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Life-History Characteristics of Coral Reef Gobies. II. Mortality Rate, Mating System and Timing of Maturation

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Life-History Characteristics of Coral Reef Gobies. II. Mortality Rate, Mating System and Timing of Maturation MARINE ECOLOGY PROGRESS SERIES Vol. 290: 223–237, 2005 Published April 13 Mar Ecol Prog Ser Life-history characteristics of coral reef gobies. II. Mortality rate, mating system and timing of maturation V. Hernaman1, 3,*, P. L. Munday2 1Department of Marine Science, University of Otago, PO Box 56, Dunedin, New Zealand 2School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland, Australia 3Present address: School of Biological Sciences, Victoria University, PO Box 600, Wellington, New Zealand ABSTRACT: High adult mortality rate is expected to select for early maturation. However, physiolog- ical constraints or size-related reproductive benefits might select for delayed maturation, especially in small-bodied species. Additionally, the mating system and the relative intensity of mate competi- tion can modify the timing of maturation. Here, we investigate the influence of mortality rate and mating system on the timing of maturation in 5 species of small coral reef goby that are either poly- gynous (Asterropteryx semipunctatus and Istigobius goldmanni) or monogamous pair-spawners (Amblygobius bynoensis, Amblygobius phalaena and Valenciennea muralis). All 5 species experi- enced high annual adult mortality rates with annual survivorship of ≤2.3%. The mean size at matu- rity, compared to maximum adult size, was smaller than is typical for fishes, indicating selection for early maturity in all of these species. The season of growth had little effect on size at maturity, but had a considerable effect on age at maturity, with summer-growing individuals exhibiting a younger mean age at maturity than winter-growing individuals. As predicted, males of the 3 monogamous pair-spawning species matured earlier and smaller than females (A. bynoensis and A. phalaena) or at the same time as females (V. muralis), but contrary to expectation, males of the 2 polygynous species (A. semipunctatus and I. goldmanni) did not mature later and at a larger size than females. Overall, the timing of maturation in these species is consistent with predictions from general life-history theory, however, the sex-specific timing of maturation may be influenced by body size constraints and the mating system. KEY WORDS: Maturity · Mortality · Life history · Body size · Gobiidae · Mating system Resale or republication not permitted without written consent of the publisher INTRODUCTION is often strongly correlated with body size (Roff 1992), the timing of maturation is also expected to vary in Life-history theory predicts that the life stage upon relation to an organism’s size. Small-bodied species which mortality exerts most influence will shape the often experience high rates of mortality throughout life timing of sexual maturation. High and unpredictable and, consequently, are predicted to exhibit early matu- density-independent adult mortality is predicted to ration and high reproductive effort. Early maturation select for early maturation and high reproductive effort confers several benefits, such as a higher probability of early in life (Schaffer 1974, Begon & Mortimer 1981, survival to maturity, shorter generation times and a Stearns 1992). In contrast, high juvenile mortality, but higher instantaneous rate of natural increase (Stearns low adult mortality, will favour late maturation with the 1992). production of many small young and the reproductive Selection for early maturity in small species may be effort spread over many reproductive events (Begon & offset, however, by selection to delay maturity to Mortimer 1981, Stearns 1992). Because mortality rate obtain size-related reproductive benefits. For example, *Email: [email protected] © Inter-Research 2005 · www.int-res.com 224 Mar Ecol Prog Ser 290: 223–237, 2005 in fishes the number of eggs produced at each spawn- Competition among males is expected to be most ing is limited by the volume of the body cavity avail- intense in polygamous mating systems and relatively able to accommodate the ripe ovaries (Wootton 1998). slight in monogamous and pair-spawning species Thus, the size of the body cavity can impose a sub- (Emlen & Oring 1977, Stearns 1992). Therefore, males stantial constraint on batch fecundity of small-bodied of the 2 polygynous species should delay reproduction species. Assuming a growth cost of reproduction, to attain a larger size, and consequently, mature later females could maximise both initial and future fecun- and larger than females. In contrast, males of the 3 dity by delaying reproduction until a larger size is monogamous pair-spawning species would not be pre- attained (Stearns 1992). Selection may also favour dicted to mature later or at a larger size than females. delayed reproduction in males if mate choice and In fact, males of pair-spawners might mature at a reproductive success are linked to body size. In situa- smaller size than females because they do not suffer tions where a large body size confers a competitive the same size-related constraints on fecundity as advantage in contests over mates, nest sites or breed- females. However, body size has been found to influ- ing territory, male reproductive success may be ence mate selection in some monogamous pair-spawn- increased by delaying reproduction to attain a larger ing gobies, with both males and females preferring body size at maturation (Emlen & Oring 1977). larger partners (Reavis 1997b, Takegaki & Nakazono For coral reef fishes, mortality rates are typically 1999). Therefore, males of the pair-spawning species highest during the early life history (Meekan 1988, should mature at either the same size or smaller than Hixon 1991, Jones 1991, Caley 1998). However, for females. many small-bodied species, adult mortality may also To investigate the timing of maturation and deter- be considerable because their small size renders them mine how it is influenced by mortality rate and the vulnerable to predation throughout life (Munday & mating system, we first determined the annual mortal- Jones 1998). Consequently, early maturity and high ity rate of each species. We then estimated the absolute reproductive effort is predicted for most small coral- size and age at maturity of males and females, and reef fishes. Here, we investigate the timing of matura- tested for sex-specific differences in the mean size and tion for 5 species of coral reef goby (Gobiidae), a age at maturity. If the mating system influenced the diverse and abundant group of small fishes found in a timing of maturation, we predicted that males of the 2 wide range of coral reef habitats (Leis & Rennis 1983, polygynous species would mature later and larger than Randall et al. 1997, Greenfield & Johnson 1999, Acker- females, whereas in the 3 monogamous pair-spawning man & Bellwood 2000). The coral reef gobies in our species, males would mature at the same size or study are all small species (<130 mm total length), with smaller than females. Finally, to compare the timing of relatively short maximum life-spans (11 to 16 mo, maturation with predictions from general life-history depending on species; Hernaman & Munday 2005, this theory, we compared the observed size at maturity for volume). The relatively short life-span of these species the 5 species considered here with the size at maturity might select for early maturation to increase the prob- reported for a range of other fishes by Charnov (1993). ability of survival to maturity, and this may be facili- tated by a phylogenetic capacity for maturation at a small absolute body size (Miller 1984). Conversely, MATERIALS AND METHODS reproductive constraints associated with a small body size might favour delayed maturation to gain size- Sample collection and preparation. Fish were related reproductive benefits. collected using a clove oil/alcohol mixture and euthan- The mating system and the intensity of competition ased by immersion in an ice slurry. Total length, stan- for mates or resources can also influence the relative dard length (nearest 0.1 mm) and weight (nearest timing of maturation. Two of the study species (Aster- 0.001 g) were recorded, and the otoliths removed for ropteryx semipunctatus and Istigobius goldmanni) are estimating age. The gonads, or body midsections con- polygynous and 3 (Amblygobius bynoensis, Ambly- taining the gonads, were dissected from each fish and gobius phalaena and Valenciennea muralis) are mono- preserved in a solution of 4% formaldehyde, 5% gamous pair-spawners (Hernaman 2003). Generally in glacial acetic acid and 1.3% calcium chloride (FAACC) fishes, males might be expected to mature smaller and for at least 1 wk and then transferred to 70% ethanol. younger than females because females gain fecundity Histological preparations of the gonads and body mid- with size at a higher rate than males (Stearns 1992). sections were used to determine the maturity stage of However, males tend to mature later and larger than each fish. Body midsections were decalcified in 10% females in mating systems where there is strong com- formic acid for 24 h prior to histological processing. After petition for females or for resources that may affect embedding in paraffin wax, midsections and gonads reproductive success (Warner 1984, Stearns 1992). were serially sectioned at 6 µm at 3 positions of the go- Hernaman & Munday: Coral reef gobies. II 225 nad (anterior, middle and posterior). Thin sections were estimates of instantaneous mortality rate (Z) (for this mounted on microscope slides, stained with Mayer’s study Z equals the natural mortality rate, M, because of alum haematoxylin and Young’s eosin-erythrosin, and the absence of fishing mortality, F). For age-based examined under a high-power compound microscope. catch curves, fish were grouped into monthly age-class Female maturity was classified on the basis of the intervals, where age was estimated by counts of otolith most advanced oocyte stage present. The terminology growth increments (Hernaman & Munday 2005). The and description of each oocyte stage followed Yama- natural logarithm of the number of fish in each age moto et al. (1965), West (1990), and Takashima & class was plotted against the corresponding age class Hibiya (1995).
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