Costs of reproduction

7.2.3 Costs of reproduction

A central tenet of life-history theory is that the be- havioural, physiological and energetic correlates of reproduction exact some sort of cost to future re- productive success in the form of reduced survival, fecundity and/or growth. Firstly, relative to a non- reproductive individual of age x, reproduction at age x can reduce the probability of survival to age x+n , where n might represent any unit of time from minutes to years. Secondly, reproduction can directly reduce an individual’s future ability to produce offspring. High energetic costs expended at age x might leave a fish with insufficient energy reserves to produce the same number of offspring at age x + n. The third cost is a consequence of the energy allocated to the behavioural and physio- logical demands of reproduction at the expense of energy that would otherwise have been allocated to somatic growth. Reduced future size-at-age concomitant with a reduction in growth rate, cou- pled with the positive association typically ob- served between fecundity and body size in fish (Wootton 1998), results in a reduction in potential fecundity, such that an individual reproducing at age x will produce fewer eggs at age x + n than an individual that did not reproduce at age x.

The seminal work in this area began with in- ductive arguments for why reproductive costs should exist and theoretical assessments of the life-history consequences thereof (e.g. Fisher 1930; Cole 1954; Williams 1966; Gadgil and Bossert 1970). The literature turned to a consideration of whether costs indeed existed and, if they did, what were the most appropriate means of measuring them (e.g. Reznick 1985). The primary challenge now lies in how to best estimate costs in natural populations, and to identify the primary physical and biological environmental factors that effect variability in the expression of costs between sexes, among individuals, among years, among generations and among populations.

To quantify reproductive costs precisely, one would manipulate reproductive effort for a spe- cific genotype and then document the genotype- specific survival and/or fecundity consequences of those changes to effort. For most fish, excepting

Life Histories

parthenogenetic species, these are experimental Lawrence River, Canada, to be more than twice criteria that cannot be met, notwithstanding the that of their breeding counterparts. Using a similar difficulty of assessing the degree to which a cost comparison of survival probabilities, Hutchings quantified under experimental conditions in the (1994) documented evidence of survival costs of re- laboratory is likely to reflect costs experienced production in three Newfoundland populations of in the wild. Nonetheless, if we are to have any brook trout that appeared to increase with age but success in applying life-history theory to our to decline with body size. Indirect evidence of a understanding of the ecology, management and negative association between reproductive cost conservation biology of fish, some attempt must and body size has also been recorded for the sand

be made to quantify reproductive costs. Reznick goby, Pomatoschistus minutus (Lindström 1998), (1985) discusses the strengths and weaknesses as- and Atlantic silverside, Menidia menidia (Schultz sociated with various means of estimating costs in and Conover 1999). As a practical tool for quantify- general, while Hutchings (1994) discusses these ing survival costs in the field, this method holds a methods in relation to the study of fish.

great deal of promise and is critical if life-history

One means of estimating costs, widely used in theory is to be applied to specific management and avian and Drosophila sp. life-history research (e.g. conservation issues. Although one will inevitably Pettifor et al. 1988; Chapman et al. 1993), is to ex-

be unable to control all the factors potentially in- perimentally manipulate some metric of present fluencing individual quality, costs estimated by effort and then document the survival and/or such a technique should tend to underestimate fecundity consequences thereof. Examples of such rather than overestimate costs, if one assumes that manipulation in the fish literature are compara- the reproductive individuals are the highest quali- tively rare and are limited to species that exhibit ty individuals (Hutchings 1994). parental care (Balshine-Earn 1995). Notwith-

Perhaps the most widely acknowledged cost in standing the attraction of such an experimental fish associated with reproduction at age x is the re- approach, it has its limitations. For example, costs duction in growth rate immediately prior to age x, estimated by manipulation of brood size will un- and thence to ages x + n, that effects a concomitant derestimate actual costs because they exclude the decrease in fecundity, generated by the diversion of physiological and behavioural costs associated energy from somatic growth to the behavioural, with producing the brood. Also, by artificially ma- energetic and physiological demands of reproduc- nipulating the size of brood to which a genotype tion (Bell 1980; Hutchings 1993a; Balshine-Earn was ‘expecting’ to provide care, one risks either 1995; Wootton 1998; Jobling, Chapter 5, this underestimating or overestimating costs if some volume). form of individual optimization (Pettifor et al.

It has been argued that the most informative 1988) or adaptive phenotypic plasticity (Hutchings method for measuring a cost of reproduction 1996; Jonsson et al. 1996) exists in the population would be to quantify correlated genetic responses under study.

estimated from a selection experiment (Reznick

One potentially informative method of esti- 1985). One such experimental protocol would be mating survival costs of reproduction is to quanti- to select only those individuals having either low fy the difference in survival probabilities between or high fecundity to breed at age x, to repeat this ages x and x + n for individuals that reproduced at selection regime over several generations and then age x and those that did not. To reduce the effects of to determine whether there has been a correlated individual differences in aspects of quality, such as response to this selection regime in the form of a body condition, on such an analysis (cf. Reznick negative association between, for example, fecun- 1985), one should control for both size and age. For dity at age x and fecundity at age x + n. Despite their example, Dufresne et al. (1990) found the survival experimental limitations, intentional selection among non-breeding 1- and 2-year-old threespine experiments in the field do have the potential sticklebacks, Gasterosteus aculeatus, in the St to provide valuable insight into how reproductive

Chapter 7

costs vary with changes to age-specific survival sitism have not been unequivocally documented, and fecundity. An example of intentional selection if such links exist, increased parasitism could is a change to age-specific mortality effected by

be implicated in acute and chronic reproductive natural predators (Reznick et al. 1990); an example costs, given observations that parasites have been of unintentional selection is a change to age- shown to have a wide range of effects on fitness specific mortality effected by fishing.

(Barber and Poulin, Chapter 17, this volume).

Many reproductive costs in fish can be attrib- These include reduced growth rate (Walkey and uted to the loss of lipids and proteins associated Meakins 1970), inhibited sperm development with various physiological and behavioural corre- (Sinderman 1987), lower gonad weight as in the lates of reproduction, such as gonad production common goby, Pomatoschistus microps (Pam- (Wootton 1998), mate competition (Grantner and poulie et al. 1999), decreased fecundity as found in Taborsky 1998) and parental care (Lindström 1998; Pacific hake, Merluccius productus (Adlerstein Mackereth et al. 1999). These energetic demands and Dorn 1998), and reduced probability of attract- can be considerable, particularly when one ing mates as observed for threespine stickleback compares the energetic losses of reproductive (Milinski and Bakker 1990). The energetic de- individuals relative to those of non-reproductive mands of reproduction might also effect acute, individuals during the same time interval. For short-term survival costs if individuals experience example, post-reproductive Arctic char, Salveli- an increased risk of predation because of reduced nus alpinus , possess 35–46% less energy than non- locomotion, reduced vigilance and/or increased reproductive char in spring (Dutil 1986). Rijnsdorp feeding rate. and Ibelings (1989) reported energy losses among

Ecological constraints of reproduction in fish reproductive North Sea plaice, Pleuronectes might result in reduced future survival probabili- platessa , to be three to five times that of non- ties, notably in the short term. Two primary means reproductive plaice. The source of energy losses by which these might be effected are through differs between sexes, with non-gonadal reduc- increased risk of predation and increased risk of tions typically being greater among males than physical injury. The former can result from behav- females (Jonsson et al. 1991; Hutchings et al. 1999), iours associated with attracting mates (Houde and presumably as a consequence of the behaviours Endler 1990) or caring for young (Pressley 1981). associated with mate competition. The magnitude Physical injury, primarily as a result of mate com- of total energy losses attributed to reproduction petition, can also be expected to negatively influ- also differs between sexes, but apparently not in a ence short- and long-term survival probabilities similar manner among, and potentially within, (Hutchings and Myers 1987; Fleming 1996). species. Energetic losses have been reported to be

Reproductive costs in fish might also result greater for females in Arctic char (Jørgensen et al. from genetic trade-offs between correlated charac- 1997) and plaice (Rijnsdorp and Ibelings 1989), ters of fitness, although evidence of such antago- equal in Atlantic salmon (Jonsson et al. 1991), yet nistic pleiotropy has not been reported for fish. greater among males in brook trout (Hutchings et al. 1999).