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Reviews in Fish Biology and Fisheries 7, 463±491 (1997) Effects of pollution on reproductive behaviour of ®shes J A C K I E C . J O N E S and J O H N D. R E Y N O L D S School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, United Kingdom Contents Abstract Introduction Fish behaviour in pollution research Case study 1: mosquito®sh and paper mill ef¯uent Case study 2: sun®sh and herbicide Comparisons between case studies Review of studies Motivation for research page 463 464 465 480

Selection of study species and pollutant Laboratory or wild Emphasis on reproductive behaviour Effects on reproductive success Experimental designs Secondary effects of pollution Prospects for the future: integrating pollution and reproductive behaviour From individual behaviour to populations Effects on future reproductive success Population size Genetic changes Adaptation Uses of reproductive behaviour studies Behavioural assays for protecting other species and habitats Conservation Conclusion Acknowledgements References 483 483 Abstract This review attempts to integrate pollution research with behavioural ecology by focusing on reproductive behaviour of ®shes. A search of Aquatic Sciences and Fisheries Abstracts and other sources showed that only 0.1% of 19 199 studies of aquatic pollution Author to whom correspondence should be addressed (e-mail: 0960±3166 # 1997 Chapman & Hall

and ®shes during the past 20 years have made this link. Effects on parental care and courtship have 3been investigated using a variety of pollutants (e.g. acidi®cation, and Jones herbicide, thermal ef¯uent) in several ®sh families (e.g. Cichlidae, Poeciliidae, Gasterosteidae, Cyprinidae). Eleven of the 19 studies found a change in behaviour from the norm. Effects on courtship included decreases or increases in frequency of displays, increased courtship duration, or performance of male-like behaviour by masculinized females. Studies of parental care have found decreased nest-building activity, decreased offspring defence, or changes in division of parental care between the sexes. Few studies have measured reproductive success or extrapolated their results to effects on populations. We develop a framework for exploring links between pollution and behavioural ecology which suggests potential impacts on life history trade-offs in reproduction, genetic changes in populations, and population sizes. Many reproductive behaviours of ®sh species are readily quanti®able and behaviours such as courtship by male guppies and other members of the Poeciliidae show some promise for pollution monitoring and behavioural toxicity tests. Choice of such assays would have to compete with the sensitivity and practicality of more traditional methods but may serve as useful complements. There is considerable scope for further research into conservation. A synthesis between behavioural ecology and toxicology should thus provide useful insights for both ®elds. Introduction Evidence of the state of many major British rivers during the reign of George III (1760 ± 1820) was made apparent by a letter reportedly written by a member of Parliament to the Prime Minister. The letter complained about the odour and appearance of the River Thames. It was written not in ink, but with water from the Thames itself (Strandberg, 1971). Historically, the Thames had been a major salmon river but towards the end of the 18th century, ®sh species had declined dramatically and large areas of the river became devoid of ®sh altogether (Wood, 1982). This was typical of many rivers in heavily populated areas of Europe. Fish populations are vulnerable because the aquatic environment is the recipient of virtually every form of human waste (Moyle and Leidy, 1992). The IUCN (International Union for Conservation of Nature) Red List (1996) records 734 ®sh species as threatened and 92 species as extinct worldwide. Water pollution is one of several contributors to such declines in ®sh populations (Clark, 1992; Moyle and Leidy, 1992; Lawton and May, 1995; Maitland, 1995). Pollution can be de®ned as ``the presence in the environment, or the introduction into it, of products of human activity which have harmful or objectionable effects'' (Oxford English Dictionary, CD-ROM). Studies of ®shes have ®gured prominently in pollution research, particularly in sublethal physiological effects (review: Kime, 1995). Many studies focus on reproduction because this is one of the most vulnerable periods in the life cycle of ®shes (Gerking, 1980; Little et al., 1985). Recently there has been development towards the use of behaviour in toxicological research (Little et al., 1985; Dùving, 1991; Smith and Logan, 1997). This represents a fusion of the ®elds of behaviour, ecology, toxicology and conservation biology. In this article, we present what might be termed a `prospective review'. The `review' element concerns studies that have examined impacts of pollutants on reproductive behaviour of

Effects of pollution on reproductive behaviour 465 ®shes. The `prospects' that we are interested in concern the value of integrating pollution research into the ®eld of behavioural ecology for gaining insights into water quality management and conservation of ®shes. Fish behaviour in pollution research Before focusing on reproductive behaviour speci®cally, it is instructive to consider the overall role of ®sh behaviour in pollution research. We searched Aquatic Sciences and Fisheries Abstracts ( ASFA) on CD-ROM from 1978 to 1997 for references containing various combinations of truncated search terms such as `behav ', to include various spellings and forms of the key words (e.g. `behave', `behaviour', `behavioral'). The result (Fig. 1) shows that only 13.8% of studies involving ®sh and pollution included behaviour and of these, only 1% involved reproductive behaviour as opposed to other behaviours such as attraction and avoidance. Thus, of the original 19 199 studies of aquatic pollution and ®shes, only 0.14% involve reproductive behaviour. This con®rms the impression from previous reviews of the paucity of such studies (Atchison et al., 1987; Beitinger, 1990; Dùving, 1991; Scherer, 1992). The lack of studies of reproductive behaviour in pollution research can be attributed in part to a perception that behaviour is dif®cult to measure and interpret. This makes behavioural assays less appealing than lethal toxicity tests; death is a rather de®nitive endpoint! However, behavioural responses may provide more sensitive early warnings than standard test methods (Smith and Logan, 1997), and ethologists have been making accurate measurements and analyses of many forms of animal behaviour for over 50 Reproduc* Behav* 26 152 Feed* Behav* 576 Predat* or Prey 366 Avoid* or Attract* 2641 Behav* 19 199 (No Extras) 0.1 1 10 100 % References With Pollut*, Fish* and... Fig. 1. Results of a search of the Aquatic Sciences and Fisheries Abstracts CD-ROM from 1978 to 1997 for references on pollution and various types of ®sh behaviour. Numbers beside each bar show the number of studies found for that category.

years. Furthermore, during the past 20 ± 30 years there has been a vigorous development of 5 the ®eld of behavioural ecology, which is concerned with how and Jones behaviour affects life histories, reproductive success of individuals and their interactions with the surrounding environment (Krebs and Davies, 1997). In linking the reproductive behaviour of individuals to their environment, one can explore how stressful conditions such as those caused by pollution will affect offspring production, survival, and population dynamics. We begin by reviewing the studies that have integrated the ®elds of reproductive behaviour and pollution research. The behaviours considered include courtship, spawning interactions and parental care. Studies that investigated effects of pollution on fecundity or reproductive success, or presence ± absence of spawning only, without measuring associated reproductive behaviours, are not included in this review. Based on the above ASFA search and an additional literature survey, 19 studies were found that investigated the effects of pollution on reproductive behaviour (Table 1). This total excludes a few studies revealed by the initial ASFA keywords that proved not to be relevant to this review. Courtship was studied most often, followed by parental care. The studies varied widely in selection of ®sh species and pollutant, and in the relative contribution that reproductive behaviour made to the research. Eleven of the 19 studies found a change in reproductive behaviour from the norm. It should be borne in mind that there may be a publication bias towards signi®cant effects of pollutants. Studies investigating parental care have found either no effect, decreased nest-building or egg-directed activity, decreased protection of the young, disruption to care or changes in division of parental care between the sexes. Effects on courtship ranged from no effect to either decreases or increases in display frequency, increased duration of courtship and performance of male-like display behaviour by masculinized females. Additional effects reported, but without strong supporting evidence, are described in Table 1. Two contrasting cases from Table 1 illustrate the range of approaches used. C A SE S T U DY F F LU E N T 1 : M O SQ U I T O FI S H AND PA P ER M ILL E Howell et al. (1980) investigated the impact of paper mill ef¯uent on a local population of mosquito®sh (Gambusia af®nis holbrooki, Poeciliidae), in Elevenmile Creek, Escambia County, Florida, USA. This research was precipitated by observations that some females in the study area exhibited morphological signs of masculinization. Many females had developed a gonopodium, the modi®ed anal ®n used by males for internal fertilization in this family of ®shes (Figs 2 and 3). Fish from above and below the ef¯uent out¯ow were compared using histological examinations of gamete abnormalities and karyotypes. Comparisons of reproductive behaviour between the two ®sh groups were also made in the laboratory. Fish were observed in each of the following combinations: (1) three pregnant masculinized females and three normal females, (2) two masculinized females, (3) a precociously masculinized male and a normal female, (4) a precociously masculinized male, a normal male and three normal females, and (5) a normal male and a normal female. No quantitative data were recorded, but descriptions of morphology and reproductive behaviour were provided. Howell et al. (1980) showed that ®sh from above the ef¯uent discharge exhibited normal sexual expression. However, all females 13 ± 45 mm standard length, collected from below the ef¯uent out¯ow, showed some degree of gonopodial development. There was no evidence of testicular tissue, and heteromorphic sex chromosomes were absent.

Table 1. Summary of effects of pollution on ®sh reproductive behaviour Behavioural category Species Courtship Guppy Poecilia reticulata Courtship Guppy Poecilia reticulata E f f e c t s o f p o l l u t i o n 4

4 Table 1. (continued) Behavioural category Species Courtship Guppy Poecilia reticulata Courtship Fathead minnow Pimephales promelas J o n e s a n d

Courtship Courtship Orange chromide Etroplus maculatus Monochloramine Either 0.025 or 0.05 mg lÿ1 from within 24 hours of pair being placed together until spawning. Mosquito®sh Gambusia af®nis holbrooki Paper mill ef¯uent. Fish collected 6.5 km downstream of the ef¯uent output. Little courtship and no spawning occurred at 0.05 mg lÿ1 , with ®sh dying or becoming ill. Comparisons between 0.025 mg lÿ1 and No spawning at higher concentration. Hatching data not given. con- trol showed: 64% increase in length of courtship period, 34% reduction in clutch size, increased ®n¯icker by males, reduced quivering and ®n-¯icker by Not females. determined. Exposed females became masculinized. Masculinized pregnant females displayed only typical male reproductive behaviour (chasing normal and masculinized females with gonopodial swings and thrust attempts). Exposed males matured precociously and exhibited typical but more aggressive courtship. A masculinized male was dominant over a normal male. Increased courtship length may increase predation risk. An additional behaviour which increased was gill-purging. This might be misinterpreted by conspeci®es as aggression and hamper pair formation. None suggested. A comprehensive study, primarily aimed at determining suitability of behavioural toxicity for pollution monitoring. Stafford and Ward (1983) No data or analyses presented. One replicate for each combination involving 1 ± 3 masculinized or normal ®sh. Interesting ®ndings from wild-exposed ®sh merit further investigation. Howell et al. (1980) continued overleaf E f f e c t s o f p o l l u t i o n 4

Table 1. (continued) Behavioural category Species 4 Courtship and aggression Mosquito®sh Gambusia af®nis Courtship and aggression Mosquito®sh Gambusia af®nis af®nis J o n e s a n d

Male courtship Cichlid Sarotherodon mossambicus Endosulfan insecticide. Three treatments: (A) adults exposed to 0.5 ìg lÿ1 for 4 weeks; (B) juveniles exposed to 0.6 ìg lÿ1 for 9 weeks (with 1.5 ìg lÿ1 for ®rst 3 days); (C) juveniles exposed to either 0.6 or 0.2 ìg lÿ1 for 6 weeks. (A) No effect on adult male sexual behaviour of female clutch production or mouthbrooding time. (B) Onset of juvenile male sexual behaviour and female clutch production delayed. Females had higher clutch production rates but lower retention times than controls, suggesting that clutch abortion was occurring. (C) More control males showed normal breeding behaviour between days 36 and 42 than exposed males. Many fry died at low exposure concentration (24 hour LC50 was 0.5 ìg lÿ1 ). Delayed breeding displays in newly maturing males may explain a reduction of approximately 75% in nests of related Tilapia rendalli in the Okavango Delta, Botswana. Concentrations were similar to those found in the wild soon after spraying. Additional direct physiological effects noted on ®sh. Matthiessen and Logan (1984) continued overleaf E f f e c t s o f p o l l u t i o n 4

4 Table 1. (continued) Behavioural category Species Nest building Cichlid Tilapia rendalli Parental care Threespine stickleback Gasterosteus aculeatus J o n e s a n d

Parental care Naked goby Episodic Gobiosoma hypoxia. bosc Field; down to ,0.5 mg l Laboratory; down to Males guarded their eggs and nests until the dissolved oxygen level reached almost lethal levels (0.15 ± 0.6 mg lÿ1 ), when 0.15 mg l abandoned. ÿ1 ÿ1 Parental care Bluegill sun®sh Lepomis macrochirus Redear sun®sh Lepomis microlophus Parental care Fathead minnow Pimephales promelas Herbicides 2,4-dichlorophenoxyacetic acid and Aquathol-K sprayed on surface of lake to obtain a concentration of 4 mg lÿ1 . Sprayed water was used as a control. they Although some males abandoned nests temporarily in each treatment, there was no signi®cant difference between them. Congeners usually intruded during male absence and some egg predation was observed in all treatments. There was no signi®cant effect on male parental care (e.g. displays towards intruding males, Waterborne lead. egg fanning). Males exposed to lead 0.5 mg lÿ1 spent signi®cantly less lead for 30 days while time in activities ®sh directed towards ceilspawned. ing of nest, including preparation of substrate for eggs, and touching ceiling with dorsal pad. The eggs died if males left the nest. If the male does not leave the nest when lethal limits are being reached he will die. Not determined. Even if there are no eggs in the nest, the male will lose mating opportunities if he abandons unnecessarily. Drastic decrease in egg production by exposed females. Role of reduced parental behaviour in reproductive output unclear. Reproductive success may be reduced due to less cleaning of nest ceiling and egg mass surface. Thorough study, unusual Breitburg in incorporating both (1992) ®eld observations and laboratory experiments. None expected Sample sizes were low from herbicide (5 ± 9 males per treatexposure. ment). A possible trend towards higher rates of temporary desertion in both species and consequently effects on egg predation might prove signi®cant with larger sample sizes. Dif®cult to interpret the cause of reduced nest maintenance behaviours, i.e. an effect of lead exposure versus fewer eggs received. Bettoli and Clark (1992) Weber (1993) continued overleaf E f f e c t s o f p o l l u t i o n 4

Table 1. (continued) Behavioural category Species 4 Parental care and aggression Convict cichlid Cichlasoma nigrofasciatum Parental care Convict cichlid Cichlasoma nigrofasciatum J o n e s a n d

Parental care Bluegill sun®sh Lepomis macrochirus Di¯ubenzuron; a pesticide 2.5 ìg lÿ1 and ÿ1 30 ìg l applied twice, ®rst application into the designated ®sh enclosures 2 months after ®sh introduced and second application 1 month later. No effects on male reproductive behaviour observed. None due to behaviour. Only one spawning event was observed in all exposure treatments (30 ìg lÿ1 ) but most spawning events (86%) took place prior to exposure. Spawning appeared to be more in¯uenced by water temperature than di¯ubenzuron exposure. Reduced juvenile growth rates. Reduced juvenile growth could have major impolications for ®sh survival during winter through starvation and increased predation risk. No statistical analysis Tanner and was performed and only Hoffett 2 replicates per treat(1995) ment used. Reproductive behaviour effects not quanti®ed and hatching success based on one spawning event at 30 ìg lÿ1 . Most spawn- ing events took place before exposure. However, focused on ecological context of effect of pesticide exposure on natural food supply, and effects on reproductive behaviour were not intended as a main focus. continued overleaf E f f e c t s o f p o l l u t i o n 4

4 Table 1. (continued) Behavioural category Species Parental care Bluegill sun®sh Lepomis macro- chirus study took place in littoral enclosures and investigated effects on reproductive success from spawning to juvenile production. J o n e s a n d

Parental care Bluegill sun®sh Lepomis macrochirus Esfenvalerate: a pesticide 0.01, 0.08, 0.2, ÿ1 1.0 and 5 ìg l applied twice, ®rst application 1 month after ®sh introduced and second application another month later. At 1 ìg lÿ1 , one male guarding a nest with embryos rimcircled rapidly. In all enclosures except 5 ìg lÿ1 , where the adults died, rimcircling occurred both before and after exposure. None due to behaviour. Adults died at 5 ìg lÿ1 . Spawning ceased for 15 days in 1 ìg lÿ1 enclo- sure following both applications and larval mortality was observed following the second application. A reduction in juvenile growth rate was measured at 1.0, 0.2 and 0.08 ìg lÿ1 . If esfenvalerate were to be applied repeatedly biweekly at concentrations greater than 0.44 ìg lÿ1 , spawning and hence juvenile production would cease. Reduced juvenile growth could have major implications for ®sh survival over winter through starvation and increased predation risk. No statistical analysis was performed and 1 replicate per treatment was used. Reproductive behaviour effects not quanti®ed but played a minor role. The rapid rim-circling that occurred in the 1 ìg lÿ1 treatment was observed in only one male. Combined data from before and after pesticide aplication were used to calculate average hatch- ing success. Tanner and Knuth (1996) E f f e c t s o f p o l l u t i o n 4

1 Effects of pollution on reproductive Jones and Fig. 2. Normal specimens of Gambusia af®nis holbrooki collected above paper-mill ef¯uent in Elevenmile Creek, Escambia County, Florida (Howell et al., 1980; reproduced by permission of Copeia). The top ®sh is a pregnant female (31 mm standard length). The bottom ®sh is a male (25 mm standard length) showing gonopodial differentiation of the anal ®n. Masculinized females exhibited some male reproductive behaviour and males exhibited precocious development of secondary sex characters and reproductive behaviour. A physiologically normal male and female when placed together exhibited normal behaviour (see Table 1 for detailed behavioural ®ndings). C A SE S T U DY 2 : S U N FI S H A N D H E R B IC ID E Bettoli and Clark (1992) investigated the effects of herbicide exposure on nesting behaviour in bluegill sun®sh, Lepomis macrochirus and redear sun®sh, L. microlophus (Centrarchidae) in Old Monterey Lake, Monterey, Tennessee, USA. Underwater video cameras were set up near nests in the wild and ®sh were ®lmed prior to, during and after herbicide application (Aquathol-K or 2,4-dichlorophenoxyacetic acid). Some of the redear sun®sh observations were also made from the lakeside using binoculars. Speci®c behaviours such as display, spawning and egg fanning were recorded, along with incidence and timing of nest abandonment. Statistical comparisons were made between males with nests in test plots sprayed with Aquathol-K, 2,4-D or with water (control). There was no difference in the number of nests abandoned nor in the actual time of abandonment between treatments (herbicide or water sprayed). When abandonment did occur, congeners usually entered the nest to feed on eggs or fry until the male returned. Finally, frequencies of rim circling, egg fanning and agonistic behaviours of the guarding males did not differ between treatments. Bettoli and Clark (1992) concluded that these herbicides, if applied properly, cause no pronounced shift in sun®sh reproductive behaviour. 1

Fig. 3. Masculinized specimens of Gambusia af®nis holbrooki collected below a paper-mill ef¯uent in Elevenmile Creek, Escambia County, Florida (Howell et al., 1980; reproduced by permission of Copeia). (A) Immature male (15 mm SL) showing precocious anal ray elongation. (B) Mature male (17 mm SL) showing precocious gonopodium. (C) Pregnant female (23 mm SL) with a gonopodium. (D) Pregnant female (28 mm SL) with a gonopodium. (E) Pregnant female (34 mm SL) with a gonopodium. (F) pregnant female (36 mm SL) with a gonopodium. C O M PA R IS O N S BE T W E E N C AS E S T U D I E S These studies show the diversity of approaches to the study of effects of pollution on ®sh reproductive behaviour. Whereas the mosquito®sh study focused primarily on morphology, with some unquanti®ed behavioural observations, the sun®sh study was restricted entirely to reproductive behaviour. Many mosquito®sh were put into each observation tank and only one replicate of each ®sh combination was used. The sun®sh study used between ®ve and nine individually sprayed areas per treatment to study effects of herbicide exposure on ®sh in the wild. Owing to the nature of the data collected in the ®rst study, no analysis could be undertaken, while in the second study a rigorous analysis of the data was performed. However, the mosquito®sh study was concerned primarily with morphological effects, with behavioural observations comprising a small part of the research. Although the behavioural data were non-quantitative, they provide a starting point for further work.

To obtain a clearer picture of effects of pollution on reproductive behaviour, we assess various aspects of the studies carried out so far. Review of studies M O T I VAT I O N F O R R E S E A RCH Some studies were aimed towards development of a behavioural assay for toxicity testing, based on changes in behaviour such as courtship (Stafford and Ward, 1983; SchroÈ der and Peters, 1988a; Bortone et al., 1989). This information could be used in a similar vein to lethal toxicity tests, but with behavioural responses as an end point (Stafford and Ward, 1983; Little et al., 1985; Bortone et al., 1989). SchroÈ der and Peters (1988a) contended that as a behavioural assay, courtship by guppies ( Poecilia reticulata, Poeciliidae) is extremely sensitive to very low concentrations of aquatic contaminants. Stafford and Ward (1983) found orange chromides ( Etroplus maculatus, Cichlidae) also to be a suitable test organism and proposed that behavioural assays are liable to be more sensitive measures of effects of toxicants than previous methods. The aims of the other studies were less clear, but many were concerned with effects on reproductive behaviour and reproductive success (Howell et al., 1980; Matthiessen and Logan, 1984; Ryabov, 1985; SchroÈ der and Peters, 1988b; Pyron and Beitinger, 1989; Bettoli and Clark, 1992; Lorenz and Taylor, 1992a,b; Weber, 1993; Tanner and Knuth 1995, 1996; Tanner and Moffett, 1995). For example, Lorenz and Taylor (1992b) tested the hypothesis that if offspring survival is reduced in an unfavourable environment (in this case due to acid stress), then parents may reduce their care to conserve energy for future reproduction (Carlisle, 1982). This was supported by tests with convict cichlids (Cichlasoma nigrofasciatum, Cichlidae), which suffered a decrease in reproductive success. Some studies went further in hypothesizing that reduced reproductive output owing to changes in behaviour may have a detrimental effect on population numbers (Douthwaite et al., 1981; Colgan et al., 1982; Krotzer, 1990; Breitburg, 1992). Krotzer (1990) studied the effect of masculinization on the behaviour of female mosquito®sh (Gambusia af®nis af®nis, Poeciliidae). It was suggested that if females became more aggressive and less receptive to males, exposed populations in the wild could suffer. The primary aim of three studies of bluegill sun®sh by one research group was to measure effects of pesticides on reproductive success from spawning to juvenile production, with reproductive behaviour playing a very minor role (Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995). Although some studies went into greater depth on the consequences of changes in behaviour than others, the information provided by most studies could be used as a starting point towards further research. S E L E C TI O N O F S T U DY S P E C IE S A N D P O L L U TAN T Studies varied widely in species and pollutant investigated. Most of those that focused on effects on the reproductive behaviour of the ®sh chose a ®sh ± pollutant combination occurring in the wild at a site of speci®c concern. Examples include ®sh ± pollutant combinations such as mosquito®sh exposed to paper mill or kraft mill ef¯uent (Howell et al., 1980; Bortone et al., 1989), cichlids (Tilapia rendalli, Cichlidae) exposed to endosulfan insecticide (Douthwaite et al., 1981), threespine sticklebacks (Gasterosteus

aculeatus, Gasterosteidae) exposed to power station thermal ef¯uent (Ryabov, 1985), naked gobies (Gobiosoma bosc, Gobiidae) exposed to hypoxic water conditions (Breitburg, 1992) and bluegill sun®sh exposed to herbicide contamination (Bettoli and Clark, 1992). Although not all of these studies were carried out in the ®eld, such combinations were known to occur in the wild. This gives the ®ndings direct relevance to such affected areas. Other criteria may affect selection of ®sh species. For example, Weber (1993) used fathead minnows ( Pimephales promelas, Cyprinidae) because this species is a standard test species for use in aquatic toxicity studies (Denny, 1987). Fathead minnows were also used by Pyron and Beitinger (1989) to investigate the in¯uence of selenium exposure. Other ®sh may be readily available, have well-documented reproductive behaviour, survive well in the laboratory, or breed readily. These were used speci®cally in the behavioural toxicity tests. For example, the suitability of orange chromide cichlids for toxicity tests was investigated under exposure to monochloramine (Stafford and Ward, 1983) and guppies were exposed to treatment-plant wastewater (SchroÈ der and Peters, 1988a). However, these ®sh species may not encounter such pollutants in the wild. Researchers have thus sacri®ced direct relevance of the environmental situation normally faced by the ®sh for the sake of practicality and standardization. L A B O R AT WILD O RY OR Studies have differed greatly in the origin of the ®sh used and the type of exposure received. Nine of the 19 studies in Table 1 used laboratory-bred and laboratory-exposed ®sh (Colgan et al., 1982; Stafford and Ward, 1983; Matthiessen and Logan, 1984; SchroÈ der and Peters, 1988a,b; Pyron and Beitinger, 1989; Lorenz and Taylor, 1992a,b; Weber, 1993). One study used wild mosquito®sh, exposed and observed in the laboratory (Krotzer, 1990) while three used hatchery-reared bluegill sun®sh and exposed them in outdoor littoral enclosures (Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995). Five studies used wild ®sh that were exposed to the pollutant in the ®eld. Of these, three observed the ®sh in the wild: sun®sh, Lepomis macrochirus and L. microlophus (Bettoli and Clark, 1992), Tilapia rendalli (Douthwaite et al., 1981), and threespine stickleback (Ryabov, 1985). The other two observed mosquito®sh under non-polluted conditions in the laboratory (Howell et al., 1980; Bortone et al., 1989) after exposure in the ®eld. Only one study used wild ®sh (naked gobies) in both wild and laboratory exposure observations (Breitburg, 1992). Differences in the results of these studies could, in part, have arisen because of the varied background and exposure conditions of experimental ®sh. Although results may be less directly relevant to the wild, there is a bene®t in using laboratory ®sh strains compared with wild ®sh because one can eliminate the potential effects of tolerance through genetic adaptation or physiological acclimation. Tolerance to pollutants has been shown in several ®sh species, including mosquito®sh, Gambusia holbrooki (Poeciliidae) (Benton et al., 1994), rainbow trout, Oncorhynchus mykiss (Salmonidae) (Pascoe and Beattie, 1979) and central mudminnow, Umbra limi (Umbridae) (Kopp et al., 1992), as well as in other taxa (Bryan and Langston, 1992; Gustavson and Wangberg, 1995). There is considerable scope for further research into differences among wild populations in pollution tolerance.

E MP H A S I S ON R EP R O D U C T IV E B E H AV I O UR Some studies were purely behavioural (e.g. SchroÈ der and Peters, 1988a; Pyron and Beitinger, 1989; Lorenz and Taylor, 1992a). Others contained combinations of reproductive physiology, morphology and behaviour (e.g. Howell et al., 1980; Weber, 1993) while others dedicated little to effects on reproductive behaviour (Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995). Usually, only a small part of the reproductive behaviour repertoire was studied, such as courtship, spawning behaviour, nest building, parental care of eggs, or defence of newly hatched fry. Ideally, the entire reproductive behaviour repertoire should be investigated (from mate choice and courtship to egg or larval independence) to see at what stages pollution exerts an effect. Time and expense will hinder such an approach, but if the purpose is to develop a toxicity test for water quality management, full reproductive cycle studies could serve as an important ®rst step, to be re®ned by simpler, focused behavioural assays. E F FE C TS O N R E PR O D U C T IV E S U C C E SS Eleven of the studies in Table 1 considered the possible effects of a change in reproductive behaviour on reproductive success. Only three studies actually measured this directly: two found a negative effect (Breitburg, 1992; Lorenz and Taylor, 1992b) and one reported an increase in reproductive success (SchroÈ der and Peters, 1988b). The latter result should be treated with caution owing to a small sample size and inappropriate experimental design (see Table 1 and general comments under `Experimental designs', below). A possible decrease in reproductive success was inferred by Douthwaite et al. (1981), who measured the age distribution of juvenile Tilapia rendalli in the Okavango Delta, Botswana, comparing sites that had been sprayed with insecticide 2 years previously with control sites. Although few studies have measured impacts on reproductive output via behavioural changes, in some cases it was likely that any such effects would have been overshadowed by physiological problems. For example, Weber (1993) found reduced egg production in female fathead minnows upon exposure to lead. Stafford and Ward (1983) investigated the effect of monochloramine on orange chromide. At levels of 0.05 mg lÿ1 , some ®sh became ill and courtship and spawning stopped, while at levels of 0.025 mg lÿ1 , female egg production was reduced. Finally, some studies estimated effects on reproductive success without trying to establish a causal link to changes in reproductive behaviour (Tanner and Knuth, 1995, 1996; Tanner and Moffett, 1995). E X PE R I M E N TAL D ES I G N S In Table 1 most of our comments concerning experimental designs are rather critical. In fairness to the authors, we wish to emphasize two points strongly. First, many of the studies were done before biologists were fully aware of the problems of nonindependence of samples within treatments (`pseudoreplication', Hurlbert, 1984). Second, as noted earlier, a combination of physiological and behavioural effects of pollutants was investigated in some studies, sometimes with effects on reproductive behaviour appearing as a secondary objective (e.g. Howell et al., 1980). Nevertheless, to evaluate our current state of knowledge in this ®eld, it must be borne in mind that many of the studies lacked adequate controls, replication, or statistical analyses. Multiple observations of the same ®sh under the same treatment cannot be counted as separate statistical data points. One ®sh may be watched 10 times when exposed to a pollutant and another ®sh may be watched 10 times in a control situation,

but effectively this still leaves one data point (e.g. mean behaviour per ®sh) under each treatment (Hurlbert, 1984). Furthermore, 10 ®sh in one aquarium exposed to a pollutant should not be compared as 10 independent samples to ®sh in a control tank. Fish within aquaria are not independent because individuals may affect each other both behaviourally and physiologically. For example, there may be in¯uences from each other's activity levels, dominance, pheromones, or metabolic wastes. These problems apply to more traditional non-behavioural tests as well. Furthermore, aquaria are bound to differ by more than the presence or absence of the pollutant concerned. For example, levels of nutrients, light intensities, or other uncontrolled and unknown factors may confound treatments. This necessitates the use of multiple aquaria per treatment in randomized or alternating spatial patterns. If multiple ®sh or observations are used per aquarium, each aquarium should yield a single mean data point in a t-test or standard ANOVA design, or observations from individual ®sh within tanks can be used in a nested ANOVA-type design. Our general impression from the information summarized in Table 1 is that many of these early studies report tantalizing results, but the use of ®sh reproductive behaviour in pollution research is still very much in its infancy. Secondary effects of pollution Additional studies are available in the literature which measure secondary effects of pollutants on reproductive behaviour. For example, silting arises from high sediment loading, and lowered oxygen levels often result from bacterial degradation under high organic pollution (Clark, 1992; Mason, 1996). Although such studies were not included in Table 1 because they did not use pollutants directly, their results could still be useful in water quality management and conservation. Silting was found to affect parental care in the ®fteenspine stickleback (Spinachia spinachia, Gasterosteidae) (Potts et al., 1988). During parental care, males use their ®ns to fan water over their egg mass. Silting increased the number of times males fanned their eggs. Nest inspection and nest pushing also became more frequent. Lowered oxygen has also been found to affect paternal care in the threespine stickleback (Reebs et al., 1984), with an increase in the length of egg-fanning bouts. When oxygen levels fell below 2.8 mg lÿ1 , males spent more time swimming outside the nest but still fanned at intervals. In the guppy, lowered oxygen levels increased the frequency of breathing at the surface by males at a cost of decreased courtship (Kramer and Mehegan, 1981). To date, such studies have not examined consequences for reproductive success. Prospects for the future: integrating pollution and reproductive behaviour There is now a growing interest in understanding sublethal effects of pollutants on aquatic organisms (Alabaster and Lloyd, 1982; MuÈ ller and Lloyd, 1994). To evaluate the usefulness of developing this ®eld further, it is helpful to integrate general theory from behavioural ecology to clarify the biological links between behavioural responses of individuals and population changes. We can then use this information to help decide the prospects for using behavioural studies to help protect populations of the ®shes themselves, as well as developing assays for protecting other species in the habitat.

F R OM I N D I V I DUA L B E H AV IO U R T O P O P U L AT I O NS 2 Jones and Figure 4 is a schematic diagram of behavioural testing procedures, responses of the animals, and potential uses for this information. Nearly all of the studies reviewed are concerned with step 1, which links reproductive behaviour of ®shes and their exposure to sublethal doses of the contaminant in question. As we have seen, few of the studies have gone on to step 2, from reproductive behaviour to reproductive success, and these have been concerned only with current broods rather than impacts on subsequent reproductive bouts. We have not found any studies that take the `®nal' step (step 3) of testing for population responses, although there was circumstantial evidence of a decrease in the numbers of Tilapia rendalli in the Okavango Delta in two areas sprayed with endosulfan insecticide (Douthwaite et al., 1981). Below, we discuss the logic and potential of these under-developed steps. Effects on future reproductive success Life history theory, supported by a large body of empirical research on a variety of taxa, suggests that commitment of resources to a given reproductive bout should have costs for survival, growth, or reproduction in subsequent bouts (Williams, 1966; Roff, 1992; Stearns, 1992; Sargent and Gross, 1993). If this were not true, animals could make huge investments in reproduction forever (Partridge and Harvey, 1985). An example from ®shes concerns male bluegill sun®sh, which have been induced to ventilate their eggs by fanning water across them more frequently when given larger broods experimentally (Coleman et al., 1985). Increased fanning reduces the time available to males for courting new females, and it reduces energy reserves through the loss of non-polar lipids (Coleman and Fischer, 1991). This may impair survival and future reproduction. Such reproductive trade-offs may be most evident under conditions of stress (Roff, 1992). For example, in the sand goby ( Pomatoschistus minutus, Gobiidae), females that initially produced large clutches before receiving a low food ration produced smaller clutches in the next bout (Kvarnemo, 1997). This trade-off did not occur with high food. Thus, environmental stressors such as pollutants could have delayed effects on reproduction which would be overlooked if only a single reproductive cycle were studied. Population size Links between individual behaviour and population biology have been much sought-after by ecologists (Sibly and Smith, 1985; Sutherland, 1996). In theory, any external force that alters behaviour of individuals from the optimum under natural and sexual selection could lead to reduced population sizes. But this effect may be far from straightforward, depending on the nature of density dependence in the population. For example, Lorenz and Taylor (1992b) showed that under conditions of low pH, convict cichlids were less able to rear their young in the presence of conspeci®cs. But if population densities of these ®sh were restricted by food or predation at a different stage of life, reduced survival of young being guarded by parents may have no impact on population size. The dif®culty of showing relationships between reproduction and population size is well known to ®sheries biologists who rarely ®nd clear patterns between stock size and recruitment (Hilborn and Walters, 1992; King, 1995). Thus, if one is concerned with conservation, a major challenge is to demonstrate clear effects of sublethal doses of pollutants on population size.

TESTS EXPOSURE USES Fish exposed to sublethal dose 1 Monitoring water quality 4 Protection of other species and habitat Effect on reproductive behaviour? ORGANISM RESPONSE 2 5 Effect on current and future reproductive success? 6 3 7 Conservation of the test fish species Effect on population? POPULATION RESPONSE Number of changes Genetic individuals Adaptation Fig. 4. Schematic diagram showing hierarchy of pollution effects on reproductive behaviour and the potential uses for such information. Circled numbers are reference points for discussion in the text. E f f e c t s o f p o l l u t i o n 4

Genetic changes 2 Effects that change on reproductive Jones Environmental impacts of pollution the reproductive behaviour of individuals (e.g. choice and of mate or oviposition site) could alter the genetic composition of populations. An example from a natural environmental parameter concerns the effects of light levels on behaviour of Trinidadian guppies (Reynolds, 1993). Under low light levels, large-bodied males have higher mating success than smaller ones, because of female choice. This pattern is reversed under higher light levels, when males may be hampered by greater risk of predation. Because male body size has a genetic basis (Reynolds and Gross, 1992), such changes in mating behaviour in response to an environmental change may have genetic consequences for the population. Genetic changes such as these have yet to be shown in the context of pollution, but given the numerous demonstrations of heritability of traits under natural selection (Falconer, 1989) and sexual selection (Pomiankowski and Mùller, 1995; cf. Alatalo et al., 1997), researchers would be well advised to bear these possibilities in mind. Adaptation Long-term selection may lead to the evolution of resistance. This depends on the intensity of selection, additive genetic variance in resistance and the population size. Benton et al. (1994) provided an example in a comparison of populations of freshwater snails ( Helisoma trivolvis, Planorbidae) and mosquito®sh from a relatively clean site and a site contaminated with a variety of heavy metals and other elements. They found that in the populations exposed to the pollutants, both species may have evolved increased tolerance. In mosquito®sh, this tolerant genotype seems to be linked to small body size. Particularly relevant here is the possibility that altered mate choice, courtship or parental care could be adaptive, leading to a buffering against environmental change. This could occur either through short-term, facultative changes in behaviour or through genetic responses to selection. This is a risky proposition, because changes in behaviour could be non-adaptive, and genetic adaptations may not evolve quickly enough. Furthermore, genetic bottlenecks and inbreeding are risks when the effective population size is reduced owing to fewer individuals reproducing (Meffe, 1986). USES OF STUDIES R E P R O D U C TI VE BE H AVI O U R Aside from gaining a better understanding of pollution in an ecological context, what direct practical uses can be made from the framework in Fig. 4? We believe the answers depend on whether one is concerned with development of general assays for protecting water quality for other species and the habitat, or with conservation of the particular species under study. Behavioural assays for protecting other species and habitats Toxicity tests may be used to screen new chemicals, and to formulate water quality criteria and standards (Council of the European Communities, 1978; Alabaster and Lloyd, 1982; Abel, 1989; Lloyd, 1992; Howells, 1994). Standardized protocols for toxicity tests, for example LC50 tests using guppies or Daphnia magna (Daphniidae), or life-cycle tests using salmonids, are often used (Alabaster and Lloyd, 1982; Lloyd, 1992; Howells, 1994; Mason, 1996). Toxicity tests are also used to assess hazards presented by ef¯uents, for example from industry or sewage treatment works. Such monitoring of ef¯uent is 2

especially useful when substances are dif®cult to analyse or where a concoction of substances is present (Alabaster and Lloyd, 1982). Whether the objective is to monitor ef¯uent water quality (arrow 4 in Fig. 4) or formulate water quality criteria or standards (arrow 5), the ideal protocol involves a species that can be reared quickly and easily, with a minimum of equipment and space, and which responds quickly to the testing procedure, in a highly repeatable manner (Alabaster and Lloyd, 1982; Smith and Logan, 1997). Given these requirements, it seems unlikely that many of the ®sh species and reproductive behaviours reviewed in Table 1 will be practical for general use. We suggest that the species that come closest might be poeciliids such as the guppy (already a standard test species for traditional toxicity tests) and mosquito®sh (Gambusia spp.). They are small and breed readily in captivity, and male courtship is easily quanti®able and occurs under a wide variety of circumstances (Farr, 1980; SchroÈ der and Peters, 1988a; Reynolds et al., 1993; Houde, 1997). Rice®sh (Oryzias latipes, Cyprnodonitidae) and killi®sh ( Fundulus, Cyprnodonitidae) are also worth exploring, although their courtship behaviour is less elaborate than in guppies. Female poeciliids have already been shown to undergo physical, and to a less extent behavioural, masculinization as a result of exposure to paper mill ef¯uent (Howell et al., 1980). It would be interesting to see whether the opposite effect ± feminization ± occurs during exposure of males to oestrogenic compounds, and whether changes in courtship could yield an early warning system for such pollutants (Purdom et al., 1994; Sumpter et al., 1996). Overall, it remains to be seen whether courtship by ®shes yields an improvement in sensitivity, practicality, and cost over existing methods. This is well worth exploring, particularly as automated behavioural monitoring techniques using videos and computers become increasingly advanced. Conservation Studies of impacts of pollutants on reproductive behaviour may be more important for understanding conservation of the test ®sh themselves (arrows 6 and 7 in Fig. 4) than as general assays for monitoring water quality and recommending criteria on behalf of other species. Such studies could complement, rather than replace traditional studies of effects on physiology and survival. The ecological framework presented (Fig. 4) suggests several reasons for focusing on reproductive behaviour. For example, behavioural studies of the impacts of oestrogenic compounds might yield insights into reproductive output in species where males provide parental care. Indeed, parental care itself, including egg guarding and ventilation, places high energetic demands on ®shes, which often lose weight during parental cycles (Sargent and Gross, 1993; Smith and Wootton, 1995). Pollutants may exacerbate these costs, as well as costs from sexual selection, including predation, courtship, territoriality, mating competition, and mate choice (Magnhagen, 1991; Andersson, 1994; Reynolds and CoÃteÂ, 1995). One or more forms of such mating competition are widespread in ®shes. Although there are numerous routes towards reduced offspring production in current and future breeding attempts (Fig. 4), we need more research on these to explore properly their links to conservation. Empirical justi®cation for focusing on reproductive behaviour comes from a recent survey of conservation of ®shes (Bruton, 1995). Cross-species comparisons suggested that ®sh with more complex reproductive behaviours are particularly at risk. Parental

care is found in 21% of teleost ®sh families (Gross and Sargent, 1985), and is particularly common in species breeding in fresh water, estuaries, and coastal marine environments. These are also the habitats that receive the greatest inputs of pollutants (Clark, 1992; Mason, 1996). Conclusion The study of effects of pollution on reproductive behaviour of ®shes has yielded some clear effects on courtship and partental care for several species, but few studies have gone far enough to draw clear inferences for effects on populations. As a tool for biomonitoring or use in water quality criteria, such studies are unlikely to be able to compete with standard toxicity tests, although they may complement them effectively, especially since there is evidence of strong sensitivity to pollutants. From the standpoint of conservation of populations of the ®shes themselves, it would be useful to explore further the links between alterations in reproductive behaviour, reproductive output, and the mechanisms that govern population dynamics. Such an integration of behavioural ecology with pollution research may provide useful insights for both ®elds. Acknowledgements We wish to thank W. Mike Howell for the photographs used for Figs 2 and 3 and for comments on the manuscript. We also thank Mike Elliott, Alastair Grant and Peter Matthiessen for helpful discussions and Nick Dulvy, Paul Hart, David Kime, Carl Smith and two anonymous referees for comments on the manuscript. References Abel, P.D. (1989) Water Pollution Biology. Chichester: Ellis Horwood Ltd. 231 pp. Alabaster, J.S. and Lloyd, R. (1982) Water Quality Criteria for Freshwater Fish, 2nd edn. London: Butterworths. Alatalo, R., Mappes, J. and Elgar, M.A. (1997) Heritabilities and paradigm shifts. Nature 385, 402 ± 403. Andersson, M. (1994) Sexual Selection. Princeton: Princeton University Press. 599 pp. Aquatic Sciences and Fisheries Abstracts. London: SilverPlatter International. Atchison, G.J., Henry, M.G. and Sandheinrich, M.B. (1987) Effects of metals on ®sh behavior: a review. Env. Biol. Fishes 18, 11 ± 25. Beitinger, T.L. (1990) Behavioral reactions for the assessment of stress in ®shes. J. Great Lakes Res. 16, 495 ± 528. Benton, M.J., Diamond, S.A. and Guttman, S.I. (1994) A genetic and morphological comparison of Helisoma trivolvis and Gambusia holbrooki from clean and contaminated habitats. Ecotoxicol. Env. Safety 29, 20 ± 37. Bettoli, P.W. and Clark, P.W. (1992) Behavior of sun®sh exposed to herbicides: a ®eld study. Env. Toxicol. Chem. 11, 1461 ± 1467. Bortone, S.A., Davis, W.P. and Bundrick, C.M. (1989) Morphological and behavioral characters in mosquito®sh as potential bioindication of exposure to Kraft mill ef¯uent. Bull. Env. Contam. Toxicol. 43, 370 ± 377. Breitburg, D.L. (1992) Episodic hypoxia in Chesapeake Bay: interacting effects of recruitment, behavior, and physical disturbance. Ecol. Monogr. 62, 525 ± 546.

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