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Hirst, A. G., D. Bonnet, D. V. P. Conway, and T. Kiørboe

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Hirst, A. G., D. Bonnet, D. V. P. Conway, and T. Kiørboe View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Plymouth Marine Science Electronic Archive (PlyMSEA) Limnol. Oceanogr., 55(5), 2010, 2193–2206 E 2010, by the American Society of Limnology and Oceanography, Inc. doi:10.4319/lo.2010.55.5.2193 Does predation control adult sex ratios and longevities in marine pelagic copepods? A. G. Hirst,a,* D. Bonnet,b D. V. P. Conway,c and T. Kiørboed a School of Biological and Chemical Sciences, Queen Mary University of London, London, U.K. bUniversite´ Montpellier 2, Laboratoire Ecosyste`mes Lagunaires, Montpellier, France c Marine Biological Association of the United Kingdom, Plymouth, Devon, U.K. dNational Institute for Aquatic Resources, Oceanography Section, Technical University of Denmark, Charlottenlund, Denmark Abstract We assess the causes of adult sex ratio skew in marine pelagic copepods by examining changes in these ratios between the juveniles and adults, sexual differences in juvenile stage durations, and mortality rates of adults in the field and laboratory (when free from predators). In the field, late copepodite stages (CIV and CV) commonly have sex ratios that are either not significantly different from equity (1 : 1), or slightly male biased. By contrast, in adults, these ratios are commonly significantly biased toward female dominance. Sex ratio skews are therefore primarily attributable to processes in adults. Members of the non-Diaptomoidea have especially skewed adult ratios; in the members Oithonidae and Clausocalanidae this is not generated from differences between male and female adult physiological longevity (i.e., laboratory longevity when free of predators). In the genera Acartia, Oithona, and Pseudocalanus, we estimate that predation mortality contributed $ 69% of the field mortality rate in adult males, whereas in Acartia, Oithona, and Calanus adult females, this is $ 36%. We conclude that (1) adult sex ratio skew in pelagic copepods is primarily due to differential mortality of the sexes in the adult stage and not in juveniles, (2) mortality rates of adult Acartia, Pseudocalanus, and Oithona are dominated by predation mortality rather than physiological longevity (except under extreme food limitation), and (3) in Pseudocalanus and Oithona, elevated mortality rates in adult males to females is predominantly due to higher predation on males. Our work demonstrates that we now need to develop a more comprehensive understanding of the importance of feeding preferences in predators. Copepods have separate sexes, and commonly the ratio dae, Parapontellidae, Pseudodiaptomidae, Sulcanidae, Te- of abundance in field populations is strongly skewed, with moridae, and Tortanidae. Although Oncaea is not in the adult females outnumbering males (Hirst and Kiørboe Diaptomoidea, given its lack of sperm-storing ability, we 2002; Kiørboe 2006). According to Fisher’s principle, at the group it together with Diaptomoidea in our analyses. point sex is determined, the ratio of males to females is Those families that can store sperm (henceforth referred to expected to be 1 : 1 (Fisher 1930) or skewed to the sex in as non-Diaptomoidea) can produce fertile eggs for a long which the female invested least in the embryo. Evidence for period (possibly a lifetime) from a single mating (Marshall sex-based differences in investment in copepod embryos is and Orr 1952; Ohtsuka and Huys 2001). Kiørboe (2006) lacking, yet adult sex ratios are often highly skewed. This attributed the greater sexual skew in the single-mating non- inequality is important because the mating success is Diaptomoidea to a more risky mate search strategy of dependent on the sex ratio (Kiørboe 2006, 2008), and the males, making them more vulnerable to predation. This availability and density of males to fertilize females might risky behavior is traded off against the relatively greater be a limiting factor to population growth (Kiørboe 2007). reward in finding and fertilizing a female. Many non- Mating success can profoundly influence population Diaptomoidea also have reduced feeding rates in the males, dynamics and species success—hence, the need to under- which results in shorter physiological longevity compared stand the dynamics of such processes. with females (i.e., in the absence of predators, males simply Great insights have recently been made in describing the have shorter lives than females), and this has also been importance of the sex ratio in population dynamics and postulated as a controlling difference in the mortality of the linking sex skew with reproductive attributes (Kiørboe different sexes and in driving the strong sex ratio skew 2006). Kiørboe (2006) found that copepods that lack (Kiørboe 2008; Ohman and Hsieh 2008). The importance seminal receptacles have a sex ratio closer to 1 : 1 than do of each of these mechanisms (i.e., predation mortality on families that possess seminal receptacles. Repeat mating is males from riskier mating behavior vs. reduced longevity necessary in the former to allow for the continued from low feeding rates) has never been critically or widely production of fertilized embryos because they cannot store assessed in the marine plankton. We have a poor sperm. Species that lack seminal receptacles include those understanding of the causes of mortality in the plankton, in the genera Oncaea, and members of the superfamily and yet this is fundamental if we are to appreciate and Centropagoidea [henceforth, we use the corrected named model the dynamics of marine planktonic populations. In for this superfamily, Diaptomoidea (Boxshall 2004)]. this paper, we use the opportunity that field sex ratios Included in the Diaptomoidea are the families Acartiidae, provide to gain insight into the causes of mortality in the Candaciidae, Centropagidae, Diaptomidae, Fosshagenii- dominant mesozooplankton, the copepods. Malestendtomaturefasterthanfemales,anda * Corresponding author: [email protected] population in growth phase will have more males arriving 2193 2194 Hirst et al. at the adult stage, which will push the sex ratio toward male the published literature. We also made additional measure- dominance. Once recruitment has stopped the adult ratio ments where data are lacking. All data are available in may then swing to females if these have a greater longevity, electronic form as supplementary appendices. if they arrive later given their slower development rates, or both. These factors add to the temporal variability of the Stage durations—That stage duration can vary between sex ratio and, together with poor count statistics, have males and females, with males often having shorter made the discernment of underlying critical factors durations, is well documented (Landry 1975; Uye et al. determining the ratios more difficult to examine (Kiørboe 1983; Jerling and Wooldridge 1991). Other than the 2006). Other causes of a biased sex ratio might include seasonal effects that this might have on adult sex ratio environmental sex determination (ESD), wherein the skew, such differences also lead to skew in seasonally environment alters the sex ratio (Irigoien et al. 2000). This averaged sex ratios of juvenile stages because the sex with has been demonstrated in the harpacticoid copepod shorter stage durations will present comparatively reduced Tigriopus californicus as a result of the temperature stage abundance, even with equal recruitment of males and experienced during development and was shown not to be females. We therefore need an assessment of juvenile stage the result of differential mortality of the sexes (Voordouw duration differences between the sexes to make corrections. and Anholt 2002). Sex (ratio) might therefore not be We compiled stage duration data from the published determined genetically in some harpacticoid copepods but, literature and only included measurements of stage rather, be altered during the developmental process. By durations when made under identical laboratory conditions contrast, in the calanoid copepod Acartia, a chromosomal for both sexes of a species and when animals were followed mechanism of sex determination has been reported, with through the full stage (e.g., using median development males being heterogametic (XO) and females homogametic times). Stage durations that were determined by use of the (XX) (Goswami and Goswami 1974; Lecher et al. 1995). A inverse of the molt rates of wild-caught animals were not variety of mechanisms to explain ESD, which could act in included here because age-within-stages variation as a different parts of the developmental life history, have been result of mortality (Hirst et al. 2005) or a cohort structure proposed (Gusma˜o and McKinnon 2009). Given these (Miller et al. 1984) can severely bias estimates of stage issues, we need to determine in which stage(s) the sex ratio duration. Data were included from the following sources: skew arises in pelagic copepods. Landry 1975, 1983; Uye et al. 1983; Kimoto et al. 1986; Identifying where sex ratio skew arises (i.e., in juvenile or Jerling and Wooldridge 1991; Escribano and McLaren adult stages) will allow the likely causes of this skew to be 1992; Ban 1994; Lee et al. 2003; Devreker et al. 2007. identified. For example, equitable sex ratios in juveniles would suggest that these are unlikely to be biased at the Sex ratios across stages—We compiled data on the point of inception. It will also give greater insight into ESD. abundance ratios of the sexes across consecutive stages Males and females of many genera are distinguishable from
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