Impacts of Large Male-Selective Harvesting on Reproduction: Illustration with Large Decapod Crustacean Resources

Taku Sato

Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Fisheries Research Agency, Ishigaki, Okinawa 907-0451, Japan

Abstract

To signal a need for caution for present large male-selective harvesting practices, negative impacts of the large male-selective harvesting on reproductive output in large decapod crustacean resources are introduced with emphasis on my own work with spiny king crab Paralithodes brevipes, coconut crab Birgus latro, and the stone crab Hapalogaster dentata. The large male-selective harvestings for several large decapod crustaceans have changed their population demographic structure by decreasing mean male size and skewing sex ratio towards females. By several field and laboratory experiments, the change of population demographic structure was anticipated to decrease female reproductive success in the resources (i.e. reproductive output of the harvested populations) through a decrease in sperm availability for females because of male size-dependent reproductive potentials and slow sperm recovery rate. Furthermore, reproductive output and stability of the large male-selective harvested resources were also anticipated to decline by a decrease in mate availability for females, attributing to combination of female mate choice for larger males with negative effects of female delayed mating and/or maternal influences. To establish the optimal management practices, the details of the mating system and reproductive ecology of each targeted species should be investigated.

Keywords

Birgus latro, Hapalogaster dentanta, large decapod crustacean, large male-selective harvesting, mating system, Paralithodes brevipes, population demographic structure, reproductive ecology, reproductive success


Received on September 7, 2011

Accepted on July 6, 2012

Online published on November 20, 2012

e-mail: takusato@affrc.go.jp


1. Introduction

Size-selective harvesting is common practice in both terrestrial and aquatic habitats. Hunting and fishing are almost always non-random and often size-selective, and larger individuals are more likely to be harvested than smaller ones (Fenberg and Roy 2008). For example, fisheries managers traditionally tend to mandate a minimum legal size limit for catch (i.e. size-selective harvesting) (Law 2000). Trophy hunters almost always target large males with large horns, antlers or tusks (Coltman et al. 2003). Size-selective harvesting can affect many aspects of the biology of harvested species, from demography, behavior, life history and genetics to the local abundance and biomass of populations (Fenberg and Roy 2008). The primary effect of size-selective harvesting in general is a decrease in body size of the harvested species. Body size decreases, attributed to the size-selective harvesting, have been reported in many species of vertebrates and invertebrates (e.g. Bianchi et al. 2000; Branch and Odendaal 2003; Roy et al. 2003; Harvey et al. 2006).

In a wide range of taxa, body size is one of the key determinants of fitness in both males and females (Andersson 1994). For example, body size is positively correlated with reproductive fitness (e.g. mating success and fecundity). Mostly, larger males are stronger competitors for females (e.g. Hoefler 2007) or can provide more ejaculated sperm (e.g. Jivoff 1997), or better care for the offspring (e.g. Kolm 2002). In females, body size positively correlates with egg size (e.g. Einum and Fleming 1999), number of spawning (e.g. Claramunt et al. 2007), number of eggs spawned (e.g. Evans et al. 2008), or quality of larvae (e.g. Berkeley et al. 2004). Therefore, mate choice is non-random in the majority of animal species (Real 1990), and males and females prefer larger mates mutually (e.g. Sandvik et al. 2000; Herdman et al. 2004; Aquiloni and Gherardi 2008), resulting in larger individuals contributing disproportionately to reproduction of populations through sexual selection. Thus it is likely that size-selective harvesting of larger individuals with higher reproductive potentials can have a greater impact on the reproductive rate of the resources.

Against the background of the concern, the maternal influences, female non-genetic and genetic factors that contribute to offspring fitness (Green 2008), has received large attention recently from fisheries scientists and managers (Palumbi 2004; Berkeley 2006; Lucero 2008; Venturelli et al. 2009). In many species, females vary in ability to produce viable offspring. Larger (and/or older) females produce offspring that have a higher survival rate than offspring from smaller (and/or younger) females, attributing to the maternal influences (Marteinsdottir and Thorarinsson 1998; Vallin and Nissling 2000; Berkeley et al. 2004; Rideout et al. 2005). Therefore, the truncation of the size (and/or age) of a population can directly influence the qualities of offspring through maternal influences and subsequent recruitment (Longhurst 2002; Scott et al. 2006; Sogard et al. 2008), and the removal of larger (and/or older) females from populations causes greater fluctuations in recruitment of commercially fished resources compared to pre-fishing conditions (Marteinsdottir and Thorarinsson 1998; Berkeley et al. 2004; Hsieh et al. 2006; Anderson et al. 2008; Venturelli et al. 2010). Thus, in these years, fisheries scientists and managers have got recognize the importance of considering the contribution of maternal influences on population dynamics and to protect big old females into management strategies for sustainable yields from fishery resources.

On the other hand, the contribution of larger males on reproductive rate of fishery resources has not been recognized among fisheries scientists and managers in comparison with that of the large females. The reason why little attention has been given to this would be that (1) the standard fishery practice use female biomass as a benchmark indicating resource health (i.e. whether targeted resource is overfished or not) because females represent the sex that produces eggs; and (2) it has traditionally assumed that variation of female reproductive success (i.e. reproductive output of the populations) has little to do with both sperm and male availability, because sperm is small and numerous compared with eggs (Parker 1984; Levitan and Petersen 1995) and then males, irrespective of their body size, retain abundant sperm and can mate with multiple females.

However, sperm availability can influence female reproductive success. Sperm production is slow and costly for males (Dewsbury 1982), and so males do not always have an ample number of sperm (Nakatsuru and Kramer 1982; Gage and Cook 1994; Pitnick and Markow 1994; Preston et al. 2001). Therefore, sperm availability for females is occasionally limited. Sperm probability is closely related to population demographic structure because male ability to provide sperm to females is influenced by their body size and mating frequency. For example, smaller males often hold less sperm than larger ones (Pitnick 1996; Jivoff 1997; Kendall et al. 2001), and thus sperm availability can be less in populations with only small males. When the sex ratio in a population is skewed toward females, male mating frequency increases. Because males deplete their sperm reserves through successive matings (Dewsbury 1982; Rutowski et al. 1987; Birkhead 1991; Pitnick and Markow 1994; Bissoondath and Wiklund 1996), female fertilization success can be reduced in a population with a female-biased sex ratio.

The population demographic structure can be changed by hunting and fishing. In several trophy hunting and fisheries, males are more likely to be harvested than female and larger males are preferentially harvested (directly or indirectly) than smaller ones (Smith and Jamieson 1991; Sainte-Marie and Hazel 1992; Coltman et al. 2003; Rowe and Hutchings 2003; Fenberg and Roy 2008). For example, in several large decapod crustacean fisheries, only large males are selectively harvested through fishing regulation (i.e. the large male-selective harvesting) (e.g. Ennis et al. 1990; Smith and Jamieson 1991; Rugolo et al. 1998; Pillans et al. 2005). Such harvesting affects the demography of the population by skewing the sex ratio towards females and decreasing mean male body size (Smith and Jamieson 1991; Abbe and Stagg 1996; Rowe and Hutchings 2003; Pillans et al. 2005; Fenberg and Roy 2008). In such harvested populations, small males replace large males in reproduction and remaining males participate in more matings than in pristine populations (Ennis et al. 1990; Sainte-Marie 1993; Carver et al. 2005; Milner et al. 2007). Therefore, the sperm availability would decrease sharply in large male-selective harvested populations consisting of smaller males and with female-biased sex ratio, which can decrease the reproductive success of females.

Reproductive output of a population subjected to the large male-selective harvesting would also be affected by the male availability. A decrease in density of male individuals in a population by the large male-selective harvesting, reduces the frequency of female encounters with males (Moller and Legendre 2001) and then causes difficulies for females to find mates, resulting in loss of mating opportunity and delayed mating of females (Powell et al. 1974; Ennis 1980; Smith and Jamieson 1991; Ginsberg and Milner-Gulland 1994; Milner et al. 2007). Negative effects of delayed mating on spawning success, fertilization and offspring quality have been reported in several animal species including fishery resources (McMullen 1969; Paul and Adams 1984; Unnithan and Payne 1991; Torres-Vila et al. 2002; Huang and Subramanyam 2003; Milner et al. 2007). For example, delays in the release of eggs after ovulation of just a few hours can reduce egg viability dramatically in Gadus morhua (Kjørsvik and Lønning 1983; Kjørsvik et al. 1990).

Therefore, the large male-selective harvesting is expected to affect the reproductive success of females (i.e. reproductive output of the populations) as well as harvesting larger females from resources. In fact, reduced fecundity and crash have been reported in ungulate populations under selective harvesting of large males, (Milner-Gulland et al. 2003; Milner et al. 2007). However, the negative impacts of the large male-selective harvesting on the reproductive output of resources have received far less attention from fisheries scientists and managers than both that of removal of large females and the direct effect of harvesting on the abundance of many species.

Thus, in this monograph, to signal a need for caution and reconsideration of the present harvesting practices for fisheries resources, I introduce impacts of the large male-selective harvesting (i.e. decreases in sperm and mate availabilities for females) on reproduction and reproductive output of the resources through change of population demographic structure (i.e. indirect effects of the harvesting on its abundance), with emphasis on my own work (Fig. 1).


Fig. 1. Schema of the focus of this monograph showing the indirect effect of large male-selective harvesting: impacts of the harvesting on reproduction and reproductive output of the resources through change in the population demographic structure.

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In my own work, large decapod crustaceans were used to study the impacts of the large male-selective harvesting on reproduction of the resources. The reproductive output of the large decapod crustacean population is determined relatively easier than, for example, that of the free-spawning species in which eggs are directly released into the water because females carry fertilized eggs externally on their body in most crustacean species. The rate of egg-carrying by females and size of the egg clutch are direct indices of a female reproductive output. Therefore, large decapod crustacean species are an ideal model to investigate impacts of the large male-selective harvesting on reproductive output of biological resources.

The sexual size dimorphism of many crustacean species favors the development of sex-biased or single-sex fisheries (Orensanz et al. 1998), and thus the large male-selective harvesting practice prevails in many commercially important large decapod crustacean fisheries, in which males grow to a much larger size than females. Because management of crustacean resources often focuses on protection of females, research into the reproduction of harvested crustaceans has generally focused on numerical aspects of female fecundity (e.g. the number of eggs in a spawn and female lifetime reproductive potential). On the other hand, little is known of male reproductive potential (Sainte-Marie 2007), and thus management decisions in most large decapod crustacean resources have been based on incomplete understanding of its reproductive ecology to date.

The lack of knowledge about the reproductive ecology of harvested species would have hindered our understanding of how current harvesting influences the resources and might have invited undesired consequence. Depletion and collapse of large decapod crustacean resources due to fishing have occurred worldwide. For example, since the 1980s the depletion and collapse occurred in most Alaskan crustacean stocks under the large male-selective harvesting, especially in red king crab Paralithodes camtschaticus and tanner crab Chionoecetes bairdi (Orensanz et al. 1998). There are some reports showing that mean female reproductive success was lower in fished areas, than in unfished areas (e.g. snow crab Chionoecetes opilio, Taylor 1996; red rock lobster Jasus edwardsii, Jack and Wing 2010; spiny lobster Palinurus elephas, Díaz et al. 2011). These facts indicate that the fishing would have a negative impact on female reproductive success through some mechanisms. In the red king crab population, fecundity of females decreased, as the sex ratio was more biased toward females (Orensanz et al. 1998). Furthermore, decreased reproductive success of females was observed in snow crab fished populations as fishing pressure on large males increased (Taylor 1996). Therefore, in recent years, decreased mate and sperm availabilities due to the large male-selective harvesting has been suspected to be the cause of reduced female reproductive success in some large decapod crustacean populations (e.g. Smith and Jamieson 1991; Orensanz et al. 1998; Sainte-Marie et al. 2002; Hines et al. 2003; Carver et al. 2005, but see Hankin et al. 1997) as well as some fish populations (Rowe and Hutchings 2003; Alonzo and Mangel 2004; Heppell et al. 2006). However, a comprehensive understanding of the mechanisms that limit reproductive output of such fished large decapod crustacean populations does not exist, because of the lack of knowledge of the reproductive ecology, especially on male's one.

To attain sustainable harvesting of large decapod crustacean resources, it is important for us to perceive that (1) its reproduction and reproductive output might have been impaired by current large male-selective harvesting and (2) what knowledge is helpful to understand how harvesting influences the resources and to construct management measures mitigating its negative influences. In this monograph, I will also refer to importance of knowledge about reproductive ecology and mating system of each targeted species for attaining sustainable use of biological resources.

This monograph begins with the introduction of reproductive characteristics of three studied species in my work (spiny king crab Paralithodes brevipes (Figs. 2a, b), coconut crab Birgus latro (Figs. 2c, d), and the stone crab Hapalogaster dentata (Fig. 2e)), and presents harvesting patterns for spiny king crab and the coconut crab (in Section 2). Effects of present harvesting on their population demographic structure are also described in Section 2. To examine the influence of the present harvesting pattern (the large male-selective harvesting) on the reproductive output of the resources, the female reproductive success in spiny king crab was investigated and compared between years with different harvesting pressure (in Section 3). In this section, to examine the influence of changes in population demographic structure, caused by the large male-selective harvesting, on female reproductive success, the relationship between population demographic structure and female reproductive success was examined using the stone crab as a model species for commercially male-selective harvested species. To anticipate mechanisms that had decreased female reproductive success in the large male-selective harvested spiny king crab population, Section 4 focuses on the influences of increased male mating frequency and decreased male body size due to the large male-selective harvesting on male reproductive potentials based on laboratory experiments. To investigate whether sperm and mate availability in the large male-selective harvested spiny king crab population is sufficient for clutch fertilization, temporal variation of male sperm reserve and male ability to ejaculate were examined through the combination between field investigations and laboratory experiments (Section 5). The following sections (Sections 6 and 7) deal with other possible mechanisms that can decrease female reproductive success in large male-selective harvested populations. Section 6 focuses on influences of changes in socio-sexual conditions, caused by the large male-selective harvesting, on female reproductive success, for example, the (1) influence of decreased size differences between males and females in mating pairs on mating success, (2) effects of female delayed mating caused by decreasing the availability of male mates on female reproductive success, and (3) effect of female-biased sex ratio on male sperm allocation pattern. Section 7 focuses on plausible interaction between maternal influence and female mate choice for reproductive rates of the resources. The final section will refer to negative impacts of the large male-selective harvesting on the resources and the importance to take into consideration, the reproductive ecology of targeted resources for sustainable use of the biological resources.


Fig. 2. Pictures of three studied species in my work: (a) spiny king crab Paralithodes brevipes in pre-copulatory mate guarding behavior; (b) boiled spiny king crab; (c) coconut crab Birgus latro; (d) steamed coconut crab; (e) stone crab Hapalogaster dentata.

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In this monograph, crab body size is expressed either in carapace length, measured from the right eye notch to the center of the posterior end of the carapace, (hereafter, CL) or thoracic length, measured from the center of the anterior end to the center of the posterior end of the thorax, (hereafter, TL) depending on the studied species. The CL and TL were measured to the nearest 0.1 mm using Vernier calipers.

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2. Effects of the large male-selective harvesting on population demographic structure

2-1. Common features in reproduction among the three studied species

The spiny king crab Paralithodes brevipes (H. Milne Edwards and Lucas 1841), the coconut crab Birgus latro (Linnaeus 1767), and the stone crab Hapalogaster dentata (De Haan 1884) belong together under the amomura, one group of decapod crustaceans. Crabs can be sexed according to the presence of pleopods which are possessed only by females. Males grow to a much larger size than females. Both females and males can have multiple reproductive seasons during their lifetime (Fig. 3). In a reproductive season, females molt once prior to mating and the molting females can mate, except for the coconut crab. Coconut crab females mate without molting. Males store many spermatophores containing a great quantity of sperm in the vasa deferentia. Spermatocytes in the testis but not in the vasa deferentia, spermatozoa (i.e. unpackaged sperm) are in both, and packaged sperm with spermatophores only in the vasa deferentia. Thus, in these species, sperm produced in the testis are transmitted to the vasa deferentia, where they are packaged into spermatophores. Sperm in the spermatophores are the only sperm available for mating.


Fig. 3. Schema of reproductive pattern of three studied species.

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During mating, males deposit a spermatophore mass, which consists of many spermatophores, over and near the gonopores on the female ventral surface because females have no spermatheca. The attached spermatophore mass is retained by the females until egg extrusion and fertilization. The time lapse between mating and egg extrusion is estimated to be less than 60 min in spiny king crab (Sato T. unpubl. data), one wk in coconut crab (Sato and Yoseda 2009b), or 20 min in the stone crab, respectively (Sato T. unpubl. data). Mated females extrude eggs and fertilize externally, within the brood-chamber formed by a flap (a pleon). Hess and Bauer (2002) suggested that the jostling and contact of eggs with spermatophores during egg extrusion may cause the spermatophores to split and release the sperm in anomuran crabs. While females extrude only one clutch in a reproductive season, males can have several matings with females. There is a positive correlation between female body size and number of eggs extruded (spiny king crab, approximately 15–110 thousand eggs (Sato et al. 2007); coconut crab, approximately 50–250 thousand eggs (Sato and Yoseda 2008); stone crab, approximately 0.3–3 thousand eggs (Sato and Goshima 2006). The incubation period is estimated to be about 11 months in spiny king crab (Sato and Abe 1941), 27–29 days in coconut crab (Schiller et al. 1991), or 110 days in stone crab (Goshima et al. 1995).

2-2. Spiny king crab Paralithodes brevipes

2-2a. Introduction of spiny king crab

The spiny king crab inhabiting northern Japan in the Sea of Okhotsk and the Bering Sea (Miyake 1982) is an important fishery resource off eastern Hokkaido, Japan, but the catch in numbers has declined in recent years (Fig. 4, Hokkaido Prefectural Government 1970–2009). In the Hamanaka Bay, east of Hokkaido, Japan (43°30' N, 145°60' E), one of the fishing grounds, females are regarded as attaining functional maturity when their CL is 82.3 mm (Sato et al. 2007), whereas all males with CL > about 55 mm are considered physiologically mature (Sato et al. 2005b). The reproductive season is ordinarily from late April to late May around the region, and receptivity of females rather synchronous in time. However, the start of the reproductive season fluctuates with environmental conditions, such as temperature (Sato et al. 2007). For example, when spiny king crabs are reared in tanks containing seawater that is slightly warmer than that in nature, the reproductive season is from mid-March to mid-April.


Fig. 4. Annual variation in catch amount of spiny king crab Paralithodes brevipes in Hokkaido (from Hokkaido Suisan Gensei 1970–2009).

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2-2b. Harvesting pattern of the spiny king crab

During a reproductive season, sexually mature crabs migrate into shallow water (Sato and Abe 1941), and are then caught in crab pots. Fishing for this crab by Japan began about 1935 off eastern Hokkaido (Sato and Abe 1941) and was unregulated until 1980. However, due to declining catches, all fishery activities were suspended completely between 1981–1983. From 1984, all females were protected from fishing and only males with CL of about 86.8 mm could be fished. In this study, carapace width was translated into CL, based on the relationship between CL and carapace width in spiny king crab with reported by Mori (1993). In 1987, only males larger than 80 mm CL and females larger than 100 mm CL without a clutch could be fished. Since 1991, only males larger than about 69.7 mm CL have been fished (i.e. large male-selective harvesting); minimum legal size has not changed. The fishing season for this species extends from 1 April until July off the coast of Hamanaka every year. Landings of the crab have still declined in spite of the application of the present fishery regulations.

2-2c. Demographic structure of harvested spiny king crab population

Field investigations of the population demographic structure of a fished population were conducted by the Kushiro Fisheries Experimental Station off the coast of Hamanaka from 1989 to 1992. Crabs were caught in crab pots at various sites and depths (<40 m) in late May and the sex and size were recorded for each crab. To compare the population demographic structures before and after the change in regulation, Sato et al. (2005b) analyzed the population demographic structures in 1989–1992. In 1991, the minimum legal size for this crab decreased from CL 80 mm to CL about 69.7 mm.

In both 1989 and 1990, there was no significant difference in size distribution between males and females (Kolmogorov-Smirnov test, in 1989: df = 2, Male: n = 262, Female: n = 274, χ2 = 4.75, P = 0.186, Fig. 5a, in 1990: df = 2, Male: n = 294, Female: n = 226, χ2 = 0.60, P > 0.99, Fig. 5b). But in both 1991 and 1992, after the change in regulation, the size distributions between males and females differed significantly (Kolmogorov-Smirnov test, in 1991: df = 2, Male: n = 381, Female: n = 749, χ2 = 339.06, P < 0.001, Fig. 5c, in 1992: df = 2, Male: n = 241, Female: n = 499, χ2 = 261.14, P < 0.001, Fig. 5d). Both the mean body size and abundance of females were apparently larger than those of males after the change in regulation (Figs. 5c, d). Mean male size differed significantly between before (1989–1990) and after (1991–1992) the change (Mann-Whitney U-test, z = –10.56, P < 0.001, before the change: 76 ± 11.0 SD mm CL, after the change: 68 ± 8.90 SD mm CL). After the change in fishing regulations in 1991, the mean male size decreased and sex ratio skewed sharply toward females. In addition, larger males just above the new legal size (about CL 69.7 mm) decreased sharply in 1991 and 1992 (Figs. 5c, d). On the contrary, mean female size in 1991–1992 was significantly larger than that in 1989–1990 (Mann-Whitney U-test, z = –10.42, P < 0.001, before the change: 74 ± 10.0 SD mm CL, after the change: 80 ± 8.70 SD mm CL). Despite that increase in the mean female size after the change in regulation, only the mean male size significantly decreased, indicating that the new regulation since 1991 influenced their population demographic structure.


Fig. 5. Size distributions of males and females spiny king crab Paralithodes brevipes late May in 1989–1991 (a–d) off the coast of Hamanaka per definite sampling efforts (10,000 crab pots d–1). MLS in (c) and (d) indicates the minimum legal size (∼69.7 mm CL). Each arrow indicates the annual average of male CL. CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 7, © 2005b, Inter-Research Science Center.

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Generally, the population structure of fished species is affected not only by an anthropogenic factor such as fishery activity but also environmental factors such as temperature. A series of atmospheric and oceanographic changes occurred over the North Pacific in 1988/89, which is difined as a "minor regime shift", and lasted for several years (Minobe 2000). However, in the Hamanaka area, there were no notable differences in either water temperature (1990: 4.5 ± 1.4 SD°C, 1991: 4.8 ± 1.5 SD°C) or the relative density of seawater (1990: 1.0244 ± 0.0013 SD g × ml–1, 1991: 1.0245 ± 0.0005 SD g × ml–1) between reproductive seasons in 1990 and 1991 when the population demographic structure changed sharply. Therefore, the large male-selective harvesting is the most plausible cause skewing the sex ratio towards females and decreasing the mean male size in the harvested spiny king crab population, although there may be other causes. The sharp increase in fishing pressure on larger males at 1991 might make the change of population demographic structure due to the large male-only harvesting come to the surface, although the changes were not observed in both 1989 and 1990.

2-3. Coconut crab Birgus latro

2-3a. Introduction of coconut crab

The coconut crab lives in coastal areas of the tropical Indo-Pacific region. Populations in most habitats have been severely depleted or have become virtually extinct (Brown and Fielder 1991; Shokita 2006). Overharvesting (Fletcher 1993) and habitat destruction (Eldredge 1996) are considered to be two of the main causes for the present depletion of the resources. Also in the Sakishima archipelago, southwest of Okinawa, Japan, the coconut crab has decreased sharply in recent years (Shokita 2006). Male: female sex ratio (hereafter, SR) of the coconut crab is 1:1 (Helfman 1973). On the Hatoma Island (24°28' N, 123°49' E), one of the islands in the archipelago, females are deemed to attain functional maturity when their TL is 24.5 mm (Sato and Yoseda 2008), whereas all males with TL >25 mm are considered physiologically mature (Sato et al. 2008). The reproductive season starts around early June and ends in late August, and most females finish extruding eggs by mid July (Sato and Yoseda 2008). Females mate in the hard-shell condition (Helfman 1977), and then extrude and fertilize eggs in burrows (Sato and Yoseda 2009a). Female pleonal expansion is strongly correlated with female reproductive activity, and the index of pleonal expansion can be used as a morphological criterion for selecting females that are able to mate (Sato and Yoseda 2009b).

2-3b. Harvesting pattern of the coconut crab

Although coconut crabs have been traditionally eaten by locals, there have been few serious attempts to manage the stocks of coconut crabs in any region (Fletcher 1993). Minimum legal size limits have been imposed in some areas, e.g. Guam and Vanuatu and capture of ovigerous females has been banned the in Guam and Federated States of Micronesia. However, these management strategies largely are not based on scientific evidence (Brown and Fielder 1991).

To investigate the harvesting pattern for this crab, Sato and Yoseda (2010) recorded the size and sex of harvested coconut crabs, that are marketed for consumption in Ishigaki Island (24°34' N, 123°16' E), which is one island of the Sakishima archipelago, southwest of Okinawa, Japan in 2008. Although there is no regulation against catching females in this region, the harvesting pattern was large male-selective harvesting, in which larger males (>40 mm TL) were almost exclusively taken approximately 21 times as many as females (Mean TL ± SE, Male: 47.8 ± 0.2 mm TL (range: 34.0–72.3 mm TL), n = 1055; Female: 41.8 ± 0.6 mm TL (range: 34.9–58.7 mm), n = 50; Fig. 6a). This unique harvesting pattern must be the result from the prevailing concept among locals that to protect females being able to extrude eggs and smaller males from harvesting will be sufficient to sustain the coconut crab resource even if larger males are excessively removed from the population (T. Sato, personal communication with local people).


Fig. 6. (a) Size and sex of coconut crabs Birgus latro marketed for consumption in Ishigaki Island in 2008 (total number of individuals: male, n = 1055; female, n = 50), and (b) size and sex of individuals in harvested population at Hatoma Island in 2007 (total number of individuals: male, n = 453; female, n = 557). TL: thoracic length. Reprinted and modified with permission from Marine Ecology Progress Series, 402, Sato and Yoseda, Influence of size- and sex-biased harvesting on reproduction of the coconut crab Birgus latro, 171–178, Fig. 1, © 2010, Inter-Research Science Center.

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2-3c. Demographic structure of harvested coconut crab population

Does the large male-selective harvesting change population demographic structure of the harvested coconut crab population? Field investigation of the harvested population, in which crabs were captured by hand all over the island and then sex and TL were recorded, was conducted from early June to late August 2007 (Sato and Yoseda 2010).

As a result, as seen in other resources subjected to the large male-selective harvesting, its sex ratio skewed significantly toward females and the mean male size would decrease. Observed SR (0.81:1) was significantly skewed toward females (Chi-square test, χ2 = 10.71, df = 1, P = 0.001). The mean TL of males was nearly equal to that of females (Mean TL ± SE, Male: 32.3 ± 0.4 mm TL (range: 11.4–61.2 mm TL, Median: 31.7 mm TL), n = 453; Female: 29.6 ± 0.2 mm TL (range: 14.9–44.6 mm, Median: 29.7 mm TL), n = 557; Fig. 6b). The difference between sexes, which was calculated by subtracting the female TL from the male TL, was 2.7 mm TL. The mean and median TL of males was nearly equal to those of females in the harvested population, nevertheless coconut crabs usually exhibit clear sexual size dimorphism in which the mean body size of females is smaller by an order of 20–25% than that of males (Fletcher et al. 1991). Fletcher et al. (1991) suggest that the difference between sexes has been attributed to the harvesting pattern, e.g. the smaller difference indicates the higher pressure of exploitation. The disappearance of sexual size dimorphism, i.e. a decrease in mean male size, in the Hatoma population would be a result of the present large male-selective harvesting. Therefore, also in the harvested coconut crab populations, the large male-selective harvesting skewed the sex ratio towards females and decreased the mean male size.

2-4. Introduction of stone crab Hapaologaster dentata

The stone crab is widely distributed in Japan, ranging from Kyushu to Hokkaido, and on the coast of the Korean Peninsula (Miyake 1982). They inhabit intertidal and subtidal cobble rocky shores throughout their life except for planktonic larval stage. They hide and cling under cobbles, and individuals that move away from cobbles are rarely seen, suggesting that this species has low mobility.

Although the stone crab is not harvested, they are closely related to commercially important lithodid crabs, such as king crab (Cunningham et al. 1992). Its reproductive behavior strongly resembles that of commercially important lithodid crabs (Goshima et al. 1995, 2000), although it has some differences from commercially important crabs, such as smaller body size, lower fecundity, and a lack of seasonal-dependent migration.

Goshima et al. (1995, 2000) reported its life history and ecology in Kattoshi on the southwest side of Hakodate Bay, southern Hokkaido, Japan (41°44' N, 140°36' E). The reproductive season is from October to March. During the reproductive season, the SR of the stone crab is 1:1. Female size at functional maturity is 7.2 mm CL; male size at gonadal maturity, estimated by histological examination of the testis and vasa deferentia is 5.3 mm CL.

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3. Effects of the large male-selective harvesting on female reproductive success

3-1. Difficulty in investigation into influence of harvesting on the reproductive output

Does the large male-selective harvesting influence reproductive output of the harvested population by skewing the sex ratio towards females and decreased mean male size? Little is known of how the large male-selective harvesting influences on the reproductive output of fished crab populations (i.e. degree and temporal pattern of decrease in reproductive success of females) despite large males are selectively harvested in several large decapod crustacean fisheries. The reason why little is known of it would be that estimation of the actual influences of commercial male-selective harvesting on the reproductive output of crab stocks is quite difficult because most large decapod crab populations are affected by commercial fisheries, that is, few control populations exist. However, comparison of female reproductive success between years or areas which are exposed to contrasting fishing pressure, could allow us to determine whether current large male-selective harvesting has negative impacts on reproductive output of harvested populations.

3-2. Relationship between fishing pressure and female reproductive success in fished spiny king crab population

Sato et al. (2007) had a good chance to compare the reproductive success of females between years with different fishing pressures for spiny king crab population. Their reproductive season is ordinarily from late April to late May in Hamanaka Bay. However, the start of the reproductive season fluctuates with the year, i.e. environmental conditions. In ectothermic organisms, physiological activities often depend on temperature (Begon et al. 1990), and water temperature is one of the most important direct causes of the start of the reproductive season in aquatic invertebrates (Giese 1959; Lancaster 1990). Indeed, when spiny king crabs are reared in tanks containing seawater that is slightly warmer than that in nature, the reproductive season is from mid-March to mid-April (Sato et al. unpublished data). Because the fishing season for this species is from April 1 until July in Hamanaka Bay every year, the time lag in the start of the reproductive season between years will produce a difference in total fishing pressure on fished populations before the start of and during the reproductive season between years. For example, in a year when the seawater temperature is relatively high, the reproductive season would be early and then the number of larger males fished before and within the reproductive season would be less than a year when the seawater temperature is low. This difference results in variations in mate and sperm availabilities within the reproductive season between years.

The reproductive season of spiny king crab in 2004 started about one month earlier than in 2003 (2003, early to late May; 2004, early to late April, Sato et al. 2007), which is not ordinary, because the seawater temperature in 2004 was unusually higher than that in 2003 in Hamanaka Bay. The time lag between years produced a difference in total fishing pressure on fished populations before the start of the reproductive season between years. There was a marked difference in cumulative landing of male spiny king crabs before the start of the reproductive season between years in Hamanaka Bay (cumulative landing before the start/total landings in each year × 100 (%): 2003, 31.7%; 2004, 6.1%, Sato et al. unpublished data). In 2003, when the reproductive season started one month later than in 2004, the proportion of legal-sized males fished before the start of the reproductive season was greater than in 2004. The reduction in number of larger males would decrease the sperm and male availabilities for females especially in 2003, compared to 2004.

Thus, to elucidate whether the large male-selective harvesting has negative impacts on their reproductive output in fished spiny king crab populations, Sato et al. (2007) compared (1) fertilization rate, (2) clutch condition, and (3) female reproductive success in the fished spiny king crab population between 2003 and 2004 with different fishing pressures.

First, ovigerous females were collected in Hamanaka Bay and then their fertilization rates were examined. More than 150 of the eggs were collected at random from several parts of each clutch using a pair of tweezers, and then cell division of a total of 150 eggs was observed under a stereomicroscope. In this monograph, the percentage of dividing eggs in the sample was taken as the fertilization rate for the clutch. Some females showed low fertilization rates both in 2003 and 2004 (mean fertilization rate ± SE, 2003: 79.4 ± 5.4%; 2004: 89.7 ± 2.0%, Sato et al. 2007) and the difference in fertilization rate between these years was almost significant (Welch test, t = 1.81, df = 41.58, P = 0.077; Levene test, P = 0.003).

Their clutch conditions, a qualitative indicator of female clutch, were also examined. In this monograph, the clutch condition is ranked into three categories: rank A, a normal clutch full of eggs; rank B, pleopods visible among eggs due to egg loss; rank C, few or no attached eggs. In both years, some females had no or partial clutches (rank B or C) (Sato et al. 2005a). The proportion of each clutch condition in 2003 was significantly different from 2004 (G-test, G = 5.30, df = 1, P = 0.021), and the proportions of no or partial clutches in 2003 were significantly higher than in 2004 (Fig. 7). Although water temperature differed between the years, the difference would have little effects on difference of the clutch condition between years because 1) examined clutches were only just spawned and 2) water temperature was not too high to deteriorate the clutch condition during which females spawned and were ovigerous in both years (2003, 7.2 ± 1.1 SD°C; 2004, 4.7 ± 0.9 SD°C). In the seed production program of the spiny king crab, water temperature for rearing of ovigerous females was recommended to be kept below 10°C (Ashidate and Sato 2009).


Fig. 7. Proportion of the clutch condition of females in fished population off the coast of the Hamanaka in 2003 (n = 34) and 2004 (n = 102). Rank A was a normal clutch with many eggs, Rank B was pleopods visible because of a small number of incubated eggs, and Rank C was few or no attached eggs.

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After that, female reproductive success for each female was estimated. The female reproductive success was estimated by: (number of viable eggs incubated by the female/(expected number of eggs at the time of spawning for each female estimated from the regression of the number of eggs against its body size) × 100. Collected ovigerous females were reared in tanks for about four months after the reproductive season to estimate the female reproductive success. The reason why ovigerous females were reared for a while are that (1) non-fertilized eggs gradually disintegrate and drop from the clutch, (2) the negative effects of delayed mating on eggs may come out during egg development if female mating had delayed (Sato et al. 2005a), and (3) female reproductive success should be estimated once it is possible to judge whether eggs retained by a female are viable or not. All eggs incubated by the females were removed in mid-September when eye pigment was visible in viable eggs and then the number of viable eggs was estimated. As a result, the female reproductive success in 2003 was more variable than in 2004 (mean reproductive success ± SE, 2003: 43.0 ± 5.2%; 2004: 63.4 ± 2.9%, Fig. 8), and the reproductive success of the stock in 2003 was significantly lower than in 2004 (t-test, t = –3.57, df = 121, P = 0.001; Levene test, P = 0.26).


Fig. 8. Mean female reproductive success of fished spiny king crab Paralithodes brevipes populations in Hamanaka Bay in 2003 (n = 35) and 2004 (n = 88). The box plots indicate median, lower and upper quartiles, with whiskers extending to minima and maxima. Reproduced from Canadian Journal of Fisheries and Aquatic Sciences, 64, Sato et al., Does male-only fishing influence reproductive success of female spiny king crab, Paralithodes brevipes?, 735–742, Fig. 5, © 2007, Canadian Science Publishing or its licensors.

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In 2004 when fishing pressure before and within the reproductive season was exceptionally lower than in ordinary years, attributing to the time lag in the start of the reproductive season, the sperm and mate availabilities during the reproductive season would be higher than in ordinary years. This difference in influence of the large male-selective harvesting on the sperm and mate availabilities between the years would result in (1) a nearly significant higher fertilization rate of the population, (2) larger clutches of most females, and (3) a higher reproductive success of females in 2004 than in 2003. Results of this comparison of the female reproductive success between years with exposure to contrasting fishing pressure indicates that the current large male-selective harvesting would have negative impacts on reproductive output of harvested spiny king crab populations by changing demographic structure of the harvested population.

3-3. Relationship between population structure and female reproductive success in manipulated populations of an unfished crab, stone crab

However, is the change of population demographic structure due to the large male-selective harvesting really a cause for decreasing female reproductive success in a harvested population? Female reproductive success can show temporal fluctuation on various temporal scales, and when decreased female reproductive success is observed, it can be very difficult to determine the respective contributions of natural and anthropic sources to the decreased female reproductive success (Sainte-Marie et al. 2002). To conquer this difficulty, Sato and Goshima (2006) conducted a massive field experiment using the stone crab as a model species to investigate the influence of changes in population demographic structure, caused by the large male-selective harvesting, on female reproductive success. Since the stone crab is not fished, inhabits intertidal cobble rocky shores, and has low mobility, their population demographic structure can be manipulated without difficulty and any fishery interferences. Therefore, the reproductive success of populations of different demographic structures can be compared; for example, comparing the reproductive success of populations with many large males with that of populations having only small males, if some populations are manipulated simultaneously.

In this field experiment, to investigate the relationship between female reproductive success and population demographic structure, 1,600 mature stone crabs were used (small male: CL 6–10 mm, n = 268; large male: CL > 13 mm, n = 268; small female: CL 8–9 mm, n = 400; medium female: CL 9–11 mm, n = 400; large female: CL > 11 mm, n = 264), and then 16 artificial stone crab populations whose demographic structure was manipulated were formed from the five groups with 100 individuals in each population. Just before the reproductive season, four types of artificial populations consisting of these sizes and sex ratios were formed and placed in intertidal cobble rocky shores respectively (Table 1): 1) 50 large males and 50 females (19 small, 19 medium, and 12 large females), 1:1 SR (=LE population (n = 4) because of the large male size distribution and equal SR); 2) 17 large males and 83 females (31 small, 31 medium, and 21 large females), 5:1 SR, (=LB population (n = 4) because of the large male size distribution and biased SR); 3) 50 small males and 50 females (19 small, 19 medium, and 12 large females), 1:1 SR (=SE population (n = 4) because of the small male size distribution and equal SR); 4) 17 small males and 83 females (31 small, 31 medium, and 21 large females), 5:1 SR, (=SB population (n = 4) because of the small male size distribution and biased SR). In this study, in the case of the size of the individual participating in mating, LE populations were most similar to the natural and unmanipulated H. dentata population, and SB populations were most similar to commercially large male-selective harvested populations. After the mating and spawning season, 425 females were collected from the manipulated populations, and then the reproductive success of each female was estimated by the same method as above. Simultaneously, the time of females mating (the first half or the second half of the reproductive season) was estimated based on the development stages of their eggs.


Table 1. Summary of types of artificial stone crab populations. SR: sex ratio. SM: small males (carapace length (CL) 6–10 mm). LM: large male (CL > 13 mm). SF: small female (CL 8–9 mm). MF: medium female (CL 9–11 mm). LF: large female (CL > 11 mm). Each artificial population was formed from the five groups with 100 individuals with manipulating its demographic structure.

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The female reproductive success of SB populations was smallest among all population types (Fig. 9). Male size, sex ratio, and the time of female mating significantly influenced the female reproductive success (Three-way ANOVA, Table 2). The female reproductive success was significantly higher in the populations consisting of large males, or in the populations with a 1:1 SR. The reproductive success of females mated in the early reproductive season was significantly higher than for females mated in the late reproductive season. Two nearly significant two-way interactions occurred between male size and SR, and male size and time of female mating (Table 2). These results strongly suggest that (1) the reproductive success of females was more variable with SR in populations consisting of small males, than in populations consisting of large males, and was lower when the SR was skewed toward females (i.e. when the predicted frequency of male mating is high), and (2) the reproductive success of females was more variable with time of female mating in populations consisting of small males than in populations consisting of large males, and was lower when the time of female mating was late. As expected, a change of population demographic structure (a decrease in male size and a skewed SR toward females) due to the large male-selective harvesting influenced the female reproductive success in the manipulated population.


Fig. 9. Temporal change in the mean female reproductive success for each population based on male size and sex ratio in the stone crab Hapalogaster dantata. L: large males in population, S: small males in population, E: equal SR, B: biased SR. See Subsection 3-3 for details. Different letters above bars indicate significant differences. For each treatment n = 4. Error bars: ±SE. Reprinted and modified with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Fig. 7, © 2006, Inter-Research Science Center.

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Table 2. Three-way ANOVA of the effects of male size, sex ratio, and timing of female mating on the estimated mean reproductive success of females of the stone crab Hapalogaster dentata populations with variable demographic structures. Cochran test: not significant. Reprinted with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Table 1, © 2006, Inter-Research Science Center.

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Furthermore, the change of population demographic structure also forms a temporal gradient of the reproductive success in response to their time of mating especially in SB populations. Such temporal gradient of the reproductive success was also observed in fished spiny king crab population (Sato et al. 2007), suggesting sperm and mate availabilities for females would decrease sharply throughout the reproductive season in populations subjected to the large male-selective harvesting.

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4. Effects of the large male-selective harvesting on male reproductive potentials

By what mechanisms does the change of population demographic structure (a decrease in male size and a skewed SR toward females) decrease female reproductive success in harvested population? Sperm limitation would be considered as one of the plausible mechanisms decreasing female reproductive success in populations subjected to the large male-selective harvesting. Sperm limitation can arise in various animal taxa (Dewsbury 1982, Birkhead 1991, Pitnick and Markow 1994). The probability that females suffer from the sperm limitation, insufficient sperm supply for fertilization, is closely related to male mating frequency and body size, because these factors are closely related to male ability to ejaculate sperm. In this section, to determine mechanisms decreasing female reproductive success in the large male-selective harvested decapod crustacean populations, the influences of decreased male body size and increased male mating frequency on male reproductive potentials are focused through laboratory experiments using spiny king crab, coconut crab, and the stone crab. The recovery rate of male sperm reserves is also examined because the recovery rate of male sperm resources is also one of the important factors influencing the degree of sperm limitation for females.

4-1. Method to extract sperm from spermatophores

To elucidate the influences of male body size and mating frequency on their reproductive potentials, we need to have a suitable method for each studied species to quantify the number of sperm retained by males or the number of ejaculated sperm. In species in which sperm is packaged in spermatophores, all packed sperm must be released and separated from the spermatophores before being able to count the sperm. Studies of some crustacean species (e.g. Rondeau and Sainte-Marie 2001; Kendall et al. 2002) reported methods to count sperm in which the contents of the female spermathecae are homogenized and filtered to collect and count sperm. However, there are some problems when this method is applied to anomuran crabs in which the spermatophores are enveloped in adhesive materials (Hess and Bauer 2002). First, examining the number of sperm is difficult when the male reproductive tract (e.g. vasa deferentia and testis) is too large to homogenize. Second, released sperm from spermatophores become enveloped in the adhesive materials during the homogenizing, forming aggregates of sperm and adhesive materials that make counts unreliable.

Sato et al. (2004), Sato and Goshima (2006), and Sato et al. (2008) established a method for anomuran crabs (spiny king crab, the stone crab, and coconut crab) to extract the sperm from spermatophores using a 20% sodium hydroxide (NaOH) solution. Sperm in the spermatophore are released when the spermatophore is dissolved by soaking with NaOH solution. The method using a NaOH solution is applicable for any size of male reproductive tract and provides disaggregated sperm for reliable counts, allowing us to quantify the number of sperm accurately and to estimate the male reproductive potential in these species.

4-2. Effects of male body size on male reproductive potentials

First, effects of male body size on their reproductive potentials (number of retained sperm, possible number of matings, number of ejaculated sperm, and fertilization rate) were investigated through several laboratory experiments.

4-2a. Number of retained sperm

The relationships between male body size and the number of sperm retained in the vasa deferentia were investigated. Males were killed outrightly by puncturing a ganglion of the central nervous system with a needle through the shell underneath the point between the bases of the first pair of pereiopods. After the puncturing, vasa deferentia were removed and placed in a tube, and the tube was filled with a fixed quantity of 20% of NaOH solution to extract the sperm. Extracted sperm were placed on a hemocytometer and counted under an optical microscope. In spiny king crab, the number of sperm both in the vasa deferentia increased significantly with increasing male size (linear regression, vasa deferentia: log10 no. of sperm = 4.87 × log10 Male size - 1.66, r2 = 0.73, P < 0.001, Fig. 10, Sato et al. 2005b). A similar tendency was observed in the coconut crab (Sato et al. 2008) and the stone crab males (Sato and Goshima 2006). Also in several decapod crustaceans, larger males have larger sperm reserves (e.g. red rock lobster, MacDiarmid 1989; American lobster Homarus americanus, Gosselin et al. 2003, blue crab Callinectes sapidus, Jivoff 2003; snow crab, Sainte-Marie et al. 2008).


Fig. 10. Relationship between male body size and the number of sperm in the vasa deferentia (n = 95) in spiny king crab Paralithodes brevipes. CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 8, © 2005b, Inter-Research Science Center.

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4-2b. Possible number of mating

The relationships between male body size and male ability to successive matings were examined. Spiny king crab males varying in body size (range: CL 74.2–128.5 mm; divided into six classes with every 10 mm CL) were placed individually with five females in an aquarium during the reproductive season, and then mating success for each male mating order was recorded. Success or failure of each mating was judged by the attachment of spermatophores on her ventral surface or the spawning of fertilized eggs. The degree of decline in percentage of male mating success with increasing male mating frequency differed significantly between the male size classes (log-rank test, χ2 = 15.60, df = 5, P = 0.008, Fig. 11), and small males could mate with only a few females compared with large males (Sato et al. 2005b). Also in the other studied species, the number of matings by males attained, increased with male body size (the stone crab, Sato and Goshima 2006; coconut crab, Sato 2011). The reason why larger males are able to achieve more matings than smaller ones would attribute to the fact that larger males have larger sperm reserves.


Fig. 11. Relationship between mating frequency by males of various body sizes and percentage of mating success in spiny king crab Paralithodes brevipes. CL: carapace length. Numbers above bars: sample size. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 4, © 2005b, Inter-Research Science Center.

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However, only in spiny king crab, males in the largest size class examined, showed a decrease in mating success with increasing male mating frequency like in the small males (Fig. 11). A similar tendency is also seen in the largest males of the red king crab (Paul and Paul 1990) and freshwater crayfish Austropotamobius italicus (Rubolini et al. 2007). These tendencies may attribute the ongoing senescence of the reproductive performance of large male although the reason is not clear.

4-2c. Number of ejaculated sperm

To examine the effects of male body size on the number of ejaculated sperm in spiny king crab, small males (CL 80.0–85.0 mm), large males (CL 100.0–110.0 mm), and females (pre-molt CL 100.0–110.0 mm) were used. Two groups of mating pairs were formed: small or large male vs. female, and then ejaculated sperm were counted for each mating pair as follows. After mating, the attached spermatophores were collected from the ventral surface by cutting out parts of the female exoskeleton. These pieces of exoskeleton with attached spermatophore masses were placed into a tube, and the tube was filled with a fixed quantity of 20% NaOH solution to extract and count the sperm.

The number of ejaculated sperm differed significantly between the small and the large males (Mann-Whitney's U test, z = –3.71, P < 0.001), and the large males passed more sperm to females than do smaller males (mean ± SD, small males, 22.4 ± 6.2 × 106; large males, 47.2 ± 10.4 × 106, Fig. 12). Larger males pass much larger ejaculates also in the other studied species (coconut crab, Sato et al. 2010; Sato 2011; the stone crab, Sato and Goshima 2007a) and other decapod crustaceans (Caribbean spiny lobster Panulirus argus, MacDiarmid and Butler 1999, American lobster, Gosselin et al. 2003; blue crab, Jivoff 2003).


Fig. 12. Effect of male body size on number of ejaculated sperm by small (CL 80–85 mm) or large (CL 100–100 mm) males to females (premolt CL 100–110 mm) in spiny king crab Paralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates.

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4-2d. Fertilization rate

To examine the effects of male body size on the fertilization rate in spiny king crab, small males (CL 80.0–85.0 mm), large males (CL 100.0–110.0 mm), and females (pre-molt CL 100.0–110.0 mm) were used, and then mating pairs were formed: small or large male vs. female. After mating and spawning, the fertilization rate for each mating pair was examined by the same method as above.

The fertilization rate also differed significantly with male size (ANOVA, F1,12 = 7.11, P = 0.021), and females mated with the large males showed a higher fertilization rate (mean ± SD, small males, 97.8 ± 2.7%; large males, 99.8 ± 0.3%). However, the fertilization rate of females mated with small males showed only a small difference from that of females mated with large males, even though the small spiny king crab males also passed significantly smaller ejaculates to females than larger males.

This discrepancy may result from artificial environments in the experimental aquaria in which the females spawned and fertilized their clutches: the aquaria had little water current even though aerated seawater flowed through all aquaria. In free-spawning species, the fertilization rate decreases as the velocity of water current increases around spawning females at spawning (Pennington 1985, Denny and Shibata 1989), mainly because dilution of the sperm in the water. Spiny king crab females spawn and fertilize their eggs externally within the brood-chamber formed by a flap under the body. This process of fertilizing eggs increases the chance of sperm loss and decreases the fertilization rate (Subramoniam 1993), and the amount of loss and decrease is influenced by the velocity of the water current around spawning females at fertilization. Although smaller male stone crabs also pass much smaller ejaculates to females than do larger males (Sato and Goshima 2007a), the fertilization rate of the females mated with smaller males does not differ from females mated with larger males when females mate in an aquarium without a water current (Sato and Goshima 2006). However, when the stone crab females mate in a natural habitat with a water current, the fertilization rate of females mated with smaller males is markedly lower than for females mated with larger males (small male: 83.8 ± 16.7%, large male: 99.9 ± 0.3%, Sato and Goshima 2007a). Furthermore, also in coconut crabs that mate and extrude/fertilize eggs terrestrially without submerging in water (Sato and Yoseda 2009a), the fertilization rate of females mated with larger males is markedly higher (small male: 80.6 ± 11.2%, large male: 99.8 ± 0.4%, Sato et al. 2010). Therefore, in these anomuran crabs inhibiting in aquatic environment, fertilization rate can be influenced by the water current around spawning females. The observed declines in fertilization rate of females mated with small males in the three studied species would result from the insufficient sperm supply from smaller males.

4-3. Effects of male mating frequency on male reproductive potentials

Second, effects of male mating frequency on their reproductive potentials (number of ejaculated sperm, and fertilization rate) were investigated through several laboratory experiments.

4-3a. Number of ejaculated sperm

Spiny king crab males (CL 80.0–83.6 mm) were placed respectively into separate aquaria, and then each male mated with three females (pre-molting CL 100.0–107.7 mm) in turn. Ejaculated sperm for each mating was counted by same method as above. Male mating frequency had a significant effect on the ejaculate size (repeated measures ANOVA, F2,12 = 91.97, P < 0.001, Fig. 13), and the number of ejaculated sperm decreased significantly with increasing male mating frequency (Sato et al. 2005b). A similar tendency was reported also in other decapod crustaceans (blue crab, Kendall et al. 2002; stone crab, Sato and Goshima 2006; freshwater crayfish, Rubolini et al. 2007; coconut crab, Sato et al. 2010).


Fig. 13. Relationship between male mating frequency and number of ejaculated sperm in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 1, © 2005b, Inter-Research Science Center.

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4-3b. Fertilization rate

To examine the influence of male mating frequency on the fertilization rate, spiny king crab males (CL 80.0–85.0 mm) and females (pre-molting CL 100.0–110.0 mm) were used. Each male mated with three females in turn and then the fertilization rates for the successive matings were examined by the same method as above. Male mating frequency also had a significant effect on the fertilization rate (Friedman test, χ2 = 6.63, df = 2, P = 0.036, Fig. 14) and the fertilization rate decreased significantly as male mating frequency increased (Sato et al. 2005b). The decrease in fertilization rate with increasing male mating frequency would be caused by a decreased sperm supply with increasing male mating frequency, that is, sperm limitation. Increased male mating frequency will increase the probability that sperm limitation occurs. The reduction in the fertilization rate with increasing male mating frequency is reported also in red king crab (Powell et al. 1974) and blue crab (Hines et al. 2003).


Fig. 14. Relationship between male mating frequency and fertilization rate in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 3, © 2005b, Inter-Research Science Center.

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4-4. Interactions between male body size and male mating frequency for male reproductive potentials

Third, the interactions between male body size and mating frequency for the male reproductive potentials (number of ejaculated sperm and fertilization rate) were examined through several laboratory experiments.

4-4a. Number of ejaculated sperm

To examine the interaction of male body size and mating frequency for the number of ejaculated sperm, coconut crab males of different body size (range 30.8–54.2 mm TL) and females (range 27.9–37.5 mm TL) were used. Three mating groups were formed: males were mated with one female each, mated with two females successively, or mated successively with three females, and then the ejaculated sperm at the last mating of each male was counted by the same method as above.

Larger males passed more sperm to females, regardless of male mating frequency (Linear regression, first mating: number of ejaculated sperm = 0.55 male TL - 11.71, r2 = 0.85, n = 14, F1,12 = 68.9, P < 0.001; second mating: number of ejaculated sperm = 0.29 male TL - 8.08, r2 = 0.72, n = 16, F1,14 = 55.0, P < 0.001; third mating: number of ejaculated sperm = 0.16 male TL - 4.70, r2 = 0.72, n = 12, F1,10 = 26.3, P < 0.001, Fig. 15, Sato et al. 2010). Smaller males passed only a small number of sperm to females in the second and the third matings. It has been observed that larger males always provide larger ejaculates to females even after successive matings than do smaller males also in spiny king crab (Sato et al. 2006) and blue crab (Jivoff 1997).


Fig. 15. Relationship between male mating frequency by males of various body sizes and the number of ejaculated sperm in coconut crab Birgus latro (first mating, n = 14; second mating, n = 16; third mating, n = 12). TL: thoracic length. Reprinted with permission from Aquatic Biology, 10, Sato et al., Sperm limitation: possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro, 23–32, Fig. 3, © 2010, Inter-Research Science Center.

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4-4b. Fertilization rate and male reproductive success

To determine the interaction of male body size and mating frequency for the fertilization rate, spiny king crab males of different body sizes (range: CL 74.2–128.5 mm; divided in to six classes with every 10 mm CL) were placed individually with five females in an aquarium during the reproductive season, and then examined the fertilization rate for each male mating.

The relationship between the fertilization rate and male mating frequency showed different tendencies between the male size classes (Fig. 16, Sato et al. 2005b). A large variation in the fertilization rate was seen with increasing male mating frequency in smaller males (<CL 100 mm, especially in the smallest males (CL 70–80 mm)) and the fertilization rates were relatively low compared with larger males (>CL 100 mm). In contrast, larger males (>CL 100 mm) showed little decrease in fertilization rate (Fig. 16). If the mating occurred in a natural habitat with a water current, fertilization rate may be lower than the results of this experiment.


Fig. 16. Relationship between mating frequency by males of various body sizes and the fertilization rate in spiny king crab Pralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 5, © 2005b, Inter-Research Science Center.

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The interaction of male body size and mating frequency for male reproductive success was also investigated using the stone crab males of different body size (small male: CL 6.0–7.0 mm; medium male: CL 9.0–10.0 mm; large male: CL 13.0–14.0 mm) and females (pre-molting CL 9.0–10.0 mm). Each male was given access to a receptive female to mate up to 5 times and then the spawning success and fertilization rates were examined. Reproductive success of males was calculated as follow: spawning success (success: 1 or failure: 0) × fertilization rate (0–100).

The degree of decline in male reproductive success with increasing male mating frequency was significantly different between the male size classes (two-way repeated measured ANOVA, male size × male mating frequency: F7.143,214.279 = 8.815, P < 0.001; Mauchly's sphericity test, df = 9, W = 0.68, P = 0.007; H-F epsilon = 0.89, Fig. 17, Sato and Goshima 2006). As male size decreased, the decline in male reproductive success with increasing male mating frequency was greater. In this experiment, all small males failed to induce females to spawn in their fourth and fifth mating.


Fig. 17. Relationship between mating frequency by males of various body sizes and the male reproductive success (spawning success × fertilization rate) in the stone crab Hapalogaster dentata. CL 6.0–7.0 mm, n = 23; CL 9.0–10.0 mm, n = 24; CL 13.0–14.0 mm, n = 16. CL: carapace length. Error bars: ±SE. Reprinted and modified with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Fig. 3, © 2006, Inter-Research Science Center.

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These results indicate that both male body size and mating frequency interact for male reproductive potentials in the three studied species. Larger males have superior ability to mate and fertilize successively than smaller males, that is, a size-dependent reproductive potential. The size-dependent reproductive potential of males would result from the number of sperm in the vasa deferentia of smaller males being smaller than for larger males. Given the male size-dependent reproductive potentials, it is valid that the mean female reproductive success in the manipulated stone crab populations consisting of small males was low both when the SR was skewed toward females and when the time of female mating was late (Sato and Goshima 2006). It is also valid that female reproductive success was higher in 2004 when fishing pressure before and during the reproductive season was lower than in ordinary years in the harvested spiny king population.

4-5. Sperm recovery rate

However, can males in three studied species recover their sperm reserves after mating? Various taxa recover sperm reserves (e.g. Birkhead 1991; McWilliams 1992; Westneat et al. 1998). If their sperm recovery rate is rapid, increase in male mating frequency ought to have little influence on male reproductive potentials even in smaller males having fewer sperm than larger ones. For example, as seen in finches (Birkhead 1991), if the recovery of male sperm resources is rapid, the males complete a number of successive matings. Thus, the recovery rate of male sperm resources is one of the important factors influencing the degree of sperm limitation for females.

Sato et al. (2006) examined the sperm recovery rate in spiny king crab using small males (CL 80.0–85.0 mm), large males (CL 100.0–110.0 mm) and females (pre-molt CL 100.0–110.0 mm). Each male was given access to a receptive female a day until the male got to be incapable of inducing a female to spawn. Males that did not induce a new mate to spawn were judged unable to mate with more females; these males were defined as "depleted males" in this monograph and then they were transferred to the separate aquarium respectively. To estimate the recovery rate of exhausted sperm, at 0, 14 and 28 days after male depletion, the vasa deferentia were removed and sperm in the vasa deferentia were counted with the method using NaOH solution.

Large but not small male spiny king crab significantly increased the number of sperm in the vasa defenrentia with increasing number of days after depletion (small male, number of sperm in vasa deferentia (×106) = 0.06 number of days after depletion +10.50, r2 = 0.024, P = 0.57; large male, number of sperm in vasa deferentia (×106) = 0.22 number of days after depletion +14.85, r2 = 0.23, P = 0.031, Fig. 18). However, the number of sperm in the vasa deferentia recovered very little even 28 days post-depletion in large males, and when the number of sperm in the vasa deferentia of the large males allowed 28 days to recover was compared with that of unmated large males, it was significantly lower than for unmated large males (t-test, t = 14.39, df = 18, P < 0.001, Fig. 18). Thus, the sperm recovery rate was very slow, which suggests that spermatophore production is costly for spiny king crab males (Sato et al. 2006).


Fig. 18. Recovery rate of number of sperm in vasa deferentia and number of sperm in vasa deferentia retained by unmated males by small (CL 80–85 mm) or large (CL 100–110 mm) males in spiny king crab Paralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Fig. 1, © 2006, Inter-Research Science Center.

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Such a slow recovery rate of sperm was also observed in the other studied species, coconut crab (Sato et al. 2010) and the stone crab (Sato and Goshima 2006). These species would recover their sperm reserves completely by the next reproductive season, in the following year. The slow sperm production leads to a sharp drop in number of ejaculated sperm with increasing male mating frequency. Males of these species will mate with females before they recover their sperm stores to be sufficient to fertilize her clutch, which causes females to be prone to have a limited sperm supply. It is likely that females suffer from sperm limitation especially when females mate with smaller males who already mated.

Therefore, the intensity of sperm limitation for females would be high particularly in the large male-selective harvested populations with few large males. Furthermore, the intensity of sperm limitation will increase sharply especially late in the reproductive season when most males would already have mated with some females. Change of population demographic structure due to the larger male-selective harvesting would decrease reproductive output of the resources through sperm limitation.

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5. Temporal variations of male sperm reserve and the ability to ejaculate

Given the male body size-dependent reproductive potentials and the slow sperm recovery rate, sperm limitation is considered as the most plausible mechanisms decreasing female reproductive success in spiny king crab populations subjected to the large male-selective harvesting, especially later in the reproductive season. However do male spiny king crabs actually deplete their sperm reserves due to many matings in the large male-selective harvested population? Does the probability that females suffer from sperm limitation actually increase as the reproductive season progresses in the spiny king crab populations?

To examine these queries, Sato et al. (2005b) investigated temporal changes in the number of sperm retained by males during the mating season in harvested spiny king crab population. To count retained sperm in the vasa deferentia at various phases of the reproductive season, male crabs were collected before (late April), during (early-middle May) and just after the reproductive season (late May) and dissected. There was a significant difference in the number of sperm in the vasa deferentia among seasons (One-way ANOVA, F1,231 = 29.53, P < 0.001, Fig. 19) and the number of sperm in the vasa deferentia decreased significantly throughout the reproductive season (Sato et al. 2005b).


Fig. 19. Variance of proportions of depleted males throughout the reproductive season in spiny king crab Paralithodes brevipes. The horizontal dotted line indicates the mean of the number of sperm in the vasa deferentia retained by males that depleted their sperm reserves (i.e. 12.22 × 106) (late April, n = 55; early–middle May, n = 26; late May, n = 45). CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 11, © 2005b, Inter-Research Science Center.

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What was the proportion of males that depleted their sperm reserves in the harvested population? To evaluate the proportion of males with depleted sperm reserves, the number of sperm retained by the depleted males that are incapable of further mating due to successive mating was estimated through laboratory experiment. Each spiny king crab male (range: CL 80.8–103.6 mm) was given access to a receptive female until the male got to be the depleted male. The depleted males were dissected to count the sperm in their vasa deferentia. The mean number of sperm in the vasa deferentia retained by depleted males (12.22 × 106 ± 4.39 × 106 SD) was compared with that retained by males in the harvested population in each phase of the reproductive season. If the number of sperm retained by a male in the harvested population was less than that of the depleted males, we defined the male as "depleted", that is, males having fewer sperm than average (i.e. <12.22 × 106) were defined as depleted males (Sato et al. 2005b).

Many males in the harvested population were classified as depleted (percentages of depleted males: before the reproductive season, 0%; during the reproductive season, 11.5%; just after the reproductive season, 42.2%, Fig. 19, Sato et al. 2005b). These percentages were calculated from the data of males larger than 80 mm CL because some males smaller than 80 mm CL had sperm numbers below the average of depleted males even before the reproductive season. The proportion of depleted males increased significantly throughout the season. A similar tendency was also reported for coconut crab populations subjected to the large male-selective harvesting, and the proportion of depleted males increased steadily, up to 50%, throughout toward the end of the mating season (percentages of depleted males: before mating season, 0%; early part of the mating season, 20%; middle part of the mating season, 40%; late part of the mating season, 50%, Sato 2011). The number of male sperm reserves decreased sharply and the depleted males appeared soon after the start of the reproductive season in harvested coconut crab population.

These results in spiny king crab and coconut crab population strongly suggest that some of these males had mated successively and depleted their sperm reserves to the point of sperm exhaustion and they were no longer able to mate. The number of ejaculated sperm decreases sharply with increasing male mating frequency and the sperm recovery rate is very slow in both species. Therefore, at least about 50% of males provided substantially fewer sperm to females throughout the process of the depletion during and after their second mating in the harvested population in both harvested populations. Risk of sperm limitation for females must increase throughout the reproductive season, and females will suffer from insufficient sperm supply to fertilize all their eggs especially later in the reproductive season.

This prediction that females suffer from sperm limitation is reasonable for spiny king crab and coconut crab populations subjected to the large male-selective harvesting. In harvested spiny king crab populations, the fertilization rate decreased and the clutch was smaller later in the reproductive season when the number of ejaculated sperm would be fewer due to male successive mating (Sato et al. 2007). In harvested coconut crab populations, the number of sperm retained by females decreased gradually as the reproductive season progressed (Fig. 20) and more than half of the females (13 of 22 females captured) retained only a small number of sperm that are insufficient to fertilize all eggs extruded (Sato et al. 2010). The temporal coincidence of temporal decrease in sperm supply (sperm availability) with the temporal decrease in female reproductive success suggests that female reproductive success in the large male-selective harvested population is restricted by sperm limitation. The decrease in female reproductive success due to sperm limitation must occur in both the harvested spiny king crab and coconut crab populations (Sato et al. 2010; Sato 2011).


Fig. 20. Relationship between the time when females were caught and number of sperm retained by females in the harvested population of coconut crab Birgus latro. Here, 24 May = 1 on the x-axis (n = 22). Reprinted with permission from Aquatic Biology, 10, Sato et al., Sperm limitation: possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro, 23–32, Fig. 6, © 2010, Inter-Research Science Center.

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6. Influence of changes in socio-sexual conditions on female reproductive success

Other mechanism decreasing female reproductive success would exist in the large male-selective harvested population. This section focuses on such mechanisms as below: (1) influence of decreased difference in body size between male and female through female mate choice, (2) influence of decreases in the encounter rate between females and males through female delayed mating, and (3) influence of skewed sex ration toward females through male sperm allocation strategy.

6-1. Decreased difference in body size between mates: female mate choice

Body size is one of the key determinants of fitness in males (Andersson 1994), and larger males, for example, are preferred by females as mates in several decapod crustacean species (e.g. rock shrimp Rhynchocinetes typus, Díaz and Thiel 2003; the stone crab, Sato and Goshima 2007b; red swamp crayfish Procambarus clarkii, Aquiloni and Gherardi 2008). Larger males will disproportionately contribute to reproduction of populations through sexual selection, resulting in the fact that several decapod crustaceans commonly exhibits clear sexual size dimorphism in which the mean body size of males is larger than that of females. Such larger males are harvested by the large male-selective harvesting, and smaller males replace larger males in reproduction (e.g. snow crab, Ennis et al. 1990; blue crab, Carver et al. 2005). However, can the smaller males really replace larger ones as mates for females in any decapod crustacean species? Does the reduction in male size (i.e. decrease in the difference in body size between males and females in mating pairs) influence on their mating success?

Sato and Yoseda (2010) investigated the effects of the difference in body size between males and females in mating pairs on mating success in coconut crab by conducting mating trials in the laboratory. Coconut crab males of different body size (25.0–58.5 mm TL) and females (28.7–37.5 mm TL) were used, and a male and a female were placed together in a tank to form mating pair at random. As result of mating trials, when the assigned male was larger than the female in the mating pair, most females mated except for one pair (Fig. 21). When the assigned male was smaller than the female, only four females mated with the assigned male. In these pairs, females were barely larger than males (differences in TL between male and female (subtracting female TL from male TL: –0.1, –1.6, –1.8 and –2.6 mm TL, Sato and Yoseda 2010). The mating success of pairs (S: success = 1 or failure = 0) was fitted by means of a non-linear modeling procedure to the logistic model:

where a and b are parameters of the logistic function. The fitted logistic regression model was statistically significant (Hosmer and Lemeshow chi-square test: χ2 = 1.199, df = 7, P = 0.991; Cox and Snell's r2 = 0.646; a = 1.07, SE = 0.785; b = –0.97, SE = 0.332, Wald χ2 = 8.561, df = 1, P = 0.003, Sato and Yoseda 2010). By fitting the logistic curve S = 1/[1 + exp(1.07–0.97 × Difference)], the difference between TLs of males and females at 50% mating success was estimated as 1.1 mm (Fig. 21). Furthermore, only when males were approximately equal to females or when females were larger than males, many male casualties were observed in the mating trial (Sato and Yoseda 2010). These results suggested that coconut crab females have mate preference for larger males.

Fig. 21. Effect of male-female body size difference on mating success in coconut crab Birgus latro. The equation of the logistic curve (solid line) that was fitted to the proportion of mating success is S = 1/[1 + exp(1.07–0.97 × Difference)] (Cox and Snell's r2 = 0.65, n = 56). The residual of 50% mating success (MS50) was estimated as 1.1 mm TL, indicated by the broken line. TL: thoracic length. Reprinted and modified with permission from Marine Ecology Progress Series, 402, Sato and Yoseda, Influence of size- and sex-biased harvesting on reproduction of the coconut crab Birgus latro, 171–178, Fig. 3, © 2010, Inter-Research Science Center.

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In some anomuran crabs, e.g. spiny king crab (Sato et al. 2005b, 2006) and the stone crab (Sato and Goshima 2006, 2007a), larger females can mate with males much smaller than themselves. However, no coconut crab females mated with males much smaller than themselves, suggesting that coconut crab females would gain stronger benefits from exercising choice favoring larger males or, on the other hand, reduce benefits by mating with smaller males. The reason why no coconut crab females mate with males much smaller than themselves is not clear (Sato and Yoseda 2010).

The large male-selective harvesting for coconut crabs might lead to depletion of the resource through a decline in its reproductive output. In the harvested coconut crab population, its sex ratio skewed significantly toward females and the mean male size would decrease (Sato and Yoseda 2010). The mean and median TL of males was nearly equal to those of females in the investigated population, nevertheless coconut crabs usually exhibit clear sexual size dimorphism in which the mean body size of females is smaller by an order of 20–25% than that of males (Fletcher et al. 1991). The disappearance of sexual size dimorphism, i.e. a decrease in mean male size, would be a result of the present large male-selective harvesting. Removal of larger males from the population can affect the female reproductive success negatively, by reducing the probability of encountering favorite mates. A decrease in density of larger males reduces mate availability for females and makes it difficult to find favorite mates. The availability or encounter rate between females and favorite mates might have been low especially for larger females due to their mate preference despite that larger females will make a larger contribution to the reproductive rate because fecundity increases exponentially with female body size (Sato and Yoseda 2008). Perhaps, some females might have failed to meet favorite mates within their receptive period to mating. Actually in the investigated coconut crab population, some females had non-fertilized clutches (T. Sato, unpubl. data), implying that the females might fail to mate in the field.

Like this, female mate preference for male body size as seen in many animal species (Andersson 1994) can significantly influence population vulnerability under the large male-selective harvesting. To avoid such negative impacts of harvesting on reproduction of the resources, it is important to investigate details of the mating system, e.g. female mate choice, for each targeted species.

6-2. Decrease in the encounter rate between females and males: female delayed mating

In larger male-selective harvested populations, reproductive outputs of harvested populations will be affected by not only sperm availability but also mate availability through female reproductive characteristics. A decrease in male density due to the large male-selective harvesting would reduce the frequency of female encounters with suitable mates and then cause difficulties for females to find mates (Gray and Powell 1964; Powell et al. 1974; Ennis 1980; Smith and Jamieson 1991). Therefore, female mating can be delayed by the decrease in availability of male mates even if females have become receptive for mating. Negative effects of delayed mating on spawning, fertilization and offspring quality have been reported in several animal species (McMullen 1969, Paul and Adams 1984; Unnithan and Payne 1991; Torres-Vila et al. 2002; Huang and Subramanyam 2003; Milner et al. 2007). What kinds of influences do the large decapod crustacean females receive from the delayed mating on their reproductive success?

Sato et al. (2005a) investigated the effects of delayed mating on the reproductive success of the female spiny king crab by laboratory experiments in which the duration between molting of females (i.e. start of female sexually receptivity) and their mating was controlled. Spiny king crab females (94.1–118.5 mm CL) were placed in aquaria (0.2 m3) individually after molting. At 4, 8, 12, 16 or 20 days after the females molting, one male (110.7–124.5 mm CL) was added to each aquarium containing a molted female for mating.

All spiny king crab females mated with an added male and spawned although other large decapod crustacean females can be successfully mated for only a limited period after they molt (red king crab, McMullen 1969; Paul and Adams 1984; snow crab, Sainte-Marie and Lovrich 1994). Some of red king crab females do not spawn when more than 10 days elapse after molting, and no females spawn after 14 days (McMullen 1969). Compared with the red king crab, spiny king crab females may be sexually receptive for a longer period after molting and can mate and spawn irrespective of the number of days after their molting within at least 20 days.

However, the fertilization rate of clutches and the number of days after molting showed a significant negative relationship (fertilization rate (%) = –1.052 number of days after female molting + 101.75, r2 = 0.21, P = 0.039). After spawning, detached eggs from their pleopods were observed for every female and some females dropped eggs daily for a week after spawning. The number of detached eggs was significantly different between the treatments (one-way ANOVA, F4,20 = 7.47, P < 0.001, Fig. 22). The number of detached eggs significantly increased when the days elapsed was more than 16 days after molting. To examine if detached eggs of females mated on days 12, 16, or 20 after molting develop normally, we collected a total of 50 detached eggs from each female, and the eggs were incubated for about two weeks in a petri dish with filtered seawater. The percentage of detached eggs that developed normally decreased significantly when the elapsed time between molting and spawning was 20 days (Kruskal-Wallis test, df = 2, H = 7.98, P = 0.019, Fig. 23).


Fig. 22. Relationship between number of days after molting of females and number of detached eggs in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. The asterisk indicates significant difference. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 2, © 2005a, The Crustacean Society.

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Fig. 23. Relationship between days after molting of females and percentage of normal development of detached eggs in spiny king crab Paralithodes brevipes. Error bars are SE. Eggs developed to the morula stage were called as eggs that developed normally. Error bars: ±SE. Numbers above bars: replicates. Different letters above bars indicate significant differences. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 3, © 2005a, The Crustacean Society.

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The clutch condition of each ovigerous female was recorded qualitatively after about three or four weeks from her spawning. The percentage of females with the rank B clutch, pleopods visible among eggs due to egg loss, and the rank C clutch, few or no attached eggs, tended to increase as the number of days after female molting increased (Fig. 24). The percentage of clutches with few eggs was highest at 20 days after molting. About four months after the reproductive season, all females that mated at 20 days after their molt had few or no eggs.


Fig. 24. Influence of number of days after molting of females on clutch condition in spiny king crab Paralithodes brevipes: Rank A was a normal clutch with many eggs, Rank B was pleopods visible because of a small number of incubated eggs, and Rank C was few or no attached eggs. Numbers above bars: replicates. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 4, © 2005a, The Crustacean Society.

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The percentage of detached normally developed eggs decreased significantly in females mated at 20 days after molting, and all females mated at 20 days after molting had few eggs after four months from the reproductive season, which indicates that a large number of days after molting deteriorates the quality of egg stored in the female ovaries. The deterioration of egg quality in the female ovaries might be caused by overmaturation and resorption of eggs. Many decapods resorb unspawned eggs in the ovaries (e.g. Mason 1970; McMullen and Yoshihara 1971). The decline in the fertilization rate and the increase in the number of detached eggs with an increasing number of days after molting would also result from deterioration of egg quality in female ovaries. Similar effects of delayed mating exist for large crustacean decapods and delayed mating induces females to clutch nonfertilized eggs (red king crab, Kurata 1961; tanner crab, Paul and Adams 1984). Spiny king crab females have an optimal duration to mate after their molt and should mate as soon as possible after their molt to fertilize and incubate their clutch successfully.

In the large male-selective harvested spiny king crab populations, some females had no or partial clutches (rank B or C) (Sato et al. 2007). Despite that some molted females reach a mature size and retain ripe eggs in their ovaries, they carry no eggs even after the reproductive season (Sato et al. 2007). These findings strongly indicate that the availability of suitable males has decreased in the harvested spiny king crab populations. Probably, the female spiny king crabs failed to meet suitable mates and to mate within the optimal duration of mating.

Such failure by females to mate within the optimal duration of mating would be promoted by sperm limitation and some female reproductive characteristics. In the large male-selective harvested populations, small males would replace large males in reproduction and experience more matings than in pristine populations (Powell et al. 1974; Ennis et al. 1988, 1990; Sainte-Marie 1993; Carver et al. 2005). However, if small males retain few sperm reserves and easily deplete their sperm reserves compared with large males as seen in studied species (Sato et al. 2005b, 2010; Sato and Goshima 2006; Sato 2011), available male mates must decrease further due to successive matings throughout the reproductive season, and then the female encounters with potent males would be more limited in such a harvested population. If females have no spermatheca to store sperm and have an optimal duration for mating, such as anomuran crabs, females would be more susceptible to the decline in availability of mates. Furthermore, if females do not choose to mate with the remaining small males, like coconut crab females (Sato and Yoseda 2010), or with the sperm-depleted males, reported in the stone crab females (Sato and Goshima 2007b), the frequency of encounters by females with mates would decrease more severely. In future, we need fishery management programs that lessen the effects of fisheries on stock reproductive success by considering female reproductive characteristics (i.e. the optimal period to mate).

6-3. Skewed sex ratio towards females: male sperm allocation strategy

The change of population demographic structure caused by the large male-selective harvesting can decrease female reproductive success through a certain male mating strategy. Because sperm production is costly and slow in many animal species (e.g. Dewsbury 1982; Pitnick and Markow 1994), males should economise their sperm reserve by efficiently allocating it to successive matings to maximise their reproductive success (Dewsbury 1982; Pitnick and Markow 1994; Warner et al. 1995; Parker et al. 1997). Various animal taxa show a sperm allocation strategy which is especially well documented in terrestrial insects (e.g. Pitnick and Markow 1994; Gage and Barnard 1996; Wedell and Cook 1999; Rondeau and Sainte-Marie 2001; Wedell et al. 2002; Pizzari et al. 2003). In recent years, interest in the topic of sperm allocation has increased considerably also in crustaceans (blue crab, Jivoff 1997; Caribbean spiny lobster, MacDiarmid and Butler 1999; snow crab, Rondeau and Sainte-Marie 2001; American lobster, Gosselin et al. 2003; common rock crab Hemigrapsus sexdentatus, Brockerhoff and McLay 2005; freshwater crayfish, Rubolini et al. 2006; the stone crab, Sato and Goshima 2007a, c; coconut crab, Sato 2011). To maximize their reproductive success, males allocate their sperm reserves depending on various factors (Wedell et al. 2002). For example, risk of sperm competition (e.g. presence of a rival male) may induce males to increase their sperm number per mating to have a greater fertilization rate (e.g. Gage and Barnard 1996; Marconato and Shapiro 1996; Wedell et al. 2002; Pizzari et al. 2003; Sato and Goshima 2007a). Males have greater reproductive success by strategically increasing their sperm numbers to females that provide larger fertilization returns (e.g. Gage and Barnard 1996; Marconato and Shapiro 1996; Wedell and Cook 1999; Wedell et al. 2002; Pizzari et al. 2003; Sato and Goshima 2007c). Males also allocate their sperm reserves depending on the probability of how many females will be encountered (e.g. Pitnick and Markow 1994; Rondeau and Sainte-Marie 2001; Wedell et al. 2002; Sato and Goshima 2007c).

The male sperm allocation strategy is sometimes a disadvantage for females due to severe reduction in sperm numbers from males. For example, a female-biased sex ratio means an increase in future mating opportunities for males, which may cause males to conserve their sperm reserves for future mating opportunities, by decreasing the ejaculate size per mating even at the expense of a reduced fertilization rate, that is sperm limitation, because it is less costly to males than depleting their sperm before mating opportunities have ended (Warner et al. 1995). Actually, snow crab males prudently allocate their sperm to successive matings by decreasing the ejaculate size per mating with an increasing sex ratio skew toward females, resulting in sperm limitation in mated females (Rondeau and Sainte-Marie 2001). Furthermore, snow crab males are not fully exhausted of their sperm reserve for additional future mating opportunities in a female-biased sex ratio (Rondeau and Sainte-Marie 2001). Such tightfisted allocation in response to a female-biased sex ratio would cause a decline in the reproductive output of the population.

Because the number of mating opportunities for males increases in the large male-selective harvested spiny king crab populations, males may allocate their sperm to successive matings by decreasing the ejaculate size at each mating at the expense of a reduced fertilization rate, which may cause the decrease in female reproductive success. Sato et al. (2006) examined by laboratory experiments whether sperm allocation by males at different sex ratios with males of different body sizes can limit sperm passed to females in fished spiny king crab populations. To examine if ejaculate size varies with SR surrounding males, small males (CL 80.0–85.0 mm, n = 19), large males (CL 100.0–110.0 mm, n = 18), and females (pre-molt CL 100.0–110.0 mm) were used. Two mating groups were formed: small male and female; large male and female, and then the ejaculate size was compared between social circumstances for the different SR (male: female = 1:1 or 1:6) of each male size class.

To estimate the ejaculate size for SR = 1, each male was placed individually in separate circular aquaria. A molted female (i.e. sexually receptive female) was transported to the aquarium to mate, and then the ejaculated sperm was collected and estimated. By contrast, to estimate the ejaculate size for SR = 0.167, each male was placed in separate circular aquaria with five nonmolting females. At the end of the period to acclimatize for a female-biased sex ratio, one molted female was transported to an aquarium containing a male and five nonmolting females, and then the ejaculated sperm was collected and estimated. Each male mated with one female a day, and mated with two females within two days.

In both small and large male size classes, two-way repeated measures ANOVA showed that only the mating frequency was significant for ejaculate size, and detected no two-way interaction between SR and mating frequency for ejaculate size (Tables 3, 4). Large males always passed larger ejaculates to females than small males regardless of mating frequency, and the ejaculate size decreased with increasing mating frequency (Fig. 25).


Fig. 25. Relationships between male mating frequency and number of ejaculated sperm at different sex ratios (male:female = 1:1 or 1:6) by small (CL 80–85 mm; SM) vs. large (CL 100–110 mm; LM) males in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Fig. 4, © 2006, Inter-Research Science Center.

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Table 3. Two-way repeated measures ANOVA of the effects of sex ratio and male mating frequency on the number of ejaculated sperm in successive matings by small males (CL 80–85 mm) in spiny king crab Paralithodes brevipes. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Table 3, © 2006, Inter-Research Science Center.

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Table 4. Two-way repeated measures ANOVA of the effects of sex ratio and male mating frequency on the number of ejaculated sperm in successive matings by larger males (CL 100–110 mm) in spiny king crab Paralithodes brevipes. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Table 4, © 2006, Inter-Research Science Center.

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The pattern of sperm allocation of spiny king crab males showed no difference between the different SR in both male size classes. By contrast, snow crab males allocate their sperm among successive matings by decreasing the ejaculate size at each mating and pass insufficient sperm for successful fertilization when the SR becomes heavily skewed toward females (Rondeau and Sainte-Marie 2001), resulting in sperm limitation in the mated female. Snow crab males usually risk sperm competition whenever males mate with a female, because females can be polyandrous (Sainte-Marie et al. 1997, 1999). Snow crab males cannot predict when they can mate with females with low risk of sperm competition. In addition, the last male that inseminates a female just before spawning usually has paternity through sperm stratification in the spermatheca of the snow crab (Urbani et al. 1998; Sainte-Marie et al. 2000). Thus, an optimal sperm allocation strategy to maximize the male reproductive success is to mate with as many females as possible by decreasing the ejaculate size at each mating, can be explained by the sperm competition theory (Pitnick and Markow 1994; Parker et al. 1997). Therefore, snow crab males decrease their ejaculate size in response to increased females availability of mates to maximize their number (Rondeau and Sainte-Marie 2001).

By contrast, spiny king crab females may be monandrous because they have no spermatheca and the period between mating and spawning is very short (approximately one hour) (Sato et al. unpublished data), indicating that males may have less risk of sperm competition, and that one male fertilizes the whole clutch of a female. In addition, when spiny king crab males mate with larger females, the sperm to egg ratio, the expected number of fertilised eggs for each unit number of sperm passed to the female, is low, indicating that larger females have a high reproductive quality for males with limited sperm reserves (Sato et al. 2006). Such larger females molt and mate earlier in the reproductive season compared with small females with low sperm efficiency (Sato et al. 2007). Therefore, more beneficial mating opportunities for males with limited sperm reserves occur early in the reproductive season. Males should attempt to mate early in the reproductive season with large females to invest their limited sperm reserve efficiently. Even if many future mating opportunities exist in a reproductive season, conserving their sperm reserve for future mating opportunities and allocating equally among successive matings is not adaptive for males because mating with smaller females means a higher sperm to egg ratio than mating with larger females (Sato and Goshima 2007c). Males should finish their sperm reserve as early as possible in the reproductive season to mate with larger females and to avoid mating with smaller females. Therefore, spiny king crab males did not change the ejaculate size in response to an increase in number of females when the SR skewed toward females.

The SR skewed towards females due to the large male-selective harvesting had no effect on the sperm allocation pattern and then will not limit female reproductive success in the harvested spiny king crab populations. Sperm allocation pattern in response to a change in SR varies with species through several factors. For sustainable use of biological resources, we should investigate the details of the mating system and reproductive ecology of each harvested species to predict and avoid negative impacts of the large male-selective harvesting on its reproductions.

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7. Plausible interaction between maternal influences and female mate choice for reproductive outputs of the resources

The change of population demographic structure due to the large male-selective harvesting might restrict reproductive rates and stability of the harvested population through interaction between maternal influences and female mate choice. Maternal influences are a major source of phenotypic variation of offspring and are closely related to offspring survival (Green 2008). For example, positive relationships between maternal size or age and offspring size exist in a range of animal taxa (e.g. Congdon and Gibbons 1987; Fleming and Gross 1990; Sinervo and Doughty 1996; Vallin and Nissling 2000; Berkeley et al. 2004; Marshall and Keough 2004). In marine fishes, predation and starvation are two major factors determining survival of offspring in the larval phase (Bailey and Houde 1989) and susceptibility of larvae to these factors depends on larval body size (Rice et al. 1987; Buckley et al. 1991a, b). Larger body sizes can reduce both the susceptibility to predation by enhancing swimming ability and the susceptibility to starvation by increasing access to a greater size range of food (Pepin 1989). Through such mechanisms, maternal influences on offspring survival contribute to the dynamics of natural populations (Vallin and Nissling 2000; Venturelli et al. 2010).

In a harvested population, larger individuals are more likely to be caught than smaller ones (Fenberg and Roy 2008). The truncation of the size and age of a harvested population can directly influence the quality of offspring through maternal influences (Longhurst 2002; Scott et al. 2006; Sogard et al. 2008), which would cause greater fluctuations in recruitment of harvested resources (Marteinsdottir and Thorarinsson 1998; Berkeley et al. 2004; Hsieh et al. 2006). These negative impacts of larger individual-selective fishing through maternal influences need to be considered in resource management strategies to attain sustainable yields from fishery resources. However, there have been very few studies on maternal influences in decapod crustaceans (estuarine grapsid crab Chasmagnathus granulate, Giménez and Anger 2003; southern rock lobster, Smith and Ritar 2007; blue crab, Darnell et al. 2009; European lobster Homarus gammarus, Moland et al. 2010), despite the fact that this group includes large numbers of important fishery resources.

In coconut crab population under large male-selective harvesting, its reproductive output may decline by reducing the probability that females encounter favorite mates (Sato and Yoseda, 2010). The encounter rate between females and favorite mates might be low especially for larger females. If larger coconut crab females produce larvae with superior qualities, harvesting large males may have even greater negative impacts on coconut crab populations through the maternal influences. To determine whether there are additional impacts of the present large male-selective harvesting on coconut crab resources due to maternal influences, Sato and Suzuki (2010) investigated the effects of female body size on larval body size, dry weight and survival period under unfed conditions by laboratory experiments.

First, hatched zoeae were taken randomly from each female (Mean ± SD, 31.1 ± 3.6 mm TL) in laboratory, and then mean larval cephalothoracic length including the rostrum as an index of larval body size was calculated for each female. Second, to determine larval weights, one hundred zoeae were taken randomly from each female (Mean ± SD, 31.1 ± 3.6 mm TL). After washing in distilled water, zoeae were placed on a watch glass. Samples were oven-dried at 60°C for 24 h, and the weight of dried zoea was calculated for each female.

Mean larval body size differed according to female TL (Mean ± SD, 1.41 ± 0.02 mm cephalothoracic length; Range, 1.34–1.45 mm cephalothoracic length) and increased significantly with increasing female TL (mean of larval cephalothoracic length = 0.0038 × female TL + 1.31, r2 = 0.21, F1,28 = 7.65, P = 0.010, Fig. 26a). Mean dried larval weight also varied with female TL (Mean ± SD, 0.074 ± 0.005 mg; Range, 0.060–0.082 mg) and increased significantly with increasing female TL (larval dried weight = 0.00059 × female TL + 0.056, r2 = 0.16, F1,28 = 5.32, P = 0.029, Fig. 26b).


Fig. 26. Relationships between female size and (a) larval size (CL: cephalothoracic length, mm) (n = 30), (b) dried larval body weight (n = 30), or (c) larval survival time in non-food condition (n = 26) in coconut crabs Birgus latro. TL: thoracic length. Reprinted and modified with permission from Journal of Crustacean Biology, 30, Sato and Suzuki, Female size as a determinant of larval size, weight, and survival period in the coconut crab, Birgus latro, 624–628, Figs. 1–3, © 2010, The Crustacean Society.

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As seen in a range of animal taxa (Vallin and Nissling 2000; Berkeley et al. 2004; Marshall and Keough 2004; Smith and Ritar 2007), positive relationships were found between maternal size and larval size, indicating that larger coconut crab females produce larger offspring. In marine species, mortality during the larval phase is generally very high, and is particularly at its highest early in the phase (Cushing 1988). Mortality decreases rapidly with increasing larval size, and larger body size reduces susceptibility to predators through both escape ability and predator gape-limitation (Miller et al. 1988). Therefore, larval size at hatching is crucial to subsequent larval survival. Larger coconut crab larvae hatched from larger females might survive longer from predations in natural conditions, and be more able to recruit the resources, compared to smaller larvae.

Next, the larval survival period was examined for zoeae hatched from females (Mean ± SD, 30.9 ± 3.8 mm TL) in laboratory (Sato and Suzuki 2010). Each zoeae was then reared individually at 28°C without feeding. Larval survival was monitored daily and the mean larval survival period under non-food conditions was calculated for each female.

The mean of larval survival days in the non-food conditions differed among female TL (Mean ± SD, 11.96 ± 1.33 days; Range, 9.06–14.28 days). Larvae hatched from larger females showed a significantly longer survival period than larvae hatched from smaller ones (Mean of survival days = 0.17 × female TL + 6.59, r2 = 0.24, F1,24 = 10.70, P = 0.011, Fig. 26c).

In marine fishes, susceptibility to starvation, one of the major factors determining survival of offspring in larval phase (Bailey and Houde 1989), decreases with increasing larval body size. The larval survival period in the absence of food increases with increasing oil globule or yolk sac volume (Berkeley et al. 2004; Fisher et al. 2007; Higashitani et al. 2007) and larger and older females produce larvae with larger oil globule or yolk sacs (Berkeley et al. 2004; Higashitani et al. 2007). Coconut crab larvae hatched from larger females would have a greater amount of energy in their yolk than larvae hatched from smaller ones and thus would have superior abilities to survive starvation in unpredictable, patchy and meager foraging conditions in the field and to recruit the resources successfully.

The removal of larger and/or older females from a breeding population might have disproportionately detrimental consequences for total survival and subsequent recruitment through maternal influences on various larval qualities (Marteinsdottir and Thorarinsson 1998; Berkeley et al. 2004; Hsieh et al. 2006; Sogard et al. 2008). The importance of maternal influences must be considered in management efforts to achieve sustainable harvesting from biological resources. However, it is possible to overlook the effect of maternal influences when size-selective harvesting is only performed on males as seen in the coconut crab (Sato and Yoseda 2010), other commercially important crabs (Sato et al. 2005b) and other biological resources (Fenberg and Roy 2008), because no females are harvested from these resources. In species such as the coconut crab in which females exert mate preference for larger males, maternal influence must be considered in resource management. This is because the frequency of encounters with favorite males would decrease in a large male-selective harvested population as female body size increases, which can result in lost mating opportunities. If, as shown above, larger females produce offspring with superior qualities, the large male-selective harvesting would have a greater negative impact than previously expected due to maternal influences. This scenario may occur in coconut crab resources.

However, it is unclear how common the maternal influences on larval qualities are in many harvested species at present. Birkeland and Dayton (2005) speculate that there are no maternal influences on vitality of larvae of short-lived fish or invertebrate species that reproduce only twice or a few times in their lives, or in pelagic species with more rapid population turnover, and it might be that it is only longer lived species that are vulnerable to the selective harvesting on the larger and older individuals. Fisheries scientists must investigate what types (in terms of life history) of exploited fishery resources show the maternal influences for sustainable use of it.

Although population size and/or age structure are increasingly being recognized as important considerations for sustainable resource management (Vallin and Nissling 2000; Sogard et al. 2008), few studies have attempted to quantify maternal influences on actual larval survival and recruitment (Venturelli et al. 2010; Beldade et al. 2012). In the future, it will be necessary to investigate details of these maternal influences and their effect on actual larval survival or recruitment in several biological resources. In addition, we must pay attention to plausible interactions between maternal influences and female mate choice for reproductive outputs of resources.

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8. General discussion

8-1. How large male-selective harvesting influences reproductive outputs of large decapods crustacean resources

The large male-selective harvestings for the spiny king crab and coconut crab populations have led to change the population demographic structure by decreasing mean male body size and skewing sex ratio towards females (Section 2). A combination of (1) the investigation of female reproductive success in spiny king crab population between years with exposal to contrasting fishing pressure (Subsection 3-2) and (2) the comparison of female reproductive success between manipulated stone crab populations with different demographic structures (Subsection 3-3) suggested that the changes of population demographic structure (a decrease in male body size and skewed SR toward females) can decrease female reproductive success. All males of the studied species showed the size-dependent reproductive potentials (Subsections 4-3, 4-4, and 4-5) and slow rate of sperm recovery (Subsection 4-6), which would be causes for temporal decrease in sperm and mate availabilities for females in the large male-selective harvested populations (Section 5). The temporal coincident of the temporal decrease in the sperm and mate availabilities with the temporal decrease in female reproductive success (Subsection 3-3) in the large male-selective harvested population, indicates that reproductive outputs of the harvested populations is limited by decreased availabilities of sperm and mate.

Furthermore, depending on the species (i.e. its mating system and reproductive ecology), the sperm availability can be influenced also by the male sperm allocation strategy in response to the skewed sex ratio towards females (Subsection 6-3). The mate availability can vary with female body size through female mate choice for large body size of males, and it would get lower especially for larger females (Subsection 6-1). Therefore, the larger females are, the more limited reproductive success would be liable to be through mating loss and female delayed mating (Subsection 6-2), despite that larger females can produce larger numbers of eggs (Section 2) and larvae with superior survival qualities (Section 7). Like this, the large male-selective harvesting decreasing both availabilities of sperm and mate can influence reproductive outputs of the spiny king crab and coconut crab populations through several mechanisms, which eventually would influence its abundance and stability of the resources (Fig. 27).


Fig. 27. Schema of how large male-selective harvesting influences reproductive output, abundant and stability of resources.

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The degree of sensitivity to the decreased availabilities of sperm and mate due to the large male-selective harvesting would differ considerably with species, given there is a large degree of variation in sperm storage and mating behavior in decapod crustaceans (Bauer 1986). For example, in many shrimps, some crayfishes, some lobsters and all anomuran crabs, females lack internalized sperm storage organs, i.e. spermatheca, and then sperm received from males are shed with the female molting (Sainte-Marie 2007). So, females must mate and newly acquire sperm for each next spawning/fertilization. Furthermore, in most species in which females have no spermatheca, the period of time between mating and spawning is short, usually hours to weeks (Sainte-Marie 2007), which would mean they have only a few opportunities to mate and remate for acquiring enough sperm to fertilize the whole clutch spawned. Thus, their reproductive success would be susceptive to variation in availabilities of sperm and mate, and their reproductive outputs are liable to decrease easily under the large male-selective harvesting. Females of three anomuran species focused in this study are especially sensitive to the decrease in availabilities of sperm and mate.

In contrast, females of other shrimps, crayfishes, lobsters, and brachyuran crabs have spermatheca (Sainte-Marie 2007). The sperm stored in the spermatheca are retained across their moltings in most species in which females show indeterminate growth and no terminal molt (e.g. Mennipe mercenaria, Cheung 1968; giant crab Pseudocarcinus gigas, Gardner and Williams 2002; but see American lobster, Sainte-Marie 2007). The stored sperm are used across multiple reproductive seasons. Also in species in which females show determinate growth and terminal molt, females can use the sperm in their spermatheca over their reproductive lifespan and produce multiple clutches (e.g. blue crab, Darnell et al. 2009; snow crab, Kon and Adachi 2005). Sperm storage would give females the opportunity to accumulate sperm from several males, and sperm storage across spawning seasons potentially releases females from the obligation to mate. Compared with species without spermatheca, they would be unaffected by variation in the availabilities of sperm and mate.

However, even if they have spermatheca, sperm limitation can occur in the course of successive spawnings if females produce multiple clutches (e.g. tanner crab, Paul 1984; snow crab, Sainte-Marie and Lovrich 1994; blue crab, Hines et al. 2003). Especially, the risk of sperm limitation would be high in species in which females have a limited window for mating, for example, the sexually receptive period is only following the terminal molt. For example, blue crab females mate only just after the terminal molt (for only two or three days, Van Engel 1958) and then produce multiple clutches. The multiple clutches produced over the female reproductive lifespan must be fertilized by sperm stored within the mating period, and thus blue crab females are apt to become sperm limited under large male-selective harvesting (Hines et al. 2003). Due to the limited window for mating, females would be susceptible to not only sperm availability but also mate availability. To understand the degree of each targeted species' susceptibility to variation of availabilities of sperm and mate and how current large male-selective harvesting influences their reproductive outputs, knowledge about details of reproductive ecology and mating system of targeted species will surely be helpful.

Above mechanisms decreasing the reproductive rate of the large male-selective harvested resources can occur not only in the large decapod crustacean species subject to large male-selective harvesting, such as spiny king crab and coconut crab, but also in other fishery resources in which the large male-selective harvesting is not mandated as a harvesting regulation. For example, in protogynous sex-changing fishes in which males are more vulnerable to fishing than females because of their larger body size and higher activity (Côté 2003) and in species in which males are vulnerable to harvesting due to reproductive behavior and temporal and spatial distribution (e.g. Morgan and Tripple 1996), above mechanisms decreasing reproductive outputs of the resources can occur (Alonzo and Mangel 2004). The large male-selective harvesting actually occurs in many marine species (Fenberg and Roy 2008). If harvesting activity thoughtlessly decreases a number of larger males in the resources regardless of the fact that the harvesting pattern is intentional or not, the harvesting can have a much greater impact on the reproductive capacity and stability of the harvested resources than when we pay attention only to the simple reduction in female biomass. This risk should be recognized among fisheries scientists and managers for sustainable use of various fisheries resources.

8-2. For the establishment of optimal management regimes

To avoid the unintentional negative impacts of the large male-selective harvesting on reproduction of harvested resources and to maintain its reproductive outputs, firstly we must determine the harvesting pattern for each resource. Secondly, if the harvesting pattern is non-random and large males are selectively harvested, we should investigate whether the harvesting pattern has negative impacts on reproduction of the resource, and then improve present management strategies to mitigate the impacts if negative impacts are expected. Although selective harvesting of large males leads to female-biased sex ratios, not necessarily leading to a reduction in the reproductive rate of resources because most harvested species show polygynous mating systems. It is reported that reproductive rates are resilient to a skewed sex ratio (Milner et al. 2007) and might even increase (Solberg et al. 2000) in terrestrial species subjected to the large male-selective harvesting. Furthermore, larger males may show the ongoing senescence of the reproductive performance depending on species. It is important for the prediction of negative impacts and the improvement of present management strategies to investigate details of the mating system and reproductive ecology, e.g. intra- and inter-sexual selection, size-dependent reproductive potentials and reproductive characteristics (e.g. negative effect of delayed mating and maternal influences) and to piece out variations in the sperm and mate availabilities due to harvesting from the above knowledge for each targeted species.

If the unintentional negative impacts of the large male-selective harvesting are predicted, i.e. if the great contribution of large males to reproduction is recognized, what management options should be applied to avoid the negative impacts (i.e. to conserve larger males) on fishery resources? Generally, to maintain the resources at an appropriate level, an overall fishing mortality is commonly controlled by a combination of increasing minimum legal size, improvements of fishing gear (e.g. mesh size), limitation to the number of operation days, and seasonal closure. However, most of these fishery management options would not protect larger males in the resources (Berkeley et al. 2004). Seasonal closures also leave larger males vulnerable to high fishing mortality for the entire time that is outside the closure season. Fishing usually selects for larger individuals by nature (Longhurst 2002) and truncation of larger individuals is the most predictable effect of fishing (Berkeley et al. 2004), indicating we have to find new types of management options to protect larger males.

Two possible management options can be available to decrease the negative impacts of the large male-selective harvesting: (1) slot size limits; and (2) marine reserves. Under a slot size limits, only intermediate size individuals are harvested selectively, and large individuals with a higher reproductive value are protected from harvesting. Protection of large males with higher reproductive potential will contribute to sustain the reproductive rate of populations. The straitened window of vulnerability for harvesting will also mitigate the decrease in population density, i.e. mate availability, due to harvesting. Of course, regulating the total number harvested from the straitened window is also essential to let the intermediate-sized males survive to become large proficient males. The slot size limits have been implemented, for example, in a giant crab fishery in Tasmania (Gardner and Williams 2002), in the sturgeon Acipenser medirostris sport fishery in Washington State and the Maine lobster Homarus americanus harvest (Law 2007), and it is recommended for coconut crab resources (Sato and Yoseda 2010; Sato et al. 2010; Sato and Suzuki 2010; Sato 2011). The slot size limits are a successful management tool for preserving and rebuilding stocks in some fish fisheries (e.g. Vaughan and Carmichel 2002; Nordwal et al. 2008). However, the slot size limits can be effective only for species that can be released unharmed after capture.

The marine reserve (permanent no-take area) offers an alternative management option that can protect all size of individuals including larger males. The marine reserves can increase densities, average size, and biomass of targeted species within the reserves (Pillans et al. 2005; Claudet et al. 2008; Pande et al. 2008; Lester et al. 2009; Hoskin et al. 2011). Therefore, this management option must maintain both sperm and mate availabilities in a portion of the population within the reserves. The reserves are anticipated to also increase fishery yields outside the reserves through export of eggs and larvae (recruitment subsidy) and adult and juvenile export (spillover) (Gell and Roberts 2003; Goñi et al. 2010). The eggs and larvae export and their effects on recruitment are anticipated to produce much greater benefits for fisheries than spillover (Moffitt et al. 2009; Díaz et al. 2011). Although at present uncertainty about larval connectivity and dispersal bars understanding about actual impact of reproductive output from the reserves to outside it, the dominant contribution of the reserves to the overall reproductive output of the targeted species must be remarkable and the reserves would contribute to attain a higher reproductive rate of the resources (Kaiser et al. 2007; Jack and Wing 2010; Díaz et al. 2011). The marine reserve is a powerful management tool for counteracting the negative impacts of the large male-selective harvesting by providing spatial refuges for harvested populations, and could be better than the slot length limits because of no by-catch mortality. However, even the marine reserves have a drawback that they cannot completely protect highly mobile species.

Therefore, the most logical management strategy for the protection of larger males would be a multipronged management option that consists of the marine reserve, the slot size limits outside the reserve, and assurance that larger males subjected to the gear can return without mortal injury (i.e. using of appropriate selective gear). Such management strategy not only would increase the sperm and mate availabilities for females (i.e. maintain reproductive output of the resources) but might also be able to mitigate negative evolutionary responses to size selective harvesting by protecting larger individuals. Harvesting has been implicated in evolutionary changes of inheritable traits (Hutchings 2004). For example, size selective harvestings have caused a significant reduction in age and length at maturity through the removal of larger individuals (Conover and Munch 2002; Hutchings 2005; Swain et al. 2007). These fishing-induced evolutionary changes can reduce yields from harvested resources (Conover and Munch 2002) and might even affect population viability (Walsh et al. 2006) and eventually recovery from collapse (Hutchings 2005). The multipronged management strategy protecting larger individuals will be one of the useful tools to reduce such anthropogenic selections and protect the long-term biomass yield (Conover and Munch 2002; Baskett et al. 2005).

In future, we must establish optimal management regimes for fishery resources that take into consideration the ecological (short-term) and evolutionary (long-term) consequences of the large male-selective harvesting in order to develop a truly sustainable harvesting system. For the establishment of the optimal management regimes, I believe the details of the mating system and reproductive ecology of each targeted species are important and they give us insight and predictive power.

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Acknowledgments

I thank Prof. Katsumi Aida for giving me the opportunity to write this monograph. I am most grateful to Prof. Seiji Goshima, Mr. Masakazu Ashidate, and Dr. Kenzo Yoseda, who provided guidance for most of the work presented in this monograph. I also extend my deep thanks to the following persons for their precious contributions to the original researches: Mr. Tadao Jinbo, Dr. Satoshi Wada, Dr. Osamu Abe, Dr. Takuro Shibuno, Dr. Koich Okuzawa, Dr. Nobuaki Suzuki, Dr. Masaru Torisawa, Dr. Michiya Kamio, members of Akkeshi and Yaeyama stations, the Stock Enhancement Technology Development Center, Fisheries Research Agency, members of Akkeshi and Usujiri Marine Stations, the Aquatic Research Station, the Field Science Center for Northern Biosphere, Hokkaido University, members of the Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Fisheries Research Agency, all reviewers of our paper and all members of the Laboratory of Marine Biodiversity, Graduate School of Fisheries Sciences, Hokkaido University. This work was made possible by the generous hospitality and cooperation of the staff of Hamanaka Fishermen Cooperative Association and the residents of Hatoma Island. My work was supported in part by a Grant-in-aid for Science Research (No. 20710184) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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List of Figures

Fig. 1 Schema of the focus of this monograph showing the indirect effect of large male-selective harvesting: impacts of the harvesting on reproduction and reproductive output of the resources through change in the population demographic structure.

Fig. 2 Pictures of three studied species in my work: (a) spiny king crab Paralithodes brevipes in pre-copulatory mate guarding behavior; (b) boiled spiny king crab; (c) coconut crab Birgus latro; (d) steamed coconut crab; (e) stone crab Hapalogaster dentata.

Fig. 3 Schema of reproductive pattern of three studied species.

Fig. 4 Annual variation in catch amount of spiny king crab Paralithodes brevipes in Hokkaido (from Hokkaido Suisan Gensei 1970–2009).

Fig. 5 Size distributions of males and females spiny king crab Paralithodes brevipes late May in 1989–1991 (a–d) off the coast of Hamanaka per definite sampling efforts (10,000 crab pots d–1). MLS in (c) and (d) indicates the minimum legal size (∼69.7 mm CL). Each arrow indicates the annual average of male CL. CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 7, © 2005b, Inter-Research Science Center.

Fig. 6 (a) Size and sex of coconut crabs Birgus latro marketed for consumption in Ishigaki Island in 2008 (total number of individuals: male, n = 1055; female, n = 50), and (b) size and sex of individuals in harvested population at Hatoma Island in 2007 (total number of individuals: male, n = 453; female, n = 557). TL: thoracic length. Reprinted and modified with permission from Marine Ecology Progress Series, 402, Sato and Yoseda, Influence of size- and sex-biased harvesting on reproduction of the coconut crab Birgus latro, 171–178, Fig. 1, © 2010, Inter-Research Science Center.

Fig. 7 Proportion of the clutch condition of females in fished population off the coast of the Hamanaka in 2003 (n = 34) and 2004 (n = 102). Rank A was a normal clutch with many eggs, Rank B was pleopods visible because of a small number of incubated eggs, and Rank C was few or no attached eggs.

Fig. 8 Mean female reproductive success of fished spiny king crab Paralithodes brevipes populations in Hamanaka Bay in 2003 (n = 35) and 2004 (n = 88). The box plots indicate median, lower and upper quartiles, with whiskers extending to minima and maxima. Reproduced from Canadian Journal of Fisheries and Aquatic Sciences, 64, Sato et al., Does male-only fishing influence reproductive success of female spiny king crab, Paralithodes brevipes?, 735–742, Fig. 5, © 2007, Canadian Science Publishing or its licensors.

Fig. 9 Temporal change in the mean female reproductive success for each population based on male size and sex ratio in the stone crab Hapalogaster dantata. L: large males in population, S: small males in population, E: equal SR, B: biased SR. See Subsection 3-3 for details. Different letters above bars indicate significant differences. For each treatment n = 4. Error bars: ±SE. Reprinted and modified with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Fig. 7, © 2006, Inter-Research Science Center.

Fig. 10 Relationship between male body size and the number of sperm in the vasa deferentia (n = 95) in spiny king crab Paralithodes brevipes. CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 8, © 2005b, Inter-Research Science Center.

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Fig. 11 Relationship between mating frequency by males of various body sizes and percentage of mating success in spiny king crab Paralithodes brevipes. CL: carapace length. Numbers above bars: sample size. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 4, © 2005b, Inter-Research Science Center.

Fig. 12 Effect of male body size on number of ejaculated sperm by small (CL 80–85 mm) or large (CL 100–100 mm) males to females (premolt CL 100–110 mm) in spiny king crab Paralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates.

Fig. 13 Relationship between male mating frequency and number of ejaculated sperm in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 1, © 2005b, Inter-Research Science Center.

Fig. 14 Relationship between male mating frequency and fertilization rate in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 3, © 2005b, Inter-Research Science Center.

Fig. 15 Relationship between male mating frequency by males of various body sizes and the number of ejaculated sperm in coconut crab Birgus latro (first mating, n = 14; second mating, n = 16; third mating, n = 12). TL: thoracic length. Reprinted with permission from Aquatic Biology, 10, Sato et al., Sperm limitation: possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro, 23–32, Fig. 3, © 2010, Inter-Research Science Center.

Fig. 16 Relationship between mating frequency by males of various body sizes and the fertilization rate in spiny king crab Pralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 5, © 2005b, Inter-Research Science Center.

Fig. 17 Relationship between mating frequency by males of various body sizes and the male reproductive success (spawning success × fertilization rate) in the stone crab Hapalogaster dentata. CL 6.0–7.0 mm, n = 23; CL 9.0–10.0 mm, n = 24; CL 13.0–14.0 mm, n = 16. CL: carapace length. Error bars: ±SE. Reprinted and modified with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Fig. 3, © 2006, Inter-Research Science Center.

Fig. 18 Recovery rate of number of sperm in vasa deferentia and number of sperm in vasa deferentia retained by unmated males by small (CL 80–85 mm) or large (CL 100–110 mm) males in spiny king crab Paralithodes brevipes. CL: carapace length. Error bars: ±SE. Numbers above bars: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Fig. 1, © 2006, Inter-Research Science Center.

Fig. 19 Variance of proportions of depleted males throughout the reproductive season in spiny king crab Paralithodes brevipes. The horizontal dotted line indicates the mean of the number of sperm in the vasa deferentia retained by males that depleted their sperm reserves (i.e. 12.22 × 106) (late April, n = 55; early–middle May, n = 26; late May, n = 45). CL: carapace length. Reprinted and modified with permission from Marine Ecology Progress Series, 296, Sato et al., Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny king crab, Paralithodes brevipes, 251–262, Fig. 11, © 2005b, Inter-Research Science Center.

Fig. 20 Relationship between the time when females were caught and number of sperm retained by females in the harvested population of coconut crab Birgus latro. Here, 24 May = 1 on the x-axis (n = 22). Reprinted with permission from Aquatic Biology, 10, Sato et al., Sperm limitation: possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro, 23–32, Fig. 6, © 2010, Inter-Research Science Center.

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Fig. 21 Effect of male-female body size difference on mating success in coconut crab Birgus latro. The equation of the logistic curve (solid line) that was fitted to the proportion of mating success is S = 1/[1 + exp(1.07–0.97 × Difference)] (Cox and Snell's r2 = 0.65, n = 56). The residual of 50% mating success (MS50) was estimated as 1.1 mm TL, indicated by the broken line. TL: thoracic length. Reprinted and modified with permission from Marine Ecology Progress Series, 402, Sato and Yoseda, Influence of size- and sex-biased harvesting on reproduction of the coconut crab Birgus latro, 171–178, Fig. 3, © 2010, Inter-Research Science Center.

Fig. 22 Relationship between number of days after molting of females and number of detached eggs in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers above bars: replicates. The asterisk indicates significant difference. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 2, © 2005a, The Crustacean Society.

Fig. 23 Relationship between days after molting of females and percentage of normal development of detached eggs in spiny king crab Paralithodes brevipes. Error bars are SE. Eggs developed to the morula stage were called as eggs that developed normally. Error bars: ±SE. Numbers above bars: replicates. Different letters above bars indicate significant differences. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 3, © 2005a, The Crustacean Society.

Fig. 24 Influence of number of days after molting of females on clutch condition in spiny king crab Paralithodes brevipes: Rank A was a normal clutch with many eggs, Rank B was pleopods visible because of a small number of incubated eggs, and Rank C was few or no attached eggs. Numbers above bars: replicates. Reprinted and modified with permission from Journal of Crustacean Biology, 25, Sato et al., Negative effects of delayed mating on the reproductive success of female spiny king crab, Paralithodes brevipes, 105–109, Fig. 4, © 2005a, The Crustacean Society.

Fig. 25 Relationships between male mating frequency and number of ejaculated sperm at different sex ratios (male:female = 1:1 or 1:6) by small (CL 80–85 mm; SM) vs. large (CL 100–110 mm; LM) males in spiny king crab Paralithodes brevipes. Error bars: ±SE. Numbers: replicates. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Fig. 4, © 2006, Inter-Research Science Center.

Fig. 26 Relationships between female size and (a) larval size (CL: cephalothoracic length, mm) (n = 30), (b) dried larval body weight (n = 30), or (c) larval survival time in non-food condition (n = 26) in coconut crabs Birgus latro. TL: thoracic length. Reprinted and modified with permission from Journal of Crustacean Biology, 30, Sato and Suzuki, Female size as a determinant of larval size, weight, and survival period in the coconut crab, Birgus latro, 624–628, Figs. 1–3, © 2010, The Crustacean Society.

Fig. 27 Schema of how large male-selective harvesting influences reproductive output, abundant and stability of resources.

Table 1 Summary of types of artificial stone crab populations. SR: sex ratio. SM: small males (carapace length (CL) 6–10 mm). LM: large male (CL > 13 mm). SF: small female (CL 8–9 mm). MF: medium female (CL 9–11 mm). LF: large female (CL > 11 mm). Each artificial population was formed from the five groups with 100 individuals with manipulating its demographic structure.

Table 2 Three-way ANOVA of the effects of male size, sex ratio, and timing of female mating on the estimated mean reproductive success of females of the stone crab Hapalogaster dentata populations with variable demographic structures. Cochran test: not significant. Reprinted with permission from Marine Ecology Progress Series, 313, Sato and Goshima, Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata, 193–204, Table 1, © 2006, Inter-Research Science Center.

Table 3 Two-way repeated measures ANOVA of the effects of sex ratio and male mating frequency on the number of ejaculated sperm in successive matings by small males (CL 80–85 mm) in spiny king crab Paralithodes brevipes. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Table 3, © 2006, Inter-Research Science Center.

Table 4 Two-way repeated measures ANOVA of the effects of sex ratio and male mating frequency on the number of ejaculated sperm in successive matings by larger males (CL 100–110 mm) in spiny king crab Paralithodes brevipes. Reprinted and modified with permission from Marine Ecology Progress Series, 312, Sato et al., Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes, 189–199, Table 4, © 2006, Inter-Research Science Center.

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