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Mortality is a fundamental component that influences life-history trade-offs in nature and human harvesting such as hunting and fishing brings additional mortality to ecosystems. Harvesting is highly selective, however, and often causes unnatural change in the life-history traits of target species (e.g. Coltman et al. 2003; Edeline et al. 2007; Garel et al. 2007). Recent reviews caution that the effects of selective harvesting are relevant in efforts to sustain wild animal populations (Coltman 2008; Fenberg & Roy 2008; Allendorf & Hard 2009; Dunlop et al. 2009; Mysterud 2011). In fisheries, especially, it has been documented that size-selective harvesting causes phenotypic and genetic change in such traits as body size (Conover & Munch 2002; Carlson et al. 2007; Swain, Sinclair & Hanson 2007), reproductive scheduling (Olsen et al. 2004; Dieckmann & Heino 2007) and other parameters (Walsh et al. 2006; Biro & Post 2008). While such changes represent the ultimate response of harvested animals, it is also well known that the life history of target species plastically alters with harvesting (Beverton & Holt 1957; Rochet 1998). However, research on the adaptive significance of these types of condition-dependent changes has been limited. Although a plastic genotype may perhaps perform better than a less plastic one across varying conditions, evidence of adaptive phenotypic plasticity is still being explored, even in natural populations (Pigliucci 2005). Moreover, a model by Ernande, Dieckmann & Heino (2004) predicts that plasticity does not act as a buffer against the evolutionary pressure of the size-selective harvesting that might cause unfavourable genetic changes.
The selectivity of fishing activity affects not only body size but also other traits and ecological processes (Zhou et al. 2010). Adult sex ratio (the ratio of mature males to mature females) is often biased to one sex because of size-selective fishing (Rowe & Hutchings 2003), intentional sex-selective fishing (Abe 1992; Carver et al. 2005; Sato et al. 2007) and fishery stocking programmes (Kanaiwa & Harada 2008). As sex ratio directly affects mating behaviour and population dynamics (Emlen & Oring 1977; Shuster & Wade 2003), harvested animals would consequently suffer a burden in their need to respond to the artificially created skew in sex ratio. In particular, the sex ratio of sequential hermaphrodites (animals that change sex) is vulnerable as a result of size-selective fishing, because their sex-change is triggered by somatic growth and large individuals after changing sex are therefore targeted by the fishing (Sadovy 2001; Alonzo & Mangel 2004; Molloy et al. 2007; Sattar, Jorgensen & Fiksen 2008).
The pandalid shrimps (Decapoda, Pandalidae, Pandalus) are a group of protandrous (male-first) species that have been treated as a model to examine plastic life-history variations with respect to sex ratio fluctuation. By defining early or late sex-change as an alternative strategy of life history in a given population of Pandalus jordani Rathbun, Charnov, Gotshall & Robinson (1978) predicted that the optimal age (size) at sex-change is attained when the average fitness of males and females becomes equal. For example, when the proportion of females consisting of old (large) breeders is low among all breeders, earlier sex-change by young (small) breeders is facilitated as a conditional response, a so-called socially mediated sex-change (SSC), and sex ratio is adjusted as a result of this SSC process. Interestingly, the pandalid shrimp is the most exploited crustacean in cold waters (Gillett 2008), with most populations being primarily exposed to unintentional female-selective fishing due to the fact that females are larger than males (Bergström 2000). This implies that a sex ratio bias in selective fishing towards the first sex (i.e. male) may trigger SSC in populations of P. jordani. A similar phenomenon has also been observed in Pandalus borealis Krøyer, the most common commercial pandalid shrimp (Charnov 1981; Charnov & Anderson 1989).
Sex ratio adjustment by the pandalid shrimp has been successfully modelled as a part of the sex allocation theory that explains resource allocation to male and female functions (Charnov 1982). However, the model has not been tested in other animals, and SSC by pandalid shrimps still leaves some doubts due to lack of concrete empirical evidence. While SSC has been thoroughly studied in sequential hermaphrodites forming small mating groups comprising two to several individuals (Warner 1988; Munday, Buston & Warner 2006), it is not clear how flexible sex-change is in hermaphrodites such as the pandalid shrimp that mate at random within a population comprising over tens or hundreds of thousands of individuals. In addition, the SSC-like phenomenon in pandalid shrimps can be explained by accelerated sex-change resulting from growth enhancement after large individuals (i.e. old females) have been harvested (Hannah & Jones 1991; Koeller, Mohn & Etter 2000). In this explanation, sex-change is genetically regulated, with sex being determined by body size based on density-dependent processes, even though it appears to be adaptive sex ratio compensation. As a result, the adaptive significance of life-history variation in pandalid shrimps is still ambiguous, and hence, the evolutionary perspective has been ignored in the fishing resources management of pandalid shrimps.
While the effects of selective fishing on the mating systems of marine organisms have been cautioned in several landmark review articles (Rowe & Hutchings 2003; Hutchings & Rowe 2008; Allendorf & Hard 2009; Zhou et al. 2010), our knowledge of how target species plastically modify their life-history strategy to maximize fitness under unnatural mating conditions remains limited. Distinguishing between a density-dependent process and an adaptive process in plastic life-history changes would greatly improve our ability to conserve wild animal populations. For example, the former process could be mainly managed by quantitative biomass assessment, a standard approach in fisheries management, while the latter process would require additional management procedures that incorporate the mating system of target species.
In this study, we explored the adaptive significance of the annual changes in the age at sex-change of the pandalid shrimp Pandalus latirostris Rathbun (Fig. 1a) and examined how selective fishing activity affects life-history variation in this species, by conducting field observations across 13 years and a controlled laboratory experiment. Even though target species can respond plastically to environmental fluctuations, it may not always be adaptive under both natural and artificial environments, because the direction and intensity of natural and artificial selection processes are different. We therefore considered whether the plastic responses by this shrimp would be favourable, negligible or negative with respect to the conservation of fishery resources.
Figure 1. Basic information about Pandalus latirostris and Lake Notoro. (a) Sketch of P. latirostris at age 2 and observed anatomical locations. (b) Life-history schematic of P. latirostris. Thick lines indicate the general life-history pattern of this shrimp. Im, M and F denote immature male, matured male and matured female, respectively. Thin lines indicate the life history of some individuals that mature as male at age 0 (early-matured males, EMM), change sex to female at age 1 (early-changed females, ECF) and do not change sex at age 2 (postponed-change males, PCM). As the occurrence of PCM is more frequent than that of EMM and ECF (Chiba & Goshima 2003; this study), solid lines have been used for the arrows to and from PCM. As this species hatches between mid-May and mid-June, we defined June as the month of ‘birth’. The light and dark grey areas indicate the maturing and breeding seasons, respectively. Bottom widths of the triangles indicate the fishing season. Age 2 and age 3 individuals are harvested just before the breeding season. (c) Map showing the location of Lake Notoro on the island of Hokkaido in northern Japan, with an outlet to the Sea of Okhotsk. Sampling stations (St. 1–5) were established in seagrass areas (shaded areas). (d) Changes in total catch and catch per unit effort (CPUE) of P. latirostris in Lake Notoro. Shrimp fishing was initiated in 1978 and it was banned during 2003 only. The CPUE indicates catch weight per cage trap, which were calculated from catch weight, date, the number of cages and the number of fishing boats in each year.
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