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Home , Piscivore, Predatory fish

12 Feeding of Piscivorous

FRANCIS JUANES, JEFFREY A . BUCKEL AND FREDERICK S . SCHARF

12 .1 INTRODUCTION group, however, are difficult to categorize and describe, which perhaps explains why no reviews exhibit tremendous diversity in feeding of their ecology exist . habits and the morphologies associated with feeding. A recent book (Gerking 1994) and various other overviews of fish feeding exist (Wootton 12 .2 ADAPTATIONS FOR 1990; Hobson 1991 ; Hart 1993) . However, most of PISCIVORY these tend to be general reviews of theory or focus 12.2.1 What is a piscivore? on smaller non-piscivorous fishes . Our intent here is to review the feeding ecology of piscivorous fish, We define piscivorous fish as carnivorous fish that a subject which to our knowledge has never previ- consume primarily fish prey. Most fish species are ously been reviewed . We focus on fish, and opportunistic and flexible in their feeding habits on species and sizes that consume juvenile and (Dill 1983) and no species consumes only fish prey; adult prey and do not consider those that feed pri- however many do ingest fish as the main prey marily on larvae or fish eggs . item. Fish that eat other fish are second in propor- tion to those feeding on benthic invertebrates and are present in a variety of freshwater, estuarine 12.1.1 Whypiscivorous fish? and marine systems . They are equally common in Piscivorous fish are broadly distributed phyloge- tropical and temperate . Keast (1985) netically and geographically, occur in most habi- examined the piscivore feeding of small lakes tats and generally occupy the top of most aquatic and streams and categorized piscivorous fish into trophic webs. Piscivorous fish also generally primary and secondary piscivores . Primary or achieve the largest body size within fish com- 'specialized' piscivores shift to piscivory within munities, are represented by some of the largest the first few months of life, whereas secondary pis- species (many elasmobranchs, , ) civores only become fish-eaters later in life . Keast and have potentially large impacts on their com- further suggests that secondary piscivores switch munities through . Finally, many pisci- to fish as a way to maintain energetic efficiency vorous fishes, because of their ubiquity and large as they grow. This can only be achieved by eating body size are among the most valuable harvestable progressively larger prey and, at a certain point, species in many of the world's . In some fish are the only prey available . Furthermore, sec- cases, they compete with for commer- ondary piscivores are not structurally adapted for cially important resource species (V . Christensen piscivory other than acquiring a large mouth as 1996; Buckel et al . 1999a) . Piscivorous fish as a they age .

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12.2.2 What are the adaptations strikes occur at high speed and missed prey are for piscivory? rarelypursued, or they can be pursuers such as trout (Salmo trutta ), where attacks start from a C-shaped Feeding behaviours and position, strikes occur at low speeds from a short morphological adaptations distanceand missed prey are chased. When observed in detail it becomes clear that pis- civore feeding behaviour is complex and flexible in Ambush This strategy is used by species that dealing with different prey types . Behaviours can attack from seclusion, although an element of generally be grouped into the following categories, chasing may also occur. Examples are morays which are also associated with particular morpho- (Muraenidae), pike (Esocidae) and summer floun- logical adaptations . der () . Few morphological similar- ities exist in species that use this behaviour other Luring Luring is a sit-and-wait behaviour where than the ability to use camouflage and high-speed prey are attracted by a 'lure', which consists of a attacks. However, distinct patterns of kinematic, stalk topped by a device that resembles a source of pressure, electromyographic and behavioural pro- food; the lure is a modification of the first dorsal files of prey capture are exhibited by ambushers spine (Gerking 1994) . Luring is typical of the an- andpursuers . glerfish (order Lophiiformes) . In addition, among the frogfish various morphological features allow Other A variety of other rarer feeding habits each the predator to blend into the rocky environments with their own specialized morphologies, particu- in which they live as a form of camouflage. Angler- larly in the dentition, include forms of parasitism fish have a considerable gape and ingest prey sizes such as blood-sucking in lampreys (Petromyzonti- that are large compared to other piscivores . dae) and catfishes (Trichomycteridae and Cetopsi- dae), scale-eating in many and characoids, Stalking Stalking is the unobtrusive pursuit of and fin and eye-biting (Gerking 1994 . prey before the attack occurs . This strategy is com- A novel feeding behaviour common to plankti- mon to trumpetfish (Aulostomidae), longnose gar vores has recently been observed for a few species (Lepisosteidae) and needlefish (Belonidae) . These of piscivores (Sazima 1998) . Ram suspension (or species have similar morphologies, long slender filter) feeding is defined as swimming through the bodies with a long snout and sharp teeth . water with the mouth wide open and opercles flared as a way of filtering small prey items out of Chasing Large piscivores are able to chase and the water column without directing attacks to- 'swim-down' prey. This strategy is best represented wards individual prey. This may be a mechanism by the (Xiphiidae and Istiophoridae) and used by piscivores feeding on relatively small prey some (Scombridae) andyellowtail orpompano in high concentrations (B . Hanrahan and F. Juanes, (Carangidae) . These fish must be able to attain personal observation( . high cruising and accelerating speeds . Their bodies can be described as thunniform or carangiform, Most piscivores ingest their prey whole . A few where thrust is maximized by a lunate tail with a species are able to tear off and ingest pieces and high aspect ratio, a narrow caudal peduncle that good examples are (Serrasalmus spp .) minimizes sideways thrust and a large anterior and African fish (Hydrocyon vittatus) . The body depth that minimizes recoil of the head end . most detailed analysis of partial prey eating has These same features, along with a relatively rigid been performed for bluefish (Pomatomus and streamlined body, also minimize drag (see saltatrix) (Juanes and Conover 1994a ; Scharf et al . Brix, Chapter4, this volume . Chasers canbe either 1997). Juvenile bluefish switch from taking prey Jungers, such as the pike ( spp . ), where attacks whole to partial prey consumption when the prey are startedat close range from an S-shaped position, to predator size ratio is about 0.35 independent of Feeding EcologyofPiscivorous Fishes 269 prey type (Scharf et al . 1997( . This ability allows length, has a fineness ratio between 3 .5 and 5 .0 bluefish to attack much larger prey sizes than can (Juanes et al . 1994) . Interestingly, offshore inverte- predators of similar size and is likely to be a func- brate-feeding juveniles (<40 mm) are already mor- tion of specialized musculature and dentition. phologically specialized for piscivory, suggesting Bluefish are also unique in that they ingest prey a trade-off between feeding efficiency and future tail-first, whereas most other piscivores that have diet. A result of this trade-off may be to accelerate been examined eat prey head-fast . Tail-first inges- the onset of piscivory. tion may be a result of pursuing prey rather than ambushing it, or a way to reduce prey mobility Life history thereby increasing prey vulnerability, as has been observed in piranhas . Onset of piscivory Most piscivorous fish under- go ontogenetic shifts in diet (Werner and Gilliam 1984; Keast 1985 ; Winemiller 1989) . These shifts Schoolingin predators generally progress from consumption of zooplank- Schooling by prey is generally thought of as an ton to consumption of benthic macrofauna or prey adaptation for evading, confusing and reducing the fish, with a concomitant increase in mean prey efficiency of predators (Pitcher and Parrish 1993 . size as predators grow . There is much variation in Schooling also has hydrodynamic and foraging the timing of the shift to piscivory among primary functions . Little empirical work has been done on and secondary piscivores (Mittelbach and Persson whether schooling by predators enhances preda- 1998; Mittelbach, Chapter 11, this volume) . A tion efficiency in piscivores . Field studies have few species of scombrids apparently forgo the shown that, in general, group attacks tend to result zooplanktivorous stage and start eating fishes at in higher capture success rates (Pitcher and Parrish first feeding, whereas others shift early in the 1993). Eklov (1992) has shown that the foraging larval period (Tanaka et al . 1996) . The shift to efficiency, measured as growth rate, varies be- piscivory invariably results in an increase in pre- tween a group-foraging, actively searching pisci- dator growth rate (Buijse and Houthuijzen 1992 ; vore (Eurasian , Perca fluviatilis) and a Juanes and Conover 1994b, Olson 1996) . Among solitary-foraging, stalking piscivore (pike, Esox the scombrids studiedby Tanaka et al . (1996, there lucius) . Under similar conditions, grouped perch was a direct correlation between the age at the grew more than single perch or grouped pike . In onset of piscivory and early growth, with those contrast, solitary pike grew better than solitary species shifting to piscivory at first feeding capable perch or grouped pike. Schooling in piscivores may of reaching 100 mm during the first month of life . have foraging costs and benefits . Prey encounter Within fish cohorts, the largest individuals are rates may be maximized but the probability of los- often able to switch to piscivory while the smallest ing a prey item to is also greater are delayed and experience reduced growth. This when predators attack in groups (Juanes and effect leads to the often-observed bimodality in Conover 1994a) . There has been anecdotal infor- size distribution of juvenile piscivores (Adams and mation collected that suggests that some piscivo- DeAngelis 1987 ; Frankiewicz et al . 1996( . Because rous fish hunt cooperatively (Pitcher and Parrish survivorship is generally size-selective in fish 1993), although potential mechanisms have not (Sogard 1997), bimodality can result in increased been quantified under controlled conditions . mortality of individuals in the smaller size mode Active piscivorous pelagic fishes are character- (Olson 1996) . ized by a range of length to maximum depth ratios (the fineness ratio), which ranges from 4 .0 to 6 .5 What allows species to shift to piscivory? The and which maximizes feeding efficiency and mini- timingof the onset of piscivory depends onpredator mizes drag (Blake 1983) . Bluefish, a primary pisci- morphology, predator and prey phenologies, prey vore that switches to fish prey at about 40 mm total abundance and abiotic factors . Clearly predators

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have to be larger than their prey in order to be able and (Forney 1971 ; Keast 1985) . Among to ingest them . Large body size and large mouth marine fish it is much more difficult to examine gapes are therefore generally considered an impor- the timing of predator and prey spawning . How- tant constraint on prey use, particularly piscivory ever, bluefish appear to have evolved a life-history (Werner 1977 ; Wainwright and Richard 1995; strategy whereby they are spawned at approxi- Mittelbach and Persson 1998) . Biomechanical fea- mately the same temperature as their future prey tures such as jaw mechanics and tooth develop- but at a more southern latitude . This divergence ment have also been implicated (Jenkins et al. 1984; allows bluefish to attain the size advantage re- Wainwright and Richard 1995) . Among piscivo- quired when they shift to piscivory after being rous scombrids, ontogenetic development of the advected to higher latitude estuaries where their digestive system (Tanaka et al . 1996) and develop- prey are abundant. ment of the visual system (Margulies 1997) have In a recent review of the litera- been correlated with the onset of piscivory . Wall- ture, Mittelbach and Persson (1998) showed that eye (Stizostedion vitreum) generally shift to pis- those species born larger and with larger mouth civorybetween 30 and 60 mm in length but are able gapes become piscivorous at younger ages and to ingest larvae when they are as small as 10 mm ; smaller sizes, although they did not find a relation- the earlier onset of piscivory may be related to ship between spawning temperature, used as an in- the abundance of prey in appropriate size ranges dicator of timing, and size at the shift to piscivory (Mathias and Li 1982) . However, because the or size at age 1 . However, species that accelerated switch to piscivory is most often preceded by an the onset of piscivory by shifting early were larger invertebrate-feeding stage, piscivores must ensure at age 1 and continued to be larger through later rapid growth during that phase so that when fish ages. prey are available the feeding shift can occur . If A potential cost of early onset of piscivory is growth is slowed during the invertebrate-feeding reduced growth and survival if habitat condi- stage, the piscivore size advantage over its fish prey tions dictate prey abundance . Furthermore, be- is reduced leading to delays in the shift to piscivory cause most piscivores are strongly size-selective (Olson 1996) . Environmental factors such as low (Juanes 1994), if availability of appropriately sized temperatures early in the growing season can fish prey is delayed, growth may be reduced also reduce growth and delay piscivory (Buijse and (Buckel et al . 1998) . Houthuijzen 1992 ; Olson 1996) . Resource polymorphisms Is acceleration of the onset ofpiscivory adaptive? Because of the dramatic increase in growth rate Adaptive trophic specialization can in some cases following the shift to piscivory and because size- lead to the evolution of resource polymorphisms, selective mortality is so prevalent among juvenile where trophically and morphologically special- fishes (Sogard 1997), natural selection should ized morphs can coexist and ultimately speciation favour life-history strategies in piscivores that can occur. Among fishes various examples of minimize the length of the zooplanktivorous trophic polymorphisms include piscivorous phase. One such strategy to attain an acceleration morphs . For example, in Arctic chary (Salvelinus of the onset of piscivory would be to match the alpinus), four trophic morphs are often recognized . timing and location of spawning with the avail- The four morphs have differing life-history strate- ability of fish prey. Freshwater primary piscivores gies, morphologies and behaviours that are gene- have evolved the ability to earlier than tically based (Skulason et al. 1993) . Using other fishes, thereby attaining sufficient size to life-history theory, Mangel (1996) has shown that allow them to consume spawned later the evolution of a large piscivorous morph in trout in the same year. This pattern has been observed ('ferox' trout) can occur if the growth rates of in largemouth bass (Micropterus salmoides), pike the different asymptotic morph sizes differ and if Feeding Ecology of Piscivorous Fishes 271 there is size-dependent mortality . Other aspects of on prey activity producing encounters and the pos- alternative life-history evolution caused by com- itive relationship that exists between body size, petitive reproductive behaviour are reviewed by prey movement and detectability. Hutchings (Chapter 7, this volume) . The estimation of encounter rates between fish predators and prey remains an elusive problem in fish ecology. Specifically, for piscivorous fishes, 12 .3 COMPONENTS OF the mobility of potential prey means that behav- PREDATION iours and movement patterns of both predator and 12.3.1 Search, encounter, pursuit, prey will ultimately affect rates of encounter . Due to the variable nature of the plethora of environ- capture, handling mental parameters that can influence the distribu- For a prey fish to be included in the diet of a pre- tion of animals in space and time, encounter rates dator, it has to be located, pursued, captured, in situ are virtually impossible to measure with manipulated or handled, and finally digested any certainty. Laboratory tanks used for piscivores (Mittelbach, Chapter 11, this volume) . Each of and their prey are generally too small to yield any these steps must be performed successfully by the realistic estimates of encounter rate, as all prey are predator in order for the predation process to be usually within the visual field of a given predator . complete. Therefore, prey have several opportun- Therefore, encounter probabilities are often esti- ities to avoid being eaten during the course of the mated using mathematical models that incorpo- interaction . The first of these is to not be detected . rate average swimming velocities of predator Predators have evolved various modes of searching and prey as well as a predator detection radius for prey. At the same time, prey have evolved an (Gerritsen and Strickler 1977( . Although theore- assortment of behaviours to reduce their chances tical models can be quite elegant, they remain bur- of being detected by potential predators (Krause dened with many assumptions that often cannot et al., Chapter 13, this volume) . The probability be tested. Because no predation can occur without of any one prey being encountered will then an encounter first, much future research will be be determined by the morphological and behavi- devoted to better understanding the factors that oural characteristics of both predator and contribute to variable rates of encounter . prey. Once prey are encountered, predators must be Most predators that consume motile prey, such sufficiently capable of capturing prey for it to be as fish, utilize one of two basic search/encounter eaten. Piscivorous fishes generally have lower modes: ambush or sit-and-wait tactics and cruis- capture probabilities compared with . ing tactics as described earlier. The types and sizes Usually about half of piscivore attacks on average of prey eaten by a predator are often associated are successful compared with 70-80% for plank- with the foraging tactics employed . For example, tivorous fishes . Capture success in piscivores has Green (1986) showed that invertebrate predators also been shown to be directly related to relative that employed ambush tactics consumed larger body sizes of prey and predator, and generally de- prey relative to cruising predators. He further clines linearly as the prey size to predator size ratio demonstrated that prey encounters for ambush increases (Fig . 12.1) . Similar size-based capture predators were strongly dependent on prey swim- success functions have been observed for several ming speeds, whereas variation in prey activity piscivore species representing different life stages had no discernible effect on encounter rates for (Miller et al. 1988; Juanes and Conover 1994a) . cruising predators . Among fish, ambush predators Differences in prey type have also been shown to have also been shown to take larger prey relative to influence predator capture success, as prey escape more actively searching predators . The inclusion proficiencies vary among species (Wahl and Stein of larger prey items in the diets of ambush preda- 1988; Scharf et al . 1998) . The strong dependence of tors is thought to be a function of their dependence piscivore capture success on prey size and type 272 Chapter 12

N 0 0 E 0 0 v i Fig . 12 .1 General empirical relationships between predation components and relative prey Prey size/predator size size for piscivores.

indicates that it plays an important role in deter- prey type, between encounter probability and mining relative vulnerabilities to predation for prey size will determine whether the profitability different prey. peak is shifted toward smaller or larger relative Similar to capture success, handling time in pis- prey sizes . Accurate profitability functions that civorous fishes is affected by both prey size and incorporate a broad range of prey and predator sizes type. Because larger prey sizes often need to be ma- can be extremely valuable for predicting piscivore nipulated before swallowing, increasing prey size diets . typically causes an exponential increase in han- dling time (Fig. 12 .1) . The rate of increase in han- 12.3.2 dling time has been shown to be unique for specific Functional and prey types (Hoyle and Keast 1987; Scharf et al. numerical responses 1998). Handling time has historically been a criti- Predatory response to variations in prey density cal parameter to estimate, as it has frequently been can be grouped into two categories . The functional used to represent the primary energetic cost of response refers to the number of prey eaten per feeding in theoretical foraging models attempting predatorper unit time as a function of prey density. to predict predator diet (Mittelbach, Chapter 11, Changes in number of predators in response to this volume) . Although foraging models have variations in prey density describes the numerical demonstrated some success in predicting diets of response. planktivorous fishes, past models for piscivores have often failed (Sih and Christensen 2001) . More recent models that incorporate differential capture Functional responses probabilities based on prey size and type have There are several different forms of functional re- proven more successful in predicting piscivore sponse . A subset of these have been classified as diets (Rice et al . 1993) . The combination of size- the type I, II and III models (Holling 1965) . The type dependent encounter rates, capture probabilities, I response occurs when the number of prey eaten energy content and handling times can be used to per predator per unit time increases linearly with construct profitability functions for specific prey increasing prey density (Fig. 12 .2a) . The proportion types. For piscivores, these functions are typically of prey density consumed stays constant and this dome-shaped curves that peak at intermediate response is also called density-independent preda- ratios of prey size to predator size (Fig. 12.1( . tion (Fig. 12 .2d) . Most vertebrates have a type II or However, most often encounter rates cannot be III functional response (Hassell 1978) . The type II estimated with confidence and curves are con- response is represented by a negatively accelerat- structed using only capture success and handling ing curve (Fig. 12.2b) ; therefore, the proportion of time functions . The specific relation, for each prey density consumed decreases with increasing

Feeding Ecology of Piscivorous Fishes 273

(a) (d) Type I (Ruggerone and Rogers 1983) and southern floun- der (Paralichthys lethostigma) preying on spot (Leiostomus xanthurus) (Wright et al . 1993) . Lake trout (Salvelinus nemaycush) were capable of high predation rates at low prey fish densities, suggest- Type I ing a type II response (Eby et al. 1995) . Petersen and DeAngelis (1992) found that type H and III models 0 (b) (e) Type II gave similar fits to field data of northern squawfish w E a (Ptychocheilus oregonensis) feeding on juvenile 6 s salmonids . Although the type III functional response has E a not been observed with regularity, it has been Type II 0 d proposed as a potential mechanism in regulating T population abundance (see Section 12 .6) . Several 0. (f) Type III factors can lead to a type III functional response, such as predator learning, prey refuge and the pres - E z ence of alternative prey (Holling 1965) . The pres- ence and accessibility of a prey refuge has been hypothesized to be a factor leading to positive den- III Type sity-dependent mortality in some piscivore-prey Number of prey present systems (Bailey 1994 ; Hixon and Carr 1997) . Alter- native prey can lead to a type III functional re- Fig.12.2 /a-c) Shapes of hypothetical functional sponse through switching behaviour (Murdoch responses : (a) type[, (b) type IIand (c) type III . (d-f) and Oaten 1975) . Prey switching occurs when the Proportion of prey consumed or percentage mortality prey type with the highest relative abundance is corresponding to the functional responses : (d) type I, included disproportionately more in the predator's (e) type II and (f) type III . diet than would be expected from random feeding (see Section 12.4.1 for an example) . prey density and is referred to as negative density- Functional responses are critical parts of the dependent predation . Under this regime the risk of multispecies virtual population analysis (MSVPA) being preyed upon is high at low prey densities but method of modelling fish populations (Shepherd decreases with increasing prey density )Fig. 12 .2e) . and Pope, Chapter 7, Volume 2) . MSVPA differs Positive density-dependent predation can result from single-species virtual population analysis when a predator feeds with a type III functional re- (SSVPA) in that interspecific and intraspecific pre- sponse . The shape of this function is sigmoidal dation are included to estimate levels of natural (Fig . 12.2c) ; when the proportion of prey density mortality, which in SSVPA is assumed constant . consumed is plotted the slope is initially positive, Generally, MSVPA has assumed a type II fun- meaning that the risk of being preyed upon is small ctional response, which may be reasonable for at low prey densities but increases up to a certain predators that do not depend on a small number of point as prey density increases (Fig . 12 .2f) . Preda- prey species, as in temperate systems, but may not tion components such as attack rate and handling be adequate for predators that do depend on few time (Section 12 .3.1) can be estimated from these prey species, as in boreal systems . Inclusion of a functions (Holling 1965; Hassell 1978). type III response can have important effects on In general, piscivorous fishes have a type H forecasts based on MSVPA, including producing functional response. For example, type IIresponses more than one solution to MSVPA equations were found in Arctic chary preying on migrating (Magnusson 1995 ; see also Shepherd and Pope, sockeye (Oncorhynchus nerka) smolts Chapter 7, Volume 2) . 274 Chapter 12

Numerical responses experiments and large-scale field manipulations to determine patterns of prey selection in several Predator numbers can respond rapidly to increas- freshwater predators, including ing prey density, as when predators aggregate on (Esox masquinongy), tiger muskellunge, and prey fish, or can respond slowly, such as increased . Results demonstrated that each of reproductive success (Peterman and Gatto 1978) . the predators consistently selected for shad prey as We know little about numerical responses in pis- opposed to Centrarchidprey. The authors conclud- civorous fish . This is surprising given its potential ed that behavioural and morphological differences importance in regulating population levels ; the between prey types resulted in differential vulner- lack of data stems from the logistical difficulties ability to predation and the observed patterns of of measuring such a response . Whenever a predator selection . Research on the feeding habits of increases in density in response to increasing prey piscivorous bluefish in marine waters off the fish density, the total predation rate response can northern Atlantic of the USA have also re- differ from the predator's functional response . A vealed evidence for selective predation on specific sigmoidal response (type III) may more typically prey types . Buckel et al . (1999b) demonstrated describe a piscivore's total response; the total that, during early summer in shallow estuarine response is a function of both the functional and habitats, juvenile bluefish consumed young-of- numerical response (Bailey 1994( . the-year striped bass (Morons saxatilis) in greater proportions than a random sampling of the prey environment, and that this positive selection was 12 .4 PREY TYPE AND directly related to striped bass abundance . In other SIZE SELECTIVITY words, they showed prey switching behaviour as referred to in Section 12 .3. During southerly au- Selective predation can be defined as the consump- tumn migrations in continental shelf waters, juve- tion of prey in different proportions than those nile bluefish have also shown the propensity for available in the predator's surrounding habitat selecting specific prey types, particularly bay (Chesson 1978; Mittelbach, Chapter 11, this vol- (Anchoa mitchilli) (Buckel et al . 1999c( . ume). This is in contrast to random feeding, where Selection for specific prey sizes maybe even more predators feed indiscriminately on prey in accord- prevalent than prey type selection among piscivo- ance with their relative availability . Predators rous fishes . A recent review of 32 laboratory and that feed in a random manner with respect to rela- field studies concluded that selection for small tive prey abundance levels are usually referred to prey from available size distributions was a com- as opportunistic feeders because they adjust their mon phenomenon for both freshwater and marine feeding habits rapidly to match variation in the piscivores (Juanes 1994) . This study also revealed local prey field . Predators that consume a narrow that most piscivorous fishes consumed prey small- range of prey types or sizes regardless of changes er than the optimal prey sizes predicted by energy in the prey field are thought of as specialists and maximization models, independent of both represent the most extreme case of selective predator and prey type as well as predator size predation . Most predators fall somewhere along a (Mittelbach, Chapter 11, this volume) . continuum between opportunists and specialists . 12.4.2 Behaviouralmechanismsof 12.4.1 Observed patterns selective feeding Numerous instances of prey type and size selec- Selective feeding can result from both morphologi- tion by piscivorous fishes have been reported in cal constraints of predators and behavioural inter- both freshwater and marine communities . For actions between piscivores and their prey . Predator example, Wahl and Stein (1988) used laboratory gape size ultimately limits the sizes of prey in- Feeding Ecology of Piscivorous Fishes 275 gested and can also affect the types of prey con- alter attack and capture rates of predators and con- sumed . However, recent studies indicate that be- tribute significantly to the observed patterns of havioural capabilities of both predator and prey selective feeding. can regulate the sizes and types of prey eaten before morphological constraints become important . In a well-designed series of laboratory experiments, B . 12 .5 PREDATOR-SIZE AND Christensen 11996) evaluated the effects of prey an- PREY-SIZE RELATIONSHIPS tipredator behaviours on the sizes of roach (Rutilus rutilus) consumed by piscivorous Eurasian perch . Because they are the top predators in many aquatic Feeding experiments were conducted at two dif- systems, knowledge of the sizes of prey included in ferent spatial scales, determined by tank volumes, the diets of piscivorous fishes is essential in order to to control the level of antipredator behaviour ex- identify their potential impact on prey survival and pressed by the prey. In smaller arenas that limited their role in structuring populations at lower troph- prey escape ability, the author found that perch ic levels . This is particularly important for the were able to consume large roach approaching gape approach to fisheries management, limitations . In larger arenas, where prey antipreda- where knowledge of interactions is critical (Pauly tor behaviours were not suppressed, the maximum and Christensen, Chapter 10, Volume 2) . Further size of roach consumed by perch was significantly discussion of how size-dependent processes struc- smaller. The author concluded that the sizes of ture communities can be found in Persson, Chapter prey eaten were largely dependent upon relative 15, this volume . From a behavioural standpoint, predator and prey mobility (Mittelbach, Chapter relative body sizes of prey and predator can have 11, this volume) . Juanes (1994) hypothesized that significant effects on predator feeding success . common patterns of selection for small-sized prey Detection and capture of prey by piscivores are by piscivorous fishes were the result of size- enhanced with increasing size for several reasons, dependent vulnerabilities of prey to predator including increased sustained and burst swimming capture, rather than predator preferences . He speeds and better visual acuity (Webb 1976) . The proposed that many examples of selective feeding escapeproficiencyofpreyalsovarieswithontogeny in fishes were actually passive selective processes as reaction distances increase and swimming abili- rather than active predator choice, with attack ties are improved with size (Brix, Chapter 4, this rates being relatively equal among different prey volume . Morphological characteristics that influ- sizes but smaller prey being consumed more fre- ence piscivore-prey interactions, such as predator quently due to ease of capture (see also Hart and gape size and robustness of prey morphological Hamrin 1990). Prey behaviour can also influence defences (e.g. spines), also scale with ontogeny . the rate of attack among different prey types Therefore, identifying patterns of prey size use by available to a predator. For example, laboratory ex- piscivorous fishes can provide important clues as periments demonstrated higher attack rates by to the mechanisms that shape piscivore diets and goby (Gobiusculus flavescens) predators on her- the effects of predation by piscivorous fishes on ring ( harengus) larvae compared with community structure . (Gadus morhua) larvae, with attack proportions being strongly related to differential levels of prey 12.5.1 General patterns activity between the species (Utne-Palm 2000) . Predictions of prey selection from most traditional and hypotheses foraging models assume that optimal choices are For piscivorous fishes, the sizes of prey consumed mainly the result of behavioural decisions by generally increase with predator size . In addition, predators (Stephens and Krebs 1986) . For piscivo- the range of prey sizes eaten typically increases in rous fish predators, the behavioural and foraging larger predators, as maximum prey size often in- capabilities of both predator and prey can clearly creases rapidly while minimum prey size may 276 Chapter 12

butions eaten by fish predators of varying body sizes . Based on ratio-scale analyses, he concluded that the range of prey sizes eaten did not change significantly with increasing body size for most predators and that older larger predators should not compete with smaller ones . Although predator size-prey size relationships for piscivorous fishes are often reported, potential mechanisms that lead to the commonly observed pattern of increasing maximum prey sizes coupled with stationary minimum prey sizes are generally lacking . Scharf et al. (2000) noted that the con- tinued inclusion of small prey in the diets of larger predators contrasts with predictions of optimal foraging models for particulate feeders, which in- dicate that the largest prey available should be con- Predator size sumed preferentially to maximize net energetic return . The authors hypothesized that the combi- Fig .12 .3 Hypothetical predator size-prey size nation of high relative abundance and high capture relationship for a piscivore, illustrating typically observed changes in minimum and maximum prey probability for small prey relative to large prey may sizes consumed with increasing predator size . lead to consistently high vulnerability to preda- tion for small prey fishes as already discussed . Because predator handling times also increase change only slightly over a broad range of predator rapidly with prey size, they suggested that the sizes (Fig. 12.3) . For example, Mittelbach and retention of small prey in the diet may reflect Persson (1998) demonstrated increasing mean and profitable foraging decisions by predators because maximum prey sizes as body size increased for 12 search, capture and handling costs remain low . species of freshwater piscivores . The authors further noted that for many of the piscivores they 12.5.2 What determines examined, minimum prey size remained fairly constant with increasing predator body size . maximum prey size? Scharf et al . (2000 revealed similar predator Maximum prey sizes eaten by piscivores can be size-prey size patterns for a group of 18 marine pis- limited by several factors . Of foremost importance civores in continental shelf waters off the Atlantic are morphological limitations imposed by preda- coast of the USA . Expanding prey-size ranges that tor gape size and throat width . Most piscivorous retain small prey in the diet of larger piscivores fishes swallow prey head first after manipulating means that prey sizes consumed by smaller preda- prey so that the largest body depth is positioned tors can be a subset of the prey sizes consumed laterally in the mouth (Reimchen 1991) . A strong by larger predators, which may result in a competi- relationship between prey body depth and predator tive disadvantage for smaller predators (Wilson gape width has been detected for several piscivo- 1975 . However, when the range of prey sizes eaten rous fishes (e .g. Hambright et al . 1991) . General is examined as a ratio of predator size rather than mouth shape and structure can also affect the on an absolute scale, ontogenetic changes are more types and sizes of prey that can be ingested . For subtle . For example, Pearre (1986 studied a large example, Keast and Webb (1966) demonstrated group of predators that included 43 species of strong relationships between mouth morphology larvae, juveniles and some small adult fishes in and the feeding ecology of several freshwater an effort to detect general trends in prey-size distri- fishes . The effects of piscivore gape limitations on Feeding Ecology of Piscivorous Fishes 277 maximum prey sizes eaten can also impact prey (natural) levels of mortality : secondly, that populations. Persson et al. (1996) examined the they do not collapse at all quickly, when potential community-level effects of predatorgape subjected to high levels of mortality . limitation in afield study of predation in European lakes . Prey fishes in four lakes were exposed to two One of the more well accepted mechanisms predators with different gape sizes and their popu- put forward to explain population regulation in lations monitored . Results indicated that prey ex- fish is density-dependent mortality in larval and posed to the smaller-gaped predator reached a size juvenile stages through interspecific predation refuge sooner, were more abundant and had slower or (see Section 12 .6.2; Myers, Chapter growth rates due to intraspecific competition com- 6, this volume; Shepherd and Pope, Chapter 8, pared with prey exposed to the larger-gaped preda- Volume 2) . tor. The effects of piscivore gape size were also Density-dependent mortality can lead to the observed at lower trophic levels, indicating the maintenance of population stability (Murdoch and potential importance of predator gape sizes on Oaten 1975 ; Hassell 1978) . Field studies provide community dynamics (Persson, Chapter 15, this evidence for density-dependent mortality in volume) . marine fishes (Myers and Cadigan 1993 ; Forrester Other factors may restrict maximum prey sizes 1995 ; Hixon and Carr 1997) . Several of these inves- eaten by fish predators before morphological limi- tigations provide evidence that piscivorous fishes tations imposed by gape size become important . are the dominant cause of density-dependent mor- The behavioural tactics used by predators to tality. However, identifying the mechanism that search for, encounter and attack prey can affect generates density-dependent predation mortality prey sizes consumed . For example, Gaughan and has been elusive (Bailey 1994). Potential mecha- Potter (1997) compared the diets and mouth sizes nisms leading to density-dependent predation of five estuarine species of larval fish and con- mortality as a result of predator behaviour are de- cluded that mouth width had only a small influ- scribed in Section 12 .3.2 . Density-dependent prey ence on prey sizes eaten and that disparate feeding responses can also influence mortality rates . For patterns among larvae were likely due to behavi- example, competition for food at high density may oural differences . Behavioural capabilities of both lead to reduced growth rates, with prey being predator and prey can also contribute considerably vulnerable to gape-limited piscivores for longer to the sizes of prey eaten. The ability of prey to periods. evade predators is related to body size, with larger prey being more efficient at avoiding predator 12.6.1 Population and strikes . Therefore, maximum prey sizes eaten effects by piscivorous fishes can often be considerably community smaller than gape sizes (Juanes and Conover 1995 ; Piscivorous fishes are known to have a dramatic B. Christensen 1996) . influence on population- and community-level dynamics (Persson, Chapter 15, this volume) . The impacts of piscivores can extend down several 12 .6 POPULATION trophic levels (Zaret and Paine 1973) . In freshwater REGULATION systems, the model describes zooplanktivore, zooplankton, and phytoplankton Shepherd and Cushing (1990) stated that abundance under high and low levels of piscivore abundance (see Carpenter et al . 1985 ; Persson, there is some basis for the belief that fish Chapter 15, this volume; Kaiser and Jennings, populations are regulated in some way . In Chapter 16, Volume 2) . When piscivore abundance fact, the evidence is twofold: first, that they levels are high, density of zooplanktivorous fish do not explode when subjected only to low is reduced, which leads to increased zooplankton

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() and reduced phytoplankton abundance in the USA after northern pike were introduced levels . Opposite abundance levels to those de- was emigration ; this led to a rapid decline in prey scribed above are observed during periods of low fish abundance and a change in community struc- piscivore density. Hambright (1994) describes how ture (He and Kitchell 1990) . the vulnerability of zooplanktivores to piscivory determines the magnitude of zooplanktivory and thus its effect on lower trophic levels . Piscivorous 12 .7 METHODS OF fish can influence the life-history strategy of their STUDYING PREDATION prey. Reznick et al . (1990) showed that under sepa- IN THE FIELD rate piscivore regimes (low vs . high predation), guppies (Poecilia reticulate) evolved different life- There are several methods used to determine the history parameters such as age at maturity, repro- effects of piscivorous fish on prey populations and ductive effort, brood size and size of offspring communities . A direct approach is to make com- (Hutchings, Chapter 7, this volume) . parisons between treatments where piscivores are Cannibalism is interesting because of its poten- present or absent . These treatments maybe natural tial role in regulating population levels through its or artificial . Modelling has been used successfully contribution to natural mortality ; however, evi- to determine the influence of predators on prey dence for density-dependent cannibalism in non- populations (Mittelbach, Chapter 11 and Persson, captive fishes has not been discovered (Smith Chapter 15, this volume) . Studies that estimate and Reay 1991) . Henderson and Corps (1997) predation mortality and compare this to total found that bass (Dicentrarchus labrax) year-class prey mortality make up another group of studies . strength had a 3-year periodicity, which they Estimates of consumption rate along with knowl- believed to result from cannibalism within the edge of diet composition, prey sizes and predator nursery . abundance are used to estimate predation mortali- Animal abundance levels are known to exhibit ty. Detailed descriptions of stomach content analy- periodicity as a result of predator-prey or host-par- sis and methods to estimate consumption rates are asite cycles . In a predator-prey cycle, increases in described by Jobling (Chapter 5, this volume) . predator abundance are concurrent with declines Tethers (usually monofilament line) are in prey population levels ; subsequent periods of used to hold prey fish in place; the fate of the prey low prey abundance can lead to predator declines fish allows one to assess relative predation inten- and prey release . We are aware of only one example sity in both space and time . Danilowicz and Sale of a predator-prey cycle for a piscivorous fish . (1999) used tethering of French grunt (Haemulon Pacific cod (Gadus macrocephalus) and flavolineatum) to determine when, over a diel (Clupea harengus pallasi) populations in Hecate cycle, predation intensity was highest . They found Strait, British Columbia have patterns of abun- that the risk of being eaten was lowest during diur- dance that are suggestive of such a cycle (Walters nal periods and highest during dusk and nocturnal et al . 1986) . The lack of evidence for a piscivore- periods. Age-0 rainbow trout (Salmo gairdneri) prey cycle may result from the flexible feeding were tethered in British Columbia lakes to deter- behaviour of piscivores, allowing them to remain mine the spatial and temporal patterns of pis- at stable population levels when one of their prey civory; it was concluded that the risk of predation populations is at low abundance . varied greatly over both space and time (Post et al . Piscivores can have indirect non-lethal effects 1998) . Clearly, tethering experiments, as with on prey fishes. These include all of the behavioural other predator-prey studies, would need to con- responses made by prey when confronted with a form to the animal ethics regulations of the coun- piscivore . These behavioural responses can lead tries and institutions involved . to differences in community structure . The domi- Filming has been used to both identify preda- nant indirect effect on prey fishes in a northern bog tors and gain insight into the intensity of piscivory. Feeding Ecology of Piscivorous Fishes 279

Carr and Hixon (1995) used filming of small patch matic recent example has been the introduction of reefs to aid in identifying pelagic piscivores and for the Nile perch (Lutes nilotica) to , the measuring their visitation rates to experimental world's largest tropical lake by surface area . The reefs . main effect of the predator introduction, similar to that observed in most systems where it has occurred, has been an accelerated decline of the 12 .8 IMPLICATIONS FOR diverse endemic fauna of the lake and the CONSERVATION AND recent extinction of at least 200 species (Seehausen MANAGEMENT et al . 1997) . However, the Nile perch introduction has also resulted in a fourfold increase in Fishing alters the age and size structure of popula- yield and a doubling of fishery-related employ- tions as older and larger fish are often removed ment (Pitcher and Hart 1995 ; Kitchell et al . 1997 . first, and eventually the fishery is supported by Piscivore stocking, particularly in freshwater the small newly recruited individuals . In many systems, has also been used as a way to improve ecosystems, large piscivorous species were the water quality in eutrophic lakes and reservoirs . initial targets of fishing . After the fishing down This process, termed 'biomanipulation', works of these populations, the fisheries shifted to through trophic cascading and has been quite smaller species at lower trophic levels (Pauly and successful in improving water quality of culturally Christensen, Chapter 10, Volume 2) . Although eutrophic lakes and reservoirs (Drenner and most marine landings are of small planktivores, it Hambright 1999, although it can also have a is fishing and the removal of large species at high variety of unexpected negative impacts . trophic levels that affects ecosystem structure Marine reserves have been effective in restoring and functioning, leading to 'top-down' control and protecting many reef fishes (Polunin, Chapter (Carpenter et al . 1985; Hixon and Can 1997 ; 14, Volume 2) and they appear to be a promising Kaiser and Jennings, Chapter 16, Volume 2) . For tool for marine ecosystem sustainability (National example, on Georges Bank, the decline in ground- Research Council 1999) . However, reserves, if fish stocks has led to a dramatic increase in forage not planned carefully enough, can have negative fish such as herring and and a replace- impacts because of potential effects of physical ment of gadid and species by small elas- factors combined with increased protection of mobranchs (Fogarty and Murawski 1998) . As more piscivorous fishes . For example, in a small reserve and more stocks become overexploited, fewer top in Barbados, size and abundance of piscivores predators will dominate oceanic food webs and were greater within the reserve than on adjacent both direct and indirect community effects will be reefs, but recruitment of grunts (Haemulidae) prevalent. Predator removals can also be a deliber- was lower because of predation pressure and ate form of fisheries management, whereby de- oceanographic patterns of larval supply (Tupper creases in predation pressure are predicted to andJuanes1999) . result. However this strategy does not always proceed as predicted (V . Christensen 1996 ; Kaiser and Jennings, Chapter 16 and Cowx, Chapter 17, 12 .9 CONCLUSIONS Volume 2). The opposite problem, with similar results, Piscivores are a diverse group of fish that show dis- occurs when predators are deliberately or inadver- tinct behaviours and specialized morphologies . tently added to ecosystems (Cowx, Chapter 17, The timing of the onset of piscivory is critical to Volume 2) . The effects of piscivore introduction many species and may have led to adaptive strate- has been documented in temperate, boreal and gies that accelerate the shift to piscivory. The tropical lakes (Zaret and Paine 1973 ; Mills et al . predation process can be better understood by 1994; Vander Zanden et al. 1999) . The most dra- examining the components of predation, and the

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predatory response to changes in prey density can Carpenter, S.R., Kitchell, J .F. and Hodgson, J.R. (1985) be estimated by generating numerical and func- Cascading trophic interactions and lake productivity . tional responses . Piscivorous fish exhibit general BioScience 35,634-9. Carr, M patterns of prey type and size selectivity driven by .H. and Hixon, M .A. (1995) Predation effects on early post-settlement survivorship of coral-reef fishes attack behaviours and prey-specific behavioural . Marine Ecology Progress Series 124,31-42 . responses by the prey. Predatory fish can have large Chesson, J . (1978) Measuring preference in selective impacts on prey communities in all habitats where predation . Ecology 59, 211-15 . they occur and are thus common targets for cons er- Christensen, B . (1996) Predator foraging capabilities and vation and management, as they are often the first prey antipredator behaviours : pre- versus postcapture species to be affected by harvesting ; however, they constraints on size-dependent predator-prey interac- tions . Oikos 76,368-80 . can also have both positive and detrimental effects Christensen, V. (1996) Managing fisheries involving when deliberately or inadvertently added to predator and prey species . Reviews in Fish Biology and ecosystems . Fisheries 6,417-42 . Danilowicz, B.S . and Sale, P.F. (1999) Relative intensity of predation on the French grunt, Haemulon flavolinea- turn, during diurnal, dusk, and nocturnal periods on a REFERENCES . Marine Biology 133,337-43, Dill, L .M . (1983) Adaptive flexibility in the foraging Adams, S .M . and DeAngelis, D .L . (1987) Indirect effects behavior of fishes. Canadian Journal of Fisheries and of early bass-shad interactions on predator population Aquatic Sciences 40,398-408 . structure and dynamics. In : W.C. Kerfoot and Drenner, R . W. and Hambright, K .D. (1999) Biomanipula- A. Sib (eds) Predation : Direct and Indirect Impacts tion of fish assemblages as a lake restoration tech- on Aquatic Communities . Hanover, NH : University nique . Archly fiir Hydrobiologie 146, 129-65 . Press of New England, pp . 103-17 . Eby, L.A., Rudstam, L .G. and Kitchell, J .F. (1995) Predator Bailey, K.M. (1994) Predation on juvenile and re- responses to prey population dynamics : an empirical cruitment variability . Netherlands Journal of Sea analysis based on lake trout growth rates . Canadian Research 32,175-89, Journal of Fisheries and Aquatic Sciences 52,1564-71 . Blake, R.W. (1983) . Cambridge: Cam- Eklov, P. (1992) Group foraging versus solitary foraging bridge University Press. efficiency in piscivorous predators : the perch, Perca Buckel, J.A., Letcher, B .H. and Conover, D .O.(1998) Ef- fluviatilis, and pike, Esox lucius, patterns . Animal fects of a delayed onset of piscivory on size of age-0 Behaviour 44,313-26 . bluefish . Transactions of the American Fisheries Soci- Fogarty, M .J. and Murawski, S .A. (1998) Large-scale dis- ety 127, 576-87 . turbance and the structure of marine systems : fishery Buckel, J.A., Fogarty, M .J. and Conover, D .O. )1999a) impacts on Georges Bank. Ecological Applications 8 Mutual prey of fish and humans : a comparison of (Suppl .), S6-S22. consumed by bluefish, Pomatomus saltatrix, Forney, J .L . (1971) Development of dominant year classes with that harvested by fisheries . Fishery Bulletin 97, in a yellow perch population . Transactions of the 776-85 . American Fisheries Society 100, 739-49 . Buckel, J .A., Conover, DO ., Steinberg, N .D . and Forrester, G .E . (1995) Strong density-dependent survival McKown, K .A. (1999b) Impact of age-0 bluefish pre- and recruitment regulate the abundance of a coral reef dation on age-0 fishes in the Hudson River estuary : fish . Oecologia 103,275-82 . evidence for density-dependent loss of juvenile striped Frankiewicz, P., Dabrowski, K . and Zalewski, M . (1996) bass. Canadian Journal of Fisheries and Aquatic Mechanism of establishing bimodality in a size distri- Sciences 56,275-87 . bution of age-0 pikeperch, Stizostedion lucioperca (L .) Buckel, J.A., Fogarty, M .J. and Conover, D .O. (1999c) For- in the Sulejow Reservoir, central Poland . Annales aging habits of bluefish, Pomatomus saltatrix, on the Zoologie Fennici 33,321-7 . U .S . east coast continental shelf . Fishery Bulletin 97, Gaughan, D . J. and Potter, I.C. (1997) Analysis of diet and 758-75 . feeding strategies within an assemblage of estuarine Buijse, A .D. and Houthuijzen, R.P. (1992) Piscivory, larval fish and an objective assessment of dietary niche growth, and size-selective mortality of age 0 pikeperch overlap . Fishery Bulletin 95, 722-31 . (Stizostedion lucioperca) . Canadian Journal of Gerking, S .D. (1994) Feeding Ecology of Fish. New York: Fisheries andAquatic Sciences 49, 894-902 . Academic Press . Feeding Ecology of Piscivorous Fishes 281

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EDITED BY PauIJ .B. Hart Department of Biology University of Leicester

AND

John D. Reynolds School of Biological Sciences University of East Anglia

Blackwell

ft Publishing © 2002 by Blackwell Science Ltd a Blackwell Publishing company

Chapter 8 © British Crown copyright, 1999 350 Main Street, Malden, MA 02148-5018, USA 108 Cowley Road, Oxford OX41JF, UK 550 Swanston Street, Carlton South, Melbourne, Victoria 3053, Australia KurfUrstendamm 57, 10707 Berlin, Germany The right of Paul J.B. Hart and John D . Reynolds to be identified as the Authors of the Editorial Material in this Work has been asserted in accordance with the UK Copyright, Designs, and Patents Act 1988 . All rights reserved . No part of this publication maybe reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs, and Patents Act 1988, without the prior permission of the publisher . First published 2002 by Blackwell Science Ltd

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