REPRODUCTIVE BEHAVIOUR AND Change LIFE HISTORIES

10.6 REPRODUCTIVE BEHAVIOUR AND Change LIFE HISTORIES

Fecundity

(b)

Reproductive behaviour is intimately linked with

Polygyny potential low

life histories because the time and energy devoted to mating behaviour and parental care usually incur costs in terms of decreased future survival and fecundity. It is a matter of semantics whether one considers parental care to be a component of life histories. Below we address briefly some areas of reproductive behaviour that have close links to life histories. Life histories are reviewed in detail

Change in Hutchings, (Chapter 7, this volume).

Age or size

10.6.1 Sex change

Fig. 10.5 The size-advantage model of sex change. (a)

and hermaphrodites

When only large males can defend resources or females, it pays to start life as a female and change sex when a

Many coral-reef fish and some temperate species competitive size/age is reached (protogyny). (b) When are sequential or simultaneous hermaphrodites. there is a low potential for polygyny, female fecundity Sequential hermaphrodites may change sex from usually increases more rapidly with size than male

male to female, female to male, or both ways. fecundity. It pays to start out as male and change to female when reaching some size/age threshold

Simultaneous hermaphrodites produce eggs and (protandry). These scenarios assume that costs of sperm at the same time and may either cross- or changing are not prohibitive. (Source: after Berglund self-fertilize. This feature of life histories could be 1997; © Oxford University Press 1997.)

Behavioural Ecology of Reproduction

among males for females, small males may be at a behaviour called egg trading. Eggs are more strong disadvantage. Then it may pay individuals expensive to produce than sperm, so a pair benefits to start out as females and remain so until they from sharing the heavy task of egg production, reach a sufficient size to compete successfully as taking turns spawning as a male and as a female. males (Fig. 10.5a). At this point the gains from However, if a ‘female’ allows its partner to play the reproducing as a male outweigh the lower-risk, ‘cheap’ male role, how can ‘she’ know that ‘she’ lower-benefit option of reproducing as a female, can be a ‘he’ next time? In other words, how is including the time and energy costs of switch- reciprocation achieved in this obvious conflict ing over their gametic function. So they switch to between the sexes? This is a classic problem in males. Experiments have shown that when domi- studies of human social conflict, known as the nant males are removed, the largest female in an Prisoner’s dilemma (Axelrod and Hamilton 1981). assemblage may initiate sex change within hours It falls in the domain of game theory, because an and become fully functional within days (Ross individual’s best response depends on what others 1990).

in the population do (see also discussion of game

Protandry, in which sex changes from male to theory by Hannesson, Chapter 12, Volume 2). female, usually occurs in species where sexual Hamlets, Hypoplectrus nigricans, have solved this selection through male–male competition is less dilemma in the same way that a computer tourna- important, for instance when breeding resources ment eventually solved it, using the ‘tit-for-tat’ are less aggregated. Individuals are then selected to strategy, i.e. always start by cooperating and then switch from male to female when the benefits do what your partner did in the previous round of higher fecundity associated with larger body (Fischer 1980; Leonard 1993). Each member of the size outweigh the benefits of remaining a male pair takes turns acting as a female and as a male. By (Fig. 10.5b). This has been suggested to explain allowing a male-acting fish to fertilize only a protandry in the anemonefish Amphiprion small parcel of eggs (egg trading) and then with- akallopisos (Fricke 1979). If the female of a pair holding eggs unless the other individual recipro- is removed, the top-ranking male changes into a cates by acting female, any loss due to cheating is female and the next highest ranking male (or an reduced (Fischer 1980). immigrant if there are no more males) fertilizes

There is one species of self-fertilizing her- the eggs (Fricke and Fricke 1977).

maphrodite, the killifish Rivulus marmoratus

Some goby species take the elements of the size- (Cyprinodontidae). Indeed, this is the world’s only advantage model one step further and switch in known self-fertilizing vertebrate, although pure both directions. In some species this is advanta- males and outcrossing may occur (Lubinski et al. geous if moving between territories is risky: after 1995). mate loss, a flexible attitude to sex increases part- ner availability and reduces mate search costs, as individuals can mate with whichever sex is avail- able (Nakashima et al. 1996; Munday et al. 1998).

10.7 REPRODUCTIVE

Thus, there is no sharp borderline between sequen-

BEHAVIOUR AND

tial and simultaneous hermaphroditism: when

EXPLOITATION

changing occurs rapidly we call it simultaneous hermaphroditism (e.g. St Mary 1994).

There are numerous links between the reproduc-

If a male, above some certain body size, gains tive behaviour of fish and exploitation (Vincent nothing by allocating further resources to sperm and Sadovy 1998; Reynolds and Jennings 2000). For production, he may instead allocate new resources example, fishers in many parts of the world take to egg production: we now have a simultaneous advantage of predictable spawning aggregations of hermaphrodite. Male size advantages may be fish, and managers often incorporate this informa- circumvented by low mate encounter rates and a tion into their plans. Reproductive behaviours

Chapter 10

may affect the vulnerability of fish to capture, as ringens , the Canadian cod and Atlantoscandian well as the resilience of populations in responding herring, which have all experienced crashes to exploitation. Other forms of exploitation, such largely due to overfishing. Large species of as fish farming and sea-ranching, may also affect groupers in the Indo-Pacific may aggregate in the fish populations. Here, altered or relaxed selection thousands at traditional sites. Unrestricted fishing pressures may lead to altered behaviour, morphol- access to these sites can result in rapid depletions ogy and life history, which in turn may affect sur- (Sadovy 1993, 1994). Orange roughy, Hoplostethus vival and reproduction (e.g. Petersson and Järvi atlanticus , gather in large spawning aggregations 1997). For example, hatchery populations of fe- at underwater peaks, i.e. seamounts. Here they are male coho salmon have lost a number of secondary vulnerable to trawling, which has proved to be a sexual characters (Fig. 10.6). Obviously, loss of considerable threat since large-scale fisheries naturally and sexually selected traits due to do- began in New Zealand during 1978. Aggregated mestication can have implications for the conser- spawning behaviour, combined with a slow life vation of wild populations, when cultured fish history (average age at maturity about 32 years; escape or are released (Fleming 1994).

Fenton et al. 1991), has led to rapid declines (see also Ward, Chapter 9, this volume). The elaborate

10.7.1 Timing and location of

sand bowers built by male haplochromine cichlids

spawning in Lake Malawi (see Sections 10.4.2 and 10.5) are

destroyed by trawlers, thereby disrupting spawn- Fish species that form spawning aggregations in ing even for the surviving males (see illustrations locations accessible to fisheries are particularly in Ribbink 1987). susceptible to overexploitation (see Reynolds et

In some parts of the world, fishers take advan- al., Chapter 15, Volume 2). This includes many tage of limited spawning sites by attracting fish to anadromous species such as salmonids and stur- artificial sites where they can be caught. An exam- geons that are targeted in estuaries and rivers. It ple is the use of bundles of sugar cane, palm fronds also applies to the Peruvian anchoveta, Engraulis or banana leaves by fishers in the Caribbean target-

Colour score

3.5 45 Hooked snout length (mm)

Breeding competition

Fig. 10.6 Relationships between breeding competition and (a) intensity of red breeding coloration and (b) hooked snout length for 11 wild populations and five hatchery populations (mean ± SE) of female coho salmon. Breeding competition for the wild populations was measured as the average female population size (measured over 3–38 years) divided by the spawning capacity of the stream. For hatchery populations, breeding competition was assumed to

be zero since spawning occurs artificially and independently of natural breeding competition. Correlations are significant even if only the wild populations are included. (Source: after Fleming and Gross 1989; reproduced by permission.) be zero since spawning occurs artificially and independently of natural breeding competition. Correlations are significant even if only the wild populations are included. (Source: after Fleming and Gross 1989; reproduced by permission.)

10.7.2 Sex change and sex-specific fisheries

An understanding of behavioural ecology is essen- tial in order to predict the effects of sex change and sex-specific fisheries on the resilience of popula- tions to fishing pressures (Vincent and Sadovy 1998; Petersen and Warner 2002). Most sex- changing reef fishes change from female to male when they reach a large size (Section 10.6.1). If this switch is under social control, i.e. triggered by the loss of large males, then one might expect that the loss of males would not impair productivity. However, there are at least two reasons why we should not take much comfort from this idea. First, intensive fishing may not allow sufficient time for females to change sex (Vincent and Sadovy 1998). This may explain why males of one species, the gag grouper, Mycteroperca microlepis, have become proportionately much rarer in the Gulf of Mexico and the southeastern Atlantic (e.g. McGovern et al. 1998). Second, although the social control of sex change is understood in some small species of reef fishes that live in permanent social groups, little is known about mechanisms of sex change in large groupers that come together only for spawning. No conclusions can be drawn about implications of male-biased fishing for stock pro- ductivity until we understand better how female- biased the sex ratio needs to become before sperm becomes limiting (see Petersen and Levitan 2001; Petersen and Warner 2002). The evidence from small reef fishes such as the bluehead wrasse is that although group spawnings may have more than ten times as much sperm released as pair spawnings (Shapiro et al. 1994), this difference does not greatly affect fertilization success (Marconato et al. 1997). However, frequently spawning male bluehead wrasse release less sperm per mating, resulting in lower fertilization success

(Warner et al. 1995). It remains to be seen whether these results apply to species of conservation con- cern such as groupers.

Sex-specific fisheries may also result from spatial and temporal segregation of the sexes (reviewed in Vincent and Sadovy 1998). As with considerations of sex change, this is apt to be most important where the sex that is targeted has the lower potential reproductive rate, and hence may limit population productivity. For example, in the coral trout, Plectropomus areolatus, females are caught selectively before spawning, leading to male sex-biases in spawning aggregations and male harassment of females that may hinder spawning (Johannes et al. 1994). In some migratory species such as plaice, Pleuronectes platessa, sexual selection is probably responsible for males arriving at spawning grounds before females (Arnold and Metcalfe 1996), leading to sex-specific fisheries during migration.

Anglers may have adverse effects on male fish that provide parental care. For example, North American male smallmouth bass, Micropterus dolomieu , will bite anything that comes near their nests, including hooks. Hook-and-release rules during the spring spawning season may allow males to survive (see Cowx, Chapter 17, Volume 2). However, an experimental study showed that when anglers ‘played’ fish to exhaustion (2 min), it took the males four times longer to return to their nests than when they were played briefly (<20 s) (Kieffer et al. 1995). Even a brief absence of the male can lead to breeding failure due to pre- dation by other species as well as neighbouring males.