Molecular Ecology (2005) 14, 653–660 doi: 10.1111/j.1365-294X.2005.02438.x MaleBlackwell Publishing, Ltd. nest site fidelity and female serial polyandry in lingcod (Ophiodon elongatus, Hexagrammidae) JACQUELYNNE R. KING and RUTH E. WITHLER Pacific Biological Station, Fisheries and Oceans Canada, Nanaimo, B.C., V9T 6N7, Canada Abstract Nest site fidelity and serial polyandry were examined in lingcod, Ophiodon elongatus, a teleost fish in which the nest-guarding male parent invests more heavily in parental care than the elusive female parent. Lingcod parental and progeny genotypes were established for fish spawning on a 200 m2 section of Snake Island reef, British Columbia in two suc- cessive years to evaluate male and female mate choice (monogamy or polygamy) and nest site reuse by the same parents (nest site fidelity) and/or different parents (nest site affinity). Thirteen nests (egg masses) guarded by nine males and 14 nests guarded by seven males were observed in 2002 and 2003, respectively. No female laid more than one nest per season or spawned in the study area in both years. In contrast, at least six (86%) and possibly all seven (100%) of the 2003 guardian males had been guardian or auxiliary males in 2002. Both nest site affinity and extreme male nest site fidelity were observed, with at least four males reusing the exact same nest site. Serial polyandry resulting from the high male and low female nest site fidelity is consistent with predictions based on a low female parental investment and high rate of progeny loss to predation and cannibalism. Male polygyny, achieved primarily by cuckoldry within seasons, was enhanced by the lack of female fidel- ity between seasons. Polygamy in both sexes of nest-tending marine fish may minimize reproductive skew and maximize genetic diversity within populations. Keywords: lingcod, nest site fidelity, polyandry, polygyny Received 24 June 2004; revision received 4 November 2004; accepted 29 November 2004 offspring, presumably have the choice between committing Introduction to monogamy with an apparently superior male or hedg- Among oviparous teleost fish, parental care may be pro- ing their bets by breeding with multiple males within a vided to offspring by either, both or neither of the parents, breeding season (polyandry) or between breeding seasons providing incentives for both sexes to maximize their (sequential polyandry). Documented examples of poly- reproductive success through a wide range of mating beha- andry are few (DeWoody & Avise 2001) and little is known viours ranging from complete monogamy to extensive poly- about the occurrence of sequential polyandry in teleost gamy. Males are the primary caregivers in many species fish. (Blumer 1979), responsible for establishing a nest or nesting Lingcod (Ophiodon elongatus) is a demersal marine teleost territory, wooing females and defending the fertilized eggs species of the eastern Pacific Ocean that inhabits nearshore resulting from their courtships. Genetic studies on nest- rocky reefs predominantly at depths from 10 to 100 m. It is tending species indicate that guardian males are commonly a large carnivore with maximum sizes of approximately polygynous within and between breeding seasons, mating 90 cm for males and 152 cm for females. Males mature at with multiple females who deposit eggs in nests guarded age two and have been known to live up to 14 years, whereas by themselves or other males (DeWoody & Avise 2001). females mature at ages 3–5 and may live to an age of 20 Females, whose fecundity is limited by body size and who years. Spawning occurs annually in January through March depend upon their partner(s) to adequately protect their but males arrive in spawning areas and establish territories as early as November. During spawning, which likely Correspondence: Jacquelynne R. King, Fax: 1(250) 756-7053; occurs at night (Low & Beamish 1978), females lay a single E-mail: [email protected] large mass of up to 500 000 eggs (referred to as a nest) in © 2005 Blackwell Publishing Ltd 654 J. R. KING and R . E . WITHLER rocky crevices or under rocks within a male territory. The monogamous within a breeding season, they may practice female leaves the nesting area after spawning but the male serial polyandry in part to counter the effects of predation remains in close proximity to the nest and actively guards and cannibalism. Observations made during nest density it against predation for 6 weeks until hatching. Two types surveys suggested that the same locations were being used of guarding behaviours have been observed: (i) males by lingcod as nesting sites between years (King & Winchell lying directly on or beside the nest and remaining nearly 2002) but provided no information on exact nest location or motionless unless touched, and (ii) males lying on a on male and female site fidelity. sentry post and defending the nest when other fish swam In this study, we have examined nest site fidelity in male close (O’Connell 1993). Males typically guard a single and female lingcod by comparing the genotypes of parents nest, but have been reported to guard up to three nests in that spawned on the Snake Island reef in 2003 with those close proximity (Low & Beamish 1978; King & Winchell observed in the 2002 study (Withler et al. 2004). Male and 2002). female genotypes for the parental lingcod were again Lingcod in the Strait of Georgia, British Columbia is determined by microsatellite analysis of tissue samples considered an overfished population (Cass 1985) with from guardian males and egg samples from their nests. early 1990s estimates of spawning biomass at only 5% of The analysis allowed us to distinguish between nest site observed historic levels (Martell & Wallace 1998). Recent fidelity (i.e. when an individual selects the same nest site success in year – class strength has been observed but the each year) and nest site affinity (i.e. when a nest site, as a stock is still considered to be of conservation concern (King result of habitat characteristics, is selected each year by dif- 2001). Nevertheless, a high degree of genetic diversity at ferent lingcod). We also tested our prediction that females microsatellite loci was observed in adult lingcod that is would practice a bet-hedging strategy of serial polyandry sampled from the region and attributed, at least in part, to by mating with different males in the second spawning a highly polygynous mating structure (Withler et al. 2004). season. Genetic analyses of tissue samples from lingcod guardian males and fertilized eggs from their 13 nests on Snake Study site Island reef in 2002 revealed that females were monogamous within breeding seasons, with each egg mass laid by a sin- Snake Island reef, situated in the Strait of Georgia (Fig. 1), gle female and no female spawning more than once. Males is the subject of ongoing lingcod nest density surveys guarded an average of fewer than 1.5 nests but achieved a (King & Beaith 2001; King & Winchell 2002). The study high degree of polygyny through cuckoldry. Thus each area, approximately 10 by 20 m with an average depth nest, consisting of the eggs of a single female, had been fer- of 10 m, was noted for recent relatively high nest densities tilized by between one and five males. Cuckolding males (King & Beaith 2001) and marked with a dive buoy included neighbouring male guardians and, likely, non- (49°12′43.7″ N; 123°53′04.7″ W) throughout the study. The guarding males. In all, the genotypes of 21 different males study site tended to be flat and open without large flora were identified among the progeny of the 13 nests attended such as Agarum spp. but containing several large rocks and by nine guardian males. boulders to provide nesting sites. Lingcod are territorial and have a narrow home range (Matthews 1992), making it possible that lingcod return to Methods the same reef each year to spawn. However, the observed polygyny may serve as a mechanism to maintain diversity Nest site identification in lingcod populations and a further increase in effective population size might occur if either males or females, As part of a genetic study investigating polygamous or both, failed to demonstrate interannual fidelity to nest mating in lingcod (Withler et al. 2004), nests were located sites, choosing to spawn on different reefs or different by scuba divers in the study site 1– 27 February 2002. Each areas of the same reef, in different years. For females, serial nest was marked with a numbered galvanized spike and polyandry would not only increase the genetic diversity the relative orientation (i.e. under a rock or in a crevice) among progeny, but also reduce the costs of a mating with was noted. The nest volume was estimated using length, a poor guardian in any one season. Lingcod eggs and width and height (nearest cm) measurements made under- juveniles often experience high levels of cannibalism and water. Given the difficulty in measuring irregularly shaped predation mainly by invertebrates, such as gastropods nests under rocks, measurements were made several times (Calliostoma ligatum) and sea stars (Pycnopodia helianthoides), and the average (nearest 0.5 L) was used. At the end of the and by sculpins (Artedius harringtoni, Jordania zonope), kelp nesting season, the galvanized spikes were replaced with greenling (Hexagrammos decagrammus) and striped seaperch rocks with plastic numbers attached. Distances between (Embiotoca lateralis) (Low & Beamish 1978; King & Beaith nests were measured to the nearest 0.5 m to develop a map 2001). This leads to the prediction that whereas female are of nest locations. © 2005 Blackwell Publishing Ltd, Molecular Ecology, 14, 653–660 LINGCOD NEST SITE FIDELITY 655 Fig. 1 Snake Island reef is located in the Strait of Georgia, British Columbia.