Behavioural Ecology of Reproduction in Fish ELISABET FORSGREN, JOHN D. REYNOLDS AND ANDERS BERGLUND

10 Behavioural Ecology of Reproduction in Fish ELISABET FORSGREN, JOHN D. REYNOLDS AND ANDERS BERGLUND

10.1 GENERAL

behaviour and responses of populations to human

INTRODUCTION

exploitation. Our review is mainly restricted to teleost fishes and is biased towards species with

Fish exhibit an enormous diversity of reproductive parental care, for the simple reason that most of behaviour. Indeed, this diversity far exceeds that the present-day knowledge on these issues comes found in birds, mammals, reptiles or amphibians. from studies of such species. Our chapter comple- For example, forms of parental care range from ments many of the others in this volume, espe- none at all in the majority of fish species, to live- cially the review of life histories by Hutchings bearing, mouth brooding or biparental guarding (Chapter 7, this volume), which covers alterna- of free-swimming young. Courtship behaviour is tive life histories stemming from reproductive also diverse, with either males or females being the conflict. dominant competitor when attracting the oppo- site sex. Social behaviour also varies greatly, from extended monogamy to promiscuity, from co-

10.2 INTRODUCTION TO

operative breeding to solitary nesting, from group

BREEDING SYSTEMS

spawning to pair spawning. Finally, fish also ex- hibit at least five major forms of hermaphroditism, The term ‘breeding system’ (or mating system) including self-fertilization, which is unique is used when describing an animal’s mating among vertebrates.

behaviour and parental care (Emlen and Oring

In this chapter we attempt to make sense of this 1977; Reynolds 1996). It applies to groups of diversity in reproductive behaviour by using gen- animals, including populations or species. eral concepts from the field of behavioural ecology. Breeding system classification focuses on varia- This approach focuses on the individual, examin- tion in various kinds of behaviour. These typically ing costs and benefits resulting from interactions include: with other individuals and the environment in

1 form and duration of parental care by each sex; order to make inferences about evolution. First, we

2 form and duration of any pair bonds; give a brief theoretical background to the under-

3 number of mates (both ‘genetic’ and ‘social’); standing of breeding systems. Then we use this to

4 forms of courtship, coercion and competition explain the diversity of parental care and sexual se-

(including competition among sperm from dif- lection in fishes. The latter emphasizes differences

ferent males);

between the sexes in courtship roles, competitive-

5 breeding resources defended and offered; ness, mate choice and numbers of mates. This

6 extent of mate choice (including choice among leads to the last section on links between breeding

sperm from different males).

Chapter 10

10.2.1 sex (reviewed in Kvarnemo and Ahnesjö 1996). A general framework

The more females a male can fertilize, the higher The fundamental difference between the sexes is his reproductive success will be. In females, on the size of the gametes. Females produce few, large the other hand, reproductive success is normally eggs, whereas males produce a vast number of tiny related to access to resources and not to the num- sperm. Sperm is a rapidly renewable resource, and ber of mating partners. Thus, the lifetime repro- males of most species could presumably fertilize ductive success of males is limited by access to hundreds of females over their lifetime if given the females, while females are not limited by access chance. Females, in contrast, must devote con- to males. This difference between the sexes leads siderable time and energy to each ovum before to an imbalance in the number of individuals of fertilization. In some species, the basic difference each sex that are ready to mate, termed the ‘opera- between the sexes is further increased through tional sex ratio’ (Emlen and Oring 1977). Typically, parental care. Female mammals, for example, usu- the operational sex ratio is male-biased because ally devote more of their time and energy to care of males are recycling into the mating pool faster offspring than males do. As a result, the potential than females. Thus, there is an excess of males and rate of reproduction is much lower in females than

a shortage of females willing to mate at any given males. The potential reproductive rate is defined time. This has profound implications for sexual as the number of independent offspring that could selection. It would pay males to compete for and

be produced per unit time by members of one sex if court as many females as possible, whereas fe- given unlimited access to members of the opposite males can afford to be more selective of their

Females Cheap gametes, Environmental

Males

Potential rate of

reproduction

shareable care, Expensive

or no care

constraints

constraints

gametes, no care

Intense mating

Weak mating competition

Less selective More selective in mate choice

in mate choice

Aggregation of

Sex ratios

resources and mates

Environment

Fig. 10.1 Framework for understanding breeding systems, based on a ‘typical’ fish where females do not provide parental care. The upper boxes under each sex indicate time or energy devoted to offspring (gametic development and parental care). Differences between the sexes cause a disparity in potential reproductive rates, which in turn leads to a male-biased operational sex ratio (OSR). The operational sex ratio affects mating competition and choosiness (lower boxes). Thus, sexual selection acts more strongly on males. The environment can affect potential reproductive rates and operational sex ratios. (Source: after Reynolds 1996; reproduced by permission of Elsevier Science.) Fig. 10.1 Framework for understanding breeding systems, based on a ‘typical’ fish where females do not provide parental care. The upper boxes under each sex indicate time or energy devoted to offspring (gametic development and parental care). Differences between the sexes cause a disparity in potential reproductive rates, which in turn leads to a male-biased operational sex ratio (OSR). The operational sex ratio affects mating competition and choosiness (lower boxes). Thus, sexual selection acts more strongly on males. The environment can affect potential reproductive rates and operational sex ratios. (Source: after Reynolds 1996; reproduced by permission of Elsevier Science.)

10.1, which exemplifies the breeding system of a typical fish. In fish, males are most often the sex providing parental care (see Section 10.3). How- ever, they can often care for several clutches simultaneously, retaining a higher potential repro- ductive rate than females. Thus, despite providing parental care, males still have much to gain from competing with each other for mates and courting females.

10.2.2 Role of the environment

The environment can influence mating systems and sexual selection in several ways. It may, for example, influence the costs and benefits of time and energy devoted to different activities. Many studies have shown that predation pressure can reduce the intensity of sexual selection, either by relaxing mate choice (e.g. Forsgren 1992) or by in- creasing the costs of attracting a mate. This shifts the optima for ornamental traits and courtship towards less conspicuous forms, exemplified by studies of Trinidadian guppies, Poecilia reticulata (reviewed in Endler 1995; Houde 1997). Predation pressure may also play a key role in the provision of parental care. It may increase the benefits to the offspring of receiving parental care, as well as the costs to the parents of providing it. In the bi- parental convict cichlid, Cichlasoma nigrofascia- tum , males sometimes desert their broods and this happens most often at sites with the lowest brood predation pressure (Wisenden 1994). Environmen- tal factors can also affect the operational sex ratio, which in turn can have strong effects on mating competition and mate choice. For example, differ- ential mortality rates between the sexes can bias the operational sex ratio towards the sex least prone to predation. Males of the viviparous Amar- illo fish, Girardinichthys multiradiatus, are more often caught by snakes than are females, biasing the sex ratio towards females (Macías Garcia et al. 1998). The operational sex ratio can also be affect-

ed by temperature through differential effects on the potential reproductive rates of the two sexes (Kvarnemo 1994; Ahnesjö 1995). Egg-guarding male sand gobies, Pomatoschistus minutus, have a

much faster potential reproductive rate in warm water when egg development is faster, while the fe- male potential reproductive rate is not so strongly affected by temperature (Kvarnemo 1994). Thus, warmer water ‘causes’ more fighting in male gobies (Kvarnemo 1998).

Another important component of the environ- ment is the spatial and temporal distribution of resources critical for breeding. If these are economically defendable, there are greater oppor- tunities for polygyny (Emlen and Oring 1977). For example, if large numbers of female bluehead wrasse, Thalassoma bifasciatum, arrive at a spawning site on a coral reef, the dominant male is unable to defend all females and additional males participate in spawnings (Warner and Hoffman 1980). Likewise, in the Japanese medaka, Oryzias latipes , the highest variation in male mating suc- cess was found when females arrived asynchro- nously (Grant et al. 1995). Similarly, if resources such as nest sites are spatially aggregated and therefore can be defended by a single male, this male can attract more mates than if the nesting sites were widely dispersed and hence impossible to monopolize. This has been shown in experi- ments with the sand goby, a species which exhibits male parental care in defended nest sites. Polygyny and the potential for sexual selection were highest when nest sites were large and females arrived asynchronously (Lindström and Seppä 1996). In the same species, nest abundance has implications for the mode of sexual selection. In areas with few nest sites, male competition is strong and the po- tential for female choice is low, while the opposite is true in areas with a high availability of nest sites (Forsgren et al. 1996a). In a field study of the slimy sculpin, Cottus cognatus, Mousseau and Collins (1987) found that the abundance of nest substrates in lakes seemed to affect whether a population was monogamous (many sites) or polygynous (few sites). The importance of ‘environmental con- straints’ is indicated in two places in Fig. 10.1; en- vironmental factors may affect each sex’s potential rate of reproduction or may directly affect the operational sex ratio. This can have profound implications for sexual selection.

Behavioural Ecology of Reproduction

227

Chapter 10

and Wootton 1995; Sargent 1997). Care-giving may

10.3 PARENTAL CARE

increase predation risk due to conspicuousness or reduced agility. In a pipefish, Nerophis ophidion,

Parental care can be defined as any behaviour that where males brood their young on their body, increases the fitness, defined in terms of develop- parental males were much more likely to be preyed ment and survival, of an animal’s offspring (see upon than non-caring males (Svensson 1988). Car- Clutton-Brock 1991). This should be in the inter- ing can also be energetically costly or reduce feed- est of the parent but, as we shall see, engaging in ing, leading to deterioration in body condition and parental care may not be as straightforward as one thereby increasing the risk of death through dis- might think.

ease or starvation. In the river bullhead, Cottus gobio , body condition of parental males declined

10.3.1 Diversity of care in fish

over the breeding season and this may have ac- counted for a peak in male mortality observed

Fish vary substantially in their parental care. A during the second part of the breeding season complete lack of care is most common, followed (Marconato et al. 1993). Caring may also be costly by paternal care, biparental care and maternal care by extending the time to next breeding or by (Blumer 1982). Parental care occurs in about 20% reducing future fecundity. In an experiment with of all teleost families and is widely distributed phy- Galilee St Peter’s fish, Sarotherodon galilaeus, a logenetically. However, it is more common among biparental mouth brooder, parental care has been freshwater than marine families (Blumer 1982). shown to decrease growth and increase the num- Among fish with parental care, male care is most ber of days until the next reproductive cycle in common, occurring in two-thirds of the families both males and females (Balshine-Earn 1995). In (Gross and Shine 1981). The forms of care provided addition, care also decreased subsequent fecundity by fish are also diverse, from defence of eggs to in females. Care can also be costly to males in more advanced forms such as guarding and feeding terms of lost mating opportunities (see Section of the larvae after hatching. The most common 10.3.3). form of parental care is brooding the eggs on a sub-

Parents may sometimes consume their proge- stratum. In this case, care may consist of actions ny, which is termed ‘filial cannibalism’ (Rohwer

directed at the eggs, such as fanning them to pro- 1978) and is especially prevalent in fish (Dominey vide oxygen, and defence of the eggs against preda- and Blumer 1984). Consumption may include the tors. Other types of care are mouth brooding and whole clutch or only part of it. Filial cannibalism carrying the eggs, externally or internally. Com- in fish with parental care is now viewed as an prehensive overviews of parental care in fish have adaptive behaviour that maximizes the parent’s been provided by Blumer (1982) and Gross and lifetime reproductive success, instead of as an Sargent (1985).

abnormal behaviour (FitzGerald 1992). Caring males may compensate for the costs of care by can-

10.3.2 Costs of care and

nibalizing part of their progeny in order to remain

filial cannibalism in sufficient physical condition to complete care of

the current brood (Marconato et al. 1993) or to Parental care is often costly in terms of reducing

be able to care for future broods (Rohwer 1978). the parent’s residual reproductive value, defined as Guardian males may also eat their entire clutches, its expected future reproductive success. These fit- especially when these are smaller than usual and ness costs are difficult to measure (Clutton-Brock the value of the clutch is lower than the costs of 1991) but can sometimes be approximated by mea- care (Petersen and Marchetti 1989). In a feeding ex- surements of time and energy devoted to care. In periment with the common goby, Pomatoschistus fish, there are a number of ways in which parental microps , which exhibits paternal care, whole care can be costly to the parent (reviewed in Smith clutch cannibalism was associated with unusually

Behavioural Ecology of Reproduction

small clutches, while partial clutch cannibalism fore, the cost for a female of providing care may be was associated with a low feeding regime considerable in terms of lowered future fecundity. (Kvarnemo et al. 1998). Cannibalism by guarding In males, reproductive success is usually not males may generate conflicts of interests between equally strongly related to size. Thus, males would the sexes, and adds another factor that females not pay such a high ‘fecundity cost’ as females by should take into account when choosing a mate.

providing care (Sargent and Gross 1993). If, how- ever, males lose opportunities for additional mat-

10.3.3 ings by providing care, this could be very costly for Who cares?

them. However, in substrate-spawning fish with Which sex should provide care? This depends on egg guarding, males can usually care for clutches sex-specific costs and benefits of care. If parental from several females simultaneously. Thus, males care can be provided by a single parent alone, both are able to court and attract multiple mates and sexes would gain the same benefits from being the provide care at the same time. Important in this sole care-giver, provided that the male has not been context is that guarding of eggs is often ‘shareable’, cuckolded. However, the costs of providing care meaning that it is no more energetically demand- may differ between the sexes, and this difference ing to defend a nest containing thousands of eggs may explain why male care is common in fish than a nest containing only a few eggs. In other taxa (Sargent and Gross 1993). The costs of care are like mammals and birds, the investment in off- related to the options available to each sex if it did spring is substantial and less shareable among off- not engage in parental care. In fish, female fecun- spring. This may explain why uniparental male dity is often closely related to body size (Hutch- care is much more common in fish than in birds ings, Chapter 7, this volume). Thus, it is important and mammals. Furthermore, females in many for females to allocate resources to growth. In addi- species of fish prefer nests containing other fe- tion, females have to produce costly eggs. There- males’ eggs (reviewed by Reynolds and Jones 1999).

(a) Biparental

Male + female +

Female Male

no care

no care

1.6 0.2 No care 79.4

Fig. 10.2 (a) Hypothetical evolutionary transitions (arrows) between parental care states in teleost fishes. Numbers in boxes show the percentages of the 422 families surveyed by Blumer (1982) that have various forms of care. Circles show families that exhibit more than one form of care. (Source: after Gross and Sargent 1985; reproduced by permission.) (b) Evolutionary transitions between biparental care and female care among Cichlidae, based on 182 genera. Figures show number of transitions and arrow widths are proportional to this number. (Source: after Goodwin et al. 1998.)

Chapter 10

Evolutionary changes in the amount of parental care provided by each sex have been reviewed for fish and compared with other vertebrates by Reynolds et al. (2002). Figure 10.2a shows hypothe- sized directions of transitions for fish based on a review by Gross and Sargent (1985). It has been suggested that male care has most often evolved from no care. Then females may, in some cases, be selected to join males due to selective advantages of biparental care. Biparental care might be unsta- ble if males are then selected to desert their mates in search of new mating opportunities, which may

be the case in mouth brooders where multiple clutches cannot be cared for simultaneously. The benefits and costs associated with this decision have been explored in a game-theory framework (Maynard Smith 1977), including a model devel- oped specifically for cichlid fishes (Balshine- Earn and Earn 1997). Indeed, studies of fish have provided the first experimental evidence demon- strating that males do desert broods in response to the availability of new mating opportunities (Keenleyside 1983; Balshine-Earn and Earn 1998). Female care, too, may be unstable through evolu- tionary time if the benefits are outweighed by the costs of uniparental female care, expressed as de- creased survival and fecundity. This leads to the interesting proposition that parental care may be a cyclical phenomenon, at least in species where the costs of care are substantial and roughly equal for both sexes (Gross and Sargent 1985). The hypothe- sis that maternal care follows biparental care was supported by Goodwin et al. (1998), who examined evolutionary transitions in cichlid fishes (Fig. 10.2b). In cichlids biparental care seems to be the ancestral state, and female care is the most com- mon form of uniparental care.