By exploring the links between life-history stages of a coral reef fish, we have demonstrated how juvenile survivorship can be significantly influenced by processes taking place in the pelagic environment or even before hatching of larvae via parental effects. Pomacentrus amboinensis
individuals that survived intense size-selective mortality, which occurred during the pelagic phase, had significantly smaller otoliths at hatching. We found that otolith size-at-hatching closely reflected a combination of early larval characteristics (i.e. larval body size and amount of yolk-sac reserves); contrary to expectations of the bigger-is-better hypothesis (Miller et al. 1988
), there was no apparent disadvantage of small size at hatching, when body size was coupled with large energy reserves. Previous studies have directly linked larval and yolk-sac size to maternal condition in this species (McCormick 2003
; Gagliano & McCormick 2007a
) and suggested that females can constrain size of offspring in favour of quality (i.e. yolk-sac size). For example, McCormick (2006)
showed that maternal stress from competition increases cortisol in P. amboinensis
ovaries and decreases larval size but not yolk-sac reserve. In the light of the present study, we suggest that ‘smaller-is-better’ may be a maternal strategy for increasing early survivorship of larvae rather than decreasing it. Clearly, the relationship between the condition of parental stock, larval characteristics and otolith size deserves further investigation. Furthermore, selective mortality of individuals with larger otoliths at hatching was also pronounced during the first two weeks following settlement on reef habitats, indicating that there was a carry-over effect on selection for this trait that operated across life-history stages.
Among the traits considered in this study, pelagic larval growth was, by far, the most influential and long-lasting trait associated with juvenile persistence on the reef. Selective mortality based on larval growth was generally nonlinear and changed form across ontogenetic stages. Such changes in the shape and magnitude of selective mortality over time may help maintain phenotypic variation in larval growth and ultimately preserve (genetic) variation in fish populations (Swain 1992
; Hare & Cowen 1997
). This could also explain why we do not see a progressive evolution towards faster larval growth rates, as might be predicted if faster-growing individuals within a cohort enjoy higher probability of survival (the growth-rate mechanism; Anderson 1988
Unlike pelagic larval growth, we detected no patterns of selective mortality based on PLD. The low variation in this trait among individuals suggests that selective mortality with respect to this trait had limited potential to occur within this cohort (cf. Sogard 1997
). There appears to be low intra-cohort variability in larval duration in this family of reef fishes (Robertson et al. 1990
) and our results combined with previous findings on other pomacentrid species (e.g. Macpherson & Raventos 2005
; Bay et al. 2006
) suggest that theoretical predictions of the stage-duration mechanism (Houde 1987
) are unlikely to be applicable to this group of fishes.
Although our results showed that larval traits strongly influenced patterns of selective mortality within this cohort weeks after settlement, juvenile characteristics also significantly shaped early survivorship of individuals on reef habitats. Specifically, smaller rather than larger initial size conferred higher survival probability to newly settled P. amboinensis
. This result contrasts with predictions of the growth-mortality hypothesis (Anderson 1988
), which proposes that faster growth at this time enhances survival through the covariation of size with behavioural, physiological and other morphological attributes, which reduce potential predation and/or starvation risks. However, the present finding supports recent evidence indicating that the extent of size-selective mortality of newly settled reef fish can differ among locations separated by only hundreds of metres (Holmes & McCormick 2006
). This suggests that the characteristics of the predator assemblage and prevailing environmental conditions can lessen or even negate any advantage to being large at settlement. Ultimately, the lack or even the possibility of negative covariance between size and survival could be indicative of a trade-off between growth and size against behavioural, physiological and other morphological attributes rather than a growth-mortality hypothesis.
Interestingly, survivors of the early juvenile period were those individuals who were slower-growing as larvae and smaller at settlement but grew faster during the first two weeks on the reef (). Our finding of an inverse relationship between the growth rates in the larval and early juvenile periods (first two weeks) is consistent with earlier laboratory studies (Bertram et al. 1993
) and recent field experiments (McCormick & Hoey 2004
), in that it demonstrates that growth rates throughout the planktonic life are not necessarily maintained during the early post-settlement period. This also suggests that changes in the direction of phenotypic selection can promote the occurrence of compensatory responses during early juvenile life (see review by Ali et al. 2003
Figure 4 Growth trajectory of a young fish from embryonic conditions in benthic nests, through pelagic life in the open ocean, to settlement and subsequent survival back on reef habitats. The arrows at the top of the diagram indicate the optimal growth rate at (more ...)
Faster growth during the first few days on the reef is expected to be advantageous by enabling initially smaller settlers to quickly outgrow high vulnerability to gape-limited predators (bigger-is-better hypothesis; Anderson 1988
). However, we found that individuals who maintained a faster growth trajectory throughout the third week post-settlement were preferentially lost from the cohort (). It may be that young fish, faced with intense selective pressure to grow at a faster rate during the earlier periods of benthic life, had high foraging motivation (Nicieza & Metcalfe 1999
) and may be willing to take a potentially greater predation risk for possible gains in food resources (Biro et al. 2004
). If this is the case, significant changes in behaviourally mediated mortality could be expected to occur over narrow time frames.
Overall, our analyses revealed that strong size- and growth-selective mortality generally removed the larger and faster growing members of the cohort (i.e. smaller-is-better). Larval growth during planktonic life was by far the most enduring of all the traits examined, influencing survivorship of young fish settled on reef habitats. The selective loss of individuals with faster larval growth observed in the present study is counter to the prediction of the growth-rate mechanism (Anderson 1988
). While the theory is supported by a large number of both field and laboratory studies, there are a growing number of examples of studies that have found that faster larval growth does not always confer greater survival benefits (e.g. Cowan et al. 1996
; Fuiman et al. 2005
) or detected no selective mortality based on larval growth (e.g. Searcy & Sponaugle 2001
). Empirical evidence from other animal systems has also demonstrated that in some environments, individuals growing slower experience a greater advantage, in terms of survival, than do faster-growing conspecifics (e.g. amphibians, Werner 1991
; mammals, Negus et al. 1992
; insects, Gotthard et al. 1994
; reptiles, Olsson & Shine 2002
). When rapid growth entails physiological changes that lead to a reduced capacity to respond to environmental stress (Arendt 1997
), the costs of growing too fast may increase under harsh conditions. So, why do some individuals still grow faster when rapid growth compromises their early survival? One possibility is that individuals follow a growth pathway defined early in their development (e.g. prior to or at hatching) and they are unable of modifying its trajectory until later in life (e.g. after settlement; see Gagliano & McCormick 2007b
). In fish, where early pelagic larvae have limited or no control of the spatially and temporally variable environment to which they are exposed, the variation per se
in growth trajectories among individuals of the same cohort may be adaptive. Ultimately, if this is the case, the lack of consistency in trends of selective mortality based on larval growth may be the result of masked ontogenetic changes in the form and intensity of selectivity. While this is clearly a complicating factor to our understanding of selective processes influencing early survival of young fish, unveiling changes in selective curves over different portions of the life history may ultimately enable us to better appreciate the dynamics governing the complex life cycles of many species.