer sediments containing 50-80% mud whereas P. duorarum extends its range to include substrata with a low (10%) mud content.

Most penaeids appear to respond to the percentage of mud in the sediment. The recorded distribution of 10 Indo-Pacific penaeids relative to percentage mud is given in Fig. 10.2. These distributions do not necessarily reflect the complete range occupied because the full range of substrata may not have been available in the area studied. Nevertheless they provide a useful indication of relative differences between species. Penaeus indicus, P. monodon and Metapenaeus monoceros are found in areas with a very high mud content. Species such as P. esculentus, M . ensis and M . endeavouri live in a broad range of mud concentrations. The least tolerant of mud is P. latisulcatus. Penaeids may live in different substrata at various life stages. Juvenile M . macleayi, for example, were found in an estuary over substrata consisting of 25-75% mud; adults were found offshore on clean substrata containing only 2-7% mud (Ruello, 1973a).

The substratum preferences of penaeids are sufficiently distinct in some areas for the prawns caught there to be identified to species on the basis

344 BIOLOGY OF P E N A E I D A E

Species Percentage mud Reference

0 10 20 30 40 50 60 7 0 80 90 100

P. indicus

M. monoceros

P. monodon

P. semisulcatus

P. merguiensis

P. esculentus

M. ensis

M. endeavouri

P. longistylus

{

{ P. latisulcatus

2

1

2

1 4 5

4

5 4

4

5

4 5

1 4 3

FIG. 10.2. Distribution of adult Indo-Pacific penaeids relative to the percentage of mud range over which most catches were made, dashed line shows range of minor occurrence. Sources of data: 1, Branford (1981a); 2, Branford (1981b); 3, Hall and Penn (1979); 4, Somers (1987); 5 , Somers et al. (1987a)

of the nature of the substratum. Hall and Penn (1979) assigned commercial catches of two species of penaeids (P. latisulcatus and P. esculentus) in Shark Bay (western Australia) to species on the basis of the type of sediment over which the prawns were captured. Somers (1987b) similarly subdivided commercial catches of the tiger prawns P. esculentus and P. semisulcatus in the Gulf of Carpentaria.

Because a full range of substrata may not be available, the apparent preference of penaeids cannot necessarily be gauged solely from field data in one area. Hall and Penn (1979) reported that in Shark Bay (western Australia), P. latisulcatus is found mainly over sediments with a mud content below 1.08%. In the Red Sea by contrast, Branford (1981a) found this species mostly on sediments with a mud content around 31%. In the Gulf of Carpentaria, Somers (1987a) found P. latisulcatus chiefly on sediments with less than 50% mud. These differences probably reflect the nature of the sediments available to the prawns as well as the influence of other factors on their distribution.

In the western Gulf of Carpentaria, Somers (1987a) found a significant correlation between depth and substratum (percentage mud). Using a


stepwise multiple regression, he showed that, after removing the effect of depth on distribution, substratum accounted for only 11% of the variation in the distribution of P. esculentus, for 16% in the case of P. semisulcatus but for as much as 25% for P . latisulcatus.

C. Organic Content

Depth of water, particle size distribution and the organic carbon content of sediments are frequently interrelated. Fine sediments, which are found in areas protected from wave action, have a high organic carbon content because a large part of the silt is composed of organic material. This organic content can influence the distribution of penaeids. Juvenile M . macleayi in New South Wales estuaries are most abundant in areas with a high (>2%) organic content (Ruello, 1973a). Grady (1971) found that in the Gulf of Mexico, the highest catch rates for commercial penaeids are from areas with a high content of organic carbon. Branford (1981a) found a similar relationship for commercial penaeids in offshore waters of the Red Sea but found no such relationship in inshore waters (Branford, 1981b). According to Somers (1987), there is also no relationship between organic carbon and the total distribution of commercial prawns in the western Gulf of Carpentaria. He suggested that organic carbon is a limiting factor only where its concentration is low. In inshore waters of the Red Sea and the Gulf of Carpentaria where organic carbon does not appear to influence penaeid distributions, the organic carbon content of the sediments is high, ranging between 0.4 and 1.4% and between 0.9 and 2.1% respectively (Branford, 1981b; Somers, 1987). In the Gulf of Mexico and in offshore waters of the Red Sea where penaeid distributions are related to organic carbon, the content is generally low, ranging only between 0.3 and 0.7% and between 0.1 and 0.5% respectively (Grady, 1971; Branford, 1981a).

D. Experimental Studies

In most substratum experiments, prawns are given a choice of natural substrata (e.g. Williams, 1958; Ruello, 1973a; Rulifson, 1981). An alternative design is to sieve out particular fractions and give the prawns a choice between different size categories (e.g. Moller and Jones, 1975; Aziz and Greenwood, 1982). A third approach is to sieve out the fractions and then to make up mixtures (Otazu-Abrill and Ceccaldi, 1981). These different approaches make it difficult to compare results of


studies except where the same method has been used for more than one species.

An experimental approach is useful in defining the limits of burrowing by individual species. Otazu-Abrill and Ceccaldi (198l), for example, found that P. japonicus is inhibited from burrowing in either fine sands or fine gravels; thus their preferred particle-size range is 500 pm to 2 mm. Williams (1958) found that Penaeus duorarum favoured mainly the coarsest substratum (shell sand), whereas Penaeus setiferus and P. aztecus burrowed most frequently on the softer, muddier substrata. Postlarvae of these latter two species also prefer fine substrata (Aldrich et al., 1968). Moller and Jones (1975) found that P . semisulcatus and P. monodon both prefer to burrow in fine grained sediments (90-250pm diameter particle size) but also occasionally burrowed in slightly coarser sediments. Penaeus monodon was more restricted in its choice of sediment type than P. semisulcatus which occasionally burrowed in relatively coarse (350-700 pm particle size) sediments. A consistent result of these experiments is that, although penaeids have a preference for particular grades they can readily burrow in a range of particle sizes. This has been found, for example, for P semisulcatus and P. monodon (Moller and Jones, 1975), M . monoceros (Joshi et al. 1979), P. setiferus, P . duorarum and P. aztecus (Williams, 1958).

The fairly wide tolerance of penaeids to the type of substratum is typified by P . semisulcatus which, under natural conditions, prefers areas with a high mud content (>75%) (Fig. 10.2). Under experimental conditions, over 90% of P. semisulcatus will burrow in substrata with no mud content, showing that mud is not essential for burrowing in this species (Moller and Jones, 1975). Juvenile (4-8 mm CL) M . bennettae prefer fine substrata (<250 pm) to coarser types, but show no preference in the particle size range <62 pm to 250 pm (Aziz and Greenwood, 1982). Similarly, when M . monoceros was given a choice of four substrata, they preferred mud but burrowed in all the types offered (Joshi et al., 1979).

Although the percentage of mud in sediments appears to be important to penaeids, experiments show that the composition of the non-mud fraction is also of significance. Williams (1958) examined the substratum preferences of P. duorarum, P. aztecus and P. setiferus by offering them a choice of natural substrata. Two of these each contained 5% mud, but one contained 62% of medium sand, whereas the other contained 33% medium sand and 30% gravel and shell larger than 2 mm. Twice as many P. duorarum were found on the coarser substratum as on the finer one. The distribution of P. aztecus was exactly the opposite: it preferred the finer substratum. Penaeus setiferus, a species that rarely burrows, was


found about equally on both types. Rulifson (1981) tested whether prawn size, population density, salinity and temperature affected substratum selection by juvenile P. aztecus, P. setiferus and P. duorarum. All sizes (73-156 mm TL) prefer a substratum containing between 21 and 49% sand (63-250 pm). He found that as juvenile P. aztecus grew and moved into higher salinities their preference changed towards substrata with a higher sand content. As P. setiferus grew and were exposed to lower temperatures, their preference changed from coarse substrata (sand and shell) towards sandy mud (<250 pm). P. duorarum apparently does not change preference with size or age.

E. Reasons for Penaeid - Sediment Relationships

Although there are differences between species, most penaeids prefer sediments with a particle size below 1 mm and above 62 pm. Several reasons have been advanced to account for this preference. These include the availability of food, the problems associated with respiring when buried, and the ease or difficulty of burrowing in various grades. Habitat selection may also be important for this preference.

Williams (1958) concluded that food was not an important factor in penaeids’ choice of substratum, because substratum preference is species- specific and is not related to the presence or absence of food. Ruello (1973a) considered that the particle sizes of sediments affected the distribution of M . macleayi more strongly than food. Nevertheless, feeding over very fine sediments can be a problem for some species. Lalithambika et al. (1980) showed experimentally that fine silt and clay decreased the preying efficiency of M . dobsoni and P. indicus on tanaids.

Difficulties with respiring when buried in very fine sediments may partly account for their avoidance of such sediments. When penaeids are buried, they irrigate their gills by taking in water through the respiratory tube formed by the anterior appendages (see Chapter 2). This tube reaches above the surface of the substratum and so the type of substratum probably does not affect the intake of w%ter. Penaeids, however, periodically reverse the flow of water in the gill chambers, apparently to flush them out. During reversed flow, water is taken in through the ventral edge of the branchial chambers. In soft substrata this could cause clogging of the gill chamber. Thus very soft sediments are unsuitable for burrowing. Species that are found over soft sediments, such as P. indicus, P . merguiensis, P. chinensis [= orientalis] and P. setiferus seldom burrow (Penn, 1984).

Breathing when buried is less of a problem in coarser sediments. In


mixed sediments with a high mud content, porosity is low and shear strength is high. This allows species such as M . macleayi to form a small vertical hole in the substratum alongside the branchial chamber (Ruello, 1973a). This hole leads to a space below the cephalothorax; it permits water to escape from the gill chamber during normal respiration and also gives a free flow of clean water during reversal (Fuss, 1964). This mechanism enables the prawns to burrow in low porosity sediments.

In coarse sediments with a low mud content, the greater porosity of the substratum removes the need for a ventilation hole and also for the respiratory siphon to reach the surface. When P. japonicus is buried, the end of its respiratory siphon is well below the surface of the substratum (Egusa and Yamamoto, 1961). Adults of this species are found in sandy sediments. Thus species such as P. duorarum that burrow in coarse, high porosity sediments can burrow deeply (Williams, 1958). According to Hall and Penn (1979), P. latisulcatus also burrows deeply into coarse sediments. Thus their respiratory adaptations enable penaeids to burrow in a wide range of sediments and it is unlikely that problems associated with respiration could explain their relatively narrow preferences.

The third reason advanced for the relationship between penaeids and substrata is the ease or difficulty of burrowing in different types. In coarse sediments the large particles tend to interlock and cannot be easily pushed aside which makes it difficult to burrow by merely pushing into the substratum. Ruello (1973a) commented that M . macleayi has difficulty in burrowing in coarse sand and cannot burrow in a mixture of coarse and very coarse sand. Penaeus japonicus cannot burrow in fine gravels (Otazu-Abrill and Ceccaldi, 1981). Thus it is likely that the upper limit of sediments suitable for burrowing is a function of the difficulty of burrowing into the coarse particles.

Subtle differences in burrowing technique may affect the choice of substratum. Metapenaeus macleayi and P. duorarum both start burrowing by fanning the substratum with the pleopods to create a depression. This method of digging is restricted by the relationship between the current speed developed by the pleopods, and the speed necessary to erode the substratum. Because the cohesion of particles increases as their size diminishes, silts and especially clays are difficult to erode. The most easily eroded particles are around 2 mm in diameter (Day, 1981). This would suggest that both P. duorarum and M . macleayi should be found chiefly in sandy rather than muddy substrata. Although this is true of the adult stages, juvenile M . macleayi occur over muddy sediments.

The difficulty of burrowing in some substrata does not fully explain sediment preferences. Many penaeids are morphologically almost identical, e.g. P. esculentus and P. semisulcatus or M . ensis and M . endeavouri, and


yet have different substratum preferences. In some species the juveniles and adults have different preferences although they are morphologically the same except for size. Moreover, although most species have distinct preferences, they are capable of burrowing in a relatively wide range of sediments. Their preferences are therefore clearly not because they cannot burrow in sediments other than the preferred type.

Penaeid-substratum relationships may perhaps be explained by habitat recognition. Substratum type may be one of the features by which penaeids identify nursery areas and spawning grounds. A preference for a particular substratum could lead to a higher population density in particular areas and increase the probability of successful mating, for the females have only a short mating period (see Chapter 7). If the substratum is used for recognition of a habitat rather than being a limiting factor, this could explain the narrow preferences of penaeids, despite their ability to burrow in a range of substrata. As burrowing is an important means of defence from predators, there is considerable selective advantage in being able to burrow in any substratum encountered.

V. Temperature

A. Effect of Temperature on Behaviour

As early as 1938, Dakin commented that there was no fishery for P. plebejus in winter because the prawns remained buried. White (1975a) similarly reported that commercial catches of P. esculentus were lowest in winter. Dall (1958) noted that M. bennettae was less active in winter; activity resumed in spring when temperatures rose which suggested that temperature affected the amount of time this species spent buried. This possibility was confirmed for P. esculentus by Hill (1985), who showed experimentally that the duration of nocturnal emergence is directly related to temperature. It ranges from around 350 midnight at 2626°C to less than 50 midnight at 16°C. Whereas nearly all P. esculentus emerged every night at temperatures above 17"C, only 5% emerged at 14°C. Fuss and Ogren (1966) found a positive correlation between duration of nocturnal emergence of P. duorarum under field conditions and temperatures below 26°C. They showed that temperature has a differential size effect: small prawns emerge more frequently than large ones at low temperatures. At very high temperatures (above about 33"C), P. duorarum emerge even during the day.

Temperature also affects the type and speed of movement. Penaeus


stylirostris and P. californiensis rarely swim at temperatures below 11°C but often swim above 25°C (Arosamena, 1976). There is a significant relationship between speed of walking and temperature in P. esculentus: it walks at around 1.3 c d s at 26"C, and at 0.3 cm/s at 16°C (Hill, 1985).

Temperature preference is well developed in penaeids, even in deep water where there is little variation in temperature there may be clear preferences. The temperatures of the water 200-1000 m deep in the Mediterranean and eastern Atlantic only range between 13 and 17°C. Nevertheless, Ghidalia and Bourgois (1961) found that the distribution of the penaeid Parapenaeus longirostris was restricted largely to water with a temperature between 14 and 15°C. Temperature preference also seems to play a role in habitat selection by young penaeids. Reynolds and Casterlin (1979b) found that at night juvenile (15-30 mm CL) P. duorarum preferred water at about 30°C which is close to the upper lethal limit of this species (35°C); the lower lethal limit is about 5°C. Reynolds and Casterlin (1979b) suggested that this preference for high temperatures may be linked with their preference for a shallow estuarine habitat. High temperature is unlikely, however, to be the sole cue for habitat recognition. Postlarvae of P. aztecus, for example, recruit to inshore shallows along the northern coast of the Gulf of Mexico in March to April when temperatures are low (1525°C); P. setifems recruit in summer when the water is warm (25-32°C). Aldrich et al. (1968) tested the effect of gradually reducing temperature on the behaviour of postlarvae of P. aztecus and P. setiferus. At 12-17°C nearly all (94%) P. aztecus but no P. setiferus buried. Aldrich et al. (1968) suggested that the burrowing response of P. aztecus postlarvae protects them from predation when temperatures are so low that they would not be able to swim or jump away from predators. Penaeus setiferus recruit at high temperatures and do not have the same problem.

B. Temperature Tolerance

Under natural conditions, low temperature appears to be a greater cause of penaeid mortality than high temperature. Gunter and Hildebrand (1951) recorded that large numbers of P. aztecus died from the cold in severe winters on the coast of the Gulf of Mexico. Eldred et al. (1961) noted that most of the recorded low-temperature kills of penaeids in the Gulf of Mexico are of P. setiferus [ = Puviatilis] and some P. aztecus but no P . duorarum. Joyce (1965) reported that when water temperatures in northeastern Florida estuaries fell to around 8"C, P. setiferus [= fluviatilis] became completely moribund and about 20% of those


collected were dead. The upper median lethal temperatures (MLT) of juvenile penaeids are

mainly around 3436°C (Kuttyamma, 1981; Aziz and Greenwood, 1981). Although MLT is not related to the sex of the individual, it is modified by acclimation temperature. The upper and lower MLT of M . bennettae acclimated at 17°C were 6.4"C and 32.9OC but increased to 7.5"C and 34.6"C for those acclimated at 32°C (Aziz and Greenwood, 1981).

C. Temperature-Salinity Interactions

Postlarval and juvenile penaeids live in inshore habitats where extremes of temperature can occur simultaneously with low salinity. Salinity stress can affect temperature tolerance. The postlarvae of P. aztecus have a significantly greater resistance to high temperature when tested at 25%0 than at either 15%0 or 5%0 (Wiesepape et al., 1972). Acclimation at low salinity modifies the salinity effect on temperature tolerance markedly and postlarvae acclimated at 5%0 are more resistant than those acclimated in higher salinities. Metapenaeus bennettae, a species which spends most of its life in low salinity estuaries in Australia shows a similar adjustment to low salinity. Dall (1958) found that the median lethal temperature of M. bennettae was higher (36.0"C) for prawns acclimated at 5%0 than for prawns acclimated at 35%0 (33.9"C).

VI. Salinity

The inshore shallow water habitats of many juvenile penaeids are generally either continuously or intermittently low in salinity. Penaeids cope with this by being euryhaline (see Chapter 5 ) which greatly increases the inshore area that can be used as nursery grounds (Joyce, 1965). Juvenile P. aztecus, P . duorarum, and P. setiferus [= fluviatilis] have all been captured from inshore areas of the Gulf of Mexico in salinities below l%o (Joyce, 1965; Williams and Deubler, 1968; Stokes, 1974). Early postlarval stages may not, however, be as tolerant as juveniles. Even in 10-30-day-old postlarval P . aztecus, tolerance was found to be related to size and age (Biesiot and Venkataramich, 1974). Large postlarvae had a wider salinity tolerance than smaller individuals of the same age.

Larger and older postlarval stages tend to be better adapted to low salinity conditions than are either the earlier stages or the adults. Dall (1981), for example, found that juveniles of M. bennettae, P. esculentus,


P . merguiensis and P . plebejus, from Australian waters, could survive exposure to lower salinities (&3%0) than could adults (7-10%0).

Tolerance is not the only way of coping with low salinity: another method is to avoid unsuitable salinities. Postlarval P. aztecus develop an escape response from low salinity when they are around 19-days old (Biesiot and Venkataramich, 1974).

The low salinity that characterizes many nursery areas appears to be used by some species of penaeids as a means of identifying these areas; the behavioural responses of penaeid postlarvae to low salinity have been proposed as a mechanism for locating and entering estuaries (Williams and Deubler, 1968; Hughes, 1969a; Young and Carpenter, 1977). Salinity responses are also involved in the emigration of some species of penaeids from estuaries. Migrations and the role of salinity as a cue for migrations are dealt with in Chapter 8, Life Histories.

When groups of P. aztecus in high and low salinity water were exposed to light, a higher proportion of those in low than in high salinity burrowed (Lakshmi et al., 1976). The authors suggested that burrowing in low salinity was a means of conserving energy to compensate for the energy demands of osmoregulation. However, since osmoregulation requires very little energy (see Chapter 5 ) , this explanation is probably not correct. Fuss and Ogren (1966) found no correlation between emergence of P. duorarum and salinity in the range 19-36%0.

VII. Oxygen

Hypoxic water (c2.0 ppm dissolved oxygen) is seasonally common in nearshore waters of Louisiana in the Gulf of Mexico (Renaud, 1985). Penaeids appear to avoid this hypoxic water, and consequently the dissolved oxygen concentration of bottom water is significantly correlated with the number of penaeids ( P . aztecus and P . setiferus). In laboratory experiments, both species detected and avoided low oxygen concentration (Renaud, 1986), although P . aztecus was more sensitive than P . setiferus. Prawns responded to reduced oxygen by an initial increase in activity and movement away from the hypoxic region. Penaeus setiferus displayed an escape reaction by rapid flexing of the abdomen.

Even buried penaeids react to a decrease in the oxygen content of the surrounding water. When the oxygen concentration drops to between 10 and 20% of air saturation, buried P . japonicus protrude the rostrum and sometimes the cephalothorax - presumably to improve irrigation of the gill chamber (Egusa and Yamamoto, 1961). The prawns emerge from the substratum when the oxygen concentration drops to around 10%.

B E H A V I O U R A L RESPONSES TO T H E ENVIRONMENT 353

VIII. Endogenous Rhythms

Naylor (1988) points out that much of the locomotor behaviour of decapod crustaceans is rhythmic, in phase with tidal, die1 or annual patterns of geophysical variables. Rhythmic behaviour of marine animals is generally considered to be controlled by an endogenous physiological pacemaker system that gives approximate periodicity; the pacemaker is adjusted by local environmental effects (Naylor, 1985). This hypothesis explains the nature of the free-running circadian and circatidal rhythms of movement as seen in many penaeids and the fact that these rhythms can be entrained to such factors as light and tide.

A. Light

Light is probably the most important single factor deciding when penaeids are emerged or buried. It also acts as a Zeitgeber in maintaining synchrony between the circadian rhythm and the light-dark cycle (Hughes, 1969d). All the species of penaeids tested respond to changes in daily light level, both directly and through an endogenous rhythm entrained to daily light changes. This rhythm has been demonstrated in several species by keeping them in constant dark or in dim light and observing their pattern of emergence or movement. The results of experiments of this type on P. monodon are given in Fig. 10.3. An endogenous rhythm has been found in M. bennettae (Dall, 1958),

12h 12h 12h 12h 12h

Expected light condition FIG. 10.3. Relative locomotor activity of Penaeus monodon kept in constant darkness

after entrainment to a 12 h light, 12 h dark cycle. Modified and redrawn from Moller and Jones (1975)


P. aztecus (Wickham and Minkler, 1975), P. duorarum (Le Guen and Crosnier, 1968; Hughes, 1969d; Wickham and Minkler, 1975), P. indicus (Natarajan, 1989a), P. merguiensis (Hindley, 1975a), P. monodon (Moller and Jones, 1975; Natarajan, 1989a), P. semisulcafus (Moller and Jones, 1975) and P. sefiferus (Wickham and Minkler, 1975).

A typical study is that by Wickham and Minkler (1975), who compared the responses of P. duorarum, P. aztecus and P . setiferus to a constant dim light. Penaeus duorarum responded by emerging for short periods at a time corresponding to night, although the amount of movement at this time was less than normal. Penaeus aztecus showed a similar response but with a greater proportion emerging at a time corresponding to night. Penaeus setiferus do not normally burrow during the day, but the rhythm was apparent in their movement, as they were more active, and frequently swam, during the expected night time.

Under constant conditions, rhythms can persist for several days although their duration varies with the species. In P . sefiferus it breaks down after one day (Wickham and Minkler, 1975), whereas in M . bennettae it continues for about seven days (Dall, 1958). Rhythmic behaviour can be suppressed by unfavourable conditions such as continuous bright light as Hindley (1975a) showed with P. merguiensis.

If day and night are reversed under experimental conditions, the presence of a rhythm is seen in a tendency to continue to emerge at the former time of nightfall. This gradually changes until the prawns have entrained to the new times. In P. duorarum, complete adjustment required about seven days (Wickham, 1967). The speed of the adjustment is related to the extent of the shift in time. When Hughes (1969d) advanced or retarded the light-dark transition time by 1 h, the time of emergence of juvenile P. duorarum changed to follow the shift. But when the time of dusk was shifted by 3, 6 or 9 h, only about half of the prawns emerged in the first dark period. They took three days to adjust completely to an 8-h shift.

Although many penaeids show strong lunar cycles in catchability , the possibility of an endogenous lunar rhythm in penaeids has been investigated only in P. duorarum. Fuss and Ogren (1966) found no evidence of a lunar rhythm in P. duorarum under experimental conditions of either constant light or constant dark. There was no difference in either movement or emergence between juvenile (1&20 mm CL) P . duorarum collected at new moon and those collected at full moon when held under conditions of constant dim light (Wickham, 1967). Aaron and Wisby’s (1964) results suggest however that P. duorarum may have a lunar rhythm in its phototaxic response to dim light. They found


that juveniles (50-105 mm TL) are attracted to dim light to a greater extent at full than at new moon.

B. Tidw

A clear tidally based endogenous rhythm with peaks of movement around high tide has been found in postlarval P. schmitti (Gamba and Rodriguez, 1987) and in juvenile P. duorurum (Wickham, 1967; Subrahmanyam, 1976). Hughes (1972) showed that even in the absence of a tidal cue, under experimental conditions postlarval P. duorurum swam against the currrent at the time when the tide was rising and with the current at the time when the tide was ebbing. The endogenous tidal rhythm is very strong and even when kept in small (0.5 1) chambers with no substratum and no tidal pressure signal, P . duorurum showed peaks of movement corresponding to high tide in the wild (Subrahmanyam, 1976). The time of high tide shifts about an hour each day. Under conditions of constant water level, the peak of activity of P. duorurum also shifts by about an hour every day (Wickham, 1967; Subrahmanyam, 1976); the tidal clock is not therefore a simple 24 h one that can be reset by light. It requires a tidal signal in order to maintain it. The tidal rhythm in P. duorurum disappeared after seven days in non-tidal conditions (Subrahmanyam, 1976).

No endogenous tidal movement rhythm in juvenile P. merguiensis was detected by Hindley (1975a), who suggested that such a rhythm would be of little value to a species that lives in tropical areas where tides do not follow a regular semi-diurnal pattern. In these areas there is a strong solar component in the tidal cycle, which results either in daily tides or in irregular mixed tides with a 12.4 h average period, but with considerable variation in the intervals between successive tides. Under such conditions, an endogenous tidal rhythm would have little adaptive significance.

An endogenous tidal rhythm of locomotor activity can be induced in juvenile P. indicus and P. monodon by exposing them to tidal hydrostatic pressure variations and also by exposure to 6 h cycles in salinity, water current or temperature (Natarajan, 1989b).

C. Food

A feeding rhythm is an important component of the circadian emergence cycle of P. duorurum; Hughes (1969d) found he could shift emergence to


around midday by feeding the prawns at this time and that this emergence could be entrained in 24 h, even though it meant the prawns emerged and fed in bright light. Feeding does not appear to act as an entraining factor for emergence or movement for either P. sernisulcatus or P. monodon (Moller and Jones, 1975).

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