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Hydrobiologia 146: 97-167 (1987) 97 0 Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands

A review of planktivorous : Their , feeding behaviours, selectivities, and impacts

I Xavier Lazzaro ORSTOM (Institut Français de Recherche Scientifique pour le Développement eri Coopération), 213, rue Lu Fayette, 75480 Paris Cedex IO, France Present address: Laboratorio de Limrzologia, Centro de Recursos Hidricob e Ecologia Aplicada, Departamento de Hidraulica e Sarzeamento, Universidade de São Paulo, AV,DI: Carlos Botelho, 1465, São Carlos, Sï? 13560, Brazil t’ Mail address: CI? 337, São Carlos, SI? 13560, Brazil

Keywords: planktivorous , feeding behaviours, feeding selectivities, electivity indices, fish- interactions, predator- models

Mots clés: poissons planctophages, comportements alimentaires, sélectivités alimentaires, indices d’électivité, interactions poissons-pltpcton, modèles prédateurs-proies I Résumé La vision classique des limnologistes fut de considérer les interactions cntre les composants des écosystè- mes lacustres comme un flux d’influence unidirectionnel des sels nutritifs vers le phytoplancton, le zoo- plancton, et finalement les poissons, par l’intermédiaire de processus de contrôle successivement physiqucs, chimiques, puis biologiques (StraSkraba, 1967). L‘effet exercé par les poissons plaiictophages sur les commu- nautés zoo- et phytoplanctoniques ne fut reconnu qu’à partir des travaux de HrbáEek et al. (1961), HrbAEek (1962), Brooks & Dodson (1965), et StraSkraba (1965). Ces auteurs montrèrent (1) que dans les étangs et lacs en présence de poissons planctophages prédateurs visuels. les conimuiiautés‘zooplanctoniques étaient com- posées d’espèces de plus petites tailles que celles présentes dans les milieux dépourvus de planctophages et, (2) que les communautés zooplanctoniques résultantes, composées d’espèces de petites tailles, influençaient les communautés phytoplanctoniques. Bien que la variabiliti: de la réponse du phytoplancton à la préda- tion par les poissons révèle l’importance d’autres facteurs (tels que la limitation en sels nutritifs et la compéti- tion interspécifique des algues), ces travaux démontrèrent que les communautés zoo- et phyl oplanctoniques pouvaient effectivement être affectées par l’alimentation sélective des poissons planctophages. Pendant les deux dernières décennies, de nombreux travaux en. limnologie se sont concentrés sur cet impact radical des poissons sur les communautés planctoniques. La réponse directe des communautés zooplanctoniques A la prédation visuelle des poissons planctophages (appelés en anglais ‘particulate fceders’) a suscité un intérêt tout particulier, alors que les effets multiniveaux causés par les poissons planctophages filtreurs (prédation sur le zooplancton plus broutage du phytoplancton) ont été plus rarement abordés. Les objcctifs de cette révi- sion so’nt de documenter les inter-relations poissons-plancton, afin (1) d’obtenir des Cléments d’appréciation de l’impact des poissons sur les communautés planctoniques, et (2) d’établir des modèlcs niécanistiques d’ali- . mentation planctophage tenant compte du répertoire alimentaire et de la sélectivité du poisson, des réponses adaptatives du plancton, et des conditions du milieu. L‘approche utilisée ici est basée sur des résultats expérimentaux de terrain et de laboratoire provenant de la littérature concernant les systèmes tropicaux et tempérés d’eau douce (parfois marilie). Quatre groupes de poissons planctophages sont distingués: les prédateurs visuels limités par la taille dc leur bouche (c’est-à-dire les larves et les espèces de petites tailles: ‘gape-limited predators’), les prédateurs visuels proprement dit (’par- ticulate feeders’), les filtreurs par pompage (‘pump filter feeders’), et les filtreurs par déplacement (‘tow-net

. ORSTOM Fonds Documentaire 98 filter feeders’). Pour chaque groupe, les mécanismes de sélection des proies sont analysés, aussi bien du point de vue du prédateur que de la proie. Afin de rechercher les mékanismes déterminant la sélectivité alimentaire du prédateur et de discuter ses effets potentiels sur les commurjautés de proies, l’acte de prédation est décom- posé en une séquence d’évènements successifs (Holling, 1966)! ía détection, la poursuite, la capture, la réten- tion et la pour les prédateurs visuels; et la capture, la rétention et la digestion pour les filtreurs. Les avantages et les inconvénients de plusieurs mesures de sélectivité (appélées indices d’électivité), aussi bien que leur utilisation appropriée sont discutés. Les modèles de sélection de proies et les théories de recherche optimale sont analysés pour les différents modes d’alimentation des planctophages. Des modèles mécanisti- ques basés sur l’approche de Holling (loc. cit.) sont proposés pour chaque mode d’alimentation afin de déter- miner les vulnerabilités différentielles des proies et l’amplitude optimale de la diète. Cette révision concerne les domaines de I’écologie générale, de la limnologie, de l’aménagement des p%che- ries (tel que, par exemple, l’utilisation des ressources planctoniques, le repeuplement, l’introduction, ou le maintien de populations naturelles de poissons), et du contrôle biologique des processus d’eutrophisation (approches par biomanipulation). Elle insiste sur le réel besoin de connaissances sur la sélectivité alimentaire et l’utilisation de la nourriture par les poissons planctophages. Elle permet de conclure que prédateurs et proies sont intimement et mutuellement adaptés. Aussi, dans la plupart des cas, il apparait peu approprié d’aborder la dynamique du plancton et la qualité des eaux sans tenir compte de l’estimation des pressions de nrédation et de broutage exercées par 1es.poissons planctophages.

Abstract

The classical approach of limnologists has been to consider the interactions between lake com- ponents as an unidirectional flow of influence from nutrients to the , to the , and finally to the fish, through successive controls by physical, chemical, and biological processes (StraSkraba, 1967). The effect of planktivorous fishes on zooplankton and phytoplankton was not recogni- zed until the studies of HrbáEek et al. (19&1), HrbAEek (1962), Brooks e9r. Dodson (1965) and Straskraba (1965). They showed that (1) in ponds and lakes in the presence of planktivorous fishes the zooplankton communities were composed of smaller bodied than in those lacking , and (2) the resulting small- bodied zooplankton cdmmunities affected the phytoplankton communities. ‘Although the variability of the phytoplankton response to fish showed the importance of other factors (such as nutrient limitation and interspecific of ), thesc studies emphasized that zooplankton and phytoplankton com- munities can be affected by the feeding selectivity of planktivorous fishes. During the last two decades, many limnological studies have focused on this dramatic impact of fish on plankton communities. The direct response of zooplankton communities to visual fish predation (i.e. particulate feeding) has been of major interest, whereas the multilevel effects of filter-feeding fish (predation on zooplankton plus on phyto- plankton) have been neglected. The objectives of this review are to document fish-plankton interrelationships in order to (1) provide insights into the impact of fish on plankton communities, and (2) outline mechanistic models of planktivory according to the feeding repertory and the selectivity of the fish, the adaptive respon- ses of the plankton, and the environmental conditions. The approach adopted here is based on field and laboratory experimental results derived from the literature on tropical and temperate freshwater (occasionally marine) systems. Four types of planktivorous fish are dis- tinguished: the gape-limited larvae and small fish species, the particulate feeders, the pump filter feeders, and the tow-net filter feeders. For each type of , the mechanisms of prey selection are analyzed from the point of view of both the predator and the prey. To investigate the main determinants of the preda- tor feeding selectivity, and to discuss its potential effects on prey communities, the predation-act is divided into a sequence of successive events (HoIIing, 1966): detection, pursuit, capture, retenlion, and digestion for partiyulate feeders; and capture, retention, and digestion for filter feeders. The strengths and weaknesses of various measures of selectivity (i.e. electivity indices), as well as their appropriate usages are considered. Avai- lable prey selection models and optimal theories are analyzed for the different planktivore feeding

.“ 99 modes. Mechanistic models based on Holling's (loc. cit.) approach are proposed for each feeding 'mode to determine differential prey vulnerabilities and optimal diet breadth. ' This review has application to several fields, including general , limnology, management (for example, utilization of planktonic resources, stocking, introduction, or maintenance of natural rish populations), and biological control of the processes (biomanipulation approaches). It emphasizes the real-need for more knowledge of the feeding selectivity and food utilization of planktivores. It concludes that predator and prey are mutually adapted. Thus, in most cases, study of plankton dynamics and water quality should include the assessment of fish predation and grazing pressures. 1 00

Contents

I. . EVOLUTION OF PLANKTON-FEEDING FISHES 102

A. i From macrophages towards microphages . 102 B. Evolution of mouth protrusibility 104

II. FEEDING MODES A. Obligate and facultative planktivores 104 B. Particulate feeders, pump and tow-net filter feeders: definitions 105 C. Switching from particulate to filter-feeding modes 106 Dependence on fish age 106 Dependence on prey composition, size, and density 106 Vision versus chemoreception 107 D. Schooling of planktivores 107

III. MECHANISMS OF PREY SELECTION 1 O7

A. Particulate feeders 1 108 1. 108 Dependence on light: importance of light contrast for visual predators 108 Prey conspiciousness: prey visibility and behaviour 109 Visual acuity of fishes: contrast perception and visual field 110 2. Prey pursuit 112 Dependence on prey size, distribution, and density 112 Dependence on fish hunger 113 Dependence on fish experience of prey 114 3. Prey capture 114 Gape limitation of larvae and small species 114 Capture efficiency: effects of experience and mouth structure 11 5 4. Prey retention 116 5. Prey digestion: of zooplankton to fish digestion processes 117 B. Filter feeders 118 1. Prey capture: a determining event for zooplankton ingestion 118 Tow-net filter feeders 119 Pump filter feeders 121 2. retention: a determining event for motionless particle ingestion 121 Mechanisms of particle retention by biological filters 122 Filtering efficiency 123 3. Particle digestion: resistance' of phytoplankton to fish digestion processes 124

IV. EVALUATION OF SELECTIVE FEEDING: A REVIEW OF ELECTIVITY INDICES, THEIR STRENGTHS AND LIMITATIONS 125

V. MODELS OF PREY SELECTION 131 A. Model conceptualization and feeding modes 131 1. Particulate feeders 132 2. Tow-net filter feeders 138 3. Pump filter feeders 139 B. Optimal foraging predictions, shifts, and feeding mode switches 140 101

VI. FIELD EVIDENCE OF PLANICTIVOROUS FISHES SELECTIVE IMPACT ON PLANK- ' ' TON COMMUNITIES 144 A. Impact of particulate feeders 144 1. Direct effect on zooplankton communities 144 2. Indirect effect on phytoplankton communities 14s E. Impact of filter feeders I49

1. Direct effect on zooplankton communities ' 149 2. Direct effect on phytoplankton communities ' 150

VII. CONCLUSIONS: BIOMANIPULATION APPROACHES FOR LAKE MANAGEMENT AND NEEDS FOR FUTURE RESEARCH 152

Acknowledgements 156

.* 102

I. Evolutiod of plankton-feeding fishes and in the open . Planktivores are involved in the main commercial fisheries of the world (ancho- A. From macrophages towards microphages vies, , , , salmonids, and many others), and in recreational fisheries (sunfish, The oldest teleostean fishes evolved as generali- trout, , , etc.). Today, zed predators (Godine, 1971) feeding on comparati- include more than 95% of the living species of fish vely large prey (macrophagy). The main divergence (Marshall, 1965), and microphagy is advanced in from this basic pattern is a trend towards feeding most of the (freshwater, at least) orders: on smaller prey (microphagy), such as the plank- - even in Acipensiformes (not teleostean but acti- ton. This evolution from macrophagy to micro- noterygean): phagy is marked by the development of specialized 0 Polyodontidae: paddlefish, Poiyodon spa- structures and the regression of others, such as: tkuia (Rosen & Hales, 1981); modification of from fixed to protrusible, - especially in : replacement of teeth by elaborate rakers on the e (Hildebrand, 1963; Longhurst, branchial arches, modification of some gill rakers 1971; Blaber, 1979): West African shads, Eth- in an epibranchiai organ on the roof of the mouth, malosa finibriata (Fagade & Olanayan, lengthening of the digestive tract (Harder, 1960; 1972), and E. dorsalis (Bainbridge, 1957, Marshall, 1965; Nelson, 1967, 1970; Durbin & Dur- 1963); gizzard shad, Dorosoma cepedianum bin, 1975) to process larger amounts of fine mate- (Velasquez, 1939; ICutkuhn, 1957; Smith, , rial without necessity of a digestive pause between 1963; Drenner, 1977; Drenner et al., 1978, meals (which is the rule in macrophages). 1982a, 1982b, 1984a; Barger & Kilambi, 1980; Members of the order Clupeiformes, the - Drenner & McComas, 1980); threadfin shad, like fishes, illustrate well this trend towards micro- D. petenense (Holanov & Tash, 1978); ale- phagy: for example, the progression from the wife, pseudoharengus (Brooks & Dod- tarpon-like ancestor (a predatory macrophage) to son, 1965; Wells, 1970; Hutchinson, 1971; the round-herring (a particulate-feeding micro- Rhodes, 1971; Warshaw, 1972; Rasmussen, phage) to the (a particulate and filter- 1973; Rhodes & McComish, 1975; Gannon, feeding microphage) to the menhaden (a fiber- 1976; Jansscn, 1976, 1978a, 1978b, 1980); feeding microphage) (Durbin, 1979). blueback herring, A haaestivalis (Brooks & The most specialized of the microphages are the Dodson, 1965; Hutchinson, 1971; Janssen, filter-feeding species. The menhaden, a filter- 1982); Pacific , Surdinops sagax feeding clupeid microphage, repeats most of these (Lewis, 1929; Arthur, 1976; Nelson, 1979); evolutionary steps during the of a single fish. Tanganyika sardine, Limnothrissa miodon The selective predation of larval menhaden is direc- (Begg, 1976); Indian oil sardine, Sardinella ted towards individual zooplankton: mainly cope- longiceps (Bensam, 1964); thread herrings, pods (June & Carlson, 1971). During the metamor- Opisthoneina spp. (Berry & Barret, 1963); phosis, particulate feeding is gradually replaced by North Atlantic and North , filter feeding on zooplankton, phytoplankton, and Ciupm harengus (Blaxter & Holliday, 1963; fine (Durbin & Durbin, 1975). Blaxter, 1966; Rosenthal, 1969; Rosenthal & Only a small fraction of the energy produced by Hempel, 1970); , Brevoor- the phytoplankton can be transferred through the tia tyrannus (June & Carlson, 1971; Peters, to the higher trophic levels, usually pre- 1972; Durbin & Durbin, 1975; Jeffries, 1975); datory macrophages. On the contrary, a greater pilchard, Sardiriops oceiiata (King & Mcleod, fraction is available for plankton-feeding fishes. 1976); This is reflected in the of planktivorous 0 Engraulidae: Northern , Engraulis fishes in freshwater rivers and lakes (for example, mordns (Leong & O’Connell, 1969; Loukash- Jenkins (1967) showed that omnivorous Dorosoma kin, 1970; O’Connell, 1972; Arthur, 1976; cepedianum and L). petenense account for 40% of Nelson, 1979); Southwest African anchovy, fish standing crops in central US. reservoirs), in E. capensis (King & McLeod, 1976); Peruvian areas of coastal marine (Ryther, 1969), anchoveta, E. ringen (Rojas de Mendiola, 103

1971); anchoveta, Cetengraulis nzysticetus Hillbricht-Illtowska & Weglenska, 1973); (Bayliff, 1963); Stolephorus spp. (Blaber, bleak, Alburnus alburnus L. (Prejs, 1976); 1979); crucian , Carassius carassius L: (Prejs, - in Salmoniformes: 1973);

Q : whitefishes and ciscoes, Core- Q Castotomidae: , Ictiobm gonus spp. (Bertmar & Stromberg, 1969; cyprinellus (Staroska & Applegate, 1970); Kliewer, 1970; Rasmussen, 1973; Giussani, - in Siluriformes: 1974; Seghers, 1975; Engel, 1976; Janssen, 0 MochoIci d ae: Braclzysynodon tis batensoda 1978a, 1980) and Leucichthys spp. (Clemens (Lauzanne, 1977; Im, 1977; Gras et al., 1981); & Bigelow, 1922); Pacific salmon, Oncorlzyn- - in Cyprinidontiformes:

chus nerka (Narver, 1970; Feller & Kaczynski, Q Cyprinidontidae: fish, Garizbu- 1975; Engel, 1976; Eggen, 1978, 1982); trout, sia uffinis (Hurlbert et al., 1972; Hurlbert & char (Nilsson, 1960, 1963), and. Atlantic Mulla, 1981); salmon, such as rainbow trout, Salino gaird- - in Atheriniformes: neri (Hartman, 1958; Galbraith, 1967; Ware, 0 Atherinidae: Melaniris chagresi (Zaret, 1971, 1972, 1973); cutthroat trout, S. clarki 1971, 1972a; Zaret & Kerfoot, 1975); brook (Andrusak & Northcote, 1971; Schutz & silverside, Labidesthes sicculus; inland silver- Northcote, 1972; Northcote et al., 1978); lake side, Menidia beryllina (McComas & Dren- trout, Salvelinus izainaycush (Kettle & ner, 1982); grunion of California, Leuresthes O’Brien, 1978) and Dolly Varden, S. malina lenuis (Lewis, 1929); (Andrusak & Northcote, 1971; Schutz & - in :

Northcote, 1972; Northcote et al., 1978); Q Gasterosteidae: three-spined stickleback, brook charr, Salvelinus fontinalis (Dawido- Gasterosteus aculeatus (Beukema, 1965; Gib- wicz & Gliwicz, 1983); son, 1980); fifteen-spined stickleback, Spina- 0 Osmeridae: , Osmerus mordax (Reif chia spinackia (Kislalioglu & Gibson, 1976); & Tappa, 1966; Rasmussen, 1973); - in Perciformes: - in Myctophiformes: e Miigilidae: mullets, genus Mugi1 (Norman

Q Myctophidae: ‘lantern fishes’ (Nafpaktitis 24 Grecnwood, 1963; Thomson, 1966); et al., 1977); * Helostomidae: Helostorna teinrnincki -,in Cypriniformes: (Ci em, 1967);.

0 Characidae: Alestes bareinoze (Green, Q Centrarchidae: sunfish, Lepoiitis 1967; Lauzanne, 1970, 1973, 1977); Hydrocy- macrochirtu (Werner, 1972, 1974, 1977; Wer- nus forskalii (Lauzanne, 1977); ner & Hall, 1974, 1976, 1977, 1979; Vinyard Gymnotidae: Rhcibdolichops troscheli & O’Brien, 1975, 1976; O’Brien et al., 1976; (Maggo-Leccia & Zaret, 1978); Werner et al., 1977, 1981, 1983a, 1983b; * : , Carassius auratus Vinyard, 1980; Gardner, 1981; Mittelbaoh, (Hester, 1968); carp, Cyprinus Carpio 1981; Janssen, 1982); northern longear sun- (HrbáEek et al., 1961, 1978; Grygierek, 19625 fish, Lepoinis niegsalotis pettastes, and pump- HrbáEek, 1962, 1969; Hillbricht-Ilkowska, kinseed, L. gibbosus (Laughlin & Werner, 1964; Grygierek et al., 1966; Prejs, 1973; 1980); white , Pomo.xis artniilarìs Losos & Hetesa, 1973; Kajak et al., 1976); sil- (Wright et al., 1983; Wright &O’Brien, 1984); ver carp, Hypophthalmicht}iys molitrix fry, Micropterus salinoides (Savina, 1965; Borutskij, 1973; Omarov & (Elliot, 1976); Lazareva, 1974; Vovk, 1974; Januszko, 1974; 0 Percidae: Eurasian , Perca jhrviatilis Kajak et al., 1975, 1977; Kajak, 1977; (Guma’a, 1978; Furnass, 1979; Stenson, 1980); Opuszynski, 1979a, 1979b, 1980); bream, yellow perch, I? flavescens (Galbraith, 1967; Abramis brama (Lammens, 1985), and tench, Wong & Ward, 1972; Rasmussen, 1973); Tinca tinca (although both species are oppor- e Ciclilidae: Congo , Tilapia rendalli tunistic and more generally benthophagous: (Caulton, 1976); blue tilapia, 7: aurea (Spa- Prejs, 1973; Hillbricht-Ilkowska et al., 1973; taru & Zorn, 1978; Goplien et al., 1983a, 104

1983b; Drenner et al., 1984b); T. esculenta truded mouth is often smaller than that of the (Greenwood, 1953); T. nilotica (Moriarty, unprotruded mouth) particularly when associated 1973; Moriarty & Moriarty, 1973); Sarothero- with a round protruded mouth orifice (better adap- don galilaeus (Lauzanne & Iltis, 1975; Spa- ted for sucking prey items than a ‘grinning’ or siit- taru, 1976; Spataru & Zorn, 1976; Lauzanne, shaped mouth), (3) increasing the distance from 1977; Gophen, 1980; Drenner et al., 1982c; which the fish can remove prey items by 25 or 50% Gophen et al., 1983a, 1983b); Haplochromis of the head length, (4) closing the mouth in the pro- nigripinnis (Moriarty & Moriarty, 1973); truded position on a prey item so tending to hold Carangidae: jack mackerel, Trachzirus it straight, pointed towards the gullet (i.e. preven- symmetricus (Carliste, 1971; Arthur, 1976); ting misdirection of the suction force and presu- * Scombridae: Pneumatophorus spp. (God- mably faciliting swallowing), and increasing the sil, 1954); Indian mackeral, Rastrelliger kana- volume of water sucked info the mouth without gurta (Bhimachar et al., 19160; Jones & Rosa, being blown out again as the mouth closes, (5) 1965; Colin, 1976; Nelson, 1979); Pacific adapting the feeding movement to the position, mackeral, Scomber japonicus (O’Connel1 & behaviour and nature of the prey item by adjustable Zweifel, 1972); wavyback skipjack, Euthyn- position mechanisms, and (6) serving to align the nus affinis (Walten, 1966). direction of the bite with that of the pushing devel- This list is not exhaustive. More general informa- opcd by the caudal and pectoral fins during fee- tion on trophic relationships between various ding. Motta (loc. cit.) emphasized that the protrusi- planktivorous fish species is available in Bigelow & ble jaws of are highly coordinated and Schroeder, 1953; Berg & Grimaldi, 1966; Keast & versatile. It results in a continuous modulated Webb, 1966; Nelson, 1967; Grimaldi, 1972; Roberts, whose adaptive significance is the abi- 1972; Fryer & Iles, 1972; Davis & Birdson, 1973; lity to make a wide variety of rapid adjustments in Prejs, 1973, 1976; Nilsson & Pejler, 1973; Giussani, the gape, biting force, and degree of protrusion 1974; Hobson, 1974; Merret & , 1974; Lowe- according to the changing position, behaviour and McConnell, 1975; De Bernardi & Giussani, 1975; nature of the prey item (Liem, 1980a). The different Svardson, 1976; Lauzanne, 1977; Nelson, 1979; feeding behaviours displayed may result in differen- Zaret, 1980; Pourriot et al., 1982, and Pourriot, tial capture efficiencies (Liem, 1980b). 1983. Protrusion may have a selective advantage, through competition, in fishes with food habits B. Evolution of mouth protrwsibility which overlap. As an example, differential mouth morphologies resulted in a replacement of the Jaw protrusibility is an advance in mouth evolu- brook silverside (Lnbidesthes sicculus) by the tion (Alexander, 1967a), and is found in numerous inlam3 silverside (Menidia beryllina) in Lake species of living teleosts (Marshall, 1965; Gosline, Texoma (Texas Oklahoma border). These two athe- 1971), mainly among Acanthopterigians, Cyprini- rinids use similar and feed selectively on dae, and Cyprinidontidae (Atheriniformes). In a the largest prey they can capture (McComas & recent review paper, Motta (1984) described four Drenner, 1982). Since Menidia has a protrusible basic mechanisms of jaw protusion and pointed and tube-shaped mouth, it can capture evasive out that: (1) the mandibule depression is the most more successfully than the v-notched common mechanism among the fish studied, (2) mouth of Labidesfhes. the twisting action of the maxilla has been overem- phasized in the past, and (3) the neurocrania1 eleva- tion and the suspensoria1 abduction may be more II. Feeding modes prevalent than realized. Of the 15 cited functions, some present an adaptative value for plankton cap- A. Obligate and facultative plnnktivores ture, among them: (1) moving the mouth suddenly nearer the prey and so increasing the velocity of Most fishes feed on plankton during at least attack and reducing the volume of water that must some period of their . Planktonic fish larvate be sucked in, (2) increasing the initial suction force consume zooplankton and, sometimes, of the water flow (because the diameter of the pro- phytoplankton. Many species switch to larger prey 105

and leave planktivory as they grow, whereas others to feed on plankton: particulate feeding and filter feed during their entire lives on plankton. Some are feeding. obligate planktivores feeding exclusively on plank- A) Particulate feeders attack single individual ton; others are facultative planktivores feeding on planktonic prey item which they visually selxct plankton as well as on other food items. from the water column (Confer & Blades, 1975; The majority of works concerning fish feeding Janssen, 1976, 1978a, 1980, 1981, 1982; Werner, on plankton have been dedicated to facultative 1977; Vinyard, 1980). Nevertheless, several prey planktivores (such as sunfishes, Lepomis spp.). may be inhaled incidentally during the capture of Facultative planktivores are more generally restrict- the pursued prey (Wright et al., 1983). ed to littoral areas where food resources are more In contrast, both pump filter feeders and tow-net diverse. They are opportunistic feeders, switching filter feeders do not visually detect individual prey to food sources other than plankton (like suspend- item, but engulf a volume of water containing the ed organic particles, periphyton, macrophytes, food organisms, and retain the planktonic prey and aquatic or terrestrial , seeds, benthic or sub- particles by passing this volume of water over en- benthic or ) during some periods of trapment structures, such as, principally, gill rakers, the year when plankton is less available. For exam- microbranchiospines on the gill arches, and bran- ple, as emphasized by Lauzanne (1977), in Lake chial tooth plates. Chad during low water level conditions (dry season), B) Tow-net filter feeders surround the prey items Brachysynodontis batensoda (a nocturnal filter- with their mouths which are held fully agape while feeding Mochocidae) switches from an exclusive rapidly (Walten, 1966; Durbin 8~ Dur- zooplankton diet to a mixed zooplankton and bin, 1975; Colin, 1976; Rosen & Hales, 1981). swimming larval and nymphal diet, while C) Pump filter feeders use rhythmic suctions to Alestes dentex (Characidae) begins feeding on, be- capture prey items, while swimming slowly, or re- sides zooplankton, insects (immature stages of maining quite stationary (Moriarty et al., 1973; Chironomids, Trichoptera, Ephemeroptera, and Drenner, 1977: Janssen, 1976, 1978a, 1980; , but mostly swimming larvae of Chao- Holaiiov & Tash, 1978; Drenner & McComas, 1980; borus), and seeds (Graminea and Cyperacea). Drenncr et al., 1978, 1982a, 1982b, 1982c, 1984a; There have been less works on the feeding Gophen et ai., 1983b). mechanics of obligate planktivores (such as alewik, I will use the above terminology in this review, Alosa pseudolzarengus, and blueback herring, A. but other terminologies may be appropriate as well. aestivalis), probably because they are extremely Hillhricht-llkowska (in litt.) emphasizes that, delicate and difficult to capture .alive (Janssen, regardless to the terminology commonly employed, 1982). Obligate planlctivores, such as herrings, live both particulate and filter feeders are feeding on only in pelagic areas where planktonic resources are ‘particles’. Thus, they are rather ‘particulate- dominant. seizing feeders’ and ‘particulate-filtering feeders’, Comparing the searching behaviours for respectively. But, to avoid using Lhe word ‘particu-, zooplankton in an obligate planktivore, blueback late’, ‘visual feeders’ may be matched with ‘filtFr herring (Alosa aestivalis) and in a facultative feeders’. planktivore, bluegill (Lepomis macrochirus), Jans- An intermediate feeding mode is described as sen (loc. cit.) observed that the methods used by the ‘gulping’ by Janssen (1976, 1978a) for the alewife, two fishes are markedly different. Blueback herring Alosa pseudoliarengus, and the cisco, uses .a very e€fective search method for zooplank- artedii. The fish use short sequences of several ton as it searches while swimming, whereas bluegill pumps which alternate with pauses of about 0.5 searches while stopped (hovering), swimming to a second. Although very similar to ‘gulping’, ‘pump prey only as soon as it is detected (see section filter feeding’, described by Drenner (1977) for giz- III.A.l.). zard shad, Dorosoma cepedianurn, is not identical. Y The shad consecutively opens and closes its mouth, B. Particulate feeders, pump and tow-net filter- pumping in water at a maximum rate of 2- 3 times feeders: definitions per second, while swimming rather slowly. Accord- ing to Janssen (in litt.), the major difference is that Planktivorous fishes use two distinct behaviours gulping is visual (at least in the light), and alewives 106 and ciscoes are size selective using this mode. Jans- coes Coregonus artedii and C. hoyi (Janssen, sen (1981) could alter the direction of gulping of 1978a, 1980). blueback herring, Alosa aestivalis, by altering the lighting scheme (i.e., the orientation of the ‘Snell’s Dependence on prey composition, size, and density. window’). While not mentioned in the paper, Jans- Switching from païticulate to filter-feeding be- sen (in litt.) could shift those fish towards tow-net haviour is a function of various factors, such as: filter feeding by turning off the light (dim red light prey density and available prey size range. High on). Unless there is no change in prey density, tur- prey densities of microcrustaceans (higher than ning the light back on induces gulping again. Moreo- 100000 m-3) elicit filtering in alewives ver, ciscoes under similar circumstances continue to larger than 160 mm TL. Particulate feeding or gulp, apparently not Selectively. Gulping is not gulping are used at much lower densities (Janssen, directed to one prey item, but it is visually oriented 9978a). Filter-feeding behaviour occurs in 50 to and size selective, and thus it must be classified as 70 mrn TL alewife, when high densities of particulate feeding. (Tabefkzria) are present. At this size, the fish diet shifts from exclusively zooplankton to phytoplank- C: Switching from particulate to filtergeeding ton, zooplankton, and detritus. High densities of modes Daphnia also induce gulping in ciscoes, but tow-net filtering never occuïs even at higher densities

Dependence on fish age. For some fishes, the feed- (2000000 Daphnia m-3). Experimentally, bong & , ing mode used to capture plankton is dependent on O’Connel1 (1969) found that high densities of Arte- fish size (i.e., fish age). When adult, some are ob- mia salina nauplii (about 0.6 mm long) elicit filter- ligate filter feeders. For example, adult Atlantic ing in Engraulis mordax, but high densities of adult menhaden, Brevoortia tyrannus, is an obligate fil- A. salina (5 - 10 mm long) elicit particulate feeding. ter feeder (Durbin & Durbin, 1975), but is a partic- Small Tilapia aurea (40 - 50 mm SL) use rapid and ulate feeder when larval and prejuvenile (smaller rhythmic suctions to capture Bosinina concentra- than 40 mm TL) (June & Carlson, 1971). An identi- tions caught in the water-surface film (Lazzaro, cal evolutionary pattern is observed during ontoge- pers. observ. in aquarium). But, they feed particu- ny in the cichlids, Tilapia aurea and Sarotherodor? lately in the watet column on evasive copepods. galilaeus (Gophen et al., 1983a, 1983b), and others. Saruthermion gsc.liltreirs use filter-feeding be- Those fishes are obligate particulate feeders when haviours to capture surface-trapped prey, midwater larval and juvenile and mainly filter feeders when prey, and prey near the bottom (Drennelr et al., adult (‘obligate’ may nat be appropriate as ir: aurea 1982~).These authors observed that S. galilaeus feed as a scraper even when very large; Drenner, in (20-42 inni SL) switch to filter feeding on remain- litt.). A transition period exists during which both ing nauplii and copepodites, after eliminating, by feeding modes can be used according to environ- particulate feeding, the large-sized prey (larger than mental conditions. Among clupeids, gizzard shad, 0.38 mm), such as , , Di- Dorosoma cepedianum, apparently change from aphanossmn, and adults of Ilfesocyclops. particulate to filter feeding when, about 25 mm SE’ Nevertheless, not all high densities of small sus- (Drenner et al., 1982a). 50 to 70 mm TL alewife, pended organisms stimulate a filtering behaviour in Alosa pseudoharengus feed just as well by gulping, obligate filter feeders. As observed by Drenner et filtering and particulate feeding, whereas smaller al. (1982b), dense concentrations of the fish only feed particulately (Janssen, 1976). Adult phytoplankter Ankistrodesmus sp. fail to induce paddlefish, Polyodon spathula, larger than the pump filtering behaviour in gizzard shad. 225 mni SL, are indiscriminate tow-net filter feed- In experimental trials with Northern anchovy, ers on plankton, while young paddlefish are selec- Engraulis mordax, O’Connel1 (1972) observed that, tive particulate feeders (Rosen & Hales, 1981). Oth- although biting (i.e. particulate feeding) increases er fishes, when adult retain the ability to use either with adult Artemia density, and filtering with particulate or filter-feeding modes: such as, the ale- nauplii density, the frequency of response for each wife (as mentioned above), the northern anchovy corresponding feeding behaviour appears lower at Engraulis mordax (Leang & O’Connell, 19691, cis- higher densities of the alternative prey type. 107

Visiori versus chemoreception. There is a lack of in- ed, depends on the nature of lhe patchiness (Eg- formation concerning the senses used by filter- gers, 1976). But, one selective advantage is obvious: feeding fish to detect their food. Nevertheless, schooling planktivores can explore larger water numerous works demonstrate that filter feeding is volumes than solitary planktivores. Because the a light independent activity. The Baikal omul, rate of prey consumption by planktivores is affect- Coregonus autuinnalis niigratorius, filter feed ed by schooling, Eggers (loc. cil.) emphasized (1) when there is not enough light to see its zooplank- the necessity to consider the effects of schooling in tonic prey (Volkova, 1973). Thus, the author pre- assessing food selection by schooled planktivores, sumed that the fish taste the prey brought into its and (2) the discrepancy that could result between a mouth (where the taste buds are located) by the predicted diet composition, based on a predator- respiratory currents, before it induces filter feeding. prey model assuming solitary behaviour of the Holanov & Tash (1978) observed that threadfin predator, and data collected from schooled fish. shad, Dorosorna petenense, filter feed under both For example, in laboratory experiments, O’Connel1 light and dark conditions, which suggests also that (1972) noted a graduation in lhe feeding response chemoreception rather than vision induces filter of Northern anchovy, Engraulis mordax, wilhin a feeding. They proposed chemoreception as a trig- school: a higher percentage of biting occurred at ger mechanism to stimulate filter feeding. At high the front, and a higher percentage of filtering at tltc light levels, they added brine nauplii or rear. Moreover, the variations in the strength and phytoplankton, which both cause visual changes by intensity of this gradient were dependent on the colouring the water. In those experimental condi- relative abundances of the two sizes of prey in the tions, the shad begin feeding only after several water. minutes. They start also filter feeding near a source of water free of any suspended matter, but previ- ously inhabited by zooplankton. lil[l[. MecAianisms of prey selection

D. Schooling of planktivores To study predation, Holling (1966) developed a model of the predalion cycle in which Since schooling prey are better protected against he considered the predation-act as a succession of predators than solitary ones (Brock & RifFenburgh, discrete events: prey search, prey encounter, prey 1960; Neill & Cullen, 1974), foraging filter feeders, pursuit, prey capture, and prey consumption. Each as well as particulate feeders, use structured and event can be measured experimentally and the pre- stable schooling behaviours, in response to preda- dator’s success rate at each event is independent of tor pressures (i.e., potential or real attacks), when the previous event. This model permits one to study feeding in open water, far from sheltered areas how a predator alters its feeding behaviour in re- where they remain when not feeding. However, sponse to prey. A similar approach to Holling’s has many shallow water zooplanktivores school when been used by Ware (1973), Werner & Hall (1974), feeding in the water column above the substrate O’Brien et al. (1976), Drenner (1977), Gerritsen & where the shelters are abundant (Hobson, 1968). Strickler (1977), Eggers (1977, 1982), Drenner et al. Thus, the differential opportunity for shelter may (1978), O’Brien (1979), Gibson (1980), and Wright not be the only selective advantage of schooling &O’Brien (19841, to study the feeding behaviour of (Breder, 1959; Shaw, 1978). various and invertebrate predators. Some The abundant literature on fish schooling has of these models are reviewed by O’Brien (1979) (see been summarized by Radakov (1973). The be- also section VA). The quantitative and qualitative haviour of schools is well documented in herring, characteristics of the sct of prey ingested by a pred- sardinella, mackerel, young Cyprinidae, anchovy, ator by unit of timc are determined by the product and menhaden. The biological value of schooling is of the different success rates (one for each event) diverse: feeding, defense, reproduction, migration, for each prey type, and corrected for the time used tolerance of diverse conditions, and others. to detect, pursue, capture, and retain a prey. In The effect of schooling on the feeding success of some cases, differential digestion efficiencies may planktivores, when plankton is patchily distribut- alter the feeding selectivity of planktivores (see sec- 108 tions III.A.5. and III.B.3.), and the digestion event Blaxter (1966)), although field observations attest has to be considered. In the following, I will use that bright moonlit nights can provide enough illu- five events for particulate feeders: 1) detection, 2) mination for some feeding. Moonlight feeding abii- pursuit (i.e., the attack is decided), 3) capture (i.e., ity is described for Clrtpea harengits (Blaxter, loc. the pursuit is successfull and the prey is sucked into cit.), Oncorhyncus nerka (Narver, 1970), arid the buccal cavity), 4) retention (i.e., the prey, ready Micropterus salmoides (Elliot, 1976). Melaniris to be ingested, is retained on specialized entrap- chagresi (Zaret & Suffern, 1976) positively select ment structures, such as, gill rackers, microbran- Diapiomus gatunensis during moonlit or starlit chiospines, branchial tooth plates), and 5) diges- nights when the water is calm. tion (i.e., the prey is attacked by the digestive In a recent paper, Gliwicz (in press) shows that iii enzymes); and three events for filter feeders: 1) cap- Cahora Bassa Reservoir (lower Zambezi, South ture, 2) retention, and 3) digestion. East Africa) fluctuations in population densities of four cladoceran species are induced by drastic A changes in mortality due to variable predation pres- A. Particulate feeders sures of Tanganyika sardines, Lininothrissa mio- don, associated with the lunar cycle. As a conse- 2 1. Prey detection quente of sardines feeding more intensively during full moon than during the new moon and remain- For successful prey detection, a visual predator is ing to feed on zooplankton throughout the night, dependent on the optical characteristics of the en- the decreases in densities are more pronounced in vironment: mainly the contrast in the water (which lcss transparent and larger Daphnia and Cerio- is determined by the ambient light in the water daphriin than in smaller Diaphanossma and Bos- column), the inherent prey conspiciousness (which mina. Moreover, change in feeding intensity with is a function of size, shape, pigmentation, contrast, the lunar cycle does not affect eight abundant and behaviour), and the visual acuity of the preda- species. Gliwicz (loc. cit.) observes that, for tor (defined by its visual field and its contrast per- a few nights after the full moon, sardines may make ception). Behavioural and environmental factors use of a ‘trap’ set up by the timing of the sunset and control the predator’s success rate at each step. the moon rise. During nights following lhe full moon, when one to three hours of complete dark- Dependence on light: inzportance of light contrast ness are followed by the sudden rise of a nearly full for visual predators. Particulate-feeding plaiik- moon, zooplankters come close to the water sur- tivorous fishes are highly selective on individual face and are suddenly exposed to sardines and deci- food items. Visual feeders are dependent on lighl to mated as soon as the moon rises. At this time feed- discriminate among prey particles. Selectivity of ing raies would be extremely high: from 1.6 to 3.2 visual predation is sensitive to light and drops off captures per second, in conditions of low prey den- at low light levels. Suffern (1973), by recording the sities (such as, 5 Bosrnina per liter). Such high feed- number of Daphnia galeata ntendotae eaten by ing rates were observed in Eimnothrissa laboratory shiners (Cyprinidae) in a given time period and for experimcnts, but only at high prey densities (i.e., 30 different light intensities, showed that feeding Bosmina per liter, and 200 Eudorina per liter) and selectivity of visual predators is light dependent. under high illumination (daylight). The higher Although the alewife (Alosa pseudoharengus) can availability of moonlight on nights around the full feed in the dark, its feeding is ‘not selective’ (Jans- moon attracting sardines to the offshore area lo sen, 1980): which means that the feeding is not feed .on cladocerans (which are less sensitive to the directed at individual prey (i.e., passive prey selec- light of the moon), together with the moon trap al- tion). lowing sardines for more efficient feeding on Particulate feeding depends on light intensity. cladocerans and copepods (which are more sensi- Many particulate feeders stop feeding after sunset tive to the moonlight) may be important in induc- when natural light intensity is almost zero (less ing the lunar cycle of zooplankton population den- than 0.1 lux for golden shiner, Noternigonus crys- sities. oleucas (Hall et al., 1970); see also references in Gliwicz (loc. cit.) emphasizes that, as the moon I

trap may be more efficient in the tropics because ments, 15-spined sticklebacks (Spinachia vertical trajectory of the moon permits more feed- spinachia) prefer darkened mysids (Neornysis in- ing by planktivorous fishes, the lunar cycle may be teger dipped in powdered carbon) to the same body considered in estimating the abundance of sized light mysids (daylight-adapted) (Kislalioglu & zooplankton. For example, samplings performed Gibson, 1976). with a frequency of a little less or a little more than In marine environments also, more visible prey 28 days would have produced either a gradual de- are selected by planktivores. Jack mackcrel crease (if started just before the full moan) or an ( Trachurus symmetricus) larvae select prefcrentially increase (if started soon after the fist quarter) over bright coloured organisms, such as the harpacti- several months. Gliwicz suggests that planktonic coid Microsetella norvegica (Arthur, animals have not yet evolved adaptative strategies 1976). According to Zaret (1980), the conspicious- to detect the moon trap because of various reasons, ness of a prey is determined not only by its inhcrent such as: 1) the trap set by the timing of the sunset total visibility (which is mainly influenced by its and the moonrise is more difficult to detect, espe- more visible body part), but also by the range of cially, by animals with life span shorter than lunar visual acuities of the fish in the present light condi- month, 2) perfectly functioning moon traps are not tions of the aquatic environment. common, 3) local populations that are adapting to Zaret (1969, 1372b) demonstrated that prefer- them may be swamped by gene flow from popula- ences by Melaniris chagresi (Atherinidae) for one tions that are not experiencing them, and 3) evolu- of two similar sized-morphs of the cladoceran tion in clones is slow whereas in vertebrate Ceriodaphni0 cornuta is highly correlated with the predators is fast. difference in diameter pigmentation. The eye of the preferred morph possesses a pigmented area up Prey conspicousriess: prey visibility and behaviour. to SOYO larger than that of the other’s. As light de- Prey conspiciousness is a function of morphologi- pendePt predators, Melaniris see more easily the cal characteristics, including size, shape, contrast, high contrast of the large black and pigmentation. It is also influenced by the prey against the rest of the transparent prey body. Con- motion behaviour (which modifies the time of di- fer & Blades (1975) suggested an alternative expla- rect exposure to the predator) and the light contrast nation for the results of Zaret (loc. cit.) as the den- between the prey and its background. Contrast is a sity of the preferred large-eyed morph of C cornuta major component of underwater prey visibility offered to Ad. chagresi was twice the density of the (Lythgoe, 1968). Both the inherent contrast be- small-eyed morph. Other laboratory experiments tween differentially pigmented areas of the prey using cqual initial densities of large-eyed morphs body and the relative contrast between these and supereyed (i.e., small-eyed morphs previously differentially pigmented areas and the environmen- fed on a solution of india ink particles develop a tal background, contribute to the total visibility of greater black pigmentation area behind the eye) the prey to the predator. For a prey to be conspi- showed that Meluniris shift their preference to- cious, its body structures must differ from each wards the small-eyed morphs with supereyes (i.e., other and the background in brightness (Le., con- the most visible among the two Ceriodaphnia trast), wavelength distribution (i.e., colors), or both morphs) (Zaret, 1972b). As a consequence of (Levine et al., 1979). changes in fish visual predation intensity, prey of As a consequence of the heavy pigmentation of lower inherent contrast (or total visibility) may be Daphnia’s (ephippia are sexual eggs of favoured against more contrasted ones. For exam- cladocerans and copepods), pumpkinseed sunfish ple, many Daphnia species produce cyclomorphic (Lepomis gibbosus) and yellow perch (Perca morphs less attractive to fish predators. As ob- flavescens) selectively feed on ephippial over simi- served by Zaret (loc. cit.), the reduced compound- larly sized non-ephippial D. galeata rnendotae in a eye morphs that are produced, suffer a lower rate of Connecticut pond (Mellors, 1975). Moreover, in fish predation. Lakes Ontario and Erie, Clemens 6c Bigelow (1922) Another example emphasizing the importance of mentioned that ephippia were abundant in the body visibility ia prey detection by visual predators stomachs of ciscoes (kucichthys spp.). In experi- was given by Zaret & Kerfoot (1975): studying 110

Melaniris feeding on Bosinina longirostris, they Daphnia may be the reason why hemoglobin is have attempted to separate the respective effects of produced only during stressful situations or in the prey body size and total prey visibility (determined absence of fish. Hemoglobin production by Daph- by Bosmina eye-pigmentation diameter) on preda- nia was observed by Fox (1948) in ponds normally tor electivity. They observed Melaniris feeding not containing fishes. selectively upon Bostnina individuals having the Aspects of prey morphology other than eye pig- greatest amount of eye pigmentation, and not ac- mentation, have been demonstrated to contribute cording to prey size. In this type of situation, size- to total visibility and vulnerability of prey to preda- selective predation appears to be a less important tors, such as: pigmentation of the in pressure than visibility-selective predation on Chaoborus obscuripes (Stenson, 1980), and gut zooplankton communities. Comparing the rela- pigmentation from ingested algae in Daphnia (Vin- tionships between eye-pigmentation diameter, be- yard & O’Brien, 1975). Motion behaviour also can- fore and after Melaniris predation, and body tributes to the conspiciousness of prey. Different ia1 length, the correlation presents both a lower coeffi- vulnerability of cyclopoids and calanoids to preda- cient and a smaller slope after predation. The tion by planktivores can be analyzed through dis- authors interpreted these results as a selective pre- criminatory considerations, such as prey motion dation of Melaniris according to eye-pigmentation behaviour (the erratic jumping motion of cyclopoid diameter (i.e., the main contrasted area of the prey copepods is more noticeable to visual planktivores body). Actually, if Melaniris remove large-bodied than the characteristic gliding motion of calanoids: Bosmina (because eye-pigmentation diameter and Rroolcs, 1968; the saltatory motion of cyclopoids body length are correlated) as well as, small- attracts the attention of fish: Confer & Blades, bodied, large-eyed Bosmina, it results in a larger 1975), prey escape ability (calanoids generally es- number of large-bodied, small-eyed Bssnzina than cape better than cyclopoids: Confer & Blades, loc. before, which makes decreasing the strength and cit.; Vinyard, 1980), prey conspiciousness (stouter the slope of the correlation. However, the eye- bodied cyclopoids are probably more conspicious pigmentation diameter of BOSininQ (as well as, than calanuids of the same body size), and fish ex- Daphnia: see HrbáEek (1977)) shows considerable periencc of prey (particulate feeders learn to recog- daily photomechanical movements according to the nize visually prey, and thus use more vigorous at- illumination (contraction in light and dilatation in tacks to capture evasive copepods: Vinyard, loc. dark) which made Confer et al. (1980) discredit cit.). So, the calanoidkyclopoid ratio is usually ob- some of this eye-size work of Zaret (loc. cit.) which served to decrease with increasing predation pres- was subsequently rebutted by Kerfoot’s (1980) eye- sure by visual planktivorous fishes (HrbáEek, 1962; diameter versus pigment-diameter commentaries. Grygierek, 1962; Brooks 8L Dodson, 1965; HrbáEelc Because the fish select the largest and more conspi- & Novotna-Dvorakova, 1965; Grygierek et al., 1966; cious individuals of the prey population, and not Wells, 1970; Hutchinson, 1971; Hillbricht-Ilkowska only the largest ones, k1elaniris shows selective pre- & Weglenska, 1973; Losos & Hetesa, 1973; Lynch, dation according to total prey visibility. But, in all 1979; Hurlbert & Mulla, 1981). Furthermore, in re- situations where the dimensions of the main pig- sponse to predation pressures, prey can develop mented area (Le., the more visible part of the prey anti-predatory behavioural patterns lo spatially body) are highly correlated with body size, the con- segregate themselves from predators during periods sequence of visual fish predation would be a reduc- of peak susceptibility (see thc abundant litcrature tion in the mean body size of the prey population, published on vertical and/or horizontal migrations even if the fish is visibility selective. of zooplankton towards less exposed habitats), or Vinyard & O’Brien (1975) have shown that the reduce individual prey vulnerability when exposed rate of predation on hemoglobin-containing D.prt- to predators (patch formation). Together, morpho- lex is higher than on individuals not containing he- logical and behavioural characteristics are responsi- moglobin. Hemoglobin-containing D. pulex are not ble for the conspiciousness or zooplankters to visu- commonly found in lakes: although this species can al zooplanktivores. produce hemoglobin, it is almost always clear. In- creased predation on hemoglobin-containing Visual acuity of jïslies: contrast perception and vis- 111 ual field. The physical and physiological properties should select the most visible prey, i.e., the larger, of the of fishes determine the effectiveness of farther one. It should be added that fish have two their vision underwater. The relevant parameters eyes and so can control the distance between prey are: the contrast perception threshold (which is the in the space by other means than by apparent-size. most important as it limits the maximum visible A fish is also moving and thus, the image of more range of an object), the spectral sensitivities (to dis- distant objects are moving on the retina slower than criminate colors), and various measures of acuity that of closer objecls (HrbhEek, in litt.), (Hemmings, 1974). Recent studies on the nature of Muntz (1974b), summarizing behavioural data fish vision have pointed out the importance of light on vision of Slardinius eryttiophtlzalrnus (Cyprini- contrast for prey detection by planktivorous fishes dae), concluded that contrast thresholds for fish (Hemmings, 1966). Hester (1968) demonstrated are very important since they determine the greatest that visibility of prey depends mainly on light con- rangc at which objects can be detected. The most trast at all light levels, and only on light contrast at visible objects underwater will presumably be large low light levels. Ingle (1971) established that fish objects that have a high inherent contrast with their visually discriminate between objects on the basis background. Smaller objects and objects having of their size, color, contrast, distance, orientation, low inherent contrast will disappear at much short- and motion. er distances. Munlz (loc. cit.) used evolutionary In experiments upon underwater resolution acui- considerations lo investigate the adaptative re- ty, Muntz (1974a) emphasized that if hypotheses sponse a predator could develop to see prey more are to be made about the visual efficiency of fish, easily, such as: nearer objects brighter than the spectral sensitivities, acuities and contrast percep- background, can bc best detected by retinal recep- tion thresholds must be known for the species con- tors less sensitive to the background (i.e., offset vis- cerned. Contrast perception thresholds for the ual pigments; so that the objects appear brighter), goldfish (Carassiusauratus) have been described by while, inversely, intrinsically less visible objects, Hester (1968), while resolution acuities have been darker than the background, will be best detected obtained for two pelagic species by Nakamura by receptors morc sensitive to the background (i.e., (1968). Hemmings (1974) suggested that measure- matched visual piginenls). Thcse arguments are in ments of optical properties of water in which the agreement with Lylhgoe’s (1968) contrast sensitivity fish live could demonstrate whether its behaviour is hypothesis for vision under photopic conditions. intensivity- or visibility-related. Planklivorous fishes, such as the common gold- In a recent paper on the ecological fish, Carassius aurwtus (Cyprinidae), are also able in fishes’ vision, Lythgoe (1979) presented evidence to discriminate among individual moving prey that in underwater environments at natural light (Protasov, 1968). In a neurophysiological study of conditions, large prey farther from the predator are trout, Galand Bt Liege (1975) recorded different more visible than closer and smaller ones. He as- types of retinal ganglion cells. Some of which are sumed that at wavelengths where the water is more specialized motion receptors, while others are on- transparent, contrasts for bright close objects may receptors, off-receptors (some of which are direc- be relatively low, but will reduce less rapidly with tionally sensitive), either spontaneous or continu- distance, until at limits of visibility all (large) ob- ously activated units. Some ganglion cells have jects remain most easily seen. These results draw their activity dependent on light inlcnsity, and otli- upon the interpretation of the previous model of er large scope units respond to movements. Thus, ‘apparent-size’ developed by O’Brien et al. (1976) as previously shown by Ware (1973), a moving prey (see section V.A.l.) to describe the selective preda- is more successfully detected by rainbow trout tion of bluegill sunfish. Their model predicts that (Salmo gairdneri) than a relatively non-moving when the fish is faced with similar prey of different one. Goldfish also possesses receptors specialized sizes, the fish selects the apparently largest one. to distinguish between two types of movements Thus, Lythgoe’s paper may provide some help in which lead to different fish behaviours (Ingle, answering the basic question of distance percep- 1968). Slow background movement induces a swim- tion: How do the fish discriminate between a large ming behaviour from the fish, while a fast moving prey farther away and a small one closer? The fish object may induce a pursuit and attack behaviour. 112

So, within the visible range of the fish‘s vision, mo- sequently, the fish must rely on other cues to distin- tion may increase the conspiciousness of a prey, in- guish prey from seston. itiating ‘the response of these specialized retinal The detection rate for each prey species is deter- photo-receptors. mined by both the concentration of the concerned Janssen (1982) determined that to forage on prey in the environment and the volume searched zooplankton a facultative planktivore, bluegill, by the predator. The volume visually searched by a uses a hover-search method in the , particulate feeder per unit of time (i.e., the reactive whereas an obligate planktivore, blueback herring, field volume) is a portion of its visual field. The im- uses a swim-search method in the pelagic coastal portance of the volume searched for feeding in rela- areas. He emphasized that the presence of motion tion to the visual field increases with increasing detectors as a part of the visual processing system fish swimming speed. The lateral position of the would be detrimental to bluegill in locating prey, fish’s eyes determined the visual field, which is because the searching while swimming fish would nearly spherical in most teleosts (Bond, 1979). be falsely stimulated by images of background ob- However, because of the elliptical shape of the reti- jects (such as vegetation) moving accross its retina. na, relatively distant lateral objects are in focus, The total search time of a bluegill is partitioned while close objects are not, and near anterior ob- into time actually searching and time moving be- jects in the binocular field are in better focus than tween search locations. Bluegill searches while more distant objects (Tamura, 1957). Although all stopped (hovering). If a prey is sighted, it swims to fishes do not have equal accomodation abilities to it, sucks it in, then to a stop, and searches distant vision, these two regions of the visual field again. Janssen (loc. cit.) suggested that hover- (mono- and binocular regions) are used differen- search used by is adapted to heterogene- tially during the predation-act. The relatively dis- ous backgrounds where detection of prey motion is tant lateral (and monocular) vision is used mainly important, and swim-search used by herrings is to detect prey (or predators), and then, the near useful where the background is not heterogeneous. sharp (land binocular) vision is used to pursue and In fact, facultative planktivores, such as bluegills, capture prey (Protasov, 1968). Vinyard & O’Brien are planktivorous in their juvenile stage. Much of (1974) found that bluegill reactive distance (i.e., the their foraging occurs in the littoral zone where the disfaince at which a prey can be seen by the fish) background is often broken by vegetation, and ses- decreases with decreasing light intensity or increas- ton is more prevalent. Works on anurians show that ing turbidity (see Fig. 1). They showed that at high a presented with one visual stimulus is not dis- turbidities and/or low light intensities the reactive tracted by a second visual stimulus (i.e., the frog at- distance becomes nearly independent of prey size. tempts to pursue the first prey detected: Pigarev & The same result was predicted by the model devel- Zenkin, 1970), because the neurological activity oped by Eggers (1977): reactive distances are in- evoked by one prey effectively ‘shuts off‘ the rest of dependent of prey size or shape if the inherent con- the prey detection system (Didday, 1976). Anurians trast of the prey object is low, if turbidity is high, search stationary and do not move their eyes, as any. or if light intensity is low. The shape and size of the eye or body movement may inhibit the detection of visual field explored by a fish during the detection movement (Muntz, 1977). The prey detection sys- step (i.e., the reactive field volume) can be estimat- tem of a frog is desactivated during jumps while ed by measuring the reactive distances (Le., the other visual processing systems remain active maxirnum distances), and corresponding angular (Pigarev et ai.? 1971). Bluebaclc herring possesses directions, at which a specific prey item is detected visual motion detectors to discern the movements (see section V.A.1. on models of prey selection). of prey and non-prey moving across the retina, un- Generally, the detection of an elusive prey elicits an til the prey is directly in front of the fish. But, as S-shaped movement from the fish. blueback herring searches above its swimming track (Janssen, 1981) the prey is never directly in 2. Prey pursuit front of the fish, until at final, the fish swims up to take it. Thus, motion may be unimportant for Dependence on prey size, disíribcctiori, and density. the detection of prey by a swimming fish, and con- At low prey densities fish feed in a rather non- 113

inittutus by captive alewives (cyclopoids were not 30- present). Werner & Hall (1974).,,in-similär laborato- ry feeding experiments, provided identical results --5 using juvenile bluegills feeding upon different size W categories of the cladoceran D. magna. 'Thcy 2 20- demonstrated that planktivore preference is a t- proportional to prey body size, and that the fish be- 2. gin to feed significantly on the smaller size categor- P ies only after the decline in abundance of the larger !$ 10- preferred prey size categories (see Fig. 2). t; w-a Dependence on fish hunger. The mechanisms of 'II: food intake regulation are not completely known. However, il is admited that the feeding in ver- O-' O-' O I 2 3 tebrates is controled by instantaneous signals sent PREY SIZE (min) from stretch receptors in the gut musculature to the -iliuminance (lux) central nervous system (Hamilton, 1965). Feeding 11-1-11 turbidity (JTU) rates and stomach fullness tend to be inversely related. In laboratory trials with rainbow trout Fig. I. Relationships between reactive distance of bluegill, Lepornis niacrochirus (Centrarchidae) and prey size for differ- (Snlrno gairdneri) deprived of food for 48 hours, ent illuminances (dotted lines, in lux units) at low turbidity Ware (1972) determined that (1) the pursuit rate on (I JTU), and for different turbidities (continuo~slines, in JTU two species decreases significantly units) at a constant illuminance (34.9 lux) (from Vinyard & with decreasing fish hunger and prey density, and O'Brien, 1976). (2) the handling time of prey (i.e., the amount of time necessary to pursue and capture an individual prey, which is equal to the inverse of the maximum selective manner on different prey types (and sizes): feeding rate) increases progressively when ap- each prey detected is pursued and eaten. At higher proaching satiation. Ware (loc. cit.) emphasized prey densities fish concentrate on the largest prey that the rate of prey pursuit by visual. planktivores sizes (Ivlev, 1961). In laboratory feeding experi- is not proportional to the prey density because a ments, Brooks (1968) showed the preferential certain time (which duration is dependent upon the removal of the largest adult-size class of Diaptoinus internai nutritional state of the fish) is required to

r -WJ IL (number of prey per olasol ?- 1.1- a Q 12 IL O or8 W Ba

2zf? 2 Q W I IV II I IV II I IV II I IV II I IV II I IV II 1

Fig. 2. Mean number of each size class of Daphnia tnagtin eaten per Lepornis macrocliirtrs (Centrairhidae) for expel inients at difrcrent prey per class densities (class IV 1.4 t 0.05 mm, class II: 2.5 t 0.07 mm, class I: 3.6 4- 0.05 mm). The striped areas repiesent the expect- ed numbers in stomach if items are eaten as encountercd (computed from the visual field ratios): deviations from the expeclcd show that positive seleclion is increasing as a function of prey density (from Werner & Hall, 1974). ~

114 handle each prey item attacked (see a discussion of an intact prey they can swallow. Because of the about the role of handling on the rate of prey con- small size of their mouths, the youngest fishes ini- sumption in Holling, 1966). tially select small zooplankton. During growth, they feed progressively upon larger prey. This maxi- Dependence on fish experience of prey. To explain mum size selection imposed by the fish’s gape is the selective interest of predators for certain prey well documented for young yellow perch (Perca types, a learning mechanism to discriminate among flavescens, see Fig.3) by Wong & Ward (1972), for prey types (and acquired by previous encounter juvenile chum salmon ( lieta) by with the prey) has been suggested by Tinbergen Feller & Icaczynski (1975), for perch fry (Perca (1960) and called the ‘searching images concept’. fhviatilis) by Furnass (1979), and for herring larvae Rosenthal & Hempel (1970) proposed this mecha- (Cfupeaharengus L.) by Blaxter (I 966) and Rosen- & nism to account for the selective feeding of herring thal Hempel (1970). 1 larvae ( harengus) on one prey type, This It is only during a brief period that larval fishes concept was used by Ware (1971) to describe the select positively the smallest and less evasive species feeding behaviour change? of rainbow trout (Salmo of zooplankton, and also, the smallest individuals gairdneri) affter repeated exposures to palatable of a siiigle species. The time duration of this gape food. He observed substantial improvements in the limitation is brief, and larvae are able to feed on thc reactive distance of an ex-prienced fish for a famil- maximuin available prey size within three to four iar food. Moreover, trout may require several days weeks of hatching (Rosenthal & Hempel, loc. cit.; of experience to transfer this learning to new prey, Wong & Ward, loc. cit.; Guma’a, 1978; Hunter, rather than the familiar me. Vinyard (1980) tested 1979). But, other factors such as the structure and the ability of bluegill sunfish to modify its pursuit the motion reaction of prey, may resull in an im- choice when encountering two distinct prey types. portant discrepancy between prey size and predator He demonstrated that the fish can use the informa- gape (Hartman, 1958). Young marine and fresh- tion concerning the prey size and escape ability. water fish larvae have a highly inefficient feeding Bluegill displays differential capture behaviours ac- behaviour aiid poor visual acuity. Food organisms cording to the prey type detected. During laborato- are most frequently perceived at very short dis- ry feeding trials, blueg;li discriminates between copepod and cladoceraz, bmgactive and vigorous motions to capture Diaptoinus pallidus and com- paratively leisury ones io capture . Vinyard (Ioc. cit.) attributed this shift to a learning process based on the rormation of searching im- ages of the prey (Tinbergen, ioc. cit.). Thus, in par- ticulate feeders, the previoùs experience of the fish for different prey types may alter, not only the pur- suit choice (if prey are detected simultaneously), but also the capture success (Confer & Blades, 1975; see section III.A.3. and V.A.I.).

3. Prey capture

The capture success rate of planktivorous fishes depends on both the capture efficiency of the pred- ator and the escape ability of the prey. PERCH QAPE WIDTH (mm) #Gapeliniitatiori of larvue 2nd miall species. Plank- Fig. 3. Relation between yellow prrch (Pb-ca ,//wescens) fry tivorous fishes (sensu Zaret, 1980) are ranked moulh gape width and body depth of Dophuia pitlicnrin found ,among ‘gape-limited predators’ (G.L.P.) when their in perch stomachs,(n = 771) of West ßlue Lake (Manitoba) dur- mouth diameter, or gape, limits the maximum size ing the summer of 1,969 (froin Wong & Ward, 1972). 115 tances (from 2 to 8 mm for yolk-sac herring larvae, as calanoid copepods, and &lysis. Copepods pos- and from 3 to 40 mm for 15-20 mm herring lar- sess mechanoreceptors which register hydrodynam- vae), and most of them are not successfully cap- ic disturbances. When darting fishes move rapidly tured because of low velocity and poor aiming of to the prey (from about 1-2 cm distance) while the fish. Fish larvae attain more than 50% of feed- sucking, they eliminate any suction current that sta- ing success after an average of four weeks of hatch- tionary sucking would cause. In the same fashion, ing, because of the process of learning, the develop- the small lake trout (Salvelinus nawzaycuslz) is able ment of fins (faster darting), and the growth of to improve its suction abilities by. increasing its lower jaws (Rosenthal & Hempel, loc. cit.). sucking intake to capture copepods over daphnids Similarly, some obligate zooplanktivore species (Kettle & O’Brien, 1978). When feeding on Dnplr- of which individuals are smaller than 7 - 8 cm long nia, bluegill rushes to a prey, brakes momentarily are ineffective in capturing the largest individual while sucking it in, and then shifts towards the ncxt zooplankters present in the aquatic environment. item (Werner, 1977). Alewives and ciscoes operi For example, a 4 cm long guppy, Poecilia reticulata, wider their mouths to capture larger prey (Janssen, is unable to catch a 5 min long D. magna (Pourriot, 1978a), so their covered mouth sides form a suction pers. commun.). Because of the smaller diameter of tube which eliminates lateral leakage and makes the the fish mouth, the reduced volume of its buccal suction more directed. cavity, and the resulting weak suction strength and From experimental works on mechanisms of wa- poor aiming, the maximum size of prey items ter flow production over the fish , three major which can be captured intact is limited. concepts have emerged: (1) the water flow over the gills is relatively continuous with perhaps a brief Capture efficiency: effects Df experience and mouth period of low or zero flow, (2) the gills form a sig- structure. Particulate-feeding planktivores use a nificant resistance to flow (Hughes, 1965, 1976; suction process to capture individual prey items. Shelton, 1970; Hughes & Morgan, 1973; Jones & The intake current is created by an expansion of the Schwarzfeld, 1974), and (3) a ‘double-pump’ mech- buccal cavity. Obligate planktivores (such as white- anism involving a buccal force pump and an oper- fish, alewives, smelt) have rounded mouths to pro- cular suction pump is responsible for moving water duce greater suction bpeeds. Facultative plankti- over the gills. Suction feeding in teleosts fishes is a vores (such as salmonids>,more adapted to capture highly dynamic process lasting only 20- 100 ms, in- larger prey, have large noched mouths. The capture volving large accelerations, and producing a single efficiency of planktivorous fishes depends on their rapid pulse of waler through the mouth cavity previous experience arta ~;leprey type (Ware, 1971, (Lauder, 1980a). Besides technical difficulties as- 1972; Confer & Blades, 1975; Janssen, 1978a; Vin- sociated with measuring rapidly fluctuating pres- yard et al., 1982). By learning to recognize prey sures, attempts to understand the hydrodynamic items, principally according to their motion be- aspects of teleosts feeding have relied heavily on haviour, plantivores may improve their capture suc- concepts borrowed from studies of fish respiratiqn cess, as demonstrated by beukema (1968) for three; (Lauder, 1980b). spined stickleback (Gusterosteus aculeatus). Beuke- A first theoretical model of suction feeding has ma’s studies support thc bearching image concept been outlined by Osse & Muller (1980) and Muller reviewed by Tinbergen . >ho). As concluded by et al. (1982). In this model, the gill bars and fila- Ware (1972), learning to recognize prey is a positive ments are not included (in contrast to models of feedback to improve the capture efficiency of ver- fish respiration: Hughes & Woakes, 1970) and the tebrate predators. plays a decisive role in generating ‘both’ While particulate feeding is used by alewives buccal and opercular cavity negative pressures. Per- (Alosa pseudoharengus) and ciscoes (Coregonus forming experimental tests of the feeding mecha- artediil to capture weak zooplanktonic swimmers nism in bluegill sunfish, Lauder (1983) refuted this (such as, cladocerans, cyclopoid copepods, and previous model and demonstrated an alternative swimming amphipods), a specialized particulate hydrodynamic model of high-speed suction-feeding feeding mode, named ‘darting’ by Janssen (1978a), processes in fishes. He showed that buccal pres- is employed to capture evasive zooplankters, such sures always exceed opercular pressures, as, in nor- i 16 mal bluegills feeding by high-speed inertial suction, eificiency by learning to recognize mobile prey and opercular pressures reach a maximum of about altering their feeding mechanics (for example, piey - 120 mmHg, whereas buccal pressures attain sucked in at a closer distance, water intake speed in- values of -500 mmHg. These large negative pres- creased, as well as other adaptative behaviours), the sures are achieved only during very rapid strikes at prey escape ability is only a secondary determinan1 elusive prey. Lauder’s results indicate unambigu- affecting the selectivity of particulate feeders for ously that (1) the gill bars function as a resistant zooplankton (Confer & Blades, 1975; Vinyard, element within the mouth cavity (and not the gill 1980). But, it is determinant in controlling the array filaments of the primary and secondary lamellae as of prey ingested by filter feeders (Starostka & Ap- during respiration), and (2) the abduction of the plegate, 1970; Drenner et al., 1978; see section operculum by the dilatator operculi plays little role III.B.l.). in generating negative mouth cavity pressures. Modelling the relative capture frequency of Lauder (loc. cit.) emphasized that these conclusions zooplankton by visual-feeding pumpkinsecd on gill resistance apply mainly to fishes feeding by (Lepomis gibbosus), Confer & Blades (1975; sec high-speed suction using extremely unsteady flows, section V.A.1.) observed that: (1) when Lepotnis (2) species that use body velocity to overtake prey was fed Daphnia for several days and rhen cspc- (for texample, tow-net fiiter feeders) will probably pods, the initial capture success for copepods (i.e., exhibit a somewhat different pattern of buccal and the ratio of the number of prey ingested to the opercular cavity pressure changes, and (3) only number of prey pursued) was low, (2) tlie capturc high-speed suction-feeding fishes and fishes using success of copepods varied daily, probably follow- a slow to moderate approach velocity are likely to ing rapid fish learning and forgetting, (3) some spe- exhibit large pressure differentials accross the gills. cies of copepods were highly successful al eluding For example, pike () which utilizes rapid ac- the fish capture (for example, they reported capture celerations from rest and large amplitude move- success of 79% and 39% for Diaplormis sicilis and ments during prey capture (Webb & Skadsen, 1980), D. asldaiidi, respectively), and (4) lhe capture suc- opens its mouth well before the prey is reached, cess of several specie.; of Daplinia was nearly 100070. maintains its mouth and operculum abducted at Emphasizing 1 he extremely dynamic capture of near maximum level till the final stages of the particulate feeders for evasive cogcpods, the strike, and possesses long and slender gill bars authors assumed that no single value was entirely which do not lie snugly against each other in the satisfactory, and uscd an 80% approximation (i.e., abdwcted position. Thus, during prey capture by the avcrage capture success for six dates). Esox, no pressure differential exists accross the gills. In contrast, bluegill has much slower attack 4. Prey retention velocity (5 -40 cm s-I) and produces the highest pressure differentials. In the normal rest position Many works have emphasized the discrepancy be- during quiet respiration, only a small opening is tween the size of the smallest prey ingested by par- present between each pair of gill bars, whereas in ticulate feeders and the minimum spacing between the early stages of suction feeding, the gill bars are their gill rakers (Galbraith, 1967; Jcliewer, 1970; abducted as the gill cover and suspensorium move Seghers, 1975). The role of the retention event in medially (Lauder, 1980a). Finally, Lauder (1983) the prey selection of particulate feeders remains of- stressed that (1) buccal pressures in all high-speed ten unclear. Theoretically, the retention probabili- suction-feeding fishes studied to date exceed oper- ties of the branchial filters are determined by the cular pressures, and (2) predictions based on cur- cumulative frequency distribution ‘of interraker rent mathematical models of feeding mechanism spacings. If truc, the passive sieving mechanism (at least for rapid prey capture by inertial suction, (generally assumed to be the dominant mechanism and despite adjustments by assuming relevant bio- in biological filters) can be tested by comparing this logical constraints) fail to characterize, even gener- distribution with the size distribution of the ingest- ally, the relative magnitudes and waveforms of ed prey. pressures measured experimentally. The attack of particulate feeders is directed at in- Since visual predator> can increase their capture dividual prey, but more than one prey may be in- 117

gested at a time (Wright et al., 1983). Small bodied pattern, and (2) the largest and most selected prey prey with poor evasive capability are often ingested have low evasion ability, as some attacks may be incidentally through passive selection (determined directed at other smaller prey. by the mesh size of the filter). The probability of incidentally ingested prey increases with increasing 5. Prey digestion: resislame of zooplmkton to ,fish prey density in the environment. In order to exam- digestion processes ine the filtering process of particulate feeders, Wright et al. (loc. cit.) trained white Some zooplanktonic or phytoplanktonic organ- (Pomoxis annularis) to attack preferentially large isms can pass undigested through the gut of plank- bodied D. magna when presented with dense as- tivorous fishes, and survive when released from the semblages of small zooplankton. Small prey, in- fecal pellets in the environment, escaping preda- gested incidentally during the active directed inges- tion. Moreover, in the presence of high levels of tion of individual D. magna, are assumed to be predation pressure, survival through resistance to included into the diet solely by retention on the gill digestive processes may have anolher adaptative rakers. The authors observed experimentally that value: it is a possible means of prey dispersal which white crappies do not ingest small non-evasive results in an evolutionary trend towards prey popu- Ceriodaphnia sp. in the proportion of their densi- lations dominated by especially resislant individu- ties in the pool. The retention probabilities deter- als. mined from the cumulative frequency of the inter- The digestion efficicncy for a specific zooplank- raker spacings on the first arch disagree with those ter in a fish gut depends upon the composition of determined by incidental ingestion estimates (com- the gastric juices (presence of effective enzymes), puted, versus prey size, as the ratio of the average the transit time, and the composition OF the percent per 0.04 mm prey size category in the stom- zooplankter's cuticule. Zooplanktonic organisms ach divided by the corresponding value in the ex- are generally easily and quickly digested by plank- perimental pool). Both retention probabilities are tivorous fishes (Cannon, 1976). Nevertheless, prey sigmoid functions increasing with prey size, but the survival after ingestion by fish can occur among curves of incidental ingestion and interraker spac- sonic zooplanktonic groups. ings reach a 100% retention success for Ceriodaph- Punipkinsced sunfish and ycllow perch feed nia sp. at different prey sizes- (0.70 mm and selectively on (darker and more conspicious) ephip- 0.24 mm, respectively). Although some experimen- pial D. galeatu nieridnfae, over similarly sized non- tal biases were mentioned by the authors, such as: ephippial D. galeuta r?iendotae (Mellors, 1975; see (1) the interraker spacing estimates may have sig- section III.A.1.). Mellors (loc, cit.) observed that nificantly overestimated the actual retention proba- some ephippial eggs of W. galeatu mendotue can bilities, as the interraker spacings increase with the survive the ingestion and the passage through the degree of buccal cavity expansion, (2)., the first arch fish gut. But the percentages of hatch and overall may not be the main functional retention site for egg survival remain low (smaller than 15%). Al- prey, and (3) individual prey smaller than 0.24 min though ephippium production increases the vulner- were not tested in the experiments, Wright et al. ability of Daphnia to fish visual predation, lhe sur- (loc. cit.) came to the conclusions that: (1) interrak- vival of ephippial eggs after the passage through er spacing measurements are seriously biased, fail the predator gut appears to reduce the conse- to estimate the actual retention capability of the quences of their selective capture. Neverthelcss, it branchial filter, and shodd be interpreted with may be noted that ephippia and other longevity great caution, and (2) the retention process appears eggs are not organisms, but resistance forms. to be more dynamic than a simple passive sieving However ostracods do not belong stricktly to mechanism (but see Drenner et al., 1984a). plankton, but to , Vinyarcl (1979) round From these results it can be emphasized that in- that 26% of the ostracods Cypriodopsis viducr in- cidental ingestion may not be a main contributor to gested by small bluegill sunfish (39-59 mm SL) the feeding selectivity of particulate feeders, except survived the passage through the fish gut, and ap- when (1) small bodied and poorly evasive prey are peared undamaged and fully active in the feces. present at high densities or distributed in a clumpy Moreover, 24% of rejected dead ostracods did not 118 show net evidence of digestion. Since ostracods in May-June. Dawidowicz & Gliwicz (loc. cit.) em- may occasionally reach high population densities phasized that resistance of sexual eggs, (Sandberg, 1964), the high percentage of surviving including ephyppial eggs of cladocerans (Mellors, ostracods has wide implications relative of both 1975) to fish digestion processes may not be only an prey and predator. For example, Ivlev (1961) ob- important to escape predation by served only a significantly negative electivity for planktivorous fishes, but also an adaptation which the ostracod Cypris sp. when fed, together with favors the fish themselves, since their planktonic Daphnia, Bosmina, and , to bleak (Al- food resources do not become overexploited. These burnus albumits), and Vinyard (1979) noted occa- authors wondered to what extent this phenomenon sional rejections of ostracods by bluegill. Fish may be considered as a Co-evolutive process. avoidance of ostracods when alternate prey are simultaneously available may be the result of a B. Filler feeders learning process. Since the fish expands energy in the capture of the prey and receives no energy in re- Contrasting with the well-documented size- turn through assimilation, the fish may learn to selective impact of particulate-feeding fish, there is recognize and avoid such undesirable prey organ- a lack of information concerning the selective in- isms. gestion of plankton by limnetic filter-fceding fish Another mechanism which reduces the fish and the dynamics of plankton communities in re- digestion efficiency has been suggested by Vinyard sponse to these fishes. Filter-feeding fish feed on (loc. cit.). High total ingestion rates, which occur in plankton by engulfing or sucking a certain volume the presence of dense prey populations (or in en- of water containing prey items into the buccal cavi- vironments rich in suspended matter), and the con- ly (see section 1I.B.). Their feeding behaviour is not secutive rapid passage through the fish gut (due to visually directed at individual prey, and therefore, reduced transit times) may result in high survival filter-feediiig fish may capture more than one prey rates of ingested prey. at a time. Prey are encountered in proportion to Studying brook charr (Salvelinusforzfinalis~pre- their densities in the water, and captured according dation on abyssoriiin tatricus copepodites to both lhe differential escape abilities of the prey (IV and V) and adults in oligotrophic Lake Zielony items, and the capture efficiency of the fish which (Tatra Mountains, Southern Poland), Dawidowicz is dependelil upon ehe feeding behaviour displayed & Gliwicz (1983) observed that a) egg-carrying Fe- (Drenner et d.,1378, 1984a). Because the detection males were highly selected over egg-free females, and pursuit events cannot cause selectivily, the males and copepodites, but b) removal from thc predaiion-act of filter feeders is reduced to only lake of most copepodites and adults of C. CI. (atri- three successive events: 1) capture, 2) retention, and cus by charr, instead of causing serious damages to 3) digcstion. the Cyclops population, rather favoured it. Gliwicz & Rowan (1984) showed that the higher survival rate of Cyclops eggs and nauplii (60%) despite 1. Prey capture: I determining event for aoaplank- heavy predation by charr on egg-carrying females ton ingestion was a natural consequence of Cyclops eggs passing unharmed through the charr guts (as eggs from the Live zooplankters are able to evade suction lake and from the rear part of the charr gut hatched generated currents. To estimate the direct escape re- in similar proportions). The eggs defecated by sponse of different zooplankter species, Drenner et charr sink to the surface of the bottom sediments al. (1978) and Drenner & McComas a(1980) used a where they continue their development. As the new- simulated fish-suction intake (Drenner, 1977; Dren- ly hatched nauplii are not fed upon by their can- ner et al., 1978) and measured specific capture nibalistic parents (because adults are already re- probabilities. The capture probabilities (Drenner, moved by charr), the new generations persist in the 1977;see Fig. 4) were highest for the cladocerans C. lake in high density till they reproduce next reticulata (96%), D,galeatn imwdolctc? (92qo) and April -May. This may explain why nauplii densities D. piilex (76Vo), intermediate for Diciplianosoiìra increase after the of egg-carying females bracfiyurvnr (49'701, Mesocyclops spp. (28%) and i 19

-4- bubbles 6 heat- killed zooplankter8 100 -qp- c. reticulata 8 ma.anvep. palaata msndotae a 2 80 a. 4 o 60 w sdp.. Chaoboruo sp. c3 i-4 3 40 o Ix w a 28

o O 5 IO 15 20 DISTANCE FROM TUBE (mm)

Fig. 4. Percent of particles and organisms capturcd by the system versus their distance rrom Ihc tube. The poiiits piottecl at dis- tance 3, 8, 13, and 18 mm represent averagcs of capture frequency (i.e. success) within the inlcrvals or 1 lo 5 inni, 6 lo 10 mni, II to 15 mm, and 16 to 20 mm, respectively. The conditional probabilities mentioned in the text for live zooplankter are the ratio brtwcen the areas under the frequency curves for the live zooplankter and Lhe non-motile bubblcs and dead zooplankters (rrotn Drciiner, 1977).

Cjvlops scutifex (24070)~and lowest for Diaptomus Flemminger Sr. Clutter (loc. cit.) studied lhe avoid- pallidus (70/0) and Chaoborus sp. (9070). Thus, ancc mechanisms used by populations of cladocerans are more vulnerable than copepods to zooplankton to lowed-nets. They concluded that: the suction capture mechanism of filter-feeding (1) zooplankters can avoid the capture by ncts, be- planktivores. These results confirm the previous cause both visual and hydrostatic pressure distur- laboratory experiments performed by Szlauer bances are detected, (2) the avoidance tends to be (1965) using a glass-tube device. He showed that less in denser populations, becausc interindividual adult copepods have the highest ability to escape, interferences may restrict the escape movements of while the cladoceran B. longirostris has a null es- zooplankters, (3) lhe light intensity has no apparent cape ability. Because algae have no escape mechan- cffect on the avoidance efficiency of copepods, be- isms, filter-feeding fish require no specific capture cause, although capable of light perception, they strategies to utilize them as food. Therefore, only probably cannot form images, (4) the apparent the retention efficiency determines the selectivity avoidance efficiency differs among copepod species for motionless particles, such as, phytoplanktonii (for example, Acarfia tonsa is more easily sampled cells or colonies. They are passively engulfed into than A. clatrsi), and (5) copcpods are capable of the fish buccal cavity, captured in proportion to directed movemenl's of escaping (for example, their density in the environment, and ingested only Labidocera aciitifrvns can directed move- according to the feeding rates of the fish for the ments at a speed of 80 cm per second, Le., 230 body different available sizes (i.e., passive selectivity). lengths per second, over more than 15 cm). ßut, di- rect observations of feeding mechanisms (using Tow-net filter feeders. Although large zooplank- high speed motion pictures, video recordings, or ters, mostly copepods, detect and avoid filter SCUBA equipments) as well as indirect evidence devices used to capture plankton, i.e., net, and (given by functional morphology studies of the pump (Flemminger & Clutter, 1965; Drenner & feeding apparatus, and stomach content analysis: McComas, 1980), tow-net filter feeders effectively see also section 111.R.2.) clearly demonstrate the cf- capture large evasive zooplankters. Experimentally, ficiency of tow-net filter feeders (compared to the 120 low capability of towed nets) in capturing large eva- long) and Ariernia salina nauplii (0.4 mm long) sive zooplankters. The Atlantic menhaden (see (Durbin & Durbin, 1975). Paddlefish, Po[yodon Fig. 5B) use high swimming speed (2.0-2.5 body spathula, swims slower and strains food from the lengths per second) with wide mouth opening to water column over their gill rakers: Daphnia and graze at high rates on adult (1.2 mm calanoid copepods represent 75% of the volume of the food ingested in the stomach (Rosen & Hales, 1981). Using an artificial pump device, Janssen . D. tertiolecta (1976) demonstrated that sucking while moving at chuii * c. the prey is more effective than sucking while sta- o S. cortatum tionary to capture calanoid copepods. . T. rotula - N. Bay Walters (1966), using high speed motion pictures, A rotulo Calif. 1. - studied lhe mechanisms of filter feeding in the '-1 lbr¡ghtwell¡ D. scoinbrid wavyback skipjack, Euthynnus aJfitiis, swimming rapidly (5.9 body lengths per second) with its mouth widely opened when feeding. The 30 rale of expansion of the orobranchial chambcr was not rapid enough to produce a noticeable water 20 flow in through the mouth. Walters also observed that a 4 cm piece of Osmeridae, used as food, was 10 not forced ahead or laterally, by the rapid approach of the fish mouth opening. Moreover, when the o mouth was opened the drag of the fish was not al- tered because the size of the gill openings remained !ü L, PARTICLE LEF'JQTH ()" constant during swimming. Thus, Walters conclud- ed that the fish swam over its prey rather than sucked it in. Another scombrid, Rasirelliger karragrrrrcc fccds with its mouth opened widely and its branchial apparatus expanded nearly at its max- imum (during up to several minutes), while swim- ming rapidly. Using SCURA equipment, Colin (1976) observed this scombrid feeding in that man- ner on freshly released eggs (0.6 inni in diameter) of Lalsridae Thcillasoma sp. Tow-net filter-feeding O 200 400 800 behaviours have also been described in another L. PARTICLE LENGTH (pm) scombrid: Scoinber joponictrs (O'Connel1 &k Zweifel, 1972), among Clupeidae: Alosa pseudo- A T. rotula - N. Bay Izarengus (Janssen, 1976, 1980), Breevoortia tyran- p. rotula - Calif. nus (Durbin & Durbin, 1975), Sardiiiops caeritlea I 0. br¡ghtWUlli (Nelson, 1979), in Engraulidae: Engrcrulis inordax * A. ralina nauplii A. tQnsa (O'Connell, 1972), and in Coregonidae: Coregonus artedii and C hoyii (Janssen, 1978a, 1980). Tow-net Fig. 5. Grazing of ßrevoorfia tyrannits (Clupeidae) (A) on 5 has been suggested for the clupeid Efh- species of phytoplankton as a function of increasing size or inafosa fimbriata from stomach content analyses, chain length (0.1 pm Dunaliellu terciolectn, 10.2 ptn Carteria but direct observations are lacking (Fagade & chuii, 7.8-55.6 pni Skeletotie/na c'oslufum, 21.6 pm Thalus- siosira rotula (Narrangansett Bay) and 19.0-70.3 pm 7: rotula Olanyan, 1972; Lazzaro, unpubl. data). Most of (California clone), and 79 pm Ditylum briglitwelli, and (B) on these fishes are pelagic schooling marine (in origin, regularly shaped phytoplankton (79 pni D. Drightwelli and at least) planktivores: this may have something to 19.0 pm single cells of 7: rotulo), Artemiu sali/rsr (430 pni long), do with the predominance o'f calanoids at sea and Acarlia lonsa (I 200 pni long) as a function of length (from (Janssen, in litt.). Durbin 61 Durbin, 1975). 121

Pump filter feeders. Pump filter feeders use rhyth- than pump filter feeders in capturing adult cala- mic suctions, not directed at individual prey, to noid copepods, 3) tow-net filter feeding is probably capture suspended organisms. Periodical unusual a rather non-selective feeding mode (Janssen, 1976; swallowing movements, probably related to the see Fig. 6; Rosen & Hales, 1981), and (4) selectivity movement of food particles from the entrapment of pump filter feeders is based on prey escape abili- structures (gill rakers, microbranchiospines, ty and mechanical retention efficiency of their or pockets) towards the oesopha- filters, whereas selectivity of particulate feeders is gus, interrupt the pumping sequences of the feed- principally based on prey detection and, pursuit ing (Drenner et al., 1982b). Few studies have been since, generally, they capture pursued prey with' done on the functioning of the capture event in high success rates, pump filter feeders, except in Clupeidae: Alosa pseudoharengus (Janssen, 1978a, 1978b, 1980), 2. Particle retention: a determining event for mo- Dorosoma cepedianurn (Drenner, 1977; Drenner & tionless particle ingestion McComas, 1980; Drenner et al., 1982a, 1982b), Dorosoma petenense (Holanov & Tash, 1978), in The feeding selectivity of filter feeders for mo- Cichlidae: Sarotherodon galilaeum (Gophen et al., tionless particles (phytoplankton, and 1983b), Haplochromis iiigripinnis (Moriarty et al., microzooplankton, such as protozoans) is governed 1973), in Coregonidae: Coregonus hoyii and C ar- by their retention capabilities which depend on tedii (Janssen, 1978a, 1980), and in Mochokidae: both the structure and the functioning of their Brachysynodoiztis batensoda (Lauzanne, 1970, 1977; Im, 1977). The capture efficiency of pump filter feeders for I small zooplankton only depends on the differential es- 20 cape responses of prey species. Since their suctions IO are not directed at individual organisms, their suck- ing intake cannot be improved according to prey types (whereas that of particulate feeders can: see also section III.A.3.). In contrast to tow-net filter feeders, pump filter feeders, which create pressure disturbances when sucking in the water surround- ing the prey items, are poorly efficient in capturing filter large evasive zooplankters (Starostka & Applegate, feeder8 1970; Drenner et al, 1978; Drenner & McConias, 1980). In laboratory feeding trials, Drenner et al. (1982~) demonstrated that pump filter-feeding Sarotherodon galilaeus have feeding selectivities in- creasing with prey capture success. The selectivities were significantly higher for Ceriodaphnia reticula-' water ta, Bosmina longirostris, Diaphanosorna brachyu- rum and Mesocyclops leuclcarti nauplii, and lower for Mesocyclops copepodites and adults. In similar trials, Gophen et al. (1983b), showed that pump filter-feeding blue tilapia, lr: aurea, are escape- selective predators on zooplankton, selectively .44 .pP 1.09 1.92 1.62 1.91 2.20 2.50 feeding on non-evasive prey, such as Bosrnina sp. Ddphnia length (mm1 and Ceriodaphnia sp., over more evasive prey, such as Therinocyclops sp. copepodites and adults. Fig. 6. Daphriin length distribution it! tcst water and Alosa In summary, (1) tow-net filter feeders are less sen- pseudoharengus (Clupeidae) stomachs of varioris feeding modes. Arrows denote median prey size for fish: particulate sitive than pump filter feeders to the escape ability feeders are highly size selective, gtilpers are less, and filterers are of prey, tow-net filter feeders are more effective not (from Janssen, 1976). 122

branchial filtering apparatus. For a long time, filter Beside sieving, direct or inertial interceptions of feeding in fishes has been considered as a simplistic particles are mechanisms which can potentially be sieving mechanism, during which particles too involved in the retention process of planktivores. large to pass through the spacings of the filtering Electrostatic attraction has not yet been demon- mesh are retained. In most fishes, the filtering mesh strated to be a determining factor. Gravitational is primarily represented by the gill rakers structure, and motile-particle depositions are probably insig- which is particularly complex in Clupeidae and nificant mechanisms for fast swimming (i.e., tow- Coregonidae (Monod, 1949). Thetgill rakers are set net filter-feeding) or sucking (i.e., pump filter- on the anterior part of the gill arches which consti- feeding and particulate-feeding) planktivores, but tute the elements of the branchial basket. In other are important for suspension feeders filtering in . fishes, such as Cichlidae and Citharinidae, slow currents (such as gargonian corals, zoanlhids, microbranchíospines are organized in a filtering and others). band along a groove located on the internal and/or The probability of capture by direct (for small external part of some or all gill arches, just above particles) or inertial interception (for large parti- the gill filaments (Gosse, 1955; Fryer & Iles, 1972). cles) is high when the particles adhere to the rilter Other entrapment structures, such as pharyngeal upon contact. Depending on surface properties of teeth and epibranchial organs, may participate in both the particles and the filter, ‘sticky filters’ (for the retention of particles, although their functions example, covered by mucillage) can readily retain are unclear. The presence of mucus, which partici- particles too small to be captured by sieving (i.e., pates in food consolidation and transportation, smaller than the smallest mesh of the filter). Small could improve the retention efficiency of the filter. organisms which possess elongated processes (such In order to assess the contribution of the retention as filaments, spines, and others) are particularly process in the feeding selectivity of planktivores vulnerable to interception by sticky filters. The (i.e., the retention efficiency), it is necessary to re- retention efficiency of sticky filters is influenced by view the theoretical mechanisms by which biologi- the density of small sized particles in the environ- cal filters remove particles from the water. For ment (which could be responsible for clogging the planktivorous fishes, the physical characteristics filter), the surface areas of the collecting structures (speed and direction) of the water inhaled into the which constitute the filter, and the water flow ve- buccal cavity are very helpful in investigating the locity. The prey morphology is obviously a deter- potential mechanisms of actual particle retention. minarit, as most of the prey organisms captured by glankthr”s fishes are neither spherical nor regu- Mechanisms of particle retention by biological lar in shape. filters. Filtration is the process by which particles Zooplankters generally are non-spherical and are removed from fluids, by the use of porous have long anleiinae and legs covered by setae (such devices. But sieving is only one, among several, as copepods and euphausids), diatoms form long- mechanisms involved. As industrial engineers use s pined chains (for exam pl e, ChaetoceroJ), blu e- man-made filters, in which pores are several orders green algae develop in long filaments (for example, of magnitude larger than the particles trapped, to’ Anabmm species), and have remove particulate matter from gases, Rubenstein processes and protrusions (for example, Ceratiun? & Koelh (1977) considered that, similarly, various and Peridinium). These large elongated organisms, mechanisms, in addition to sieving, could be by increasing their surface areas (i.e., their gross responsible for the selectivity of biological filters. size), are less susceptible to be ingested by, even Characteristics of the suspended particles (such as large, filter-feeding zooplankters (but see the rnech- size, shape, surface properties), the water flow (ve- anism of gape narrowing between the edges of the - locity, direction), and the filter (morphology, sticki- carapace valves of large cladocerans in presence of ness, physical or behavioural alteration capabilities dense net-phytoplankton: Gliwicz, 1980; Gliwicz & of the mesh size, mode of particle transportatiton Siedlar, 1980), but become more v~ilnerable to from the filter to the esophagus, ability to modify retention on the branchial apparatus of filtering the cleaning rate of the filter) all have to be consid- fishes, because of their appropriate size range. ered. Filter-feeding fishes have increasing feeding selec- 123

tivities and rates for increasing sizes or chain clean their filters. For example, pump filter feeders lengths of phytoplankton. For example, men- may behave by slowing down their swallowing haden’s filtering rates increase with algal size (Dur- movement frequeñcy. By doing this, accuniulated bin & Durbin, 1975; see Fig. 5A). 300-600 pm particles, then functioning themselves as filters, long trichomes (6 pm in diameter) of Oscillatoria could improve the retention efficiency for smaller agardhii together with Aphanizornenon flos-aquae particles. Another mechanism affecting the reten- dominate in the food of (Kajak et al., tion efficiency of the fish filtering apparatus has 1977). As its gill racker spacings range from 20 to been suggested by Omarov & Lazareva (1974) for 25 pm (Voropaev, 1968), siver carp feeds selectively silver carp (Hypoplithalmichthys molitrix): the fish on particles larger than 20 pm (Boruckij, 1973). could vary the quality and quantity of the mucus Surface properties of the prey, which have been secreted under different food conditions. demonstrated to an important role in the differential or selective feeding of small filter- Filtering efficiency. The spacings (also feeding daphnids or copepods (Poulet & Marzot, called gill raker gaps by King & McLeod (1976)) 1978; Gerritsen & Porter, 1982), are probably less have long been considered as the most important important in particle retention by filter-feeding determinant of the filtering capability in plank- fish. Because water moves, rather slowly, over (and tivorous fishes. King & McLeod (loc. cit.) proposed not through) its filtering mesh, the particle reten- a formula for the computation of the gill raker tion of Daphnia is strongly influenced by the sur- gaps: . face chemistry of the particles, which corresponds to their surface charge (ionic interactions) and wet- G = [T- (R .W)]/[R- 11 tability (hydrophobic-hydrophylic interactions) (Gerritsen & Porter, loc. cit.). The capture efficien- where T = the total gill arch length, R = the total cies for the smallest particles are greater for neutral number of rakers along the arch, and W = the than for net negatively charged particles, and de- mean raker width. However, the inaccuracy of this crease with increasing wettability (obtained by ad- methad when applied to three species of teleosts, dition of a surfactant) of both the particles and the made Nelson (1979) recommend direct incasiires of filter. Such a mechanism, which has not yet been gill raker spacings rather than their computation. demonstrated to occur in filter-feeding teleosts, Direct measurements of gill raker spacings may probably may not contribute to the retention of the not be accurate in determining the lower threshold smallest particles by fish, because the water flow of filtration: they lead to a discrepancy between the passing over the branchial apparatus is generally expected size of the smaller prey retained by simple rapid, and thus the viscous forces are comparative- sieving through the filtering apparatus, and the size ly insignificant. of the smaller prey effectively ingested (Kliewer, Although mucus covers the rakers of Brevoortia 1970; Seghers, 1975; King & McLeod, 1976; Dur- tyrannus, even prolonged experimental feeding tri- bin, 1979; Nelson, 1979), because either the consid- als on densities of small algae Skeletonerna costa- ered fishes possess ramified gill rakers (microspines turn higher than those found in coastal marink or denticles), or the surface properties of the gill waters, never caused either a drop in the maximum rakers make them act as sticky filters. For the form- particle size filtered (13-16 pm), or an increase of er type of fishes, denticle or spacings (when the feeding rate on the smallest particles with time, measurements can be done) rather than gill raker which both correspond to a clogging situation of spacings may be better correlated with the size the gill rakers (Durbin & Durbin, 1975). Conse- range of prey items ingested. quently, these authors estimated that such a situa- Comparing the diet and the morphological tion may be reached only in some extremely turbid specializations of the branchial arches of three with very high loads of detritus. But, it is filter-feeding marine teleosts, Nelson (1979) ob- conceivable that filter-feeding fish may alter their served that each species is capable of ingesting retention efficiency for a certain size range of prey much smaller prey items than can be retained by its organisms (the more abundant, or preferred, per- gillrakers by a simple sieve action. Engraulis mor- haps), by simply changing the rate at which they dax possesses rather fine gill raker gaps 124

(140-210 pm), while Rastrelliger kanagurta has ciency (see modelisation procedures of retention ef- finer denticle gaps (40-76 pm): when adult, the ficiency by filter feeders in sections V.A.2. and\ former is primarily zooplanktivorous, whereas the V. A. 3 .) . latter is predominantly phytoplanktivorous. Ad- The role of the epibranchial organs in the filter- vanced structural specializations of the branchial feeding selectivity of fishes, as well as the mechan- basket occur among clupeids. An increased com- isms of food consolidation and traflsportation into plexity of the gill rakers structure of Brevoortia the esophagus still remain unknown. Consolida- tyrannus is associated with a change from a tion and transportation functions have been zooplankton to a phytoplankton diet during hypothesized for the epibranchial organs and the growth (June & Carlson, 1971). Radioisotope tech- pharyngeal teeth, although their morphologies niques demonstrate that juveniles of B. tyrannus rather more suggest that they may play a role in the (around 188 mm 1ong)i can filter phytoplanktonic retcntion of prey items. cells (Nannochforis)ranging from 1 to 2 pm (Chip- man, 1959; Peters, ¡972), whereas the minimum J. Particle digestion: resistance of phytoplankton to size threshold for filtration (i.e., the smallest prey fish digestioli processes size at which the filtering rate differs significantly from zero) by adults is 13-16 pm (Durbin & Dur- Since, at least, some filter feeders use bin, 1975). Similarly, the switching of Ethmalosa phytoplankton as food, and some phytoplanktonic fimbriata towards dominant phytoplanktivory oc- forms are resistant to digestive processes (such as, curs with the development of an impressive three- particularly, dinoflagellates and diatoms) it is es- dimensional system of ramified branchiospines on sential to consider the fish digestion efficiency to the edges of the gill rakers (Monod, 1949, 1961; assess the phytoplankton responses to Fagade & Olanyan, 1972). The filtering capability limnetic filter-feeding fish. Moreover, defecation of by simple sieving is thus extended down to 10 pm partially digested phytoplanktonic cells, immedi- or smaller, while particle collection by inertial im- ately attacked by , contributes to the nutri- paction probably increases by several orders of ent loading processes of lakes. In the elaboration of magnitude (Lazzaro, unpubl. data). energetic models of grazing and predation by filter- The functional morphology of the branchial bas- feeding plamktivorcs, the digestion event, in most ket of filter-feeding clupeids and scombrids reveals cases, must be considered (see also the resistance of the importance of the denticle gaps in the collec- zooplankton to fish ,digestion processes in section tion of the smallest particles. The expansion of the arT.A.5.). branchial basket in a dorso-ventral plane provokes Low gastric pH, associated with vigorous the erection of the gill rakers along the longitudinal mechanical breakage in à gizzard-like stomach (of- axis of the , and presents the deilticle ten filled with fine sand grains), and prolonged ex- edges tovirards the direction of the water flow. Con- posure to digestive enzymes along a particularly sequently, the denticle edges become the primary long digestive tract are essential conditions for ef- collection sites for the small particles, such as the fective disruption of hard covered (Le., the solitary phytoplanktonic cells (Nelson, 1979). prokaryotic wall) phytoplanktonic cells, and Nevertheless, complex raker structures (such as, for the desintegration of their protoplasm (especially example, in E. fitnbriata) make impossible the ac- in colonial or filamentous blue-green algae Micro- curate assessment of the retention efficiencies for cytis and Anabaena, diatoms, and dinoflagellates different particle sizes through direct measure- such as Peridiniunz). Digestive processes among ments of denticle or raker gaps. are extremely specialized to utilize more When direct measurements of the filtering gaps efficiently the algal resources. pH as low as 1.25 (i.e., the spacings between gill rakers, microbran- (Moriarty, 1973; Bowen, 1976; Caullon, 1976), and chiospines, microdenticles) are possible, the filter- even 1.0 (Payne, 1978) can be reached by their stom- ing efficiency for a particular particle size can be ach fluids during active digestion. Tilapias are par- calculated using the mean cumulative frequency of ticularly well adapted to destroy blue-green algal interraker distances (hyperbolic curve) as an esti- cell walls (Bowen, 1982), but not all fishes are so ef- mate of the probability function for retention effi- ficient.

, 125

The presence of numerods viable algal cells in IV. Evaluation of Selective feeding: a review of elec- the feces of herbivorous planktivores is not rare tivity indices, their strengths and limitations among various groups of fishes. For example, in Cichlidae: Spataru & Zorn (1978) observed that To quantify selective predation, different meas- Microcystis spp., and frequently Peridiniuin spp. ures of preference are used (see reviews in Chesson, had their integrity after passage through the gut of 1978, and Lechowicz, 1982; see also Fig. 7) based II: aurea. Preliminary experimental cultures of fecal on the comparison between measurements of the pellets freshly released by II: aurea fed twice a day, relative occurrence frequencies of prey types (or exclusively on natural lake plankton, led within a prey species) in a predator’s diet and in its environ- few days to a rapid algal growth (Lazzaro, pers. ob- ment. serv.). But, Peridinium cinctuin, the preferred food First, some caution must be used in the interpre- of S. galilaeus in Lake Kinneret (Israel), had tation of the predator’s stomach contents. The broken-up theca and progressively more digested main problem is our own estimation of prey ‘availa- protoplasm, down to the end of the fish digestive bility’ in the environment, which depends prin- tract (Spataru & Zorn, 1976; Gophen, 1980; Dren- cipally on the sampling device used (see a review of ner et al., 1982~).In Cyprinidae: Malyarevskaya et limitations in O’Brien & Vinyard, 1974). One ques- al. (1972), using epifluorescence microscopy, de- tion the fish feeding ecologist is interested in an- tected great amounts of dead and live cells in the swering is: ‘which prey items present iri the preda- excrements of herbivorous silver carp, fed on toxic tor’s environment are really ‘available’ to this blue-green algae Microcystic aeruginosa. No differ- predator?’ It may be answered by examining wheth- ences were observed by Kajak et al. (1977) between er the prey is consumed (a lot or not much), or not. the structures of filamentous blue-green algae cells The availability of one prey item to a particular (mainly colonial forms of Aplzanizornenoff flos- predator is a result of the relative physiological and aque, selectively ingested) in the final part of the behavioural properties of both the predator and the gut of silver carp, Hypophthalmichthys molitrix, prey. Werner & Hall (1974) and Mittelbach (1981) and in the plankton of four Masurian Lakes used laboratory experiments to estimate amifabili- (North-Eastern Poland), demonstrating that these ty. Prey consumption is affected by prey size, shape, algae were not digested. Moreover, in periods of pigmenlation, contrast, motion behaviour and es- mass ‘water-blooms’ of filamentous blue-green al- cape ability, while predator efficiency is affected by gae, fish kept in net cages suffered high mortality its sight, preference, experience, hunger, feeding be- rate, due to their lack of access to bottom food haviour, and capture success. sources, and smaller size range of algae. Unlike the I1 is obvious that the detection and capture abili- blue-greens, Ceratium hirundinella and diatoms ties of a fish for one particular prey are dependent were well digested, as crushed sculptured envelopes upon the conspiciotisness And escape behaviour of of C. hirundinella and empty were this prey, while the sampling of this same prey by abundant in the final part of the fish gut. Accord- the experimenter is only dependent upon the selec- ing to Prowse (1964), most phytophagous fishes di- tivity of the device used. Thus, one prey abundant- gest only diatoms, but do not digest Chlorococ- ly captured in the enviromnent by the experimenter cales, Eugleninae, and blue-green algae. Savina might be absent from the stomach cohtents of the (1965) showed that Oscillatoria granulata Gardner fish, only because it cannot be seen or captured by and Anabaena werrzeri Brunnth, passed un- the fish. Moreover, to measure electivity, one needs damaged through the guts of silver carp, whereas to know the horizontal and the vertical distribu- only diatoms and Protococcales were digested. In tions of both fish and prey during the feeding peri- addition, Vovk (1974) demonstrated that decom- od preceding the fish capture (O’Brien & Vinyard, posing algae were better assimilated than live ones. 1974). In Clupeidae: Velasquez (1939) and Smith (1963) An additional bias can result from differential found 46 genera of algae (mainly Chlorophyceae prey digestion rates which may affect measures of and Myxophyceae) which survived gizzard shad gut selectivity based on stomach content analysis. passage. Since quickly digested prey tend to be underesti- mated in the fish diet, they may be considered as 126

D

o,ö 0.4 0.8

E’

0.0 O. 4 0.8

h E*

0.4 os

010 0.4 0.8

PROPORTION IN ENVIRONMENT (%I

Fig. 7. The values of various electivity îndices as functions of availability (pi) and utilization (ri) of a food item i: Ivlev’s electivity in? (E); forage ratio (E’): Jacob’s modified forage ratio (log Q); Strauss‘ linear preference index (L); Chesson’s and Vanderploeg & Scavia’s relativized forage ratio (a,W); Vanderploeg & Scavia’s relativized electivity index (E*) (from Lechowicz, 1982). 127

apparently negatively selected (i.e., avoided) al- proposed by Jacobs (1974) in an attempt to achieve though this may be false (Gannon, 1976). This situ- independence from the influence of the relative ation occurs in alewife (Rhodes, 1971), where abundances of the prey types in the environment. Daphnia the most rapidly digested of any In fact, Di is only slightly less sensitive to sampling zooplankter tested (including Mesocyctops, Cy- errors for rare prey types than either Ei or FRi, clops, Bosnzìrza, Simocephalus, and midge larvae while Qi is unusually sensitive when either ri or pi Cltironoinus) in fish stomachs, appeared to be is less than about 0.1 (Lechowicz, 1982). They are avoided when measures of selectivity were applied. defined by: Similarly, Daphnia was verified to have higher pas- sage rate from the stomach of bluegill sunfish Qi = [ri(l-pi)]/[pi(l-ri)] and (Werner et al., 1981), and Daphnia plus other small Di = [ri-pi]& + pi-2ripiI food particles to pass through fish stomach faster than larger items (Windell, 1978). where ri and pi have the same definitions as those The most simple indice, initially proposed by above. . Shorygin, is the forage ratio indice (FRi) of Ed- Jacobs recommended the use of log Qi and Di in monson & Winberg (1971): laboratory feeding trials as differential mortality rates, to quantify the selection of food i relative to FRi = ri/pi food j. i and j may be two specific food types or groups of food types. j may be also the sum of all where ri = the ration of food type i, and pi = its food types in the environment, except food type i. proportion in the environment. FRi values range Quotient Qi varies from O to +I for negative from O (avoidance) to + 00 (when selection is high- sclection, and from 4-1 to + CQ for positive selec- ly positive). FRi = 1 for random , i.e. no tion. Relative difference Di varies from - 1 to O for selection or avoidance occurring: the prey type i is negative selection and from O to +1 for positive consumed in the same proportion as it is present in selection. With the range of log Qi from -0.6 to the environment. t-0.6, there is no ‘a priori’ difference between log The most commonly used measure of electivity is Qi and Di measures. the indice Ei of Ivlev (1961). Its calculation is a sim- In order to overcome the problem of variation of ple ratio: selectivity measure variation with the abundance in the environment of the foods other than the con- Ei = [ri-pi]/[ri + pi] sidered food i, Chesson (1978) proposed a measure of preference (ai) based on a simple biological where ri =the proportion of food type i in the stochastic model involving probability of encounter fish’s .ration, and pi = the proportion of the food and probability of capture upon encounter. Ches- type i in the environment. Ei values range from - 1 son provided a normalization of Ivlev’s forage ratio (avoidance) to + 1 (positive selection). When Ei = O defined by: there is no selection: the food is eaten in the same

proportion as it is present in the environment. Ei ai = [(l + Ei)/(l-Ei)]/[Etni= 1 (1 + Ei)/(l-Ei)] I values between -0.3 and +0.3 are generally con- sidered not significantly different from O, and thus Here, m = the number of prey types, and Ei = the to indicate non-selective feeding. measure of electivity (Ivlev’s indice) calculated for These two indices present a main weakness: both prey type i, with Er= I ai = 1. are highly influenced by the relative abundance of When ai = I/m (with i = 1,. . , ,m) selective pre- the prey types in the environment. For example, giv- dation does not occur, when ai > l/m more of spe- en a fixed proportion of the food i in the predator’s cies i occurs in the diet than expected by random diet (ri = constant), an increase of the abundance feeding, and when ai < l/m less occur than expect- of i in the environment (pi) decreases the predator ed. electivity for this food, whereas its preference for Preference g = [ai. . . . .am] reflects any devia- this food remains unchanged. tion from random sampling of the prey in the en- Modified versions Qi and Di of FRi and Ei were vironment. Alternatively, & can be derived from 128 the proposed stochastic model of prey encounter to +1 (preference). The indice value for random and capture which accounts for: prey distribution, feeding is O under all conditions. The normal distri- prey visibility, searching behaviour of the predator, bution of Li allows statistical comparisons between pursuit upon encounter, escape ability of the prey, calculated values, or between a calculated value capture efficiency of the predator, preference for and a null hypothesis value (such as O). prey, experience, hunger, time and predation con- But, Li suffers the identical disadvantages that straints for feeding. Based on a biological model, Ivlev's and Jacobs' indices do: (1) Li is vulnerable su_ is a useful measure for quantifying predator to sampling error for prey rare in the environment preference. or in the diet (and partiqularly more vulnerable, as Paloheimo (1979) assumed that a preference in- pi increases), and (2) extreme indice values only can dice really independent of relative prey abundances be reached under unrealistic conditions where can be derived from standardized forage ratios, so ri = O and pi =1 (Li =Al), and ri =1 and pi =O that the sum of the forage ratios of the different (Li = +l). Unfortunateby, with Li it is not possible prey types equals one. So, he recommended a nor- to compare electivities for a particular prey item be- malization of FRi which can be defined by: tween samples where the abundances of prey items are different, either in the environment, or in the NFRi = [ri/pi]/[Cm ri/pi] diet. This main weakness eliminates any compari- I= I son between electivity values obtained from the Vanderploeg & Scavia (1979) proposed the same ficld. expression symbolized by Wi. It is convenient to Moreover, its main disadvantage is that prefer- note that although ai, Wi, and NFRi are presented ence rankings obtained from Li measured on field as different, in fact they are identical, since: da@ disagree with rankings by other indices (Lechowicz, 1982). [1+ Ei]/[l -Ei] = [1+ (ri - pi)/(ri + pi)]/[l - (ri- To achieve a possible range from +1 to -1 and -pi)/(ri + pi)] = ri/pi ' O value far random feeding, Vanderploeg & Scavia (1979) proposed n relativiaed electivity indice Ei* and similarly Er= [l Ei]/[l-Ei] = ET" ri/pi similar to Ivlev's Ei, but using the selectivity coeffi- + I= 1 cient Wi and the number ni of food types available then ai = [ri/pi]/[Er= ,ri/pi] = Wi = NFRi in thc environment:

Thus, ai, Wi, and NFRi have the advantage of Ei* = [Wi--(l/m)]/[Wi + (l/m)] being independent of the relative abundance of food types, and are therefore appropriate for Similar to ai, Ei* is a measure of preference meaningful comparisons between samples having which estimates any deviatiron from random feed- the same number of food types. But, they have the ing and makes possible comparisons of electivity undesirable property of being sensitive to the dura- rank orders between samples. Nevertheless, some tion of the feeding experiment (Pearre, 1982). In undesirable properties still remain: (1) as for Li, the that way, they are similar td Ei which is also affect- maximum preference value (Ei* = 1) can only be ed by experimental duration and depends on the in- reached under unrealistic conditions where ri = 1.0, itial spectrum of prey distributions (Vanderploeg & pi = 0.0, and m = CO, (2) when m increases, Ei* be- Scavia, 1979). comes more vulnerable to sampling errors for food To avoid some undesirable properties of either Ei rare in the diet or rare to moderately common in or FRi, such as dependence upon relative and abso- the environment, and (3) parametric statistical lute sample sizes and relative abundance and rarity comparisons of electivities are only amenable be- of prey species in the environment, and to permit tween samples with the same number of food types. statistical comparisons between samples, Strauss Electivity indices give general information on the (1979) proposed a simple linear indice: quatltitative feeding patterns of predator. But, of- ten, observed feeding I preferences need to be Li = ri-pi statistically tested to know if the predator feeds at random on available prey types, if respective prefer- which ranges from - 1 (avoidance or inacessibility) ences differ betweén samples, or if two prey types 129

are really preferred in a differential manner under Gras & Saint-Jean (loc. cit.), investigating the de- certain conditions. crease in the stock of the filtering planktivore Thus, to provide appropriate means for sig- Brachysynodontis batensoda (Mochokidae) in nificance testing, Pearre (1982) proposed two Lake Chad during the lowering of the water level, statistically testable indices derived from a chi- concluded that a decrease in the useful fraction of square formulation with one degree of freedom: the zooplankton (Bu/Bt) may well play a role in the growth slowing down of the planktivore. Vi = [niNo-n~Ni]/[abde]"~ To show that, they used the large, spherical, slow moving cladoceran Moina rnìcrura as reference and Ci = f [[ IniNo - noNi I - n/2]2/abde)1/2 Prey. They proposed another way to calculate Si, with- . where the sign of Ci is given by the consideration out calculating ri and pi, for various sample series of (niNO-noNi), Ni and No are respectively the having the same reference prey. In this particular number of any prey type i, and the sum of all other case, Si can be expressed as: prey types except i in the environment, ni and no are respectively the corresponding numbers in the Si = [N'i/Ni]/[N'R/NR] diet, and a = ni + Ni, b = no + No, d = ni + no, e = Ni t No, and n = ni + Ni + no t No. where Ni and NR are, respectively, the density of Because neither ai nor Wi can be directly tested, prcy type i and the density of the reference prey R the calculation of Vi and Ci may be a good measure in the environment, and N'i and N'R are the num- of selection probability of any sample size. bers o€the same prey types in the diet. The expres- Finally, Gras & Saint-Jean (1982), wishing to re- sion of Si possesses the important property of be- late the stock of planktivores to the stock of plank- ing effectively independent of the relative ton useful for planktivores through prey selection abundances of prey types, because it is based on considerations, proposed a normalized-like forage absolute prey densities. ratio Si, defined by: But., Si presents two main weaknesses: (1) the col- lecting efficiency of the reference prey (SR) is un- Si = [ri/pi]/[rR/pR] realistically assumed to be equal to 100V0, and (2) the measures of collecting efficiencies in a sample where R is a reference prey which must satisfy depend closely on the choice of the reference prey. several conditions, of which the first important is As emphasized by Paioheimo (loc. cit.), the hdi- to be one of the most selected prey (i.e., which has ces FRi and Ei on the one hand, and Qi and Di on the highest FRi value). The selection indice Si is ex- the other hand, are directly deductable one from pressed as the ratio FRi/FRR, with SR = 1 and another: Si < 1 for i = R. Thus, Si represents the percentage of selection of prey i in comparison to prey R. Ei = [FRi-i]/[FRi t 11, and These authors used Si to assess the useful bi- Di = [Qi-l]/[QÌ+l], omass of prey Bu = E,'"=, SiBi, where Bi is the bi- omass of prey i, and Ce = Bu/Bt the collecting effi- and .the necessity to have two indices is not justi- ciency of the predator (i.e., the useful fraction of fied. Similarly, as previously demonstrated: prey biomass), where Bt is the total biomass of ai = Wi = NFRi. Prey. Nevertheless, the main conclusion which can be A hindrance decision has to be made on the drawn from the critical analyses following the choice of the reference prey R, since several prey works of Ivlev is that no indice based on prey types may be taken as reference prey,'and prey R is countings in the diet and in the environment can frequently different between samples. To make furnish an absofute predator feeding preference, ex- rR/pR as accurate as possible by minimizing sam- cept in the extreme case (rather rare) where a preda-

' pling errors, the reference prey R must not be only tor consumes one or two prey types among many easily identified, and abundant both in the environ- available prey types. This conclusion, implicit in ment and in the diet, but particularly, must be the some works (Gras & Saint-Jean, loc. cit.; most highly positively selected prey. Lechowicz, loc. cit.), is clearly demonstrated by 130

Paloheimo (loc. cit.). At best, these ihdices repre- its selective foraging pattern. ‘A priori’, this data sent the ‘apparent selectivity’ for different prey could permit close quantitative analysis of the rela- types, according to changeable modalities (often tionships between plankton and planktivores. unknown), such as combination of ‘sensu-stricto’ Another potential advantage of Si is that it could preferences, capture capabilities, resiective distri- be calibrated, by comparing experimentally the butions of predator and prey, and so on. selectivity for the reference prey with the selectivity In correct terms, it turns out that: (1) the mini- for a standard prey which might be, for example, a mum of information which can be expected from spherical inert particle having a well known di- ’ an electivity indice is a prey ranking by increasing ameter and a maximum collecting efficiency. A (or decreasing) order of apparent selection, and (2) similar approach as been used by Rrenner (1977) to the maximum of information is the expression, by assess capture efficiencies of siphon-like pump proportional factors, of differential Selections be- filter-feeding planktivore for different prey types, , tween prey (for example: the prey ranked first with using air bubbles and heat-killed zooplankton as an indice value of x is two times less selected than standard prey having maximum capture probabili- the prey ranked second with an indice value of 2x). ties. From the comparative analyses clonducted by In fact, Si possesses other potential uses, which Paloheimo (loc. cit.), Gras & Saint-Jean (loc. cit.), emphasize the importance of this kind of indice: its Lechowicz (loc. cit.), and Pearre (loc. cit.), it can be significance remains to be explored, ‘A priori’, the conciuded that: (1) all indices provide similar rank- problems might arise with the choice of the refer- ings of food preferences, except Strauss’ Li which ence prey (or group of prey), atld with the variabili- gives changeable rankings according to the relative ty of the intrinsic selective feeding pattern of the abundances of prey in the diet or in the environ- predator. Apart from these problems, the weakness ment, (2) the indices Ei, Qi, Di (and Li) vary with of Si is that, expressed as a ratio based 011 particu- relative abundances of prey, and obscure or modify lar prey (ie., the refcrence prey), it cannot represent variably the proportional factors which express the a general measure of selection. As previously men- differences in selection between prey (it could be tioned, only NFRj can fit this criterium. demonstrated that Ei* follows this general trend It follows firstly, that the complementary use of (Saint-Jean, pers. commun.); in this sense, the these two indices could be recommended, which respective behaviours of Vi and @i might be otherwise are simply reldted: profitably tested), and (3) only the indices FRi, NFRi (thus cui and Wi), and Si give the maximum Si = NFRi/NFRk of information. See also Fig. 7. Among the last three indices, FRi must be ex- The main conclusion which can be reached from cluded because its absolute value varies with tlie the critical analysis of the use of these electivity in- abundance of prey, which makes coniparative dices is that they are oiily ‘relative measures of studies difficult. This variation factor is eliminated preference’. In the present review paper, I folow the from NFRi and Si, which therefore have the doubleq conventional and most commonly used terms con- advantage of being independent from the relative cerning relative food selection: i.e., avoidance (or abundance of prey, and to reflect accurately the negative preference), random feeding, and (low, differences in apparent selection existing between medium, highly positive) preference. them. Since these measure of relative preference reflect NFRi has the advantage over Si of not requiring not only the predator ‘preference’ (behavioural any preconditions, and representing a single, identi- and/or mechanical), but also the relative prey cal, measure of selection, applicable to any situa- abundance, the prey detectability, and the prey cap- tion. Nevertheless, its main weakness is to vary with ture ability, the indices of electivity are composite. the considered number of prey. Si expresses more Thus, they are useful for discerning and comparing directly (directly if 1/Si is utilized) the previously feeding patterns, but obviously not meaningful for mentioned proportional factor Fhowing the predicting levels of food utilizaticm The latters can differential selection between prey. As already men- only be done through the use of appropriate meas- tioned, Si may be used to assess the fraction (Bu) ures of food intake, like the various available ex- of the prey stock available to a predator, based on pressions of feeding, filtering, and ingestion rates. V. Models of prey selection corporable into an optimization framework, as they are simply constraints that, if added to forag- A. Model conceptualization and feeding modes ing models, modify the predictions of prey selec- tion (Werner, in litt.) Within the last 20 years, there have been several The original approach used by Hoiling (1966) to very interesting theoretical works on the area of examine the predation-act has been followed in prey selection by planktivorous fishes. A large body numerous studies dealing with the feeding selectivi- of theory has been developed to explore and predict ty of planktivorous fishes (among which those of how foraging patterns of planktivorous fish are Ware, 1973; Werner & Hall, 1974; O’Brien et aì., related to plankton composition and density. A 1976; Drenner, 1977; Eggers, 1977; Durbin, 1979; considerable attention has been paid to optimal O’Brien, 1979; Gibson, 1980; Wright & O’Brien, foraging theory, but relatively few field tests of op- 1984). The approache! used have been proposed as timal foraging models have been attempted (e.g., quantitative models able tò predict the potential Werner et al., 1983a, 1983b). A predictive theory of impact induced by changes in the level of predation individual fish foraging pattern has been used as a pressure from particulate feeders, or pump filter mechanistic basis of a more comprehensive theory feeders, on the structure of the zoopiankton com- on the selective utilization of plankton species by munities. Thc vulnerability of a prey type i to a par- planktivore populations. Most models of prey ticular planktivore can be estimated by its pkobiibil- selection were dedicated to particulate feeders, and ity of being consumed by the fish. This probability especially to the mechanisms by which fish concen- is the product of the conditional probabilities that trate feeding on particular zooplankton size classes each event constitutifig the predation-act is success- upon detection. Few models have concerned filter fully colnpleted (O’Brien, 1979; Wright & O’Brien, feeders, probably because most research have been 1984; after Hollin$, 1966) The vdfnerabilky (Vi) of done in temperate zones where visual planktivores a prey type i to the cansuniption by the planktivore are generally dominant. (Le., the eEfíciency of the fish t In natural or man-made aquatic , pre- type) is a function of both its dation models are useful to assess and predict tion probhbifities (noted li and DI, respectivejy): qualitative and quantitative utilization of plank- tonic resources, and shifts in plankton composition Vi = Ii - Di and abundance in relation to changes in the nature and/or the predation level of planktivores. They ac- Since the sequehce of successive évents which de- curately help decision making in the field of lake or termines tite probability of ingestion is dependent reservoir management in order to (1) preserve ade- upon the feeáifig behaviour used by the fish, dis- quate water quality levels for drinking or recrea- tinct expressions are proposedhfor tional uses, and/or (2) optimize planktivore ers, tow-net filter feeders, and pu production €or sport fishihg (where planktivores (see below in the respective sections). Because these are used as fish foods for ), craft or com-. functional relationships can merciaf fisheries. perimentally, they may helb to d Theories related to mechanisms of diet optimiza- importance of variods mechanis tion (such asj for example, energy maximization per differential patterns (sekctive o unit of time) have been abundantly used to build lection and consequent dietary models of predation by planktivorous fishes. Potentialities of feeding selectivity can be inv‘es- Nevertheless, Zaret (1980) emphasized that sensory tigated for a fish tfsi the áppropriate expressioli cues (such as, vision, chemoreception, and (accordihg to the knowledge of the feeding reperto- mechafioreception), hunger, experience, and feed- ry the fish can display at particulat- sizes (i.e.4 ages), ing repertory, rather than actual energetic consider- and to the physical characteristics of the aquatic ations (realistically unmanageable by a fish), are environment) applied to the efitire sei of (readily) factors which can readily govern the foraging pat- available prey types. These last can be identified tern and the feeding selectivity of planktivores. from the knowledge of the respective migrdtory be- Factors such as hunger and learning are easily in- haviours of the fish and the prey which determirie 132 the duration of exposure of the prey to fish preda- breadth of the fish’s diet decreases and the fish be- tion pressures, and the relevant prey characteristics comes more selective on the basis of prey size. This for detection, pursuit (these two for particulate is consistent with the more recent studies of Eggers feeders only), capture, retention, and digestion. (1977) and Miller (1979). Werner & Hall (loc. cil.) Below, in the first part of this section, and for attributed this change in diet breadth to the ability each planktivore feeding mode, the main models of fish to respond to prey density changes in an ‘op- available are discussed, and then, following the timal foraging’ pattern (based on cost of prey cap- Holling’s approach of the predation-act, equations ture in terms of energy and time), although they did for differential prey vulnerabilities and differential not describe its mechanism. Their model is more feeding rates on prey are presented. In the second adapted for high prey densities, when the swim- part of this section, the need to consider eventual ming distance of fish is larger than the reactive dis- switches of feeding modes in response to (seasonal) tance of prey (i.e., the distance at which a prey is de- changes in resources within an habitat, or to (spa- tected; see section III.A.1.) or when several prey are tial) differences between habitats successively ex- often detected simultaneously. It assumes that a plored, are emphasized to improve the flexibility prey detection probability is proportional to the and the realism of the modelling approach. cube of its reactive distance. A model more appropriate for low prey densities, 1. Particulate feeders when the swimming distance is larger than the reac- tive distance, was developed by Confer & Blades Quantitative models, most of them based on op- (1975) for Leponzis gibbosus. They proposed that timal foraging theories, have been used to attempt the detection probability is rather proportional to the description of the modes of prey selection and the square of the reactive distance, because when the feeding strategies of visual planktivorous fishes moving from prey to prey the fish search out cylin- (Werner & Hall, 1974; Confer & Blades, 1975; drical volumes. Calculating values of Ivlev’s (1961) O’Brien ef al., 1976; Eggers, 1977; Gerritsen & electivity index, they showed that Galbraith’s (1967) Strickler, 1977; Gibson, 1980; Gardner, 1981: Eg- data and the measurements of fish reactive distance gers, 1982; Wright & O’Brien, 1984; see reviews on reported in Werner & Hall (loc. cit.) and in their optimal foraging approaches in Mac Arthur & Pi- own work support a model of continuous increase anka, 1966; Schoener, 1969, 1971; Werner, 1972; in fish predation intensity with prey size. They Krebs, 1973, 1978; Charnov, 1973, 1976; Pearson, demonstrated that feactive distance is a linear func- 1974; Pyke et al., 1977; Pyke, 1979; Charnov & Ori- tion of prey size. But, differential ptey conrspicious- ans, 1979; Mittelbach, 1981; Werner et al., 1983a, ness (size, plus motion behaviour) and escape abili- 1983b). ty may affect reactive distances of similar-sized One of the first models using an aptimization prey. More translucent D. pule2 elicit significant approach based on time constraint for feeding ac- shorter reactive distances than similar-sized D. ma- tivities was proposed by Werner & Hall (1974). This gna. hIesocyclops edax, a vigorously swimming ‘optimal foraging model’, based on differential copepod, elicit longer reactive distances than visibility of prey, maximizes the net energy intake similar-sized Diaptornus sicilis copepodites and per unit of time for each prey eaten by bluegill sun- adults. The regression line for copepods is steeper, fish in experimental ponds. The conceptualization with a lower intercept, than that of cladocerans of this model is developed in Werner (1972). At low (even Daphnia). Small copepods elicit significantly densities of different-sized instars of the cladoceran smaller reactive distances than either Daphnia of , bluegill are not selective and prey the same size. The reactive distance of the largest items of different sizes are eaten as detected. With 2.3 mm Diaptomus teptopus females is not signifi- increasing prey densities, however, fish select the cantly diiferent from [hat of a 2.3 mm D. magna. largest prey sizes, while the smaller sizes are ig- Some copepod species are highly successful at elud- nored. As the prey densities increase, prey sizes are ing capture: the capture ability of D. sicilis by L. eliminated from the diet sequentially, beginning gibbosus is 21 070 compared to 61 % for D, ashlandi. with the smaller ones. As in accordance with Ivlev’s This conflicts with the model of Allan (1’974) who (1961) observations, at higher prey densities the proposed that the intensity of fish predation on 133 cladocerans increases with prey size up to some in- mum reactive distance, which is proportional to the termediate size after which predation intensity re- square root of the projected surface area, increases mains constant. Looking at the energy ingestion by with prey size. For similar-shaped prey, the reactive L. gìbbosus in presence and absence of predaceous distance is proportional to the prey length. But, zooplanktonic prey (D. sicilis, Epischura lacustris), rounded prey which have a greater projected sur- Confer & Blades’ model predicts that, large and face area, are detected at a greater distance than more conspicious, predaceous zooplankton in- elongated prey of similar size. This is consistcnt crease the energy uptake of planktivorous fish. with Confer & Blades’ (loc. cit.) observation, where Based on the predation cycle, Eggers (1977) used individual Daphnia (round body) have greater reac- a ‘differential detection rates model’ to analyse the tive distances than similar-sized individual cope- effects of prey distribution, detection rate, handling pods (long body). Mobility increases the retinal time, capture success, and optimal foraging on area stimulated. Thus, moving prey are detectcd at zooplankton selection by visual planktivores. He greater distances than non-moving prey. Second, established that the prey detection rate is the prod- when the inherent contrast of the prey is low, tur- uct of the reactive field volume by the prey density. bidity is high, or light intensity is low, reactive dis- Since the visibility of a prey underwater depends tances are independent of prey size or shape. Third, upon its contrast with the background, the limits of whcn the water illumination to which fish eyes are the fish visual acuity are given by the contrast acclimated decreases, the contrast threshold threshold above which prey are detected. The con- decreases. The resulting effect on reactive distance trast threshold is not constant but decreases with is obscured by interactions between water illumina- increasing area of the retinal image, and increasing tion, contrast threshold, extinction properties of water illumination to which eyes are acclimated. the water, and area of the retinal image. The apparent contrast of a prey underwater can be Because fish are very large and mobile compared expressed as: to their prey, handlink times (i.e., time needed to pursue, capture, retain, and digest prey) are short, Ca = Co exp( - a D) and differences among prey types are likely to be negligible. Handling time per prey is also assumed where a = the water extinction coefficient, and to be constant in Werner & Hall’s model. The han- D = the distance between the prey and the retina. dling time is inversely related to hunger (Ware, Co is the inherent contrast of the prey defined by: 1972), and increases exponentially as prey size reach the planktivore mouth gape (Werner, 1974). CO= (Ib-Io)/Ib Soine zooplankter forms are able to avoid cap- ture by darting out of the fish visual field. The cap- where Ib = the illumination of the background (ex- ture efficiency (Le,, the proportion of prey pursued pressed in light flux per unit area) and Io = the illu- that is successfully captured) increases with fish mination of the prey. As defined, Co is indepen- size (i.e., age), and is specific to prey type. dent on prey size or shape. However, differences in For a particular prey assemblage, the strategy of colors among prey are responsible for differences in ’ prey selection that maximizes the energy intake rate inherent contrast. The area of the retinal image is unique (Mac Arthur & Pianka, 1966; Werner, (RA) depends on the surface area of the prey 1972; Charnov, 1973, 1976; Pearson, 1974; Werner projected (PS) onto a plane perpendicular to the & Hall, 1974). The optimal set of prey consists of sight line and the distance (D) between the retina all prey whose expected energy ifitake per handling and the prey: time is greater than a given value. It is derived by mathematical analysis performed on a prey distri- RA = f PS/D2 bution ranked according to the ratio of energy in- take to handling time. Werner (1972) and Werner & where f = the focal length of the eye. Hall (1974) implied that this ratio increases with To compute the maximum reactive distance, prey length. But, this may not be valid if larger in- three situations must be distinguished. First, when dividuals of a given prey type escape better the fish the inherent contrast of the prey is high, the maxi- capture. In such a case, the fish may avoid pursuing 134 larger and more evasive individuals of a prey type, selects the apparent largest prey. However, when in order to maximize energy intake. Eggers (loc. Daphnia and Diaptonzus are offered at the same cit.) emphasized that the assumed optimization time, the pursuit probability is higher for Daphnia criterion for foraging time may be incorrect, as the than for Diaptomus of equal apparent size (Vin- fish must be able to discriminate between prey yard, loc. cit.). Vinyard demonstrated also that types according to the assumed criterion, or, at when one Daphnia and one Diaptonius are offered least, to some highly correlated factor (Schoener, simultaneously, the average percentage of choice 1971). For two limiting cases, Schoener (loc. cit.) for the non-evading prey (Daphnia) increases with demonstrated that, to maximize the net energy in- the increasing number of feeding trials and reaches take rate while foraging, the optimal foraging a maximum value of about 90-95%. These results strategy was to minimize foraging time when the suggest a substantial intrinsic preference of biuegill predator was constrained by minimum energy re- for Daphnia which might be attributed to some quirement, or to maximize energy assimilated when learning process. An alternative interpretation time available for foraging was limited. (Confer & Blades, 1975; Eggers, 1977) could be that The ‘apparent-size model’ of prey selection the round body of Daphnia stimulates a greater described for bluegill sunfish (O’Brien et al., 1976; retinal image area than the elongated body of Vinyard, 1980), and white crappie, Pornoxis an- similar-sized Diaptomus. Nevertheless, in the same nularis (Wright & O’Brien, 1984), assumes that the situation, Diaptomtis is selected in favor of Daph- predator choice between prey is based on the prey’s nia by Perca ftuviatilìs (Furnass, 1979). According apparent sizes (see Fig. 8). The apparent size of a to Wright & O’Brien (loc. cit.) this inverse prefer- prey is defined as its angular height subtended at ence could only occur when Diaptontus is not mov- the fish‘s eye. When two prey, differing in apparent ing. Thus, interspecific pursuit choices would be size by an arc tangent of, at least, 0.2 degree (0.4 de- based on the comparison of differential specific gree for white crappie) are offered, bluegill sunfish motion bchaviours of the prey. Nevertheless, the basic assumption of the ‘apparent-size model’ con- flicts with the fact that the size of the retinal image of a prey object is determined by its area rather than by the visual angle subtended (Lamar ef al., 1947). Gibson (1980) tested the apparent-size model for three-spined sticklebdck (Gasterosteus aeulealus) over a wide range of densities of two size classes of D. imgna, and found that the model was valid be- low visual densities of 1100 prey per visual field, and failed above. He emphasized that an alterna- tive mechanism of prey choice must be operating under high prey densities. As many recent works are demonstrating that fish can discriminate be- tween different-sized prey (see Werner et al., 1983b), Werner (in litt.) believes that fish do not al- ways use apparent-size in prey selection. Compar- DIFFERENCE IN APPARENT SIZE ing the optimal foraging model with alternative ’ models of differential detection rates and apparent- Fig. 8. Apparent size choices for white crappie (Pomoxis an- size, Werner et ai. (1983b) showed that bluegill ac- nufaris, Centrarchidae) simultaneously presented two Daphnia tively selects zooplahkton according to prey sizes magna. Each point designates a 0.05 angle interval. The right- and densities, as well as to the energelical cost of hand side of the graph represents the percentage of the time the procuring them. Werner et d. (loc. cit.) aggreed apparently larger prey is initially pursued. The left-hand side with Kramer (1979), Mittelbach (1981), and Eggers represents the percentage of the time the apparently smaller prey is initially pursued. The curve is fitted by cye (from Wright 6r (1982) that bluegill do not appear to feed by O’Brien, 1984). apparent-size. 135

As mechanisms involved in size selective preda- ber of Daphnia eaten by a fish during a three tion at high prey density (i.e., several zooplankton minutes trial (43 prey in clear pools: 1 NTU, and 22 detected simultaneously) remained unclear, Gard- prey in the most turbid pools: 190 NTU), Because ner (1981) tested the differential detection rate the number eaten is proportional to the number de- hypothesis versus the apparent-size selection tected, size selectivity is independent of the number hypothesis, explored the role of decision, and pro- detected (i.e., density, as perceived by the fish). posed a ‘past detection rates model’. In laboratory Thus, when several prey are detected simultaneous- feeding trials with bluegill sunfish, he manipulated ly, the detection rate and the feeding rate are not turbidity in order to control the number and proportional to the reactive volume, but to the vol- proportion of two Daphniapulex size classes (1 and ume of water actualfy searched. To compensate 2 mm, added at the same initial density: 14 in- partially for the reduced reactive distances in turbid dividuals per liter) detected simultaneously by a waters the fish can increase its swimtning speed. fish. Gardner tested two alternative mechanisms: As, at the prey size ranke used (i to 2 mm), the cap- (a) the fish consumes zooplankton as detected, ture ability of Daphnia is ifidependent of size, and without making decisions: the larger sizes being size selectivity is not due to differential detection eaten more frequently because of a perceptual bias rate, Gardner concluded, as Werner & Hall (loc. (Bggers, 1977: Miller, 1979), or (b) the fish decides cit.), that size selectivity is caused by the fish deci- to ignore or pursue detected prey: the larger sizes sion to ignore small 1 mm Daphnia upon detection. being actively selected (Eggers, 1977). Since, (1) even when Daphnia is detected one di a Differential rates of detection, pursuit, or cap- time the fish still setects by size, and (2) selectivity ture may generate a size-biased distribution of prey does not decrease qith decreasing fiumber of simul- in the fish gut. At equal density of all prey sizes the taneously detected prey, Gardner disagreed with fish detect a gfeater proportion of larger zooplank- O’Brien et aÍ. (loc. cit.) that a fish coúld cbmpdre ton. Thus, detection rate increases with prey size, and select apparent largest prey appearing in its vis- This perceptual bias towards larger zooplankton re- ual field. quires no decision by the fish. Alternatively, the Based on his results, Gtirdnet. sdggested ari Biter- fish may ignore smaller zooplankton. This deci- native mechanism. The decision was established on sion, at the pursuit step, results in an active selec- the only reliable estimate of prey density available tiofi towards larger zooplankton. The pursuit prob- to the fish: i.e., past detection rates, implicitly used ability increases with prey size, or apparent-size in several foraging models (Schoener, 1971; Werner (Vinyard & O’Brien, 1975; O’Brien et al., 1976; & Hall, 1974; Charnov, 1976). When previous de- O’Brien, 1979). But, the fish’s decision to ignore or tection rates are very low, the fish has a low esti- pursue upon detection induces differential pursuit mate of prey density and eats zooplankton as de- rates for similar-sized prey (O’Brien, loc. cit.). Be- tected. When they are high, the fish has a high cause capture ability of crustacean zooplankton is estimate And chooses to pursue only the larger independent of prey size (Werner, 1974), it cannot zooplankton. Nevertheless, Gardner formulated cause size selectivity, but determined well the two limitations. First, the prediction of these results differential selectivity between taxa: e.g., copepods by an optimal foraging model is equivocal, as only versus cladocerans (Allan, 1976; Drenner et al., the larger 2 mm Daphnia shoúld have been eaten in 1978). all ex’periments. But, the decline in selectivity after Increasing turbidity level makes reactive dis- four minutes of feeding trials may suggest that tances decreasing and becoming independent of change in diet breadth is not continüous with prey prey size (Ware, 1971; Vinyard & O’Brien, 1976; Eg- density, but is saltatory, and depends on the mini- gers, 1977). In highly turbid water, the probability mum threshold value of the detection rate for the of simultaneous prey detection is very low, and the larger Daphnia, as predicted by optimal,foraging fish detects prey in the proportions of their actual theory (Werner & Hall, loc. cit.; Pyke et al., 1977). size class distributions in the water column. Gard- Second, the fish’s judgment capability may be ner (loc. cit.) observed that turbidity does not have limited. As Daphnia are not perfect spheres, the a significant effect on the size selectivity of bluegill, fish may misjudge their sizes when the ahgle be- but have a significant effect on the mean total num- tween its sight line and the Daphnia broad side is 136

too large. Thus, the constant but biased selectivity within and above the head portion of the visual pattern may represent a consistent error in the fish’s field. The authors emphasized the use of the ‘scan- evaluation of detected prey: that remains to be test- ning area model’ to predict diet composition, as it ed. reflects not only the pattern of fish vision (i.e., acui- Janssen (1982) stressed that only one prey selec- ty and sensitivity), but also may reflect the skewed tion model may not be adequate for all fishes. distribution of detected prey (as prey closer to the Based on visual detection differences between a search trajectory are generally attacked before facultative planktivore, bluegill, and an obligate reaching the transverse plane) or the apparent in- planktivore, blueback herring (see section III.A.l.), creasing rate of prey movement which enhances the Janssen (loc. cit.) proposed an alternative ‘first- conspiciousness of those prey approaching the sight model’ in which bluegill pursues the first prey cruising fish. detected. This hypothesis is behaviourally simpler Numerous studies have emphasized the role of and consistent with previous works on bluegill various components in the alteration of the general feeding on Daphnia in which it is assumed that the pattern of size selectivity of visual planktivorles on fish inventories the prey, then makes a decision, zooplankton communities, such as: the gape lirnita- choosing the most energetically rewarding prey to tion for larvae and small species (Blaxter, 1966; optimize energy intake, or choosing the largest Rosenthal $I Hempel, 1970; Wong & Ward, 1972; apparent-sized prey (i.e., the most likely to be de- Feller & Kaczynslti, 1975; Guma’a, 1978; Furnass, tected first). Janssen underlined also that this pro- 1979; Hunter, 1979, the role of prey visibility posal is different from a detection model, because (Zanet, 1972; Ware, 1973; Zaret & Kerfoot, 1975; bluegill will bypass potentially encountered prey as Kerfoot, 1980), prey motion and escape (Zaret, it pursues the first detected prey, and thus no choice 1980; Kerfoot et al., 1980; Vinyard, 1980), adapta- is required. tive responses of prey (vertical migration, helmet While models of prey detection based on reactive development, reduced pigmentation) (Zaret, 1972b; distance versus prey size relationships are sufficient Zaret & Suffern, 1976; Eggers, 1978; Hairtson, to predict the actual prey size-class frequencies in 1980; Wright et al., 1980; Fraser & @erri, 1982), the the fish diet (Ware, 1972; Werner & Hall, 1974; dependence on light and turbidity (Vinyard & O’Brien et al., 1976; Eggers, 1977; Gibson, 1980), O’Brien, 1976)’ the effects of hunger and prey den- models based on both actual reactive distances and sity (Wart, 3972)’ the effects of experience (Ware, volume-searched shapes are required to predict 1971), the effects and advantages of schooling (Eg. quantitative diets (Confer et af., 1978). For a cruis- gers, 1976). ing fish, such as lake trout (Salvelinus namaycush), So, at present, the generally referred ‘size- the reactive field (i.e., the volume searched) is rather selective pr cdation hypothesis’ appears to be a sim- .cylindrical and the prey detection rate is only plified approach to 1he more complex process con- proportional to the transverse visual plane area trolling prey selection by visual planktivores. It is (Confer et al., loc. cit.). For a fish, such as bluegill, evident that fish can discrimifiate between large which searches for each prey while stationary, the and small prey, but it is not through direct size per- reactive field can be defined by detection probabili- ception. The ‘visibility-selectivepredation hypothe- ty profiles for various visual planes (Luecke & sis’ supported by Zaret (1980) is based on both opti- O’Brien, 1981). To elucidate the role played by the cal properties of objects in underwater reactive field ih the prey detection event, Dunbrack environments and visual acuities of fishes. The vul- & Dill (1984) determined the scanning area (i.e., the nerability of a prey to a particulate feeder is deter- entire three-dimensional prey-reactive field) of mined by both its inherent total visibility (which is juveniles coho salmon (Oncorhynchus kisutch). In mainly influenced by the more visible part of the nature, coho salmon feeds with its body almost sta- body and the motion pattern; Lhe prey escape abili- tionary in running water, or actively searching in ty is secondary because, by learning to recognize still water. The fish attacks prey, in most cases, prey, visual planktivores can reach high capture ef- ahead and above the horizontal plane. Thus, Dun- ficiencies), and the range of visual acuities OF the brack & Dill (loc. cit.) found the greatest reactive fish in the present light conditions of the aquatic distances to be adjacent to the transverse plane environment (which is mainly influenced by its 137 spectral sensitivities and its contrast perception by the fish (i.e., the proportion of digested prey thresholds). upon ingestion). The Holling’s predation-act model implies that, For particulate feeders, the detection rate (DRi) for particulate feeders (larvae and small species, as determines the maximum (i.e., potential) rate at well as post-larvae: juveniles and adults), the prob- which a prey type i is available to the consumption ability of ingestion of a prey type i (Ii) is defined by the fish. DRi is the product of the prey environ- by the product of four conditional probabilities mental density (EDi) by the square of the reactive (with always Vi = I: - Di distance (RDi) of the fish for this prey (at the actual illumination and turbidity IeveIs of the water en- vironment), by the fish swimming speed during search (SSs), and by its searching frequency (SF): where di, pi, ci, and ri are the probabilities that the prey type i is detected (i.e., encountered in the visual DRi = EDi .RDi2 * SSs SF field), pursued, captured (in the buccal cavity), and retained (on the branchial apparatus), respectively. The searching frequency (i.e., the proportion of The probability di accounts for the differences time spent foraging dedicated to searching) is the between prey in size, shape, inherent contrast, con- ratio: trast with the background, color (i.e., pigmenta- tion), and motion behaviour. It is quantified by the SF = Ts/Tf with Ts = Tf-Th reactive distance (RDi) at which each a prey type i i$ detected. For each prey type RDi varies with the where Tf = the time spent foraging, Ts = the time illumination of the water. spent searching for prey, and Th = the time spent The probability pi reflects tfie decision of the fish handling prey. to ignore or pursue detected prey. According to the The detection rate (DRi), successively corrected model adopted, its calculation is based on past de- by the fish ‘relative preference’ (PPi, in Yo) for pur- tection rates, apparent-size, or net rates of energetic suit upon detection (through decision, or not, when intake. The decision may be influenced by the fish no (i.e., effects of experience and hunger), or one or hunger level, and by its previous experience of prey several prey types are detected simultaneously; this (i.e., searching image concept). But, it may requires proportion depends on the model adopted: no decision by the fish if the first-sight hypothesis differential detection rates, past-detection rates, is used. apparent-size, or first-sight), and efficiencies For The probability ci accounts for the differential capture (CEi, in Olo), retention (REi), and digestion escape ability of prey, and represents the fish cap- (DEi), Le., the proportion of individual prey type i ture efficiency for each prey type. digested), represents the predicted fish feeding rate The probability ri evaluates the retention capabil- (FRi) on the prey type i: ities of the branchial basket. It is estimated roughly

by the value of the cumulative frequency of inter- FRi = DRî + PPI. DEi - REi DEi raker (or intermicrobranchiospine) spacings cor: responding at the size of the prey type i, and cor- An optimal foraging approach, based on Werner rected for differences between similar-sized prey in & Hall’s (1974), Pearson’s (1974), Charnov’s (1976), shape, surface properties (relative to the filter), and Mittelbach‘s (1981), Eggers’ (1982), and Werner et palatability, on the functional characteristics of the al.’s (1983b), may be used to predict the optimal diet filter (i.e., stickyness, and possible adaptative alter- breadth (i.e., the optimal range of prey types eaten) ations of the mucus secretion rate; mesh size, and by a given-sized fish. Similarly to these models, the its possible mechanical or behavioural adaptative net rate of energy gained by a particulate feeder alterations), and on the characteristics of the water foraging in habitat j (NEj/Tfj) is the ratio: current passing over the entrapment structures (i.e., strength and direction). NEj/Tfj = [CKl(FRij.Eij)-Cs]/ The digestion probability of a prey type i (Di) [l+CE,FRij .Hij] represents the digestion efficiency of this prey type 138

with Eij = (A.ECij) - (Chi. Hij) filter-feeding copepods, the filtering efficiency of a (tow-net or pump) filter-feeding fish can be estimat- where NE = the net energy gained while foraging ed from the cumulative frequency of its interraker (in Joule), Tf = the time spent foraging (in second), spacings. The simple sieving model is assumed, and FRi = the feeding rate (but not the detection rate, then tested as a null hypothesis. The distances be- unlike the mentioned models) for prey type i (in tween gill rakers are measured, and used to build a number per second), Ei = the energy gained while cumulative frequency of interraker spaces. When foraging on prey type i (in Joule), Cs = the energy rakers are elongated and nude (as in several cost for searching (in Joule per second), Hi = the clupeids), the interraker spaces may, more accurate- handling time for prey type i (in second), A = the ly, be weighted by the raker length (Drenner, 1977). assimilable fraction of an individual prey type i (in Drenner et al. (1984a), using two gizzard shad (13.6 Vo), ECi = the energetic content of an individual and 16.3 cm SL) pump filter feeding in a 80 liter prey type i (in Joule), and Chi = the energetic cost pool, determined that the proportion of artificial of handling prey type i (in Joule per second). spherical particles removed by fish increases as a The optimal diet is determined by ranking prey function of particle size, leveling off at about types from highest to lowest NEij/Tfj ratios, and 60 pm. They showed that the sellective ingestioli of adding prey types to the diet until the ratio NEj/Tj these particles by gizzard shad can be predicted us- is maximized. ing a model of cumulative frequency of interraker The energetic costs of searching (Cs) and han- distances. In similar feeding exDeriments using dling (Chi) can be estimated from fish oxygen con- polystyrene microspheres ranging from 7 to 52 pm sumption as a function of fish length, swimming in diamcter, Drenner et al. (1984b) determined that speed (SSs and SSh, respectively), and water tem- four size classes of blue tilapia (7: aurea) between perature; the energetic content of a prey type can be 4.3 and 10.7 CM SL, pump filter feed selectively on determined by converting the prey length to dry microspheres larger than 25 gm. But, for blae tila- mass, and then multiplying by the appropriate pia particle retention byt $ííl rd~elrhis secondary energy equivalent (Mittelbach, 1981). and, small mucus-covered microbranchiospines lo- cated in a single row on the second, third, and 2. Tow-net filter feeders fourth gill xches, may first account far the effi- cient retention of small particles by cichlids (Gosse, For tow-net filter feeders, the Holling’s preda- 1955; Fryer & ales, 1972). tion-act model implies that,the probability of inges- Overlooking the spacing frequency distributpn tion (Ii) of a prey type i is defined by the product of of the branchial filter of the tcnw-net filter-feedmg only two conditional probabilities: Atlantic merih8derr, Durbin & Durbin (1975) used anuther calculation of the filtering (Le., retention) Ii = ci’sri efficiency (FEi) for several phytoplankffon species ditferirig in sizes. For each particle size i4 the where ci and ri are the probabilities that the prey authors computed FEi as the ratio between the type i is captured and retained, respectively. specific filtering rate (i.e., the water volume swept Since tow-net filter feeders do not provoke water clear per unit of time: Fi, in liter per fish per minute) pressure disturbances ahead while foraging at, and the maximum filtering ratk (Le., the total vol- generally, high swimrhing speeds (see section ume of water passing over its gill rakers: Fmax, in III.B.l.), it is probable that the capture event cannot liter per fish per minute). Fi was the product of the cause selectivity. So, the prediction of particfe tank water volume (Y, in liter) by the specific feed- selection by tow-net filter feeders may be reduced to ing rate (FRi, in number of particle Size i ingested -l the only assessment of the retention efficiencies of per fish per minute). PKi was computed from the their branchial filters. Nevertheless, very few atten- regression curve between the log particle- tion has been paid to the modelling of this feeding concentration and time. Fmax was calculated 2s the 1 mode. product between thle mouth opening area (MA) and Extrapolated from Boyd’s (1976) and Nival & the mean swimming speed of the fish (SSf) duhg Nival’s (1976) analysis of the particBe selection by the foraging period. 139

Although not well documented, it is probable 3. Pump filter feeders that the optimization of particle retention by tow- net filter-feeding plantivores, through behavioural As for tow-net filter feeders, for pump filter feed- or mechanical modifications of their filter, may ers, the Helling's predation-act model implies that play a role in their selective feeding. For example, the probability of ingestion (Ii) of a prey type i is the paddlefish can change its swimming speed defined by the product of two conditional probabil- which controls the velocity of the water flow in ities: through its filter, and can control, through muscu- lar contractions, its mesh size (Rosen & Hales, Ii = ci a ri 1981). Filtration rates by other tow-net filter feeders can roughly be considered as constant, because where ci and ri are the probabilities that the prey swimming speeds during feeding are generally un- type i is captured and retained, respectively. changing. Contrary to tow-net filter feeders, the capture Thus, for tow-net filter feeders, the capture rate event may well determine the selectivity of pump (CRi) determines the maximum (i.e., potential) rate filter feeders (see section III.B.l.). The escape abili- at which a prey type i is available to the consump- ty of prey determines the capture efficiency of tion by the fish. CRi is the product of the prey en- pump filter feeders foi. zooplankton. But, non- vironmental density (EDi) by the maximum filter- evasive particles are captured in proportion to their ing rate (Fmax) of the fish: dcnsities in the environment, and selected only ac- cording to the fish retention efficiency. CRi = EDihFmax Thus, for pump filter feeders, the capture rate determines, as for tow-net filter feeders, the maxi- Fmax is the product of the fish mouth opening mum (Le., potential) rate at which a brey type is area (MA) by its swimming speed during the towing available to the consumption by the fish. sequences (SSt) and by the towing frequency (TF): The capture rate (CRi) of a prey type i is thc product of the prey environmental density (EDO by Fmax = MA .SSt .TF the maximum filtering rate (Fmax) of the fish:

TF (Le., the proportion of time spent towing dur- CRi 1= EDi Hmax ing a foraging period) is the ratio: An approach similar to Durbin & Durbin’s may TF = Tt/Tf with Tt = Tf-Th be used to predict the retention efficiency (FEi = Fi/Fmax) of a pWnp for a prey where Tt = the time spent towing, Tf= the time type i without direct measurements of its filter. In spent foraging, and Th = the time spent handling this case, Fmax can be computed from the product prey (i.e., the duration of the swallowing move- of the buccal pumping rate (PR) by the buccal vol- ments during which the food bolus is transported ume (BV) and by the pumping frequency (PF) from the filter into the oesophagus). (Drenner et al., 1982b): The capture rate (CRi), successively corrected by the fish efficiencies (in Oro) for retention (RE& and Fmax = BV.PR.PF digestion (DE$ represents the predicted fish feed- ing rate (FRi) on the prey type i: Contrary to tow-net filter feeders, Fmax of pump filter feeders may not be completely considered as FRi = CRi REi DEi constant (Drenner, in litt.) because pumping rates may vary. Buccal pumping rates can be determined The net rate of energy gained by a tow-net filter from films or video recordings, and buccal volumes feeder is computed from the equation used for par- (i.e., maximum suction volumes) by injection of ticulate feeders, and the optimal diet is predicted by plaster (Drenner, 1977; Drenner et d.,1982b), sili- following the mentioned procedure. cone, or dentist casting past (such as, Geltrate@ :Lazzaro, in progress). Drenner et al. 140

(loc. cit.) developed this pump filter-feeding rate cause they were based on body size, which has been model for 5-15 cm SL gizzard shad. Buccal vol- considered for a long time as the primary prey ume is a (nearly cubic) power function of shad characteristic responsible for the selectivity of standard length, while pumping rate (determined planktivores. Now, it is manifest that the considera- from 16 mm films at 64 frames per second) declines tion of (even empirical) information on a) other in- exponentially. Filtering rate (in liter per minute) is teractive prey characteristics, such as, visibility and a positive power function of shad standard length, motion (for particulate feeders), and escape ability but a negative power function of shad body weight. (for filter feeders), b) previous fish experience for They tested the model during four 1.5 hour labora- prey, c) fish hunger level, and d) fish capability for tory feeding trials with and nauplii. The feeding mode switches and habitat shifts, are essen- prey densities declined exponentially with time. Ac- tial when attempting to make models more realistic. tual and predicted densities were not significantly Flexibility limits often the realism of ecological different. But, the authors emphasized that the models which may fail to predict changes a) in predicted filtering rates are potential and not abso- planktivore diet and in habitat use, as a conse- lute measurements. quence of plankton alterations, and b) in The pumping frequency (i.e., the proportion of plankton communities induced by planktivorous time spent foraging dedicated to pumping) is the fishes. ratio: An example emphasizing the plasticity of the trophic interactions between planktivores and their PF = Tp/Tf with Tp = Tf-Th food is done by Eggers (1982), who estimated the relative frequencies of various prey species and size where Tf = the time spent foraging, Tp = the time categories occurring in stomach contents of Lake spent pumping, and Th = the time spent handling Washington juvenile (Oncorhyn- prey. Contrary to particulate feeders which handle chus tzerka) at different seasons of the year. He prey individually, tow-net and pump filter feeders showed that sockeye have a high, but extremely dy- stop towing and pumping, respectively, to handle namic preference for large non-evasive prey, ac- simultaneously all organisms and particles con- cording to their seasonal availability in the water stituting the food bolus trapped during the filtering column. $mali as well as evasive prey are pursued sequence from the gill rakers, the microbran- and captured during periods when large non- chiospines, or the pharyngeal pockets into the evasive forms are scarce or absent. He pointed out oesophagus. Far example, gizzard shad display un- the extreme flexibility of prey preference by plank- usually large ‘swallowing’ movements, between tivoraus fishes as an adaptative response to changes each, pumping sequence (Drenner et al., loc. cit.). in prey composition. The capture rate (CRi), successively corrected by Aquatic environments are generally heterogene- the fish efficiencies (in Yo) for retention (REi), and ous. So, the expressions proposed for each plankti- digestion (DEi), represents the predicted fish feed- vore feeding mode might include parameters ac- ing rate (FRi) on the prey type i: counting for the fishes ability to (visually) detect prey patches, and for their foraging strategies (e.g., feeding mude switches, when behaviourly available, in response to changes in the food resources of the The net rate of energy gained by a pump filter enviroriinent) itn discriminating between patches feeder is computed from the equation used for par- and using them. Theory of habitat ‘patch’ use are ticulate feeders, and the optimal diet is predicted by based on empirical studies where an experimental following the mentioned procedure. habitat of homogeneous structure includes areas of different prey densitics (e.g., Krebs et al., 1974). B. Optimal foraging predictions, habitat shvts, and Most foraging models dedicated to habitat use$ by feeding mode switches freshwater planktivores concern particulate feeders, and almost exclusively bluegill sunfish, Lepomis By the past, numerous planktivoire models have macrochirus. In contrast, the selective advantage of been developed in a rather quantitative way, be- the filter feeding modes (in term of net energy 141

gained by foraging this way towards that gained by ently cannot (Janssen, 1976, 1978a). If the size of particulate feeding) remains still little explored. prey is small relative to that of the fish and their Using a statistical approach based on a stepwise density sufficiently high, filtering may be more regression analysis, Lammens (1985) developed a profitable than particulate feeding. Only the largest conceptual model of pump filter feeding bream, alewives (30 g) filter feed (Janssen, 1976). But, Abramis brama. Comparing stomach contents of small alewives (50-70 mm SL) may filter in the 9-35 cm SL bream and zooplankton samples col- field at dusk (Janssen, 1978b). Actually, filter feed- lected from a small shallow eutrophic lake, he test- ing may be more frequent at night (Janssen, 1978b, ed three hypotheses: a) the average prey size in- 1980) because, as light levels decline, the size of the creases with bream length, while standard deviation visual field and the detection rates of prey decrease declines, b) the prey size is strongly correlated with (Vinyard & O’Brien, 1976) and the selective advan- available prey size, and c) the prey density has little tage of switching to filtering should increase effect on prey size selection (i.e., clogging of the gill (Holanov & Tash, 1978). rakers does not occur). Lammens (loc. cit.) demon- The use of different feeding modes is dependent strated that the three assumptions cannot be reject- upon prey-predator size ratios, prey density, and the ed for bream pump filter feeding on 0.36-0.56 mm ability to switch feeding modes. For example, Bosmina coregoni, and for bream larger than whereas menhaden particulate feed on larger prey 20 cm SL pump filter feeding on 0.90-1.52 mm (prey size/fish size ratios from 1/20 to 1/200), they Daphnia hyalina. For bream smaller than 20 mm filter feed on smaller prey (ratios from 1/50 to SL feeding on D. hyalina, all assumptions were re- 1/20000) (Durbin, 1979). jected because the fish use particulate feeding or a Crowder & Binkowski (loc. cit.) suggested the ex- combination of particulate and pump filter feecl- istence of a switching competitive balance between ing. Thus, as stressed by Lammens for bream, it is alewife and bloater as, if prey sizes shift towards urgent to develop foraging models combining par- smaller prey, alewife could take advantage over ticulate and filter feeding and including the ability bloater due to their ability to profitably switch to to switch between feeding modes. Built-in switch- filter feeding on these prey. Using Janssen’s (1976) ing mode procedure, in response to spatial or tem- data on alewife, they showed that, at an experimen- poral changes of plankton composition and density tal density of 254 Daphnia per liter, a) handling in the fish environment, will improve model predic- time per prey increases from small ,(0.068 mg wet tions. weight) to large (0.241 mg wet weight) Daphnia, Quantifying the cost of feeding on prey (Le., the and from filtering, to gulping, and then particulate handling time per prey weight) for particulate feed- feeding, b) the fecdiiig rate on small Daphnia ing alewife (Afosa pseudoharengus) and bloater (0.068-0.70 mg wet weight, 0,020-0.026 104 fish- (Coregonushoyi) and for alewife using a combina- prey weight ratio) is the highest (13.65-14.57 Daph- tion of particulate, gulping and filtering modes, nia eaten per second, 0.95 -0.99 mg dry weight eat- Crowder & Binkowski (1983) examined the energet- en per second), when the filter fee.ding mode is ic advantages of feeding mode switches. Fish were used, c) the feeding rate on large Daphnia fed Daphnia and Mysis in laboratory experiments. (0.205-0.241 mg wet weight, 0.180-0.301 lo4 fish- Cost curves for particulate feeding bloater and ale- prey weight ratio) is the lowest (1.98-2.32 Daphnia wife are very similar. They are lowest for the largest eaten per second, 0.48-0.51 mg dry weight eaten prey avaiiauie in me open iaKe (ilvrysis)ana increase per second) when the particulate feeding mode is exponentially for smaller prey. But, if alewife cost used, whereas d) the gulping mode used to feed on curves are adjusted for switches in feeding mode intermediate-sized Daphnia (0.124 0.160 mg wet (i.e., gulping, filtering), as observed to occur by weight, 0.055 -0.124 lo4 fish-prey weight .ratio) Janssen (1976), relative costs of feeding on small provides intermediate feeding rates . (3.10-4.73 prey are much reduced. Daphnia eaten per second, 0.46-0.65 mg dry Feeding mode switches in alewife are correlated weight eaten per second). with relative time costs of particulate feeding versus Because most optimal foraging models of plank- filter feedirfg. Whereas alewife can switch from tivorous fishes are based exclusively on the particu- particulate feeding to filter feeding, bloater appar- late feeding mode although many obligate plankti- 142 vores also filter zooplankton, Crowder (1985) for switches in feeding modes the relative costs of hypothesized that feeding mode switches may be feeding on small prey is much reduced (Crowder & predictable from the costs and benefits of foraging Binkowski, 1983), and b) in tanks with known sizes in various modes. As in fishes that switch feeding and densities of zooplankton (Janssen, 1976), large modes, small individuals generally particulate feed fish (30 g) filter feed, medium-sized fish whereas large individuals filter feed (Leong & (12.7-22.5 g) gulp, and small fish (8.0-12.9 g) O’Connell, 1969; Janssen, 1976; Holanov & Tash, particulate feed, Crowder (loc. cit.) assumed that 1978; Durbin, 1979; Drenner et al., 1982c), Crowder the cost curves may well explain the feeding mode (loc. cit.) pointed that the different feeding modes switch observed to occur near the prey-fish weight may be dependent on both the fish-prey size ratio, ratio for which the cost curve including filtering the relative densities of large and small prey, and has a hwer cost/bene€it ratio than that for particu- the ability to switch feeding modes. late feeding. Nevertheless, as a) the actual energetic To support his hypothesis, Crowder (loc. cit.) costs of filtering versus particulate feeding are analyzed three quantitative examples of switch poorly knowii (Durbin, 19791, b) the costs of swim- from particulate feeding to filter feeding. For eack; ming while Filtering might be slightly higher, and c) independent case, he noted a surprising agreement the thlieshold value of the prey-fish weight ratio in- between the feeding mode switch observed and the: ducing feeding mode switch must certainly dcpenld relative profitability of each mode. on prey density, Crowder emphasized that this as- First, using bong & O’Connell’s (1969) data on sumption still need additional testing. Northern anchovy, Engraulis mordax, feeding on Besides, as microscale patches in zooplankton various densities of Artemia nauplii and adults, are frequent and average zooplankton densities are Crowder (loc. cit.) determined the equal return rate significantly lower than densities found in patches isopleth (i.e., the curve representing the combined (Steele, 1974; McNaught, 1979; Owen, 1981), Crow- densities of adults and nauplii which would provide der stressed that patchly distributed zooplankton an equal return rate (mg dry wet per minute) to an may frequently support filtering and it would be anchovy filtering nauplii or particulare feeding on very advantageous for fish to be able to rapidly adults). Plotting on the same graph the percent o€ switch back and forth between feeding modes to observations in which schooling wer% forage in such patchly environments. Finally, he particulate feeding on various densities of adult remarked that by comparing plankton yields, using Artemia, in tanks containing an average of 200 to alternatively particulate and filtering modes, fishes 400 nauplii per liter (O’Connell, 1972), Crowder may be able to assess better which provides the noted that the isocline for 50% particulate feeding greatest net energy gain. He concluded that includ- is closely parallel to the isopleth of equal return ing feeding mode switches (based on optimal forag- rates. This demonstrated that feeding modes ?t ing theory) in models, to respond to spatial and different densities of large and small prey may be temparal patchiness (i.e., to account for bath ef- accurately predicted by optimal foraging theoriesr. fects on detection rates and sampling between However, the response is graded as, when filter. modes), should improve their predictions. feeding should be more profitable, some particulate A main goal responsible for the expansion of op- feeding is observed and conversely. timal foraging theories in prey selection models is Second, using similar experimental data on Pa- the prediction of planktivore diet and habitat use as cific mackerel, Scomber japonicus (O’Connel1 & a function of food resource availability and benefit Zweifel, 1972), Crowder (Ioc. cit.) determined that for the fish. This knowledge has a potential rele- a density of 2.007 adult Artemia per liter should vance to the study of aquatic community interac- provide equal return rates through particulate or tions in lalces. It represents a potential basis to sup- filter feeding. Again, this density predicted by an port mechanistic theories of competition and optimal foraging hypothesis is close to that (1 or 2 species packing for the prognosis of aquatic com- Artemia per liter) derived from observations and munity structures (Werner, 1977). intuition of O’Connel1 & Zweifel (loc. cit.). Studying the ecological Segregation be tween Third, considering comparable data on alewifk, three sunfish species in small ponds, Werner & Hall as a) when the clost curve (Werner, 1977) is adjusted (1976) disclosed that, as segregation increases with 143

resources decline, and niche shifts depend on the changes in the resource levels of these habitats, cali presence of congeneric sunfishes, experimental be predicted by foraging models. Applying the op- studies of foraging behaviour mechanics are essen- timal foraging approach to the study of fish feed- tial to understand the organization of aquatic com- ing behaviour, Werner et al. (1983a, 1983b) ex- munities. To identify the competitive mechanisms plored the capabilities of bluegill sunfish to assess responsible for habitat shifts of bluegill sunfish in short term changes in their environment, and their presence of a congener, green sunfish (Lepomis flexibility to respond to these changes in ways cyanellus), Werner & Hall (1977) confined each predicted by the model. The optimal foraging mod- species alone and with the congener in homogene- el (which conceptualization is developed in Mittel- ous patches of vegetation habitat. Morphological bach, 1981), based on detection rates versus prey and behavioural attributes permit bluegill to ex- size and density, and fish length, plus the laborato- ploit a broader array of habitats (Keast, 1970; ry assessment of foraging costs, permitted Werner Werner & Hall, 1976; Werner, 1977; Werner et al., et al, (loc. cit.) to predict actual food selection with- 1977), although their more protrusible mouth are in habitats, as well as, foraging rate differences be- more efficient in capturing small zooplankton. tween three habitats (open water, sediments, and This habitat flexibility eclipses the competitive ad- vegetation). Deviations from predictions of the vantage of the sit-and-wait foraging behaviour of model allowed them to discover additional green sunfish in vegetation environment. As the mechanisms controling the prey preference by blue- mechanisms involved in habitat shifts among cen- gill. Even, the acurate bredictions of the size- trarchids are similar to those applying among frequency distribution of Daphitiapulex, as a func- salmonids (e.g., between allopatric populations of tion of the fish body length, made the authors sug- brown trout, Salmo trutta, and arctic char, Salveli- gested that the size-selective pi-edation by bluegifl nus alpinus, in Sweden: Nilsson, 1960, 1963: be- may bc related to ‘some enérgetic considerations’ tween trout, Salino clarki, and char, Salvelinus by the fish. Nevertheless, slig malma, in sympatric and allopatric populations in mated prey detection rates or Canada: Andrusak & Northcote, 1971, and Schutz ter the accuracy of the diet pr & Northcote, 1972), Werner & Hall (loc. cil.) er et al. (loc. cit.) Stressed that the assessment of the stressed that studies documenting habitat shift and zooplanktoh densities actuaily partitioning afe essential .to understand aquatic fish while foraging is a crucial community assemblages. As, in natural lakes, small bluegill are rektricted Werner et al. (1981) demonstrated that fish learn- to weedbeds and their foraging rates conflict with ing (i.e., experience related effects) can readily alter those predicted by optimal habitat use models (Hail the predictions of foraging models. Thus, they & Werner, 1977; Mittelbach, 1981); Werner et al, recommended to explore the various mechanisms (1983a) postulated that the pr involved and include them in models of prey selec- by piscivorous largemouth tion, in order to improve habitat use predictions salnzoides) is responsible for this deviation fram and test submitted theories. In field tests of an op- predicted foraging behaviour. The p timal foraging model, Mittelbach (1981) and Wern- caused vulnerable small size classes of bluegill to er et al. (1983a) demonstrated the importance of forage in less profitable, but safer, vegetation habi- the size-related predation risk for differences in tat, These data provided experimental support for habitat use between various size classes of bluegill the hypothesis of Hall & ner (loc. cit.) and Mit- sunfish, telbach (loc. cit.) that s fishes are limited to Werner & Hall (1974), Mittelbach (1981), and weedbeds because of a behavioural response to thé Werner et al. (1983b) demonstrated that bluegill greater predation risk suffered in more open sunfish can respond to changes in the resource level habitats. Nevertheless, the cues úsed bJI fish to of the environment by modifying their food parti- evaluate the predation risk are unknowh. Werner et cle size selection, in close agreement with predic- al. (loc. cit.) noted that predation risks tend ¿o con- tions by foraging models. Similarly, Werner (1982) centrate the young of many fisfi species in the vege- and Werner et al. (1983b) showed that habitat shifts tation of iiatural iakes (Hall 6 Werner, loc. cit.; by biuegili in small ponds, as a consequence of Laughlin & Werner, 1980; Mittelbach, 1984). So,

I 144 they suggested that competition and predation may to transport the food bolus €rom the branchial ap- interact in subtle, but critical ways, in fish commu- paratus into the oesophagus) to reference threshold nities. values. Past detection rales (Gardner, 1981) and In conclusion, field (or laboratory) tests of past swallowing rates are probably the only reliable foraging models are essential to evaluate the knowl- estimates of prey density available to the fish. edge of mechanisms involved in the selective (or Preliminary feeding behaviour experiments with random) use of plankton by planktivorous fish. the concerned fish are essential to determine if the More studies are needed to explore the (ecological, foraging model must incorporate tow-net and/or physiological, or behavioural) cues used by fish to pump filter feeding in addition to particulate feed- assess short term change in the relative resource lev- ing, and procedures for feeding mode switches in els of their habitats. Predictions of diet and habitat addition to procedures for habitat shifts. The use of individual fish should help to determine knowledge of the feeding mode repertory permits potential changes in plankton (and other aquatic) to explore all the alternatives available to the, fish to communities that could be generated by fish popu- maximize its net energy gained while foraging. As lations. In addition, models of prey selection and the feeding mode repertory depends generally on habitat use might include input variables (rather the fish age, a foraging model may not be valid for than state-variables, as suggested by Bakule & the entire life of a single fish. This has considerable StraSkraba, 1982) to mimic optimization con- consequences Por modelling the habitat use by fish straints (such as, influences of previous experiences populations (see also the effects of schooling on for the various food types, hunger level, intra- and feeding mode and selectivity in section 1I.D.). To interspecific competition for resources, predation predict feeding mode switches, it remains to estab- risk from upper trophic levels, on feeding be- íish in which circumstances and habitat types tow- haviours within habitats and foraging patterns be- net and pump filler feeding have the selective ad- tween habitats) to improve their soundness. vantage over particulate feeding to increase the fish It means that models must modulale their diel breadth. Apart from improving the flexibility responses (i.e., feeding modes, rates, and selectivi- and rcalism of fish foraging model$, such studies ties, feeding mode switches, foraging patterns, hab- should give veiy interesting insights about the driv- itat shifts) to cdanges in the environment, by adapt- ing forces responsible, through , ing their own structures to new constraints, just as for the cliffwentiation and the fitness of the various natural systems do. For example, when particulate feeding rvlodes used by planktivorous fish. feeding within an habitat is no more beneficial for Wc now have Substantial evidences that fish for- the fish (becausle the energy gained by feeding this age on plankton in an ‘optimal-like way’. Thus, it way does not compensate the costs, or the presence appcars pressing that future models of prey selec- of piscivores in this habitat makes too dangerous to tion by planktivores should include both habitat feed this way during the day), is it more profitabk shift and feeding mode switch abilities, together (in the sense of optimizing the fish diet breadth) to with changes in feeding mode repertory following shift habitat (i.e., to continue particulate feeding in fish growth (i.e., size). This is essential for model- an habitat of higher profitability, or lower preda- ling accurately plankton selection by planktivore tion risk, respectively), or to remain in this habitat populations. but switch feeding mode (i.e., to use filter feeding in that habitat if it is more beneficial for increasing the net energy gained, or to avoid predation in that VI. Fidd evidence o€ planktivorods fishes selective habitat by filter feeding at night, respectively)? impact on plankton communities Such alternatives might be investigated, using a mechanistic approach similar to Holling’s. Feeding A. Impact of particdate .feeders mode switches hnd habitat shifts could be predicted by comparing actual past detection rates for partic- I. Direct effect on zoopllanlctolz communities 1, ulate feeders (Gardner, 1981) or past ‘swallowing’ Ivlev (1961), summarizing ten years of Russian rates for tow-net and pump filter feeders (i.e.s the fish feeding research (and mostly on non- rates at which towing and pumping are interrupted planktivores), first presented evidence for the im- 145

portance of prey size to fish predators. According susceptible to fish predation, and their replacement to Novotna & Korinek (1966), the pioneer works ex- by smaller, less vulnerable, forms. The studies of ploring in experimental ponds the effects of the HrbáEek et al. (loc. cit.) showed the same selective fish stock on the zooplankton composition and pattern in carp ponds, and the authors hypothe- abundance were realized by Walter (1895), Contag sized that the changes observed in the zooplankton (1931), Pliszka (1934), Weimann (1938, 1939, 1942), composition were the result of size-selective feeding and Susta (1938), whereas the changes in plankton by carp. communities induced in a lake by the concentration These papers have been followed by a great num- of the fish population, consecutive to a drop in wa- ber of publications emphasizing the size-related al- ter level to half its optimal value, was studied by terations in zooplankton communities as a conse- D’Ancona & Volterra D’Ancona (1937). However, quence of planktivorous fishes. Itl Lake Albert, HrbAEek et al. (1961) definitively showed, in small Green (1967) related the differential selection of European carp ponds, that zooplankton species planktivores for two prey morphs of D. limholld composition and size range was influenced by the to a difference in prey body size. Hall et al. (1970) predation pressure of planktivorous fishes. Later observed shifts towards smaller sizes OF zooplank- on, Brooks & Dodson (1965) concluded that the in- ton following bluegill introduction into experimen- troduction of marine planktivorous alewives (A. tal ponds. The replacement of larger D. pulex by pseudoharengus) into small southern New England smaller D. dubia as a consequence of smelt (OS- lakes caused marked changes in zooplankton com- merus mordax) intraduction was observed by Reif position. By comparing the zooplankton distribu- & Tappa (1966) in Harvey’s lake, Pennsylvania. tions of some of these lakes, the authors demon- Selective predation by alewives in Lake Michigan strated that (1) large zooplankters were particularly resulted not only in the decline of the largest cala- , vulnerable to predation by alewives, and (2) as a noids, and cladocerans, but also in the decrease of consequence of this piscine planktivore predation, the average size and the size at onset of maturity of alewife lakes were characterized by the absence of D. retrociIrva, while smaller species increased in large zooplankters (see Fig. 9). Thus, they pro- number (Wclls, 1970: see Fig. 10). In the same man- posed that selective predation by alewives results in ner, a shift in zooplankton size distribution towards the elimination of the larger zooplankters more smaller forms, plus a decrease in size and minimum egg-bearing size of D. galeatu were consequences of alewife introduction in Lake Wononskopomuc, Cormecticut (‘Warshaw, 1972). ‘Size-selective’ rain- bow trout (S. gairdneri) and yellow perch (R flavescens) introduced into two Michigan lakes, fed only upon Daphniapulex over 1.3 mm long, which are mature, as well as immature in Sportley Lake, and are mostly mature in Stager Lake (Galbraith, 1967). Thus, predation on Daphnia can be consid- ered age specific as well as size specific. In Sportley Lake (see Fig. 11) the daphnid population was dra- . matically affected by the fish introduction (com- plete elimination of D. pulex, progressive replace- ment by two smaller species, decrease in averagk 0.2 0.4 0.6 O8 1.0 1.2 c‘. ZOOPLANKTON LENOTH (mm) size of daphnids From ¡A to 0.8 mm, decrease in percentage of daphnids larger than 1.3 mm from Fig. 9. Mean size of zooplankton in Crystal Lake, comparing 53.8% to 4.7%) but in Stager Lake none of these b- ten years before the introduction of Alosa aestivalis (Clupeidae) changes occurred. Galbraith‘s results pointed out with ten years after: the usual large-sized crustacean dominants the necessity to consider the matdration Size of (spp. of Daphnia and Diaptomus: respectively 1.3 and 0.8 mm daphnids for interpretirig trophic relationships be- long) are eliminated’ and replaced by small sized, basically iitto- ral species (especially Basnzina longirosfris 0.3 mm long) (from tween daphnids and planktivorous fishes. Brooks & Dodson, 1965). Comparing the populations of Daphnia cuculla- 146

ta in two eutrophic Mazurian lakes (Southern Po- 1954 I land), Gliwicz e¿ al. (1981) showed that a smaller mean individual size and a younger age structure in (predation dominating) Lake Mikolajskie contrast- ed with a larger mean individual size and an older ..... age structure in (food concentration limiting) Lake Majcz. They observed a decreased clutch size (i.e., mean number of eggs carried per female) ih the larger size classes of Daphnia populations as a con- sequence of the selective removal of the (more con- spicious and less evasive) larger females carrying a greater number of eggs and the females of the same size (age) class carrying greater number of eggs. Plotting the body length versus the average or max- imum clutch size of various cladoceran species of daphnids and sidids, Gliwicz (1981) determined that, for sirnilar body lengths, cladocerans typical in lake epilimnia have their clutches smaller than those of cladocerans common in small and fishless water bodies. Because this was also true for cy- clopids and calanids, Gliwicz emphasized that Daphnia LENt3TH (mm) selective predation by visual planktivores should be considered as a determinant factor Controlling the Fig. 10. Length distributions of female Daphnia refrocurva from Lake Michigan samples of 1954, 1966 and 1968 (darkly clutch size in planktonic . As Zaret shaded portions represent mature individuals) (from Wells, (197%; see section III.A.l.) speculated that eqgs or 1970). ephippia pirvduction was probably related to preda- tion pressures, Gliwicz (loc. cit.) gave an alternative interpretation to Zaret’s work concerning the fish selective removal of the more conspicious cyclo- ruiosrphic morph cif Ceriodaphnia cornuta. Not cnfyits larger compound eye, but also its four times greater clutch size could be responsible for the greater vulnerability of the unhorned morph to vis- ual planktivorous fishes, against the horned morph. But, both food limitation and selective predation may induce a decreased mean number of eggs per female and a decreased fecundity of a cladoceran population (Gliwicz, loc. cit.). So, Gliwicz et al. (1981) stressed that the entering reproduction by smaller cladoceran females may be rather a long- term evolutionary strategy than a demographic re- sponse of a cladoceran population to an incre;ase in planktivorous fish predation pressure (Galbraith, 0.4 1:s 2.9 1967; Wells, 1970). An increase in plankti\iorous ’ Daphnia LENOTW (mm) fish predation induces better food conditions. It results in an increase in the fecundity of younger Fig. If. Size frequency distribution of Daphnia in net’plankton cladoceran instars which enter earlier in reproduc- of Sportley Lake during toxaphene treatment toxic to fish [Sep- tember, 1958), and five years after rainbowl trout (Solmo gaircf- tion. Comparing the of neri) introduction (September, 1964) (from Galbraith, 1967). cladocerans in Lake Mikolajskie inhabited by rich 147 populations of planktivorous fishes and in a fish nus qtladrideittata. In control pools (without fish) free pond, Dawidowicz & Pijanowska (1984) sug- insects and D. pulex became abundant. tn ex- gested that planktivorous fishes might be the main perimental ponds, Hurlbert & Mulla (1981) found factor responsible for the different patterns of that predation by mosquitofish produced a shift to- cladoceran abundance. They showed that the com- wards smaller species of rotifers (from Keratella petitive exclusion principle (Le., species with similar quadrata to K. cochlearis), as well as, a decrease in ecological requirements are not able to co-exist in the calanoidkyclopoid ratio (from L)ií7ptOFnl/Spal- a stable environment: Hardin, 1960), which lidus to Cyclops venzalis). As Brooks (1968) sug- seemed.realized in the pond, was not supported in gested that the erratic jumping motion of cyclo- the lake. The planktivorous fishes, by selectively poids is more conspicious to fish than is the removing the best competitors (i.e., the larger typicaily gliding motion of calanoids, an increasing zooplankters), reduce the interspecific competition calanoidkyclopoid ratio might be expected as a re- I within zooplankton and allow a few cladoceran sult of Gariibusia predation. To explain the diffcr- species to reach their highest densities simultane- ence between the observed change in cala- ously, thus disregarding this principle. noidkyclopoid ratio and the expected onc, In shallow plastic pools, Hurlbert et al. (1972) Hurlbert & Mulla (loc. cit.) assumed that the in- observed that, in less than three months, the creased survival of predaceous cyclopoid copepo- mosquitofish (Ganzbusia affinis) eliminated insects dites (as a consequence of Gambusia’sselective pre- (benthic chironomid midge larvae, surface nymphs dation on adult cycloyoids) resulted in a grealer of the family Baetidae, and surface larvae selective removal of calanoids over cyclopoids (see and pupae of the Diptera family Ephydridae) and Fig. 12). D. pulex populations. Moreover, the fish signiiï- Decline in abundance or removal of planktivorc cantly reduced populations of the rotifer Brachio-, populations induce generally a partial reversal of

Fig. 12. Some principal ways in which the ratio of calanoid to cyclopoid copepods is influenced by zooplanktivorous fish, predaceous zooplankters, and nutrients (from Hurlbert 6( Mulla, 1981). 148

the previous size distribution of zooplankton popu- lations. Experiments (HrbáEek et al., 1961; -HrbáEek, 1962; Galbraith, 1967; Wells, 1970; An- dersson et al., 1978; Stenson et al., 1978; Fott et al., 1979; Shapiro et al., 1982; Shapiro & Wright, 1984) in which fish were removed (by poisoning) from water bodies where zooplankton communities were initially dominated by smaller species, always produced a shift towards larger filter-feeding zooplankton (such as Ceriodaphnia spp.). Warshaw (1972) also observed an increase in the number of Grygierek et al., 1966; Grygierek, 1’9671,anNd allow large zooplankton species (Daphnia, , identification of water bodies stocked wirIr fis1 Epischiura) following the die-off of Alosa. from those unstocked (Gliwicz, 1967; fhlersson Because zooplankters have short generation 1968; Grygierek, 1979). According to Kajrtk el u( times, changes in their community structure and (19761, the increasing density and biomass if srnal dynamics, in response to changing fish predation zooplankters not ‘only result from a comprmator pressures, may be relatively quick. Grygierek (1962) effect, but also from the general improvement ii showed that in carp ponds these changes occurred food availability for all zooplankters, as shown b after a few weeks, whereas in Lake Warniak they the increasing size and fecundity of larg: disap took place during several months. Thus, Weglenska (1971) considered that the size and fecundity of resulting populations of crustaceans and rotifers can be used as sensitive indicators of trophic condi- tions in free waters. It may be noticed that most studies have been devoted to the direct effect of fish visual predation on zooplankton. However, Hillbrichr-Ilkowska Sr. Weglenska (1973) emphasized that not only direct fish selective predation was responsiblc for changes smaller prey species. Thus, Diaphdnosori~~ in zooplankton dynamics, but the indirect effect by hraci”iywnrnr, although not susceptible to pxdatioi means of habitat transformations also played. a sig- by old stacked fish, progressively disappeai ed fron nificant role. Following Brooks & Kaodson (1965), year to year. they proposed that the disappearance of large her- bivores (which have low produdion;’consumption 2. Indirect t?fjÌect on phytoplanlcton conm unities by fish ratios, such as, Diaplianosoma and Eiidiap- The results presented in section III show tha tornus species) from Lake Warniak was, as well, a particulate feeders are ‘active visibility-selectiv consequence of the habitat being occupied by predators’ on zooplankton and do not (sonsum small, fast growing and quickly reproducing herbi- vores (such as, Ceriodaplznia, Bosmina, Keratella and Polyarthra species). The latter, filter feeding mostly on small suspended particles and bacteria, and not selectively removed by fish, were favoured by the increasing density of detritus resulting from the fish feeding activity. The authors concluded that the overall effect of increasing fish stock on zooplankton resulted in (1) the increase in density, biomass, production, fecundity and size of small transparency improved. Gambusia feeding did nci filtering (i.e., cladoceran and rotifer spe- affect phytoplankters larger than 15 pm [such a cies), (2) the decrease in density and biomass of Pandorina, Pediastrum, Sceriedesmus, and Hm large filtering herbivores (i.e., mainly large cladoce- matococcus species), but altered the cy:ling o 149

phosphorus by enhancing particulate phosphorus tage from passing through guts. Lynch & concentrations by an order of magnitude. Follow- Shapiro (loc. cit.) stressed that phosphorus and ing the mechanistic interpretation of the zooplank- nitrogen enrichments have a rather distinct effect ton community dynamics of Pleasant Pond (Min- on phytoplankton. These enrichments may (1) shift nesota) on the basis of predation and competition algal species composition without increasing total considerations (Lynch, 1979), Lynch 8c Shapiro algal biomass, and (2) increase primary produclivi- (1981) analyzed, through a combination of en- ty without affecting phytoplankton abundance or closure experiments, the differentia1 role of grazing species composition (as previously observed by Eo- and nutrient enrichment on its phytoplankton com- SOS & Hetesa, 1973). munity. They observed that in bluegill enclosures: Although decreases in phytoplankton biomass (1) the large herbivores (O.pulex, D. clavipes, and following zooplanktivore introductions have been C reticulata), which dominated both control en- reported, they correspond to particular situations closures (without fish) and the pond, were removed (1) where uptake of nutrients by abundant macro- and replaced by smaller B. longirostris and rotifers, phytes limit the phytoplankton response to and (2) the total algal biomass (initially represented zooplankton removal by fish (Hall et al., 1970), or by Cryptornonas marsonìi, C. (2) where the bottom sediments of shallow water tetrapyrenoidosa, and Heterochromas globosa, by bodies are stirred up by the fish feeding activities, desmids Cosmarium spp., Closterium moniliferum, inhibiting phytoplankton through a and Penium sp., and by the Ceratiurn decrease in light penetration (Grygierek, 1962, hirundinella) increased over the control densities by 1979; Spodniewska & Hillbricht-Ilkowska, 1973; more than an order of magnitude, because of the Hillbricht-Ilkowska & Weglenska, 1973). enhancement of other algal species (Oocystis lacus- tris, Anabaena civernalis, Aphanizoinenon sp.), ß. Impact of filter feeders mostly undetectable in absence of fish. Shapiro (in litt.) believes that Lynch (loc. cit.) misidentified the 1. Direct effect on zooplankton con”nitìes Aphanizomenon species: it probably was not A. Contrasting with the relatively well documented fios-aquae which exists only as flakes. impact of particulate feeders on plankton commu- Thus, the selective removal of zooplankton by nities, little attention has been devoted to the im- visual predation of bluegill resulted, rather, in an pact of filter-feeding fishes. Almost nothing is alteration of the phytoplankton community, than known about the impact of tow-net filter feeders, in a simple enhancement of algal species. Siínul- whereas more information is available for pump fil- taneously, the significant drop in soluble reactive ter feeders. (i.e., available) phosphorus concentration occurring Pump filter feeders are ‘passive escape-selective in fish enclosures, suggests that phosphorus turno- predators’ on zooplankton plus ‘passive size- ver rates may increase, following its regeneration by selective grazers’ on phytoplankton (see section both fish and resulting dense populations of domi- III.B.2.), whereas particulate feeders are only ‘ac- nant small herbivores. Dense blooms of filamen- tive visibility selective predators’ on zooplankton tous blue-greens persisted in enclosures with in-’ (see section III.A.1.). Thus, it might be expected creasing fish predation pressures (Anabaena that filler feeders (which have highest feeding rates, circinalis), or developed at the highest fish preda- i.e., passive feeding selectivities for the most easily tion pressures (Anabaena sp.). These blooms were, captured zooplankters, and feeding rates on nevertheless, different from the ‘grass-blade’ phytoplankton increasing as (log) functions of par- blooms occurring usually in the pond (only when ticle size) have an effect on both phyto- and the bottom waters were well oxygenated), as they zooplankton community structures different from consisted of various Co-existing species of single the effect of particulate feeders (which usually lo- filament colonies. As an exception, the gelatinous cate and preferentially attack zooplankters on the blue-green Chroococcus dispersus (the .only species basis of their body visibility, and do not consume ungrazeable by large herbivores) decreased in the phytoplankton). absence of large herbivores which were removed by Pump filter-feeding gizzard shad reduce popula- bluegill, possibly by losing the nutritional advan- tions of Keratella sp., copepod nauplii, cyclopoid 150 copepodites, do not affect Chaoborus and Di- zoloplankters, such as calanoid copepods (for ex- uphanosoma, and enhance Diaptornus pallidus ample, Diuptomus sp.). Nevertheless, this general populations (Drenner et al., 1982a; and reanalysis trend may be altered by the fish filtering simultane- in Drenner et al., 1984a) (see Fig. 13). In pond ex- ously and selectively on the phytoplanktonic food periments, Drenner et al. (1984b) showed that the of the herbivorous zooplankton. impact of pump filter-feeding blue tilapia, T. aurea, on the zooplankton community is somewhat simi- 2. Direct effect on phytoplankton comniunities lar to that observed for gizzard shad. The fish sup- In enclosure experiments carried out in the eu- press the rotifer Keratella sp. (a weak swimmer), trophic pond Lake Warniak (Mazurian lakeland, and enhance copepodid and adult stages of the Northern Poland), Kajak et al. (1975) looked al the large copepod Diaptomus sp. (the most evasive polential use of omnivorous silver 1 carp, zooplankter in the pond). Thus, predation pressure Hypoththaknichthys .niolitrix, to overcome algae by pump filter-feeding fish tends to shift the blooms and, thus, to improve water quality. Using zooplankton communities towards the more evasive replicated shallow plastic enclosures (Il .5 ni decp)

66

40

ED

5

44 1 Diaptomur

2

I

June July Aug Sept June July Aug -Shad Fig. 13. Mean changes in densities of dominant zooplankton in replicate ponds containing gizzard sllacl (Dorosorna cepedio'nun!) and control ponds without fish. The bais represcnt the range ol observed densities (Drenner e,f nl., 1982a). 151

opened to the sediment, with no fish (control), any access to the bottom food sources. Third, the moderate and high fish densities (respectively, 450 indirect effect of silver carp on phytoplankton and 1350 kg per ha), the authors demonstrated through the consumption of filter-feeding that silver carp reduced by 4.5 times the average bi- zooplankton seems to be even more important than omass of phytoplankton, regardless to fish density its direct grazing effect. Actually, the grazing pres- (and 16 times the biomass of zooplankton at the sure of herbivorous zooplankters on nanno- highest fish density). Higher fish densities reduced phytoplankton decreases whereas fish grazing on blue-green algae and enhanced dinoflagellates and net-phytoplankton shifts the competitive balance in nannophytoplankton. Moreover, in the gut con- favour of smaller phytoplanktonic forms, as well tents of the fish kept permanently on natural food as, modifies the dynamic of physical and chemical in net cages, Microcystis aeruginosa was dominant factors. (together with some crustaceans and rotifers). Thus, filter-feeding silver carp favour nanno- Kajak et al. (loc. cit.), Kajak (1977), and then Ka- phytoplankton against netphytoplankton, as not jak et al. (1977), comparing the feeding of silver only its competitor (netphytoplankton) is removed, carp in eutrophic lakes of various plankton compo- but also its (filter-feeding zooplankton), sition and biomass, emphasized that the fish im- as confirmed by Kajak et al. (1975)’s results. Kajak pact may differ according to the environmental et al. (1977) suggested another mechanism which conditions. First, the elimination of the consumed may play a role in the enhancement of nanno- seston from the water column by the way of feces phytoplankton. Although data on silver carp feed- sedimentation may have contributed to the deple- ing selectivity on zooplankton are lacking, the tion of plankton and to the enrichment of benthos authors expected that predatory cyclopoids can (especially Oligochaeta). This falling down of sub- avoid the capture by the filtering fish. Thus, by in- stances to the bottom, certainly advantageous for creasing the predation pressure upon the filtering the purity of water, is more likely to occur in strati- zooplankton and leaving their predators, silver fied water bodies where long-term isolation of sub- carp would decrease the invertebrate grazing pres- stances from the circulation in the epilimnion may sure, and consequently enhance nannophytoplank- take place. But, it would probably not happen in ton. (frequently or permanently) well-mixed aquatic Nevertheless, Januszko (1974) found that, in systems, or in shallow habitats in presence of inten- ponds, generally netphytoplankton and particular- sive mixing of bottom sediment by benthophagous ly diatoms were stimuláted by silver carp, whereas fish. Second, silver carp is able to feed on bottom narinophytopiankton was inhibited. Since the fish sediments, allowing its successful survival during does not feed on nannophytoplankton, selecting periods of low plankton biomass and its sufficient only particles larger than 20 pm (Bordckij, 1973), abundance to meet and overcome developifig algae Kajak et al. (1975) stated that the observed decrease blooms. But silver carp cannot digest the ingested of nannophytopfankton abundance resulted well cells of filamentous blue-green algae (larger from the transformation of the environment by trichomes 300-500 pm in length and 6 pm in di- fish, but not from grazing. Such transformations ameter of Oscillatoria agardhii, and colonial forms have been shown in experiments where the propor- of Aphanizornenon flos-aquae), whereas Ceratiurn tion of nannophytoplankton increased but its abso- hirundinella and diatoms are well digested. Blue- lute biomass strongly decreased. green algae are consumed only when abundant, In pond experiments with two replicates, Dren- Even, in some cases, silver carp avoid blue-green al- ner et aí, (1984b) showed that blue tifapia sup- gae (Omarov & Lazareva, 1974; Vovk, 1974). When pressed significantly populations of the largest blue-green algae are dominant the fish stop feeding Uroglenopsis (500 pn) and Ceratiurn (Savina, 1965; after Vovk, loc. cit.), its growth rate (18Ox 150 pin) algal species. Oocystis (25 x 15 pm) slows down (Omarov & Lazareva, loc. cit.), and and Nauicula (60 x 30 pm), though of appropriate t’ spitting out of food may occur (Savina, loc. cit.). In dimensions to be consumed efficiently, were not addition, silver carp suffer high mortality rates dur- supressed probably because smaller algae have ing periods of mass ‘water-blooms’ of filamentous generally higher growth rates (Banse, 1976; Schlesin- blue-green algae when kept in net cages without ger et al., 1981; Smith & Kalff, 1982). The smallest

, 152

Rhodomonas (8 x 5 pm), Chrysochromulina tionships between the planktivores and their plank- (6 x 5 pm), Chlamydomonas (5 pm), and Cyclotella tonic foods, and (3) discuss respective potential (6 x 3 pm) species were enhanced in the presence of vulnerabilities of various plankter types to foraging fish, possibly due to inefficient filtration, nutrient activities of planktivores. regenersltion by fish, nutritional advantage from The information presented here is expected to be passing through herbivores gut, higher growth appropriate and helpful in documenting rates, or modification of herbivorous zooplankters fish/plankton interactions, discerning mechanisms community. of selective (or random) prey collection by plank- Drenner et al. (1984a), using similar field ap- tivorous fishes, and elucidating observed changes proaches, showed that omnivorous filter-feeding in plankton community structures. It is obvious gizzard shad only significantly suppressed Cerati- that laboratory experiments, coupled with com- um (170x48 x 30 pm). They did not significantly af- plementary field data analysis, are indispensable fect populations of Synedra (170 x 1 pn),Peridini- for meaningful tests of proposed mechanisms and um (20x24 pm), (16x3 pm), accurate predictions of community responses to Kirchneriella (8 x 1.5 pm), Cyclotella (6 x 3 pm), fish predation pressures. and Chlamydomonas (5 pm), but enhanced popu- Since, in addition to competition for food and lations of Ankistrodesmus (20 x 1 pn), Cryptomo- nutrient limitation, predation is generally recog- nas (16x6 pm), Cosmarizinz (lox 1 pm), Rhodorno- nized as an important dfiving force structuring nas (6x4 pm), and 2-4 pm algae and bacteria. communities in freshwater systems, the structure sf Thus, filter-feeding fish have a different effect on limnetic plankton communities can be predicted plankton community than visual particulate- from the knowledge of the types and the impor- feeding fish. However, the enhancement of nan- tance of the predators present (Zaret, 1980). The nophytoplankton by filter-feeding gizzard shad and level of predation pressure and the nature of the blue tilapia looks similar to that observed in pres- piaiiktivorous fishes may well predict the respective ence of visual feeding fish (Andersson et al., 1978; vulnerabilities of the different available planktonic Hurlbert & Mulla, 1981; Lynch & Shapiro, 1981), prey species. These predictions (see section V. OR probably as a response to pond nutrient levels (not models) cail be used to study meaningfully the monitored), fish digestive activities, and zooplank- potential impacts of the concerned planktivores on ton suppression. plankton conimunities. Filter-feeding fishes are ‘passive size-selective Experimental studies investigating the mechan- grazers’ but, their direct grazing impact on isms of ecosystem tiophic level alteration by plank- phytoplankton is a consequence of the relation be- tivorous fishes have been scarce. Hurlbert & Mulla tween fish feeding rates and algal growth rates. The 119819, summarizing the effects of fish introduction latter ukually decreases with increasing algal size. (or removal) prcsented in the literature, emphasized As filter-feeding shad and tilapia have the highest that many studies (including those of HrbdEek et feeding rates for the larger slow growing algae, they QI., L961; Brooks & Dodson, 1965; Straikraba, have the potential to suppress directly the larger 1967; Wells, 1970; Hutchinson, 1971; Hillbricht- phytoplankters such as Ceratium. Ilkowska & Weglenska, 1973; and Andersson et al., 1978) have been done only in a rather descriptive or quasi-experimental manner, usually lacking con- VII. Conclusions: Biomanipulation approaches for trols or replications. Hurlbert & Mulla (loc. cit.) lake management and needs for future research noticed that the few really experimental studies (among which are those of Gfygierek, 1962; In summary, the Holling’s approach is extended Grygierek et al., 1966; Hall et al., 1970; Hurlbert et in this review from particulate feeders to filter feed- al., 1972; Losos & Hetesa, 1973; Lynch, 1979; and ers so as, for each planktivore type and in various their own study on Gambusia affinis) have not environmental conditions, to (1) determine the rela- been designed to allow successful application of in- tive importance of the different factors responsible ferential statistics. for the planktivore selectivity, (2) outline qualita- It also appears that even knowledge coming from tive mechanisms of functional or adaptative rela- well desigfied experimental field studies in con- 153

trolled environments (such as tanks, experimental thivorous fish on both phytoplankton and physico- ponds, or ‘in situ’ plastic suspended enclosures) chemical water conditions of eutrophic Swedish may not be working properly for understanding the Lakes Trummen and Bysjön. The authors observed functioning of natural environments’if the feeding that in fish enclosures (stocked with bream, Abra- mechanics of the experienced fish are unknown. If mis brama, and roach, Rutilus rutilus, in Lake laboratory measurements concerning feeding be- Trummen, and only with crucian carp, Carassitrs haviours, selectivities and rates are lacking, it is dif- carassius, in Lake Bysjön) water turbidity in- ficult to separate direct from indirect effects of fish creased, blue-greens Microcystis spp. developed predation. Dynamic views considering the commu- blooms (whereas phytoplankton populations at the nity modifications as a combination of direct con- beginning o€ the experiment consisted of cryp- sequences of the fish predation plus indirect, often tomonads, small blue-greens, and diatoms), and dominant, consequences of resulting pH became more basic. As previously shown by interactions are prevalent concepts among the more Lamarra (1975), HrbiEek et al. (1978) and Nakashi- recent studies. The current tendency is to use three ma & Leggett (1980) fish may contribute to the nu- complementary interactive approaches: laboratory trient budget of lakes because of their digestive ac- experiments of fish feeding mechanics, field tests tivities, but the importance of this process remains of plankton community responses to fish preda- still debatable (see Shapiro & Carlson, 1982, and tion, and ecological models of trophic state modifi- Nakashima & Leggett, 1982). Hurlbert et al. (1972) cations of lakes based on fish/plankton interac- remarked that, although in nature, Garnbusia and tions. The laboratory feeding trials determine the other zooplanktivores are limited by the predation feeding behaviours, selectivities and rates of the of piscivores, in some cases the man-caused altera- fish, and serve to build the predation model. Then, tions in fish populations (rather than man-caused the model is used to generate predicted alterations increases in nutrient inputs) may result in the eu- of the which are statistically trophication symptom of excessive algal growth. compared with alterations observed during field ex- Their idea coincides with Shapiro et al.’s (1975) sug- periments (Wright & O’Brien, 1984; Drenner et al., gestion to use the artificial increase of 1984a). The discrepancy between the observed and populations as a potential biological control of the predicted alterations permits one to discern the phytoplankton levels (unless undesirable enhance- actual mechanisms involved and to produce new ments of filamentous algae and higher plants have ideas to be tested. These are basic goals in ecology. occurred), and emphasized that fish ought to play Lynch & Shapiro (1981) addressed the plank- a more important role in the restoration ap- tivorous fish from the community standpoint. They proaches of eutrophicated water bodies. emphasized that the reponse of a lake to enrich- &I a more recent study conducted in man-made ment not only depends on its initial nutrient capac- ponds with adequate controls and replications, ity, but also on the structure and density of its Hurlbert & Mulla (1981) examined in detail the pianktivorous fish community. They suggested that community effects of Gambusia predation, and in lakes with planktivorous fishes, the phytoplank- particularly its most conspicious effect of increas- ton community may respond more dramatically to ing phytoplankton biomass. Andersson et al. (1978) enrichment than in lakes free of planktivores where and Hurlbert & Mulla (1981) increased the credibili- algae are maintained in critical nutrient availability ty of Shapiro et al.‘s (loc. cit.) suggestion of plank- situations. From the limnological viewpoint this tivorous fish biomanipulation as a potential meth- has considerable consequence, and implies that not od for reducing phytoplankton densities. . only trophic conditions of lakes are somewhat Numerous studies demonstrated that a reduction ‘t- related to the presence of planktivorous fishes in fish populations resulted in an evolution of the (HrbáEek, 1969), but besides, that the ‘ecological towards oligotrophic conditions buffer capacity’ of lakes (term defined by Jerrgen- (HrbáEek et al., 1961; Novotna & Korinek, 1966; t‘ sen & Mejer, 1977) may be lowered at higher plank- Losos & Hetesa, 1973; Andersson et al., 1978; Sten- tivore predation pressures. son et al., 1978; Weglenska et al., 1979; Cronberg, Using enclosures, Andersson et al. (1978) studied 1980; Leah et al., 1980; Stenson, 1982, 1983; the indirect effect of planktivorous and ben- Reinertsen & Langeland, 1982; Langeland & Reinertsen, 1982; Olrik et af., 1984; Reinertsen & disk transparency (2.1 m and 4.8-6.0 my before Olsen, 1984). Andersson et a/. (1978) tested, on a and after, respectively), (2) a marked decrease in large scale, the biomanipulation approach of con- chlorophyll a concentrations (up to 12 pg i-'? and trolling trophic states. Extensive experimental less than 5 pg I-I, before and after, respectively) removals of planktivores, and simultaneous associated with a change in algae composition releases of piscivorous fishes were realized in Lake (from by various Chlorophycae species Trummen. Although the zooplankton was not sig- to dominance of Cryptomonas erosa) and a de- nificantly affected either in composition or in crease in algae densities, (3) a change in her- abundance, the total phytoplankton biomass, total bivorous crustacean community (from small- P and total Nydecreased moderately. However, An- bodied Bosmina iongìrostris, Ceriodaphniu dersson et al. (loc. cit.) concluded that, not only do reticulata, and Daphnia ambigua to latge-bodied fish directly affect the biomass of their prey, but D. parvula, D. galeata mendotae, and dominant B. they also have an indirect influence on trophic level pulex) asso iated with a decrease in abundance and .I interrelationships, minleralization processes, and a considera le increase in mean size of herbivorous nutrient availability. zooplankte s, and (4) a decrease in epilimnetic con- A rather extensive literature is devoted at present centrations of total P (and, to a lesser extent, tola1 'I to the feasibility of biomanipulation approaches to N). Additi na1 bioassay experiments showed that restore lakes and reservoirs (e.g. Shapiro, 1978, the grazing pressure imposed by the resulting her- 1979; and Leventer, 1981). Thanks to the increasing bivorous Daphnia populations (mainly D. pulex knowledge of the role of community interactions in and D. galeatuI mendotae) was able to keep low eutrophication processes, besides classical restora- chlorophyll concentrations and algal abundances, tion procedures involving almost exclusively en- even at high inorganic N and P concentrations. gineering techniques, we now have an alternative This suggested that the oligotrophication sym- approach (in order to avoid high economic as- ptom resulted only from the changes in herbivore sociated costs and/or common irrelevance of more populations. Shapiro & Wright (loc. cit.) calculated conventional approaches) consisting of more subtle that the biomanipulation increased two to three ecological shiftings of trophic state balances. times the grazing pressure responsible for the To check the importance of biotic feedback inter- reduced chlorophyll and nutrient concentrations. actions in the trophic properties of lake, Henrikson i accompanying a shift in her- et al. (1980) removed fish population (by means of ktsn from small-bodied Bosmi- rotenone) from a Swedish lake. Roach (Rutififsmti- to large-bodied Daphnia commu- lus) elimination resulted in oligotrophication sym- served by Stenson et al. (1978) and ptoms, such as: (1) a shift of predominant small cladocerans (Bosmina longirostris) towards larger (1984) supported that, by copepods (Eudiaptomits gracilis), (2) an incrase of aphrtia actively transport net-phytoplankton biomass where dominant nutrients downward out of the epilimnion. The Peridiniirm acicirliferum (30 ,um) were replaced by authors suggested that biomanipulation could alter Ceratiuni hirundinella (300 pm), (3) a decrease in the importance of the nutrient depletion in the nannoplankton abundance followed by an increase epilimnion by changing the migratory patterns of in transparency, (4) a dramatic 90% lowering of the zooplankton community. However, the absence limnetic , and (5) a decline in of replicates in the experimentations of Henrikson pH, total P and total N. Itl order to reduce the abundance of algae in Round Lake (a small urban lake in Minnesota), Shapiro & Wright (1984) tested the applicability of the biomanipulation approach, using rotenone to eliminate planktivorous and benthivorous fish. Over a two-year period following this manipulation they observed a shift towards less eutrophic condi- tions, such as: (1) a significant increase in secchi 155 knwon to be strong enough to kill most zooplank- the community point of view. Planktivorous fish ters in a few hours (most species of rotifers: Keratel- communities usually comprise both particulate la, Trickocerca, Asplanchna, Synchaeta, Polyar- feeders and filter feeders, but it always remains un- thra, Filinia; copepods: Diaptoïnus, Euryternora, known how the differential effects of these plankti- Cyclops; and highly vulnerable cladocerans: Di- vores combine between them to structure plankton aphanosoma, Daphnia, Ceriodaphnia, Bostnina), communities. and also some phytoplankters (such as Ceratium Filter-feeding fishes have the potential advantage hirundinella) (Almquist, 1959). Although less sen- over visual planktivores, to consunle selectively net- sitive than fishes, benthic are vulnera- phytoplankton, to create situations . in which ble to rotenone concentrations above 0.5 ppm nanno-phytoplankton is favoured, and thus to in- (Lindgren, 1960): for example, all instars of duce better water quality levels. But, environmental Chironomus sp. were exterminated by a long term conditions affecting processes and effect of rotenone treatment (Koksvik & Aagaard, nutrients regeneration, such as water temperature, 1984). As Round Lake was newly stocked with mixing pattern, residence time, surface level fluctu- planktivorous, piscivorous, and benthivorous fish, ation, and initial trophic state, must play a decisive the effects of biomanipulation only persisted for role in obscuring the beneficial impact of filter- two years, whereas they lasted for at least four years feeding planktivores. Tests of the potential ability in a lake kept free of fish (Henrikson et al,, loc. of filter-feeding planktivores to control algae cit.). The limited duration effects of a single bi- blooming are still dramatically lacking over a wide omanipulation treatment support that (1) bi- range of environmental conditions. For example, it omanipulation must be combined with more tradi- might be expected that in tropical aquatic environ- tional approaches, and (2) long-term beneficial ments, due to higher water temperatures, the pres- effects could be maintained only through succes- sure of filter-feeding pldnktivores on the whole eco- sive implementations of adjusted biomanipulation system could be even higher at much lower fish treatments, in order to sustain the best desirable densities, than in temperate zones where filter feed- trophic improvements. ing is generally less important (even occasionally However, biomanipulations is not yet a science, lacking) than particulate feeding, and where large as not all interactions may be always under control: herbivorous zooplankters account for most of the but it is still experimental. Two examples may be grazing pressure on algae. Much attention ought to used to show the hardness to control some indirect be paid to filter-feeding planktivorous fishes (and effects of predation by visual planktivores on filler- particularly in the tropics; for example, see Nifssen, feeding crustacean zooplankton and phytoylank- 1984) for their potential for biological control of ton communities: (1) resulting dominant popula- net-phytoplankton, Special interest might be dedi- tions of large Daphnia may be unable to regulate cated to the control of undesirable filamentous, the growth rate of such an alga as Aphani*4oineiion usually toxic, algae, through direct fish grazing or spp. (not readily grazeable by large herbivorous indirect enhancement of grazing by large efficient zooplankters) which may efficiently use the herbivorous zooplankters (such as, Daphnia pulex; nutrients available of lakes (Shapiro, 1978), and (2) see Lynch, 1980; Holm et a!., 1983; Carlson & visual planktivorous fishes may indirectly influence Schoenberg, 1983). Looking at natural and han- the zooplankton grazing pressure and thus the algal modified balances between dominant visual plank- growth, if they selectively remove carnivorous tivore communities (i.e., particulate feeders), and zooplankters, such as chaoborids (Stenson, 1972, dominant filter-feeding planktivore communities, 1978, 1980; Northcote et al., 1978) and cladocerans in lakes and reservoirs of various trophic states, Leptodora and Bythotrephes species (De Bernardi latitudes (effect of temperature), mixing patterns, & Giussani, 1975), which are efficient predators on residence times, and surface level fluctuations, may Daphnia. give interesting insights for understanding and con- As the selective (often differential) impacts of trolling eutrophication. various species of planktivorous fishes are now well Information on fish feeding ecology based only documented, a main motivation in limnology on stomach content analyses readily discerns the ought to consider the planktivore influence from trophic levels of the fish food, but it is insufficient 156 to quantify its utilization. The mechanisms govern- changes in the water environment induced by nutri- ing fish feeding selectivity and resource use are not ent enrichments generate changes in the fish com- always well understood. More studies are needed to munity, which in turn generate additional changes identify dominant mechanisms and to predict long- in the water environment. Applying this concept, term changes in plankton communities exposed to Opuszynski (loc. cit., 1980) showed that the in- fish predation. Combined laboratory experiments, troduction of single species of fish to counteract field tests and simulation models will give profita- eutrophication appears erroneous. He suggested ble insights. To reach the goal of considering plank- that management approaches tised against tivore influence as multi-level effects coupled with eutrophication processes should try to maintain the interactive community responses, it appears impor- original ichthyofauna structure (in order to increase tant ta document some strategic mechanisms, such the precision of the self regulating capability of the as (1) the indirect response of phytoplankton to the system), instead of introducing species improvirilg selective depletion of zooplankton by particulate the fishery production. Such a concept remains to feeders, (2) the differential utilization of be tested. phytoplankton, detritus, and suspended organic Aquatic ecosystems functioning could be better particles by pump and tow-net filter feeders, (3) the understood if considered from the point of view of selective removal of zooplankton by pump and tow- optimized community interactions versus environ- net filter feeders, (4) the contribution of plank- mental condition changes (temperatute, mixing tivorous fish feeding activity in the nutrient load- pattern, residence time, surface level fluctuation, ings and dynamics of lake ecosystems, and (5) the and trophic state). Nevertheless, predation 19y digestion efficiencies of filter-feeders for algae (es- planktivorous fishes is not always the main deter- pecially large undesirable species). Obviously, pre- minant responsible for the changes in plankton dation pressures by other trophic levels (piscivores, communities (for example, see Gliwicz & Prejs, non-piscine vertebrate planktivores, invertebrate 1977). As concluded by Zaret (1980), it is essential planktivores), as well as, mineralization processes, to idcnlify what circumstances make predation, external nutriefit loadings, and competition for t-attrsr tlml competition or nutrient limitation, to food sources, must not be neglected. More infor- becorne the dominant structuring force. mation on the driving forces governing the struc- ture and dynamic of freshwater coininunities is ur- gently needed to understand better the functioning of limnological ecosystems, and to make good deci- sions in the field of lake and reservoir mannge- I wish to rhanli first Thomas Zaret and Ray ment. Drenner who provided me thc opportunity to work Exotic fish introduction are clear examples of with them over several months. They encouraged this critical necessity (see Gophen et al., 1983a, me to learii extehsively about planktivory and to 1983bl. General information on the role played by begin the first drafts of this review paper. I appreci- fish populations in the eutrophication process are ate their enthusiasm, their friendly support, and lacking. More studies should be devoted particular- the benericial discussions we had on planktivore ly to the interactions between trophic state modifi- ecology, evolution, and feeding mechanics. Special cations and changes in the fish community. Stress- thanks go to Ray Drenner for invaluable contribu- ‘ing that relatively few works document the effects tion to the improvement of the manuscript. My of the fish fauna on the eutrophication processes thanks go also to Henry Dumont, Douglas Eggers, compared to the numerous ones illustrating the ef- Maciej Gliwicz, David Hambricht, Anna fects of eutrophication on the fish community and Hillbrichl-Ilkowslta, Jaroslav HrbBZck, John Jans- production, Opuszyliski (1979b) studied the inter- sen, Zdzislaw Kajak, Laurent Lauzanne, Christian actions between fish stock compositions and eu- Lévêque, Paul Nival, Karol Opuszyliski, Serge POU- trophication processes, using increasing densities let, Roger Pourriot, Aiidrzej Prejs, Lucien Saint- of common carp and silver carp, alone or com- Jean, Joseph Shapiro, Paul Testard, Earl Werner, bined, in experimental ponds. He developed the and David Wright for reviewing the manuscript and ‘ichthyoeutrophication concept’ which assumes that $or their helpful comments and criticisms. 157

I would like to dedicate 'in memoriam' this re- Bensam, P., 1964. Differences in the food and feeding adapta- view to Thomas Zaret whom I feel privileged to tions between juveniles and adults of the Indian oil sardine, Sardinella longiceps Valenciennes. Indian J. Fish. II: know not only as a scientist, but also as a friend. 377-390. He gave me the original inspiration for this work. Berg, À. & E. Grimaldi, 1966. Ecological relationship$ between planktophagic fish species in the Lago Maggiore. Verh. int. Ver. Limnol. 16: 1065-1073. Berry, F. H. & I. Barret, 1963. Gill raker analysis and speciation References in the thread herring genus Opisthonerna. Bull. inter. Amer. Trop. lha Comm. 7: 113-186. Ahlgren, I., 1978. Response of Lake Norrviken to reduced nutri- Bertmar, G. & C. Stromberg, 1969. The feeding mechanisms in ent loading. Verh. int. Ver. Limnol. 20 846-850. plankton eaters. I. The epibranchial organ in whitefish. Mar. Allan, J. D., 1974. Balancing predation and competition in Bid. 3: 107-109. cladocerans. Ecology 55: 622-629. Beukema, J. J., 1968. Predation by the three-spined stickleback

1 Allan, J. D., 1976. Life history patterns in zooplankton. Am. (Casterosteils acitleatus L.): the influence of hunger and cx- nat. 110 165-180. perience. Behaviour 31: 1-126. Alexander, R, McN., 1967a. The functions and mechanisms of Bhimachar, B. S., E À. Sc. & P. C. George, 1960. Observatiohs the protrusible upper jaws of some acanthopterygian fish. J. on the food and feeding of the Indian mackeral, Rastrelliger b Zool., Lond. 151: 43-64. kanagurtn (Cuvier). Indian 3, Fish. 7: 275 - 306. Alexander, R. McN., 1967b. Functional design in fishes. Hutch- Bigelow, H. B. & W. F. Schroeder, 1953. Fishes of the Gulf of inson University Library, 160 pp. Maina Fish. Buk U.S.A. 53: 1-577. Almquist, Z., 1959. Observations of the effect of rotenone emul- Blaber, S. J. M., 1979. The of filter-feeding teleosts in sives on fish food organisms. Inst. Freshw. Res. Drottnin- Lake St. Lucia, Zululand. J. Fish. Biol. 15: 37-59. gholm 40 146-160. Blaxter, J. H. S., 1966. The behavior and physiology of herring Anderson, R. S., 1968. A preliminary report on zooplankton and other clupeids. In: F. S. Russel (ed.), Advahces in Marine distribution and predatory-prey relationships in Alpine lakes. Biology. Academic Press, New York 1: 261-393. Can. Service, Limnol. Sect. Rep., 31 pp. Bond, C. E., 1979, Biology of fishes. Saunders College Publish- Andersson, G., H. Berggren, G. Cronberg & C. Geh, 1978. Ef- ing, Philadelphia, 514 pp. fects of planktivorous and benthivorous fish on organisms Boruckij, E. V., 1973. Feeding of Hypophthalrnichlhys molitrìx and water chemistry in eutrophic lakes. Hydrobiologia 59(1): (Val,) and Aristichtliys nobilis [Val,) in natdral waters of Sovi- 9-15. et Union, [Pitanie belogo (Hypophtkalmichthys nioliti.ix Andrusak, H. & T. G. Northcote, 1971. Segregation between (Vai.)) i pestrogo (Arisfichtliysridbilis (Val,)) tolstoiobikov V adult cutthroat trout (Salmo clarki? and dolly varden (Salveli- estestvennych vodoemach i prudaclr SSSR] In: G. V. Nikd- nus malma) in small coastal British Columbia lakes. J. Fish. skij & P. L. Piroznikov (eds), nofologia vodnych zivotnych. Res. Bd Can. 28: 1259-1268. Itogi i zadaci. Iedattelstvo 'Nauka', Moskva: 299- 322. Arthur, D. K., 1976. Food and feeding of larvae of three fishes Bowen, S. H., 1976. Mechanism for digestion of detrital bacte- occurring in the California Current, Sardinopi sagax, En- ria by the cichild fish Sarotkerodon tnossambictis (Peters). graulis niordax and Tractturus symmetricus. Fish. Buk Nature, Lond. 260: 137 - 138. U.S.A. 74: 517-530. Bowen, S. H., 1982. Feeding, digestion and growth - qualita- Bainbridge, V., 1957. Food of Ethmalosa dorsalis (Cuvier and tive considerations. In: R, S. V. Pullin & R. H. Lowe- Valenciennes). Nature, Lond. 179: (4568): 874- 875. McConnell (eds), The Biology and Culture of Tilapias. Bainbridge, V., 1963. The food, feeding habitats and distribu- ICLARM Conferehce Proceedings 7, 432 pp. International tion of the bonga, Ethrnalosa dorsalis (Cuvier and Valen- Center for Living Aquatic Resources Management, Manila, ciennes). J. Cons. perm. int. Explor. Mer 28: 270-284. Phillippines: 141- 156. Bakule, L. & M.StraSkraba, 1982. On multiple objective optimi- Boyd, C. M., 1976. Selection of particle sizes by filter-feeding zation in aquatic ecosystems. Ecol. Modelling 17: 75-82. copepods: a plea for reason. Limnol. Oceanogr. 21: 175-180. Banse, K., 1976. Rates of growth, respiration and photosynthesis Breder, C. M., 1959. Studies on social groupings in fishes. Bull. of unicellular algae as related to cell size - a review. J. am. Mus. qat. Hist. 117: 393-482. Phytol. 12: 135-140. Brock, V. E. & R. H. Riffenburgh, 1960. Fish schooling: a possi- Barger, L. E. & R. V. Kilambi, 1980. Feeding ecology of larval ble factor in reducing predation. J. Cons. perm. int. Explor. shad, Dorosoma, in Beavor reservoir, Arkansas. In Proceed- Mer 25: 307-317. ings of the Fourth Annual Larval Fish Conference. United Brooks, J. L., 1968. The effects of prey size selection by lake States Fish and Wildlife Service, FWS/OBS-80/43, Ann. planktivores. Syst. Zoo]. 17: 272-291. Arbor, Michigan, USA: 136- 145. Brooks, J. L. & S. I. Dodson, 1965. Predatiori, body size and the Bayliff, W. H., 1963. The food and feeding habits of the an- composition of plankton. Sciences 150: 26- 35. choveta Ceterigraulis mysticetus, in the Gulf of Panama. Carliste, J. G., 1971. Food of the jack mackeral, 7iachurusspn- Bull. inter. Amer. Trop. TUna Comm. 7: 399-459. metricus. Calif. Fish and Game 57: 205-208. Begg, G. W., 1976. The relationships between the diurnal move- Carlson, R. E. & S. E. Schoenberg, 1983. %ontroll~ngblue-green ments of some of the zooplankton and the sardine tiin- algae by zooplankton grazing. In: Lake restoration, protec- nothrissa miodon in Lake Kariba, Rhodesia. Limnol. tion, and management. Il Annual Conference of the Nortb Oceanogr. 21: 521-539. American Lake Management Society, Vancouver, British 158

Columbia, October 26-29, 1982, EPA 440/5-83-001: pressure by planktophagous fish. Verh. int. Ver. Limnol. 19: 228-233. 2906-2912. Caulton, M. S., 1976. The importance of pre-digestive food Didday, R. L., 1976. A model of visuomotor mechanisms in the preparation to Tilapia rendalli Boulanger when feeding on frog optic tectum. Math. Biosci. 30: 169-180. aquatic macrophytes. Trans. Rhod. Sci. Assoc. 57: 22-28. Drenner, R. W., 1977. The feeding mechanics of the gizzard Charnov, E. L., 1973. Optimal foraging: some theoretical explo- shad (Dorosoma cepedianum). Ph.D. Thesis, Univ. Kansas, rations. Ph.D. Thesis, Univ. Washington, Seattle, 95 pp. Lawrence, 91 pp. Charnov, E. L., 1976. Optimal foraging: The marginal value Drenner, R. W. & S. R. McComas, 1980. The role of aooplank- theorem. Theoretical Population Biology 9: 129- 136. ter escape ability in the selective feeding and impact of plank- Charnov, E. L. & G. H. Orians, 1979. Optimal foraging: some tivorous fish. In: W. C. Kerfoot (ed.), Evolution and Ecology theoretical explorations. Center for Quantitative Sciences, of Zooplankton Communities. The Univ. Press of New En- Univ. of Washington, Seattle 98195, USA, 160 pp. gland, Hanover, New Hampshire, USA 587-593. Chesson, J., 1978. Measuring preference in selective predation. Drenner, R. W., F. de Noyelles Jr. & D. Kettle, 1982a. Selective Ecology 59: 211-215. impact of filter-feeding gizzard shad on zooplankton cornrriu- Chipman, W. C., 1959. The use of radioisotopes in studies of niry structure. Limnol. Oceanogr. 27: 965 -968. the foods and feeding activities of marine animals. Publ. Drenner, R. W., W. J. O’Brien & J. R. Mummert, 1982b. Filter- Staz. Zool. Napoli (Suppl.) 31: 154-174. feeding rates of gizzard shad. Trans. am. Fish. Soc. 111: Clemens, W. A. & N. K. Bigelow, 1922. The food of ciscoes 210-215. (Leucichthys) in Lake Erie. Publ. Ontario Fish. Res. Lab. 3: Drenner, R. W., J. R. Strickler & W. J. O’Brien, 1978. Capture 39-53 (Univ. Toronto Stud. Biol. Ser. no 20). probability. The role of zooplankter escape in the selective Colby, P. J., G. R. Spangler, D. A. Hurley &A. M. McCombie, feeding of planktivorous fish. J. Fish. Res. Bd Can. 34: 1972. Effects of eutrophication on salmonid communities in 1310-1373. oligotrophic lakes. J. Fish. Res. Bd Can. 29: 975-983. Drenner, R. W., J. R. Mummert, F. de Noyelles Jr. & D. Kettle, Colin, P. L., 1976. Filter feeding and predation on the eggs of 1984a. Selective particle ingestion by a filter-feeding fish and Thallasoma sp. by the scombrid fish RustreNiger kunaguria. its impact on phytoplankton community structure. Limnol. Copeia: 596-597. Oceanogr. 29(5): 941-948. Confer, J. L. & P. I. Blades, 1975. Omnivorous zooplankton and Drenner, R. W., S. B. Thylor, X. Lazzaro ¿k D. Kettle, 1984b. Par- planktivorous fish. Limnol. Oceanogr. 20 571 -579. ticle grazing and plankton community impact of an om- Confer, J. L., G. Applegate & C. A. Evanik, 1980. Selective pre- nivotous . %:ans. am. Fish. Soc. 113: 397-402. dation by zooplankton and the response of cladoceran eyes to Drenner, K. W., G. L. Vinyard, M. Gophen & S. R. McComas, light. In: W. C. Kerfoot (ed.), Evolution and Ecology of t982c. Feeding behavior of the cichlid, Sarofherodongalilae- Zooplankton Communities. The Univ. Press of New England, um: Selective predation 011 Lake Kinneret looplankton. Hanover, New Hampshire, USA: 604-608. Hydrobiolngia 81: 17-20. Confer, J. L., G. L. Howick, M. H. Corzette, S. L. Kramer, S. Dunbïack, R. I.. & L. M. Dill, 1984. Three-dimensional prey Fitzgibbon & R. Landesberg, 1978. Visual predation by reaction fi& of the iuvenile coho salmon (Oncorhynciius planktivores. Oikos 31: 27-37. kisutch). Cad. J. Fish. .squat. Sci. 41: 1176-1182. Contag, E., 1931. Der Einfluss verschiedener Besatzstarke auf Dunbin, A. O., 1979. Food selection by plankton feeding fishes. die naturliche Ernahrung zweisommriger Karpfen und auf die In: R. H. Stroud & M. Clepper (eds), Predator-Prey Systems Zusammensetzung der Tierwelt ablassbarer Teiche. Z. in Fisheries Ii4anagement. International Symposium on Fischerei 29: 569-597. Predator-Prvy Systems i11 Fish Communities and their Role in Cronberg, G., 1980. Phytoplankton changes in Lake Trummen . Atlanta, Georgia, July 24-27, 1978. induced by restoratiorí. Long-term whole-lake studies and ex- Sport Institute, Washington D.C., 4: 203 -218. perimental biomanipulation. Ph.D. Thesis, Univ. of Lund. Durbin, A. G. & E. G. Durbin, 1975. Grazing rates of the Atlan- Crowder, L. B., 1985. Optimal foraging and feeding mode shifts tic menhaden as a function of particle size and concentration. in fishes, Envir. Biol. Fishes 12(1): 57-62. Mar. Biol. 33: 265-277. Crowder, L. B. &F. P. Binkowski, 1983. Foraging behaviors and Edmondson, W. T., 1977. Trophic equilibrium of Lake Washing- the interactions of alewife, Alosapseudoharengus, and bloat- ton. US. Environmental Protection Agency er, Coregonus hoyi. Envir. Biol. Fishes 8(2): 105-113. EPA-600/3-77.087. D’Ancona, V. & L. Volterra D’Ancona, 1937. Experienze in Edmondson, W. T. & G. G. Winberg (eds.), 1971. A manual on natura sul plancton del Lago di Nemi. Int. Revue ges. methods for the assessment of secondary in fresh Hydrobiol. 35: 467-482. waters. IBP Handbook no. 17, Blackwell, Oxford, 368 pp. Davis, W. P. & R. S. Birdsong, 1973. fishes which for- Eggers, D. M., 1976. Theoretical effect of schoofing by plank- age in the water column. Helgolander wiss. Meeresunters. 24: tivorous fish predators 011 rate of prey consumption. J. Fish. 292- 306. Res. Bd Can. 33: 1964-1971. Dawidowicz, P. & M. Gliwicz, 1983. Food of brook charr in ex- Eggers, D. M., 1977. The nature of prey selection by plank- treme oligotrophic conditions of an alpine lake. Envir. Biol. tivorous fish. Ecology 58: 46-59. Fishes 8(1): 55-60. Eggers, D. M., 1978. Limnetic feeding behavior of juvenile sock- Dawidowicz, P. & J. Pijanowska, 1984. Population dynamics in eye salmon in Lake Washington and predator avoidance. Lim- cladoceran zooplankton in the presence and absence of fish- nol. Oceanogr. 23: 1114-1125. es. J. Plankton Res. 6(6): 953-959. Eggers, D. M., 1982. Planktivore preference by prey size. Ecolo- De Bernard¡, R. 8( G. Giussani, 1975. Population dynamics of gy 63(2): 381-390. three cladocerans of Lago Maggiore related to the predation Elliot, G. V., 1976. Diel activity and feeding of schooled lar- gemouth bass fry. Trans. am. Fish. Soc. 105(5): 624-627. Gliwicz, 2. M, &A. Prejs, 1977. Can planktivorous fish keep in Engel, S. S., 1976. Food habits and prey selection of Coho salm- check planktonic crustacean populatiotts? A test of size- on (Oncorhynchus kisutch) and cisco (Coregonus artedit] in efficiency hypothesis in typical polish lakes. Ekol. pol. 25(4): Palette Lake, Wisconsin. Trans. am. Fish. Soc. 105: 607-614. 567-591. Fagade, S. O. & C. I. O. Olanyan, 1972. The biology of West Gliwicz, Z. M.& hd. G. kowan, 1984. Survival of Cpclops abys- African shad, Ethtnalosa fimbriata (Bowdich) in the Lagos sorutn tatricus (Copepodai Crustacea) ln alpine lakes stocked Lagoon, Nigeria. J. Fish. Biol. 4(4): 519-533. with planktivorous fish. Limnol. Oceanogr. 29(6): Feller, R. J. &Va M. Kaczynski, 1975. Size selective predation by 1290- 1299. juvenile Chum Salmon (Oncorhynchus keta) on epibenthic Gliwicz, Z. M. &E. Siedlar, 1980. Food size limitation and algae prey in Puget . J. Fish. Res. Bd Can. 32 1419-1429. interfering with food collection in Raplztiia. Arch. Hydrobiol. Flemminger, A. & R. 1. Clutter, 1965. Avoidance of towed nets 88(2): 155-177. by zooplankton. Limnol. Oceanogr. 10: 96-104. Gliwicz, Z. M., À. Ghilarov & J. Pijanowska, 1981. Food and Fott, J., L. Pechar & M. Prazakova, 1979. Fish as a factor con- predation as major factors limiting two natural populations of Ruphnia ClJCUllUh? Sarg. Hydrobiologia 80: 205 -218. # trolling water quality in ponds. In: J. Barica & L. R. Mur (ed’s), SIL Workshop on Hypertrophic Ecosystems, Vaxjo, Godsil, H. C.b 1954. A descriptive study of certain tona-like Sweden, Sept. 10-14, 1979. fishes. Calif. Dept. Fish. and Bull. 97: 185 pp. Fox, H. M., 1948. The hemoglobin of Ruphnia. Proc. R. Soc. Gophen, M., 1980. Food sources, feeding behavior and growth Ser. 135: 195-212. rates of ij‘arotherodon galilaeutn (Linnaeus) fingerlings. Fraser, D. F. & R. D. Cerri, 1982. Experimental evaluation of 20: 101-115. predator-prey relationships in a patchy environment: conse- Gophen, M., R. W. Drenner & G. G. Vinyard, 1983a. Fish h- quences for habitat use patterns in . Ecology 63(2): troduction into Lake Kinneret - Call for concern. Fish 307-313. Management 14(1): 43-45. Fryer, G. & T. D. Iles, 1972. The cichlid fishes of the great lakes Gophen, M., R. W, Drenner & G. G. Vinyard, 1983b. Cichlid of Africa. T.F.H. Publications, Neptune , New Jersey, stocking and the decline of $the Galilee Saint Peter’s fish USA. (Sarotherudun guil/aeus) in Lake Kinneret, Israel. Can. J, . Furnass, T, I., 1979. Laboratory experiments on prey selection Fish. aguat. Sci. 40(7): 983-986. by perch fry (Perca fluviutilis). Freshwat. Biol. 9: 33-43. Gosline, W. A., 1971. FQnctiondl morphology and classification Galand, G. & B. Liege, 1975. Reponses visuelles unitaires chez of teleostean fishes. Honolulu, Univ. Press of Hawaii. la truite. In: M.A. Ali (ed.), Vision in fishes. Plenum Publish- Gosse, J. P., 1955. Dispositions sp es de l’appareil branchial ing Corporation, New York an¿ London: 127-135. des Tilapia et Citharinu Soc. Royale Zool. de Belgique, An- Galbraith, M. G. Jr., 1967. Site-selective predation on Daphnia nales 86: 303-308. by rainbow trout and yellow perch. Trans. am. Fish. Soc. 96: Gras, R. & L. Saint-Jean, 1 s about fvlev’s eíectivi- 1-10, ty index. Revue Hydrobiol. trop. 15(1): 33-37. Gannon, J. E., 1976. The effects of differential digestion rates of Gras, R., L. Lauzanne& L, Saint-Jean, !98L Rhgime alimentaire zooplankton by alewife, Alosa pseudoharetzgus, on determi- et sélection des proies chez les BracliJqwodohtis bdtensoda nation of selective feeding. Trans. am. Fish. Soc. 105: 89-95. (Pisces, Mochochidae) du Lac Tchad en pkriode de Gardner, M. B., 1981. Mechanism of size selectivity by plank- eaux. Rev. Hydrobiol. trop. 14(3): 223-231. tivorous fish: A test of hypotheses. Ecology 62: 571-578, Green, f., 1967. The distribution and varkiltion of Daphrr Gerritsen, J. & K. G. Porter, 1982. The role of surface chemistry holtzii (Crustacea: ) in relation to fish predation in in filter feeding by zooplankton. Science 213: 1225-1227. Lake Albert, East‘Africa, J, Zooi., Lund. 151: 181-1976 Gerritsen, f & J. R. Strickler, 1977, Encounter probabilities and Greenwood, P. H., 1953. Feeding mechanisms of the cichlid

community structure in zooplankton: a mathematical model. fish; Tilapia esculenta Graham. Nature 172 207-208. I J. Fish. Res. Bd Can. 34: 73-82. Grimaldi, E., 1972. Lago Maggiore: effects of exploitation abd Gibson, R. M., 1980. Optimal prey-size selection by three-spined introductions on the salmonid community. J. Fish. Res. Bd sticklebacks (Casterosteus aculeafus):a test of the apparent Can. 29(6): 177-785. size hypothesis. Zeitschrift fur Tierpsychology 52: 291- 307. Grygierek, E., 1962. The influence of increasing carp fry popu- Giussani, G., 1974. Planctofagia selettiva del Coregone ‘Bondel- lation on crustacean plankton. [Wplyw zageszczenia narybku la’ (Curegonus sp.) del Laggo Maggiore. Mem. Ist. Ital. karpi na faune skorupikow pjanktonowych]. Rocz-i Nauk. Idrobiol. 31: 181-203. Roh. Ser. B, 81(2): 189-210 (Eriglish summary). Gliwicz, Z. M., 1967. Zooplankton and temperature-oxygen Grygierek, e.,1967, Formation of fish pond biocenosis exempli- condition of two alpine lakes of Tatra Mts. Pol. Arch. fied by planktonic crustaceans. Ekol. pol, A, 15: 155-181. r Hydrobiol. 14(27): 53-72. Grygierek, E., 1979. Plankton as an ecological indicatot of the Gliwicz, Z. M,, 1980. Filtering rates, food size selection, and influence of farming measures on pond biocenosis. Pol. Ecol. feeding rates in cladocerans - another aspect of interspecific Stud. 5(4): 77-140, competition in filter-feeding zooplankton. In: W. C. Kerfoot Grygierek, E., A. Hillbrkkt-Iikowska & I. Spodniewska, 1966. 7- (ed.), Evolution and Ecology of Zooplankton Communities. The effect of fish on plankton community in ponds. Verh. int. The Univ. Press of New England, Hanover, New Hampshire, Ver. Limnol. 16(3): 1359-1366. USA: 282-291. Guma’a, S. A., 1978. The food and feeding habits of young Gliwicz, 2. M., 1981. Food and predation in limiting clutch size perch, Perca fluviatilis, in Windermere. Freshwat. Biol. 8: of cladocerans. Verh. int. Ver. Limnol. 21: 1562-1566. 177-187. Gliwicz, Z. M., in press. A lunar cycle in zooplankton. Ecology. Hairtson, N. G. Jr., 1980. The vertical distribution of diaptomid

I 160

copepods in relation to body pigmentation. In: W. C. Kerfoot on coral reefs in Kona, Hawaii. Fish. Bull. 72: 915-1031. (ed.), Evolution and Ecology of Zooplankton Communities. Holanov, S. H. & J. C. Tash, 1978. Particulate and filter fceding The Univ. Press of New England, Hanover, New Hampshire, in threadfin shad, Dorosoma petenense, at different light in- USA: 98-110. tensities. J. Fish Biol. 13: 619-625. Hall, D. J. & E. E. Werner, 1977. Seasonal distribution and Holling, C. S., 1966. The functional response of invertebrate abundance of fishes in the littoral zone of a Michigan lake. predators to prey density. Mem. Entomol. Soc. Can. 48: Trans. am. Fish. Soc. 106: 545-555. 1- 86. Hall, D. J., W. E. Cooper & E. E. Werner, 1970. An experimen- Holm, N. P., G. G. Ganf & J. Shapiro, 1983. Feeding and as- tal approach to the production dynamics and structures of similation rates of Daphnia pulex fed Aphanizomenon flos- freshwater communities. Limnol. Oceanogr. 15: aquae. Limnol. Oceanogr. 28(4): 677-687. 839 - 928. HrbBEek, J., 1962. Species composition and the amount of Hall, D. J., E. E. Werner, J. F. Gilliam, G. G. Mittelbach, D. zooplankton in relation to the fish stock. Rozpr. CSAV, Ser. Howard, C. G. Doner, J. A. Dickerman & A. J. Stewart, 1979. mat. nat. sci. 72: 1-117. Diel foraging behaviour and prey selection in the golden shin- HrbáEek, J., 1969. Relations between some environmental er (Notemigonus crysoleucas). J. Fish. Res. Bd Can. 36 parameters and the fish yields as a basis for a predictive mod- . 1029-1030. el. Verh. int. Ver. Limnol. 17: 1069-1081. Hamilton, A. L., 1965. An analysis of a freshwater benthic com- HrbáEek, J., 1977. Competition and predation in relation to spe- munity with special reference to the Chironomidae. Ph.D. cies composition of fieshwater zooplankton, mainly Thesis, Univ. of British Columbia, Vancouver, B.C., 216 pp. cladocera. In: J. Cairns Jr. (ed.), Aquatic Microbial Commu- Harder, 1960. Vergleichende Untersuchungen zur Morphologie nities. Garland Publishing Inc., New York and London: des Darmes bei Clupeiodea. Z. Wiss. Zool. 163: 65-167. 305-353. Hardin, G., 1960. The competitive exclusion principle. Science HrbáEek, J. & M. Novotna-Dvorakova, 1965. Plankton of four 131: 1292-1298. back-waters related to their size and fish stock. Rozpravy Hartman, G. F., 1958. Mouth size and food size in young rain- Cesk. Akad. Ved. Rada. Mat. Prirod. Ved, 75: 1-64. bow trout, Salmo gairdneri. Copeia: 233-234. HrbáEek, J., B. Desorlova & J. Popovsky, 1978. Influence of the Hemmings, C. C., 1966. Factors influencing the visibility of ob- fish stock on the phosphorus-chlorophyll ratio. Verh. int. Ver. jects underwater. In: R. Bainbridge, G. C. Evans & O. Rack- Limnol. 20: 1624-1628. ham (eds), Light as an Ecological Factor. Brit. Ecol. Soc. HrbáEek, J., M. Dvoiakova, V. koiinek & L. Prochdzkóva, 1961. Symp. 6: 359-374. Demodstration of the effect of the fish stock oh the species Hemmings, C. C., 1974. The visibility of objects underwater. In: composition of zooplankton and the intensity of metabolism G. C. Evans, R. Bainbridge & O. Rackham (eds), Light as arí of the whole plankton association. Verh. int. Ver. Limnol. 14 Ecological Factor II. The 16th Symposium of the British Eco- 192 - 195. logical Society, 26-28 March 1974, Blackwell Scientific Pub- Hughe$, G. M., 1965. Compaiative Physiology of Vertebrate lications: 543 -548. Respiiation. Harvard Univ. Press, Cambridge. Henrickson, L., H. G. Nyman, H. G. Oscarson & J. A. E. Sten- Hughes, G, M., 1976. Fish respiratory physiology. Ia: P. S. Da- son, 1980. Trophic changes, without changes in the external vies (ed.), Perspectives in Experimental Biology, Vol. i, Zool- nutrient loading. Hydrobiologia 68(3): 257 -263. ogy. Pergamoa, New York: 235-245. Hester, E J., 1968. Visual contrast thresholds of the goldfish Hughes, 6.M. & M. Morgan, 1973. The structure of fish gills (Carassius auratus). Vision Res. 8: 1315-1336. in relation to their respiratory function. Biol. Rev. 48: Hildebrand, S. F., 1963. Family Clupeidae. In: Sears Found 414 - 475. (ed.), Fishes of the Western North Atlantic. Mar. Res. Mem. Hughes, G. M. & A. J. Woakes, 1970. An elechc analogue I. Yale Univ., New Haven 3: 257-454. model of the fish ventilatory system. J. Physiol., Lond. 207: Hillbricht-Ilkowska, A., 1964. The influence of fish population 49-50. on the biocenosis of a pond using Rotifera fauna as an illus- Hunter, J. R., 1979. The feeding behaviour and ecology of ma- tration. Ekol. pol. A 12: 453-503. rine fish larvae. In: J. E. Bardach (ed.), The Physiological and Hillbricht-Ilkowska, A., 1966. The effect of different periods of Behavioural Manipulation of Food Fish as Production and utilization of fish ponds on the occurrence and abundance of Management Tools. plankton Rotatoria. Ekol. pol. A 14 111-124. Hurlbert, S. M. C M. S. Mulla, 1981. Impacts of Mosquito fish Hillbricht-Ilkowsk~,A. & T. Weglenska, 1973. Experimentally (Gambusia affinis) predation orí plankton communities. increased fish stock in the pond type Lake Warniak. VIL Hydrobiologia 83: 125-151. Numbers, biomass and production of zooplankton. Ekol. Hurlbert, S. M., J. Zedler & D. Fairbanks, 1972. Ecosystem al- POI. 21: 533-552. teration by Mosquito fish (Gambusia affinis) predation. Hillbricht-Ilkowska, A., A. Prejs & T. Weglenska, 1973. Ex- Science 175: 639-641. perimentally increased fish stock in the pond type Lake War- Hutchinson, B. P., 1971. The effect of fish predation on the niak. VIII. Approximate assessment of the utilization by fish zooplankton of ten AdÎrondack lakes, with particular refer- of the biomass and production of zooplankton. Ekol. pol. 21: ence to the alewife, Alosa pseudoharengus. Bans. am. Fish. 553-562. SOC.100: 325-335. Hobson, E. S., 1968. Predatory behaviour of some shore fishes Im, B. H., 1977. Etude de l’alimentation de quelques espèces de in the Gulf of California. Res. Rep. US. Fish Wild]. Ser. 73: Synodoritis (Poissons, Mochochidae) du Tchad. Thèse Doct. 1- 92. SpCc. Unh. P. Sabatier de Toulouse, Biol. ani. Opt. Hydrobi- Hobson, E. S., 1974. Feeding relationships of teleostean fishes ol., ORSTOM, Paris, 150 pp. 161

Ingle, D., 1968. Spatial dimensions of vision in fish. In: D. Ingle Kajak, Z., I. Spodniewska & R. J. Wisniewski, 1977. Studies on (ed.), The Central Nervous System and Fish Behaviour. Univ. food selectivity of silver carp, Hypophtalrnichthys molitrix of Chicago Press, Chicago: 51-59. (Val.). Ekol. pol. 25(2): 227-239. Ingle, D., 1971. Vision: the experimental analysis of visual be- Kajak, Z., J. Zawiska & A. Hillbricht-Ilkowska, 1976. Effect of haviour. In: W. S. Hoar & D. I. Rendall (eds), Fish Physiolo- experimentally increased fish stock on biocenosis and recov- gy. Vol. V. Academic Press, New York: 59-77. ery processes of a pond type lake. Limnologia, Berlin iO(2): Ivlev, V. S., 1961. Experimental ecology of the feeding of fishes. 595-601. Yale Univ. Press, New Haven, 302 pp. (English translation of Kajak, Z., J. I. Rybak, I. Spodniewska, W. A. Godlewska- the original Russian book edited in 1955 and based on re- Lipowa, 1975. Influence of the planktonivorous fish ’ search between 1939 and 1949). Hypothtalmichtlzys molitrix (Val.) on the plankton and ben- Jacobs, J., 1974. Quantitative measurements of food selection. thos of the eutrophic lake. Pol. Arch. Hydrobiol. 22(2): Oecologia 14: 413-417. 301-310. Janssen, J., 1976. Feeding modes and prey size selection in the Keast, A., 1970. Food specialization and bioenergetic interrela- alewife (Alosa pseudoharengus). J. Fish. Res. Bd Can. 33: tions in the fish faunas of some Ontario waterways. In: 5. H. 1972 - 1975. Steele (ed.), Marine Food Chains, Oliver & Boyd, Edinburgh: Janssen, J., 1978a. Feeding behaviour repertoire of the alewife 377-411. (Alosapseudoharengus, and the ciscoes Coregonus hoyi and Keast, A. & D. Webb, 1966. Mouth and body form relative to C. artedii. J. Fish. Res. Bd Can. 35: 249-253. feeding ecology in fish fauna of a small lake, Lake Opini, On- Janssen, J., 1978b. Will alewives feed in the dark? Envir. Biol. tario. J. Fish. Res. Bd Can. 23: 1845-1874. Fishes 3: 239-240. Kcrfoot, W. C., 1980. Commentary: transparency, body size and Janssen, J., 1980. Alewives (Alosapseudoharengus) and ciscoes prey conspiciousness. In: W. C. Kerfoot (ed.), Evolution and (Coregonus artedi4 as selective and non-selective plankti- Ecology of Zooplankton Communities. The Univ. Press of vores. In: W. C. Kerfoot (ed.), Evolution and Ecology of New England, Hanover, New Hampshire, USA: 609-617. Zooplankton Communities. The Univ. Press of New England, Kerfoot, W. C., D. L. Kellog & J. R. Strickler, 1980. Visual ob- Hanover, New Hampshire, USA 580-586. servations of live zooplankters: evasion, escape, and chemical Janssen, J., 1981. Searching for zooplankton just outside Snell’s defenses. In: W. C. Kerfoot (ed.), Evollltion and Ecology of window. Limnol. Oceanogr. 26(6): 1168-1171. Zooplankton Commbnities. The Univ. Press of New England, Janssen, J., 1982. Comparison of searching behavior for Hanover, New Hampshire, USA: 10-27. zooplankton in an obligate planktivore, blueback herrink Kettle, D. & W, J8 O’Brien, 1978. Vulnerability of arctic (Alosa aestivalis) and a facultative planktivore, bluegill zooplankton species to predation by small lake trout (Salveli- (Lepomis macrochirus). Can. J. Fish. aquat. Sci. 39(12): nus namaycltsh). J. Fish. ties. Bd Can. 35: 1495-1500. 1649-1654. King, D. P. F. & P. R. Mckod, 1976. Comparison of the food Janusko, M., 1974. The effect of three species of phytophagous and filtering mechanism of pilchard, Sardihops ocellata, and fish on algae development. Pol. Arch. Hydrobiol. 21: anchovy, Engraulis capeitsis, of South West Africa, 431 - 454. 1971-1972. Sea Fisheries Branch Inv. Rpt. no. 111, 29 pp. Jeffries, H. P., 1975. Diets of juvenile Atlantic menhaden Kislalioglu, M. & R. N..Gibson, 1976. some factors governing (Brevoorfia tyrannos) in three estuarine habitats as deter- prey selection by 15-spined stickleback, Spinachia spinachia mined from fatty acid composition of gut contents. J. Fish. L. J. exp. mar. Bio!, Ecol. 25: 159-169. Res. Bd Can. 32: 587-592. Kliewer, E. V., 1970. Gill raker variation and diet in lake white- Jenkins, R. M., 1979. Predator-prey relations in reservoirs. In: fish Coregonus clupeaforrnis in Northern Manitoba. In: R. H. Stroud & M. Clepper (eds), Predator-Prey Systems in C. C. Lindsey & C. S. Woods (eds), Biology of Coregonid Fisheries Management. International Symposium on Fishes. IJniv. of Manitoba Press, Winnipeg: 147-165. Predator-Prey System in Fish Communities and Their Role in Koksvik, J. I. & K. Aagaard, 1984. Effects of rotenone treat- Fisheries Management. Atlanta, Georgia, July 24-27, 1978, ment on the benthic fauna of a small eutrophic lake. Verh. int. Sport Fishing Institute, Washington D.C., USA: 123-134. * Ver. Limnol. 22: 658-665. Jones, S. & H. Rosa Jr., 1965. Synopsis of biological data on In- Kramer, M., 1979. Selektionsverhalten und Grossenunter- dian mackerel Rastrelliger kanagurfa (Cuvier, 1817) and short Scheidung bei Elritzen (Phoxinus luevis) gegenuber Beu- bodied mackerel Rastretfiger brachysuma (Bleeker, 1851). tesiganismen (Daphnia pulex). Ph.D. Thesis, Unh. of Mun- FAO Fisheries Synopsis no. 29. chen, Munich, Germany. Jones, D. R. & T. Schwartzfeld, 1974. The oxygen cost to the Krebs, J. R., 1973, Behavioural aspects of predation. Ih: P. P. G. metabolism and efficiency of breathing in trout (Salmogaird- Bateson & P. H. Klopfer (eds), Plenum Press, New York- neri). Resp. Physiol. 21: 241-254. London: 73-111. Jergensen, S. E. & H. F. Mejer, 1977. Ecological buffer capaci- Krebs, J. R., 1978. Obtimal foraging: Decision rules for preda- ty. Ecol. Modelling 3: 39-61. tors. In: J. R. Krebs & N. B. Davies (eds), Behavioral Ecolo- Jim, F. C. & F. T. Carlson, 1971. Food of young Atlantic men- gy: An Evolutionary Approach. Blackwell Scientific Publica- haden, Brevoortia tymnnus, in relation to metamorphosis. tions: 23 - 63. Fish. Bull., USA 68: 493-512. Krebs, J. R., A. Kacelnik & P. Bylor, 1978. Test of optimal sam- Kajak, Z., 1977. Feeding habits of silver carp, pling by foraging great tits. Nature 275: 27-31. Hypophtalmichthys Ntolirrix (Val.), and the problem of clean Krebs, J. R., J. C. Ryan & E. L. Charnov, 1974. by ex- water. [Odzywianie sie tolpygi bialej, Hypophtalmichthys pectation or optimal foraging? A stiidy of patch use by chick- tnolitrix (Val.), a problem czystoici wód]. Wiadomosci adees. Animal Behavior 22: 953 -964. Ekologizne 23(3): 258-268. Kutkuhn, J. M., 1957. Utilization of plankton by juvenile giz- 162

zard shad in a shallow prairie lake. Trans. am. Fish. Soc. 87: anabantoid fish, Helostoma temmincki. J. Morphol. 80-103. 121: 135-158. Lamar, E. S., S. Hect, S. Shlaer & C. D. Hendley, 1947. Size, Liem, K. E, 1980a. Adaptative significance of intra and inter- shape, and contrast in detection of targets by daylight vision. specific differences in the feeding repertoires of cichlid fishes. I. Data on analytical description. J. Opt. Soc. am. 37: Am. Zool. 20 295-314. 531-545. Liem, K. E, 1980b. Aquisition of energy by teleosts: adaptative Lamarra, V. A. Jr., 1975. Digestive activities of carp as a major mechanisms and evolutionary patterns. In: M. A. Ali (ed.), contributor to the nutrient loading of lakes. Verh. int. Ver. Environmental Physiology of Fishes. NATO Advanced Study Limnol. 19 2461-2468. Inst., Ser. A, Life Sciences. Plenum Press, New York: Lammens, E. H. R. R., 1985. A test of a model for plank- 299- 334. tivorous filter feeding by bream, Abramis brama. Envir. Biol. Lindgren, P. E., 1960. About the effect of rotenone upon ben- Fishes 13(4): 289-296. thonic animals in lakes. Inst. Freshw. Res. Droltningholm 39: Langeland, A. & H. Reinertsen, 1982. Interactions between 172- 184. phytoplankton and zooplankton in a fertilized lake. Holarct. Longhurst, A. R., 1971. The clupeoid resources of tiopical . Ecol. 5(3): 253-272. Oceanogr. Mar. Biol. Ann. Rev. 9: 349-385. Larkin, P. A. & T. G. Northcote, 1969. Fish as indices of eu- Losos, B. & J. Hetesa, 1973. The effect of mineral fertilization trophication. In: Eutrophication: causes, consequences, cor- and of carp fiy on the composition and dynamics of plank- rectives. Proceedings of a Symposium. National Acad. Sci. ton. Academia Publishing House of the Czechoslovak Acadc- Washington: 256-273. my of Sciences, Prague 1973: 173-217. Lauder, G. V., 1980a. The suction feeding mechanism in sun- Loukashkin, A. S., 1970. On the diet and feeding behaviour of fishes (Lepomis): an experimental analysis. J. exp. Biol. 88: the northern anchovy, Engraulis mordax (Girard). Proc. 49-72. Calif. Sci. Fourth Series 37: 419-458. Lauder, G. V., 1980b. Hydrodynamics of prey capture by teleost Luecke, C. & W. J. O’Brien, 1981. Prey location volume of a fishes. In: D. Schneck (ed.), Biofluid Mechanics, Vol. 2. Ple- planktivorous fish: a new measure of prey vulnerability. Can. num Press, New York: 161-181. J. Fish. aquat. Sci. 38: 1264-1270. Lauder, G. V., 1983. Prey capture hydrodynamics in fishes: ex- Lynch, M., 1979. Predation, competition, and zooplankton perimental tests of two models. J. exp. Biol. 104 1-13. community structure: an experimental study. Limnol. Laughlin, D. R. & E. E. Werner, 1980. Resource partitioning in Oceanogr. 24(2): 253 -272. two coexisting sunfish: pumpkinseed (Lepomis gibbosus) and Lynch, M., 1980. Aphanizornenon blooms: alternate control northern (Lepomis megalotis peltasies). Can. and cultivation by Daphnia pulex. In: W. C. Kerfoot (ed.), J. Fish. Aquat. Sci. 37: 1411-1420. Evolution and Ecology of Zooplankton Communities, The Lauzanne, L., 1970. La sélection des proies chez Akstes Wniv. Press of New England, Hanover, New Hampshire, baremoae (Pisces, Characidae). Cah. ORSTOM, sér. Hydrobi- USA; 299- 304. 01. 7(1): 71-76. Lynch, M. L J. Shapka, 1981. Predation, enrichment and Lauzanne, L., 1973. Etude qualitative de la nutrition des A.llesfes phytoplankton community structuie. Limnol. Oceanogr. barernoze (Pisces, Characidae). Cah. ORSTOM, sér. Hydrobi- ?6(1): 86-102. 01. 7(1): 3-15. Lythgoe, J. N., 1968. Visual pigments and visual range under- Lauzanne, L., 1977. Aspects qualitatifs et quantitatifs de water. Vision Res. 8: 997-1012. l’alimentation des poissons du Tchad. Thèse Doct. Sc. Nat,, Lythgoe, J. N., 1979. The Ecology of Vision. Clarendon Press, Univ. P. M. Curie Paris VI et MNHN, 282 pp. Oxfoid. Lauzanne, L. & A. Iltis, 1975. La sélection de la nourriture chez Mac Arthur, R. H. & E. R. Pianka, 1966. On optimal use of a Tilapia galilaea (Pisces, Cichlidae) du Lac Tchad. Cali. OR- patchy environment. Am. Nat. 100: 603-609. STOM, sér. Hydrobiol. 9(3): 193-199. Mago-Leccia, F. & T. M. Zaret, 1978. The taxonomic status of Leah, R. T., B. Moss & D. E. Forrest, 1980. The role of preda- Rhabdolichops iroscheli (Kaup, 1856), and speculations on tion in causing major changes in the limnology of a hyper- gymnotiform evolution. Env. Biol. Fishes 3: 379- 384. trophic lake. Int. Revue ges. Hydrobiol. 62: 223-247. Malyarevskaya, A. YA., T. I. Birger, O. M. Arsan C% V. D. Lechowicz, M. J., 1982. The sampling characteristics of electivi- Soloniatina, 1972. Metabolic relationship between blue-green ty indices. Oecologia 52: 22-30. algae and fish. Hydrobiological Journal 8(3): 35 -41. Leong, R. J. & C. P. O’Connell, 1969. A laboratory study of Marshall, N. B., 1965. The Life of Fishes. Weidenfeld and Nicol- particulate and filter feeding of the northern anchovy, En- son, London 402 pp. graulis mordax. J. Fish. Res. Bd Can. 26: 557-582. McComas, S. R. & R. W. Drenner, 1982. Species replacement in Leventer, H., 1981. Biological control of reservoirs by fish. a reservoir fish community: silverside feeding mechanics and Bamidgeh 33(1): 3-23. competition. Can. J. Fish. aqaut. Sci. 39: 815-821. Levine, J. S., P. S. Lobel & E. F. McNichol Jr., 1979. Visual com- McNaught, D. C., 1979. Considerations of scale modelihg large munication in fishes. In: M. A. Ali (ed.), Environmental aquatic ecosystems. In: D. Scavia & A. Robertson (eds), Per- Physiology of Fishes. Plenum Press, New York and London: spective on Lake Ecosystems Modeling. Ann Arbor Science, 447 -475. Ann Arbor: 3-24. Lewis, R. C., 1929. The food habits of the California sardine in Mellors, W. K., 1975. Selective predation of ephippial Daphnia relation to the seasonal distribution of microplankton. Bull. and the resistance of ep’hippialeggs to digestion. Ecology 56: Scripps Inst. Oceanogr. Tech. Ser. 2: 155-180. 974 - 980. Liem, K. F., 1967. Functional morphology of the head of the Merrett, N. R. & H. S. J. Roe, 1974. Patterns and selectivity in 163

the feeding of certain mesopelagic fishes. Mar. Biol. 28: Nelson, G. J., 1970. The hyobranchial apparatus of teleostean 115-126. fishes of the families Engraulidae and Chirocentridae. Ameri- Miller, R. J., 1979. Relationships between habitat and feeding can Museum Novitates, no. 2410. mechanisms in fishes. In: R. H. Stroud & H. Clepper (eds), Nelson, D. W., 1979. The mechanisms of filter feeding in three Predator-prey systems ih fisheries management. Sport Fishing teleosts: Engraulis mordax, Sardinops caerulea and Rastrel- Institute, Washington D.C., USA: 269-280. liger kanagurta. Univ. of Washington, Seattle, Zool/Fish 575, Mittelbach, G. G., 1981. Foraging efficiency and body size: a 4 Dec. 1979, 17 pp. study of optimal diet and habitat use in bluegills. Ecology 62: Nilsson, N., 1960. Seasonal fluctuations in the food segregation 1370- 13 86. of trout, char, and whitefish in 14 North-Swedish lakes. Rep. Mittelbach, G. G., 1984. Predation and resource partitioning in Inst. Freshw. Res. Drottningholm 41: 185-205. two sunfishes (Centrarchidae). Ecology 65(2): 499-513. Nilsson, N., 1963. Interaction between trout and char in Scan- Monod, T., 1949. Sur l’appareil branchiospinal de quelques dinavia. Pans. am, Fish. Soc. 92 276-285. téléostéens tropicaux. Bull. I.F.A.N. ll(1-2): 36-76. Nilsson, N. A. & B. Peiler, 1973. On the relation between fish Monod, T., 1961. Brevoortia Gill 1861 et Ethmalosa Ragan 1917. fauna and zooplankton composition in north Swedish lakes. Bull. I.F.A.N. 23(A): 506-547. Rep. Inst. Freshw. Res. Drottningholm 53: 51-56. # Moriarty, D. J. W., 1973. The physiology of digestion of blue- Nifssen, J. P., 1984. Tropical lakes - and fu- green algae in the cichlid fish Tilapia nilotica. J. Zool., Lond. ture development: the need for a process-oriented approach. 171: 25-39. Hydrobiologia 113: 231-242. Y Moriarty, C. M. & D. J. W. Moriarty, 1973. Quantitative estima- Nival, P. & S. Nival, 1976. Particle retention efficiencies of an tion of the dialy ingestion of phytoplankton by Tilapia niloti- herbivorous copepod, Acartiu clausi (adult and copepodit ca and HupIochrotnis nigripittnis in Lake George, Uganda. J. stages): effects on grazing. Limnol. Oceanogr. 21: 24-38. Zool., Lond. 171: 15-23. Norman, J. R. & P. H. Greenwood, 1963. A History of Fishes. Moriarty, D. J. W., J. P. E. C. Darlington, E. G. Dunn, C. M. Ernest Benn Limited, London, 467 pp. Moriary & M. P. Telvin, 1973. Feeding and grazing in Lake Northcote, T. G., J. Walters & J. M. B. Hume, 1978. Initial im- George, Uganda. Proc. R. Soc. Lond. B. 184: 299-319. pacts of experimental fish introductions on the macro- Motta, P. J., 1984. Mechanics and functions of jaw protrusion zooplankton of small oligotrophic lakes. Verh. int. Ver. Lim- in teleost fishes: a review. Copeia 1984(1): 1-18. nol. 20: 2003-2012. Muller, M., J. Osse & J. H. G. Verhagen, 1982. A quantitative Novotna, M. 8r V. Korinek, 1966. Effect of the fish stock on the hydrodynamical model of suction feeding in fish. J. theor. quantity and species composition of the plankton of two Biol. 95: 49-79. backwaters. Academia Publishing House of the Czechoslovak Muntz, W. R, A., 1974a. Visual pigments and the environment. Academy of Sciences, Hydrobiological Studies 1: 297- 322. In: M. A. Ali (ed.), Vision in Fishes. Plenum Publishing Cor- O’Brien, W, J., 1979. The predatory-prey interactions of plank- poration, New York: 565-578. tivorous fish and zooplankton - a recent research with Muntz, W. R. A., 1974b. Behavioural studies of vision in a fish planktivorous fish and their zooplankton .prey shows the and possible relationships to the environment. In: M. A. Ali evolutionary thrust and parry of the predator-prey relation- (ed.), Vision in Fishes. Plenum Publishing Corporation. New ship. American Scientist 67: 572-581. York: 705-717. O’Brien, W. J. & G. L. Vinyard, 1974. Comment on the use of Muntz, W. R. A., 1977. The visual world of the amphibia. In: Ivlev’s electivity index with planktivorous fish. J. Fish. Res. F. Crescitelli (ed.), The in . Bd Can. 31: 1427-1429. Springer-Verlag, New York: 275 - 307. O’Brien, W. J., N. A. Slade & G. L. Vinyard, 1976. Apparent Nafpaktitis, B. G. R. H., J. E. Backus, R. L. Craddock, B. H. size as the determinant of prey selection by bluegill sunfish Haedrich, Robison & C. Karnella, 1977. Family Myctophidae. (Lepomis macrochirus). Ecology 57: 1304- 1310. In: Sears Foundation for Marine Research, Fishes of the O’Connell, C. P., 1972. The interrelation of biting and filtering Western North Atlantic. Mem. I, Yale Univ., New Haven 7: in the feeding activity of the northern anchovy (Engraulis 13-258. mordax). J. Fish. Res. Bd Can. 29: 285-293. Nakamura, E. L., 1968. Visual acuity of two Katsuwonus O’Connell, C. P. & J. R. Zweifel, 1972. A laboratory study of pelarnb and Euthynnus affinis. Copeia 1: 41-49. particulate and filter feeding of the Pacific mackeral, Scotn- Nakashima, B. S. & W. C. Leggett, 1980. The role of fishes in ber japonicus. Fish. Bull. 70 973-981. the regulation of phosphorus availability in lakes. Can. J. Olrik, K., S. Luridoer & K. Rasmussen, 1984. Interactions be- Fish. aquat. Sci. 37: 1540-1549. tween phytoplankton, zooplankton, and fish in nutrient rich Nakashima, B. S. & W. C. Leggett, 1982. How important is shallow Lake Hjarbaek Fjord, Denmark. Int. Revue ges. phosphorus excretion in fish to the phosphorus dynamics of Hydrobiol. 69(3): 389-405. Y lakes? Can. J. Fish. aquat. Sci. 39: 364-365. Omarov, M. O. & L. P. Lazareva, 1974. Nutrition’ of Narver, D. W., 1970. Diel vertical movements and feeding of un- Hypophthalmicltthys molitrix Val. in water bodies of deryearling sockeye salmon and the limnetic zooplankton in Daghestan. [Pitade belogo tolstolobika v vodoemach 1. ‘ Babine Lake, British Columbia. J. Fish. Res. Bd Can. 27: Dagestana]. Gidrobiol. Zh. lO(4): 100- 103. 281-316. OpuszynSki, K., 1979a. Silver carp, Hypopfzthahichthys Neill, S. R. & J. M. Cullen, 1974. Experiments on whether molitrix (Val.), in carp ponds. I. Fishery production and food schooling by their prey affects the hunting behaviour of relations. Ekol. pol. 27(1)! 71-92. and fish predators. J. Zool., Lond. 172: 549-569. Opuszyhski, K., 1979b. Silver carp, Hj‘pophlhalmichtlzys Nelson, G. J., 1967. Epibranchial organs in lower teleostean rnolitrix (Val.), in carp ponds. III: Influence on ecosystem. fishes. J. Zool., Lond. 153: 71-89. Ekol. pol. 27(1): 117-133.

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Opuszyxíski, K., 1980. The role of fishery management in coun- ment. Sport Fishing Institute, Washington D.C., U.S.A.: teracting eutrophication processes. In: J. Barica & L. R. Mur 199- 202. (eds), SIL Workshop on Hypertrophic Ecosystems, Vaxjo, Pyke, G. H., H. R. Pulliam & E. L. Charnov, 1977. Optimal Sweden, Sept. 10- 14, 1979, Developments in Hydrobiology foraging theory: a selective review of theory and tests. Quar- ’ 2: 105-116. terly Review of Biology 52: 137-154. Osse, J. & M. Muller, 1950. A model of suction feeding in teleos- Radakov, D. V., 1973. Schooling and the Ecology of Fish (transl. tean fishes with some implications for ventilation. In: M. A. from Russian by H. J. Mills). John Wiley and Sons Inc., New Ali (ed.), Environmental Physiology of Fishes. Plenum Pub- York, 173 pp. lishing Co., New York: 335-352. Rasmussen, G. A., 1973. A study of the feeding habits of four Owen, R. W., 1981. Microscale plankton patchiness in the larval species of fish, Alosa pseudoharengus, Coregonus hoy!, Per- anchovy environment. Rapp. P. -V. Reun. Cons. int. Explor. ca flavescens, and Osrnerus mordax at three sites on Lake Mer. 175: 364-365. Michigan, as compared to phytoplankton, zooplankton and Paloheimo, J. E., 1979. Indices of food type preference by a water chemistry of those sites. Ph.D. Thesis, Michigan State predator. J. Fish Res. Bd Can. 36: 470-473. Univ., East Lansing, Mich., 104 pp. Payne, A. I., 1978. Gut pH and digestive strategies in estuarine Reif, C. B. & D. W. Tappa, 1966. Selective predation: smelt and grey mullet (Mugilidae) and tilapia (Cichlidae). J. Fish. Res. cladocerans in Harveys Lake. Limnol. Oceanogr. 11: Bd Can. 13(5): 627-629. 437-1138, Pearre, S. Jr., 1982. Estimating prey preference by predators: Reinertsen, H. & A. Langeland, 1982. The effects of a lake fer- uses of various indices and a proposal of another based on tilization on the stability and utilization of a limnetic ecosys- X2. Can. J. Fish. aquat. Sci. 39: 914-923. tem. Holarct. Ecol. 5(3): 311-324. Pearson, N. E., 1974. . Quant. Sci. Pap. Reinertsen, H. & Y. Olsen, 1984. Effects of fish elimination on 39, Cent. Quant. Sci., Univ. of Washington, Seattle, 48 pp. the phytoplankton community of a eutrophic lake. Verh. int. Peters, D. S., 1972. Feeding selectivity in juvenile Atlantic men- Ver. Limnol. 22 649-657. haden Brevoortia fyrannus (Pisces: Clupeidae). The ABS Rhodes, R. J., 1971. The food habits of the alewife in Indiana Bulletin, Vol. 19, no. 2, 91 pp. waters of Lake Michigan. M.Sc. Thesis, Ball State Univ., Pierce, R. J., T. E. Wissing & B. A. Megrey, 1981. Aspects of the Muncie, Indiana, 82 pp. feeding ecology of gizzard shad in Acton Lake, Ohio. Trans. Rhodes, R. J. & T. S. McComish, 1975. Observations on the am. Fish. Soc. 110: 391-395. adult alewife’s food habits (Pisces: Clupeidae: Alosa pseudo- Pigarev, I. N. & G. M. Zenkin, 1970. Dark spot detectors in the harengus) in Indiana’s water of Lake Michigan in 1970. Ohio frog retina and their role in organization of feeding behavior. J. Sci. 75: SO-55. Neurosci. Trans]. 13: 29-33. Roberts. T. R., 1972. Ecology of fishes in the Amazon and Con- Pigarev, I. N., G. M. Zenkin & S. V. Girman, 1971. Activity of go basins. Buk Mus. Comp. Zool. Havard 143: 117-147. the retina’s detectors in unrestrained . Fiziol. Zh. SSSR Roja:, de Mendiola, B., 1971. Some observations on the feeding Im. I. M. Sechenova 57: 1448-1452. of the Peruvian anchoveta Engraulis ringen J. in two regions Pliszka, F., 1934. Materjaly do typologii slawow. Plankton of the Peritvian . In: J. D. Costlow, Jr. (ed.), Fertilily of stawow doswiadczalnych w Rudzie Malienickiej. Race i the Sea. Gordon and,Rreach, New York: 417-440. Spraword. Zakl. Icht. i Ryb. 37: 235-261. Rosen, R. A. Er U. C. Hales, 1981. Feeding of paddlefish, Po!v- Poulet, S. A. & P. Marzot, 1978. Chemosensory grazing by ma- odora spnthula. Copeia 2: 441-455. rine calanoid copepods (Arthropoda: Crustacea). Science Rosenthal, H., 1969. Untersuchungen uber das Beutefan- 200: 1403 - 1405. gprhalten bei Larven des Hering Clupea harengus. Mar. Biol. Pourriot, R., 1983. Influence sélective de la prédation sur la 3: 208-221. structure et la dynamique du zooplankton d’eau douce. Acta Rosenthal, H. & G. Hempel, 1970. Experimental studies in feed- Oecologica, Oecol. Génér. 4(1): 29-41. ing and food requirements of herring larvae (Clupea haren- Pourriot, R., J. Capblancq, P. Champ & J. A. Meyer, 1982. gus L.). In: J. H. Steele (ed.), Marine Food Chains. Oliver and Ecologie du plancton des eaux continentales. Masson, collec-. Boyd, Edinburgh: 344-364. tion d’Ccologie, no. 16, 198 pp. Rosenzweig, M. L., 1979. Optimal habitat selection in two spe- Prejs, A., 1973. Experimentally increased fish stock in the pond cies competitive systems. Forschritte der Zoologie 25: type Lake Warniak. IV. Feeding of introduced and 283 - 293. authochthonous non-. Ekol. pol. 21: 465 -505. Rubenstein, D. I. & M. A. R. Koehl, 1977. The mechanisms of Prejs, A., 1976. Fishes and their feeding habits. In: E. Pieczyns- filter feeding: some theoretical considerations. Am. Nat. 111: ka (ed.), Selected Problems of Lake Littoral Ecology, War- 981-984. shaw University Press, Warszawa: 155 - 171. Ryther, J. H., 1969. Relationship of photosynthesis to fish Prejs, A., 1978. Eutrophication of lakes and the ichthyofauna. production in the sea. Science 166: 72-76. [Eutrofizacja jezior a ichthyofauna]. Wiadomosci Sandberg, P. A., 1964. The ostracod genus Cyprideis in the Ekologiczne 24(3): 201-208. Americas. Stockholm Contrib. Geol. 12: 1-78. Protasov, V. R., 1968. Vision and near orientation of fish. Israel Savina,. P. A., 1965. Filter feeding of silver carp Program Scient. Trans., Jerusalem (1970). Hypophtha/michtl?ys molitrix (Val.). [Filtracionnoe pitanie Prowse, G. A., 1964. Some limnological problems in tropical belogo tolstolobika Hypophlhalmichthys nzolitrix (Val.)]. fish ponds. Verh. int. Ver. Limnol. 15: 450-484. Vopr. Ichtiol. 5: 135-140. Pyke, G. H., 1979. Optimal foraging in fish. In: R. II. Stroud & Schlesinger, D. A., L. A. Molot Sr B. J. Shuter, 1951. Specific H. Clepper (eds), Predator-Prey Systems in Fisheries Manage- growth rates of freshwater algae in relation to cell size and 165

light intensity. Can. J. Fish. aquat. Sci. 38: 1052-1058. mouth buffalow, lctiobus cyprinelltrs, in Lake Poinsett, Schoener, T. W., 1969. Models of optimal size for solitary preda- South Dakota. Trans. am. Fish. Soc. 99: 571-576. tors. Amer. Nat. 103: 277-313. Steele, J. H., 1974. The structure of marine ecosystems. Harvard Schoener, T. W., 1971. Theory of Feeding Strategies. Ann. Rev. University Press, Cambridge, 128 pp. Ecol. Syst. 2 369-404. Stenson, J. A. E., 1972. Fish predation effect on the species Schutz, D. C. & T. G. Northcote, 1972. An experimental study composition of the zooplankton community in eight small of feeding behavior and interaction of coastal cutthroat trout forest lakes. Rep. Inst. Freshw. Res. Drottningholm 52: (Salmo clarki clarki) and dolly varden (Salvelinus malma). J. 132-148. Fish. Res. Bd Can. 29 555-565. Stenson, J. A. E., 1978. Differential predation by fish on two Seghers, B. H., 1975. Role of gill rakers in size-selective preda- species of Chao&orus (Diptera, Chaoboridae). Oikos 31: tion by lake whitefish, Coregonus clupeafortnis (MitchiIl). 98-101. Verh. int. Ver. Limnol. 19: 2401-2405. Stenson, J. A. E., 1980. Predation pressure from fish on two Shapiro, J., 1978. The need for more biology in lake restoration. Chaoborus species as related to their visibility. In: W.‘C. Ker- Contrib. # 183 from the Limnological Research Center, Unk. foot (ed.), Evolution and Ecology of Zooplankton Commltni- of Minnesota, Minneapolis, for the USEPA National Confer- ties. The Univ. Press. of New England, Hanover, New Hamp- ence on Lake Restoration, Minneapolis, MN, Aug. 22-24, shire, USA: 618-622. 1978, 17 pp. Stenson, J. A. E., 1982. Fish impact on rotifer community struc- Shapiro, J., 1979. The importance of trophic level interactions to ture. Hydrobiologia 87: 57-64. the abundance and species composition of algae in lakes. In: Stenson, J. A. E., 1983. Changes in the relative abundance of J. Barica & L. R. Mur (eds), SIL Workshop on Hypertrophic Polyarthra vulgaris and I? dolichopfera, following the elimi- Ecosystems, Vaxjo, Sweden, Sept. 10-14, 1979, Develop- nation of fish. Hydrobiologia 104: 269-273. ments in Hydrobiology 2: 105-116. Stenson, J. A. E., T. Bohlin, L. Henrickson, B. I. Nilsson, H. G. Shapiro, J. & R. Carlson, 1982. Comment on the role of fishes Nyman, H. G. Oscarson & P. Larson, 1978. Effects of fish in the regulation of phosphorus availability in lakes. Can. J. removal from a small lake. Verh. int. Ver. Limnol. 20 Fish. aquat. Sci. 39: 364. ! 794 - 801. Shapiro, J. & D. I. Wright, 1984. Lake restoration by bi- StraSkraba, M., 1965. The effect of fish on the number of inver- omanipulation: Round Lake, Minnesota, the first two years. tebrates in ponds and streams. Mitt. int. Ver. Limnol. 13: Freshwat. Biol. 14 371-383. 106-127. Shapiro, J., V. Lamarra & M. Lynch, 1975. Biomanipulation: an StraSkraba, M., 1967. Quantitative study on the littoral ecosystem approach to Lake Restoration. In: P. L. Brezonik zoop1ankton of Poltruba Backwater with an attempt to dis- & J. L. Fox (eds.), Symposium on Water Quality Management close the effect of fish. Rozpr. Csl. Akad. Ved. 77: 7-34. Through Biological Control, Jan. 20-23, 1975, Unh. of Strauss, P.. E., 1979. Reliability estimates for Ivlev’s electivity in- Florida, Gainesville, Dept. Env. Eng. Sci. & USEPA: 85-96. dex, the foragc ratio, and a proposed linear index of food Shapiro, J., B. Forsberg, V. Lamarra, G. Lindmark, M. Lynch, selection. Trans. am. Fish. Soc. 108: 344-352. E. Smeltzer & G. Zoto, 1982. Experiments and experiences in Suffern, J. S., 1973. Experimental analysis of predation in a biomanipulation - studies on biological ways to reduce algal freshwater system. Ph.D. Thesis, Yale Univ. abundance and eliminate blue-greens. Limnological Research Susta, J., 1935. Food of the carp and other pond fish. IVyziva Center, Univ. of Minnesota, Minneapolis, Minnesota, lntern Kapra e jeho druziny rybnicne]. 2nd Edition. in Czech, Pra- Report no. 19: 251 pp. ha. Shaw, E., 1978. Schooling fishes. Am. Sci. 66: 166-175. Svardson, G., 1976. Interspecific population dominance in fish Shelton, G., 1970. The regulation of breathing. In: W. S. Hoar communities of Scandinavian lakes. Rep. Inst. Freshw. Res. & D. J. Randall (eds), , Vol. 4. Academic Diottningholm 55: 144-171. Press, New York: 293-359. Szlauer, L., 1965. The ability of plankton animals before Smith, W. L., 1963. Viable algal cells from the gut of gizzard plankton eating animals. Pol. Arch. Hydrobiol. 13(26): shad Dorosoma cepedianurn (Le Sueur). Proc. Okla. Acad. 89-95. Sci. 43: 148-149. Tamura, T., 1957. A study of visual perception in fish, especially Smith, R. E. & J. Kalff, 1982. Size dependent phosphorus up- on resolving power and accomodation. Bull. Japan Soc. Sci. take kinetics and cell quota in phytoplankton. J. Phycol. 18: Fish 22: 536-557. 275 -284. Thomson, J. M., 1966. The mullets. Oceanogr. Mar. Biol. Ann. Spataru, P., 1976. The feeding habits of Tilapia galilae (Artedi) Rev. 4: 301-335. in Lake Kinneret (Israel). Aquaculture 9: 47-59. Tinbergen, L., 1960, The dynamics of insect and popula- Spataru, P. & M. Zorn, 1976. Some aspects of natural food and tion in pine woods. Arch. Neerl. Zool. 13: 259-473, feeding of Tilapia galilae (Artedi) and I: aurea (Steindach- Vanderploeg, H. A. & D. Scavia, 1979. Two electivity indices for ner) in Lake Kinneret. Bamidgeh 28: 12-17. feeding with special reference to zooplankton grazing. J. Fish. Spataru, P. & M. Zorn, 1978. Food and feeding habits of Tilapia Res. Bd Can. 36: 362-365. aurea Steindachner (Cichlidae) in Lake Kinneret (Israel). Velasquez, G. T., 1939. On the viability of algae obtained from Aquaculture 13: 67-79. the digestive tract of the gizzard shad, Dorosoma cepedia- Spodniewska, I. & A. Hillbricht-Ilkowska, 1973. Experimentally num (Le Sueur). Am. Middl. Nat. 22 376-412. increased fish stock in the pond type Lake Warniak. VI. Bi- Vinyard, G. L., 1979. An ostracod (Cypriodopsis vidua) can re- omass and Production of phytoplankton. Ekol. pol. 21(32): duce predation from fish by resisting digestion. Am. Middl. 519-532. Nat. 102: 188-190. Starostka, V. Ja& R. L. Applegate, 1970. Food selectivity of big- Vinyard, G. L., 1980. Differential prey vulnerability and preda- 166

tor selectivity: the effects of evasive prey on sunfish (Lepomis) Wells, L., 1970. Effects of alewife prcdation on zooplankton predation. Can. J. Fish. aquat. Sci. 37: 2294-2299. populations in Lake Michigan. Limnol. Oceanogr. 15: Vinyard, G. L. & W. J. O'Brien, 1975. Dorsal light response as 556- 565. an indes of prey preference in bluegill (Lepomis nzacrochi- Werner, E. E., 1972. On the breadth of diet in fishes. P1i.D. The- rus). J. Fish. Res. Bd Can. 32: 1860-1863. sis, Michigan State Univ. Vinyard, G. L. & W. J. O'Brien, 1976. Effects on light and tur- Weiner, E. E., 1974. The fish size, prey size, handling time rela- bidity on the reactive distance of bluegill (Lepomis macrochi- tion in several sunfishes and some implications. J. Fish. Res. rus). Can. J. Fish. Res. Bd Can. 33: 2845-2849. Bd Can. 31: 1531-1536. Vinyard, G. L., R. W. Drenner & D. A. Hanzel, 1982. Feeding Werner, E. E., 1977. Species packing and niche complementarity success of hatchery-reared Kokanee salmon when presented in three sunfishes. Am. Nat. 111(975): 553-578. with zooplankton prey. Prog. Fish. Cult. 44: 37-39. Weiner, E. E. & D. J. Hall, 1974. Optimal foraging and the size Volkova, L. A., 1973. The effects of light intensity on the availa- selection of prey by the bluegill sunfish (Lepomis macrochi- bility of food organisms to some fishes of Lake Baikal. J. rus). Ecology 55: 1042-1052. Ichthyol. 13: 591-602. Werner, E. E. & D. J. Hall, 1976. Niche shifts in Sunfishes: ex- Voropaev, N. V., 1968. Morfologiceskie priznaki, pitanie i perimental evidence and significance. Science 191: 404-406. nekotorye rybovodnye pokazateli tolstolobikov i ich gibridov. Werner, E. E. & D. J. Hall, 1977. Competition and habitat shift In: G. V. Nikolskij (ed.), Novye issledovanija po ekologii i in two sunfishes (Centrarchidae). Ecology 58: 869-876. razvedeniju rastitelnojadnych ryb, Izd. Nauka, Moskva: Werner, E. E., G. G. Mittelbach & D. J. Hall, 1981. The role of 206 - 21 7. foraging profitability and experience in habitat use by bluegill Vovk, P. S., 1974. The possib es of using silver carp sunfish. Ecology 62(1): 116-125. Hypophthalmichthys molitrix (Val.) to increase the fish Weiner, E. E., J. F. Gilliam, D. J. Hall & G. G. Mittelbach, productivity and to decrease the eutrophication of the Dniepr 1983a. An experimental test of lhe effects of predation risk on reservoirs. [O vozmoznosti ispolzovanija belogo tolstolobika habitat use in fish. Ecology 64(6): 1540-1548. (Hypophthalmichtlzys molitrix (Val.)) dla povysenija Wetner, E. E., G. G. Mittelbach, D. J. Hall & J, E Gilliam, ryboproduktivnosti i snizenija urovnija evtrofikacii Dneprov- 1983b. Experimental tests of optimal use in fish: the role of skich vodochranilisc]. Vopr. Ikhtiol. 14: 406-414. relativc habitat piofitabilily. Ecology 64(6): 1525 -1539. Walter, E., 1895. Uber die Moglichkeit einer biologischen Werner, E. E., U. J. Hall, D. R. Laughlin, D. J. Wagner, L. A. Bonitierung von Tiechen. Munchen. Wilsinann & E C. Funk, 1977. Habitat partitioning in a Walters, V., 1966. On the dynamics of filter feeding by the wavy- community. J. Fish. Res. Bd Can. 34: back skipjack (Euthynnus affinis). Bull. mar. Sci. 16: 360-370. 209-221. Windell, J. T., 1978. Digestion and the daily ration of fishes. In: Ware, D. M., 1971. Predation by rainbow trout (Saln70 gaird- S. D. Qerbing (ed.). Ecology of Freshwater Fish Production. neri): the effect of experience. J. Fish. Res. Bd Can. 28: John WiIey and Sons, New York: 159-183. 1847 - 1852. Wmg, R. i% E J. Ward, 1972. Size selection of Daphniapulicaria Ware, D. M., 1972. Predation by rainbow trout (Salmo gaird- by yellow perch (Perca Jhescens) fry in West Blue Lake, neri): the influence of hunger, prey density, and prey size. J. Manitoba. J. Fish. RCS. Bd Can. 29: 1761-1764. Fish. Res. Bd Can. 29: 1193-1201. Wright, D. 1. & W. J. O'Brien, 1984. Modeling the plank- Ware, D. M., 1973. Risk of epibenthic prey to predation by rain- tivorom feeding vhtivity of white crappie (Pornoxis an- bow trout (Salmo gairdnerr]. J. Fish. Res. Bd Can. 30: nitlaris): a succesbful field test. Ecological Monographs 54: 787-797. 65-98. Ware, D. M., 1975. Growth, metabolism and optimal swimming Wright, D. I. & J. Shapiro, 1984. Nutrient reduction by bi- speed of a . J. Fish. Res. Bd Can. 32: 33-41. omanipuliilion: an unespected phenomenon and its possible Warshaw, S. J., 1972. Effect of alewives (Alosa pseudoharengus) cause. Verh. int. Ver. Limnol. 22: xm-xxx. on the zooplankton of Lake Wononskopomuc, Connecticut, Wright, D. I., W. J. O'Brien & C. Luecke, 1983. A new estimate Limnol. Oceanogr. 17: 816-825. of zooplankton retention by gill rakers and its ecological 5ig- Webb, P. W. & J. M. Skadsen, 1980. Strike tactics of eso.^. Can. nificance. Trans. am. Fish. Soc. 112: 638-646. J. 2001. 58: 1462-1469. Wright, D., W. J. O'Brien & G. L. Vinyard, 1980. Adaptative Wegleriska, T., 1971. The influence of various concentrations of value of vertical migration: a simulation model argument for natural food on the development, fecundity and production the predation hypothesis. In: W. C. Kerfoot (ed.), Evolution of planktonic crustacean filtrators. Ekol. pol. 19: 427-473. and Ecology of Zooplaiikton Communities. The Unh Press Wegleriska, T., K. Dusoge, J. Ejsmont-Karabin, I. Spodniewska of New England, Hanover, New Hampshire, USA: 138-147. & J. Zachwieja, 1979. Effect on winter-kill and changing fish Zaret, T. M., 1969. Predation-balanced polymoi phisin of Cerio- stock on the biocenose of the pond-type Lake Warniak. Ekol. daphnia cornuta Sars. Limnol. Oceanogi. 14: 301-303. POI. 27(1): 39-70. Zaret, T. M., 1971. The distribution, diet, and feeding habits of Weimann, R., 1938. Planktonuntersuchungen in niedersch- the atherinid fish Melaniris chagresi in Gatun Lake, Panama, lesischem Karpfenzuchtgebiet. 2. Fischerei 36: 109-183. Canal Zone. Copeia 1971: 341-343. Weimann, R., 1939. Uber Plankton, Dungung und Fischertrage Zaret, T. M., 1972a. Predator-prey interaction in a tropical in niederschlesischen Karpfenteichen. Arch. Hydrobiol. 34: lacustrine ecosystem. Ecology 53: 248-257. 659-693. Zaret, T. M., 1972b. Predators, invisible prey, and the riature of Weimann, R., 1942. Zur Gliederung und Dynamik der Flach- polymorphism in the Cladoceia (Class Crustacea). Limnol. gewasser. Arch. Hydrobiol. 38: 481 -524. Oceanogr. 17: 171-184. 167

Zaret, T. M., 1980. Predation and Freshwater Communilies. Zaret, T. M. & J. S. Suffern, 1976. Vertical migration in Yale Univ. Press, New Haven, 187 pp. zooplankton as a predator avoidance mechanism. Limnol. Zaret, T. M. & W. C. Kerfoot, 1975. Fish predation on Bosniina Oceanogr. 21: 804-813. longirostris: Body-size selection versus visibility selection. Ecology 56 232-237. Received 22 July 1986; accepted August 1986.