ICES mar. Sei. Symp., 199: 13-18. 1995

Potential depensatory mechanisms operating on reproductive output in gonochoristic molluscs, with particular reference to strombid gastropods

Richard S. Appeldoorn

Appeldoom, R. S. 1995. Potential depensatory mechanisms operating on repro­ ductive output in gonochoristic molluscs, with particular reference to strombid gastro­ pods. - ICES mar. Sei. Symp., 199: 13-18.

Molluscs are typically sessile or slow moving, yet successful reproduction requires close proximity to potential mates. Three mechanisms are identified whereby repro­ ductive potential of a population can be limited under conditions of low density. The first is the reduction in numbers of spawners as abundance decreases. The second reflects the difficulty in finding mates, and takes the form of either (1) search time for slow but motile , or (2) wasted spawning (or non-spawning) for sessile species, where gametes are not fertilized. The third mechanism is a breakdown of a positive feedback loop between contact with males (either direct or through chemical cues) and rate of gametogenesis and spawning in females, i.e., sexual facilitation. The second and third mechanisms are functions of local density, rather than overall abundance. Literature review and present studies on strombid gastropods indicate the potential for these mechanisms to occur. Many species are characterized by behaviours, such as aggregative settlement, that serve to overcome this problem. Intensive fishing prac­ tices may invoke these depensatory mechanisms as local density and abundance are reduced, thereby increasing the chance of recruitment failure.

Richard S. Appeldoom: Department of Marine Sciences, University of Puerto Rico, Mayagiiez, Puerto Rico 00681-5000 [tel: (+809) 899 2048, fax: (+809) 899 5500],

Introduction dation, cannibalism, competition, and starvation) occurring during early life stages. Only a few studies Successful reproduction is essential to stock mainten­ have emphasized mechanisms operating at other life ance. This salient point has been recognized both in stages, particularly those controlling reproductive nature and in management. Strong selective pressure potential (factors affecting fecundity, egg size, etc.) has, over evolutionary time, resulted in reproductive (Larkin et a i, 1964; Nikolskii, 1969; Bagenal, 1973; behaviours consisting of multiple mechanisms acting in Ware, 1980). The majority of these are concerned, as parallel to ensure successful reproduction (Audesirk above, with compensatory mechanisms. Larkin et al. and Audesirk, 1985). In fisheries, intense exploitation (1964) recognized the importance of possible depensa­ can adversely affect stock maintenance by reducing tory mechanisms, i.e., those mechanisms acting to dis­ spawning-stock size to a point were reproductive poten­ proportionately reduce recruitment when stock size is tial is insufficient to ensure adequate recruitment. Re­ reduced. However, their treatment of this was limited to cruitment overfishing can have serious consequences, the effects of predation. and its prevention has become a principal objective of This article reviews possible depensatory mechanisms management theory and practice (Gulland, 1983). affecting recruitment in molluscs, through control of Theoretical approaches to stock-recruitment re­ reproductive potential, at both the individual and popu­ lationships have largely been concerned with compensa­ lation levels. 1 do not intend to argue here that these tory mechanisms (e.g., Ricker, 1954). Such mechanisms mechanisms are of overriding importance and must be serve to maintain stock-size stability by increasing re­ considered in the practical management of molluscan cruitment rate at low spawning-stock levels and de­ resources, although there may be species where this is creasing recruitment at high stock levels. Additionally, so. My purpose is to explore the evidence for their emphasis has been placed on mechanisms (e.g., pre­ existence and possible significance in an attempt to 14 R. S. Appeldoom ICES mar. Sei. Symp., 199 (1995) understand reproductive processes and their population may result from an excess of eggs being produced, consequences more fully. whereupon recruitment is primarily independent of Throughout this article particular emphasis is given to stock size and dependent upon environmental varia­ conchs, large marine gastropods of the genus . bility. However, where environmental factors have been Conchs support a valuable commercial and recreational accounted for, underlying stock-dependent recruitment fishery throughout the Caribbean region, with the queen has been found (e.g., Crecco et al., 1986). The effect (S. gigas) being most important. Conchs repeat­ may also go unobserved because some compensatory edly copulate and spawn over a protracted spawning mechanism is operating, such as increased survival season, with maximum rates of spawning occurring among eggs and larvae. However, as stock size declines during summer months (Randall, 1964; Davis et al., a point is reached beyond which the loss of egg produc­ 1984; Weil and Laughlin, 1984). Females lay demersal tion cannot be compensated. egg masses and can store viable sperm from a single This first mechanism is obvious. In conjunction with copulation for several weeks (D’Asaro, 1965; Weil and age-specific fecundity rates, it is usually incorporated Laughlin, 1984). Spawning occurs at discrete sites. Esti­ into models attempting to quantify the effects of harvest mates of spawning rate are few. For queen conch, Weil strategy on reproductive potential (e.g., Botsford and and Laughlin (1984) reported an average of 8.7 days Hobbs, 1986; Prager et al., 1987). between spawnings in isolated females during the height of the spawning season. Davis and Hesse (1983) and Davis et al. (1984) reported a maximum rate of 8.3 days Mechanism 2: Number of eggs fertilized (via between spawnings. Averaged over the entire 6-month copulation) or fertilization rate (broadcast season, the time between egg masses per female was spawning) are a positive function of density 24.4 days. Maximum observed spawning rates for S. In molluscs, because they are sedentary or slow moving, pugilis are somewhat higher (Reed, 1992). Taking an stock density is also important. In conchs, males must average of 400000 eggs per egg mass (Thorson, in find and copulate with females. As long as individuals Robertson, 1959; Randall, 1964; Weil and Laughlin, are aggregated this should not be a problem. However, 1984), with an egg mass spawned every 24.4 days over a in heavily fished areas aggregations are destroyed when 6-month spawning season, a female S. gigas would be harvested, with only scattered individuals remaining. expected to spawn 3000000 eggs/year. This estimate is When this happens there is added a “search time” cost to similar in magnitude to those for other large molluscs reproduction, both in terms of energy and time. Conchs (see, e.g., Galtsoff (1964) for oysters; Hahn (1989) for unable to find mates at all or at a rate insufficient in abalone). Conch eggs hatch in a few days, producing comparison to their rate of gametogenesis will not repro­ planktotrophic veligers with an estimated larval life of duce to their full capacity. This density effect is additive two to five weeks (see review in Mitton et al., 1989). to the stock abundance effect given above. This mechanism ought to operate similarly in sessile species with broadcast spawning. Here the loss at low Depensatory mechanisms density takes the form of wastage of gametes not ferti­ lized. Low densities of eggs and sperm will reduce the Presented below are three potential mechanisms relat­ probability of their contact (demonstrated by Levitan ing stock to reproduction and recruitment, one depen­ (1991) for sea urchins). dent upon total abundance and two dependent upon This effect of density on reproduction, although density. The former is characteristic of all species; occur­ recognized (Thorson, 1950; Audesirk, 1977), has not rence of the latter two will depend upon species-specific been studied specifically for any mollusc. Yet, its im­ characteristics. After each mechanism is defined, evi­ portance is manifested by the number of mechanisms dence for their existence is reviewed. evolved to counteract the effects of low density, and the use of more than one mechanism by many species. These are briefly reviewed below. Mechanism 1: Total reproductive output is a Although interest here is with gonochores, it is worth positive function of the number of spawners mentioning an evolved strategy that specifically acts to The influence of total abundance follows along the lines offset low density: hermaphroditism. Theoretical of typical stock-recruitment relationships, as observed studies have generally shown hermaphroditism to be or implied in other species. As abundance of spawners increasingly advantageous as density decreases or declines there is a concomitant reduction in egg produc­ motility is reduced (Tomlinson, 1966; Ghiselin, 1969). tion for the population. At high stock levels this relation­ Hermaphroditism is common among many bivalves and ship may often go unnoticed (for examples in finfishes, gastropods (Coe, 1942; Audesirk and Audesirk, 1985). see Hennemuth (1979), Hennemuth et al. (1980)). This Facultative sex determination is another obvious i c e s mar. Sri. Symp., 199 (1995) Depensatory mechanisms and reproductive output in gonochoristic molluscs 1 5 mechanism, often found in sequentially hermaphroditic ing several times per season. I illustrate this mechanism species. Here the presence of one sex stimulates a later using conchs; here this mechanism would operate as a recruit to develop into the other sex. In Iow-density positive feedback between spawning and gameto­ environments this increases the chances that gametes genesis. will be fertilized. The best example is that of Crepidula In conchs, the mechanism operates on two assump­ fornicata (Coe, 1948). tions: (1) contact with males stimulates gametogenic Perhaps the most widely adopted strategy is that of activity in females, and (2) spawning females are more aggregation. This can be achieved in two ways: by likely to copulate than non-spawning females. If these aggregative settlement, and in motile species by post­ conditions are met, then positive feedback will exist settlement aggregation. Post-settlement aggregation is between spawning and gametogenesis. The mechanism found among many gastropods, e.g., Nucella, Thais, works as follows. Female gametogenic activity is stimu­ Conus, nassariids, littorinids (Fretter, 1984), and squids lated by contact with males, primarily at the time of (Arnold, 1984). In Aplysia and Thais, spawning individ­ copulation. The greater the degree of contact, the uals are known to release a pheromone that attracts greater the stimulation. Females so stimulated would others to the aggregation (Audesirk, 1977; D’Asaro, produce larger and more frequent egg masses. For males 1966). Aggregative settlement is common in many to copulate, they must first find and “catch” females. species of molluscs, e.g., Mytilus edulis (Bayne, 1969), This would be easiest when females are laying eggs, a Crassostrea virginica (Hidu, 1969), and can result from time of 24 h or more in which they do not move passive aggregation by hydrodynamic forces or selective (D’Asaro, 1965). Thus, females laying eggs should have settlement by individuals attracted by physical or chemi­ a higher rate of copulation and therefore a higher degree cal properties of the environment, including presence of of gametogenic stimulation. In essence, the more fre­ conspecifics (Crisp, 1965; Meadows and Campbell, quent a female lays eggs, the greater the degree of 1972). copulation, leading to more frequent egg deposition, A strategy specifically suited to avoid wastage and and so on. Such behaviour has been observed in Aplysia; enhance fertilization of spawned gametes is the stimu­ through the action of pheromones, copulation stimu­ lation of simultaneous spawning among individuals in an lates spawning, which in turn stimulates copulation area, and this has been documented for a wide variety of (Audesirk, 1977). It is not known, however, whether molluscs (see Thorson, 1950). Stimulation may be enhanced gametogenesis results as well. through a common environmental trigger, such a rapid Evidence that contact with males stimulates gameto­ change in temperature, or the detection of conspecific genic activity in females (Assumption 1) is only indirect gametes in the water. with respect to conchs. Work on other species is also In a similar manner, pairing of males and females will limited, but it does document a strong coupling between enhance fertilization and minimize wastage. In some female gametogenic production and stimulation by species of prosobranchs individuals are known not to males. Working with lizards, Crews et al. (1986) found spawn unless sufficiently close to another of the opposite that isolated females produced fewer eggs per spawn and sex (Thorson, 1950). Evidence of pairing has been ob­ spawned at a frequency half that of females kept in the served in the surf clam, Spisula solidissima (Flowers and presence of males. In many instances no ovulation Sissenwine, 1972), the shipworm, Bankia gouldi occurred in the absence of sexually active males (Crews, (Purchon, 1977), and in several genera of limpets 1977). Identical results were found in Drosophila (Fretter, 1984). A related phenomenon is the obser­ (Crews et al., 1985), suggesting that the phenomenon is vation of dwarf males in association with females widespread across taxonomic lines. (Morton, 1976; Turner and Yakovlev, 1983; O’Foighil, Little is known about the behavioural and hormonal 1985; Pascual etal., 1989). control of reproduction in prosobranchs; studies that have been done have dealt primarily with hermaphro­ dites (Jousse and Geraerts, 1983). Generally, in mol­ Mechanism 3: Total reproductive output luscs it is evident that one sex is capable of stimulating increases with density due to enhanced sexual the other, either through direct physical contact (e.g., facilitation mating behaviour in Helix pomatia, Jeppesen, 1976) or Mechanism 3 would become operational under the same through the influence of pheromones (e.g., sex determi­ conditions given above for Mechanism 2. This mechan­ nation in Crepidula fornicata, Jousse and Geraerts, ism is more subtle than the previous one and involves 1983; stimulation of spawning in Aplysia californica, sexual facilitation, i.e., enhanced rates of gametogenesis Audesirk, 1977; Audesirk and Audesirk, 1985). and spawning due to stimulation by members of the In S. gigas a consistent lag at the start of the spawning opposite sex (Crews, 1977; Crews et al., 1985, 1986). It season between first observations of copulation and first would most probably be limited to those species spawn­ spawning has been reported (Randall, 1964; Hesse, 16 R. S. Appeldoorn ICES mar. Sei. Symp., 199 (1995)

1976; Brownell, 1977; Weil and Laughlin, 1984). Lags appeared to attract more males than females only copu­ range from 2 to 4 weeks, averaging three. It is possible lating, and they hypothesized that females were releas­ that this lag represents the latency period between first ing a pheromone while spawning. In response, males stimulation of gametogenesis and oocyte maturation were orienting preferentially toward these females. The and/or the production of egg-capsule laying substance advantage to the females under this hypothesis is (ECLS) (Ram, 1977). It is interesting to note that the obvious: spawning decreases their stock of stored smallest lag time (2 weeks) was reported for the densest sperm, which must be replenished, and another cycle of population (Los Roques; Weil and Laughlin, 1984), oogenesis and/or maturation must be stimulated. The where because of the proximity of males and females the release of pheromones during spawning is well docu­ rate of copulative stimulation should have been highest. mented in Aplysia (Audesirk, 1977; Audesirk and In Aplysia it is known that copulation stimulates the Audesirk, 1985), and in the prosobranch, Olivella, atrial gland to produce a substance that subsequently males can recognize and track a female-secreted phero­ stimulates spawning (Jousse and Geraerts, 1983). mone (Fretter, 1984). Davis and Hesse (1983), in the Turks and Caicos Quantitative support for Assumption 2 comes from Islands, assumed that the high rate of egg production by year-long surveys of reproductive activity in the milk S. gigas in their enclosures was due to the close proxim­ conch, S. costatus (Appeldoorn, 1988), and the fighting ity of males and females. This is essentially invoking conch, S. pugilis (Reed, 1992). In the former study, Mechanism 2, above, since natural populations were 46.7% of spawning females were also copulating. considerably less dense due to fishing. Weil and Among non-spawning females (assuming a 1:1 sex Laughlin (1984), in Los Roques, obtained even higher ratio), only 6.1% were copulating. Thus, spawning rates of egg production, which they thought were due to females were 7.7 times more likely to copulate than non­ their higher density. Indeed, within their study the spawning females. In the latter study, copulation involv­ highest rates of egg production were found in the area of ing a non-spawning female was so infrequent as to be highest density. Again, density-dependence is obvious. negligible. However, the density differences between Turks and Caicos and Los Roques do not appear to be large enough for egg production differences to be accounted for by Discussion differences in search time alone, which may imply the role of Mechanism 3. Stock-recruitment relationships have been developed Lastly, Weil and Laughlin (1984) noted that egg for highly mobile marine finfish species. These species masses spawned by female S. gigas after 6 weeks in typically have set spawning grounds to which they isolation were noticeably smaller than previous egg migrate (Cushing, 1982), and size of the spawning area masses. Six weeks is the approximate limit of sperm tends to expand or contract with the size of the spawning viability (D’Asaro, 1965), as witnessed by the low or stock (Lough et al., 1981; Cushing, 1982). In this way non-viability of resulting eggs (Weil and Laughlin, density for spawning purposes can be conserved to some 1984). Thus, the presence of viable sperm seemed to degree. This is not the case for sessile bivalves and slow- stimulate egg production. moving gastropods, where reproductive production can In support of Assumption 2, that spawning females be subject to density-dependent processes not necess­ are more likely to copulate than non-spawning females, arily significant in finfish species. it is first noted that concurrent spawning and copulation If the density-dependent mechanisms presented in S. gigas has often been reported. Hesse (1976) ob­ above are significant, the resulting recruitment curve served a particularly high incidence of this (90%) in should differ from the more typical Ricker (1954) or clusters of one female and several males. Even in iso­ Beverton and Holt (1957) models in having an inflection lated pairs it was observed “often”. Weil and Laughlin point (Fig. 1). The curve would be similar at high stock (1984) also reported spawning and copulation as being densities, but as stock size declines, and density at common. spawning is not conserved, the decline in reproductive A common observation is a single female ac­ output would cause recruitment to decline more rapidly. companied by several (up to 8) males (Hesse, 1976; The point at which recruitment barely exceeds replace­ Brownell, 1977; Weil and Laughlin, 1984). In the fight­ ment or even falls below it due to a lack of significant ing conch, S. pugilis, males have been reported to reproduction would occur at a larger relative stock size. passively “guard” females after copulation (Bradshaw- This also implies that, under these conditions, a species’ Hawkins, 1982) or aggressively attempt to block other ability to compensate is reduced, since the area under males from copulating (Reed, 1992). This implies that the curve, but over the replacement line is reduced in females are hard to find, and once found are pursued. both the horizontal and vertical directions, i.e., the Weil and Laughlin (1984) noted that egg-laying females potential range of stock sizes over which compensation i c e s mar. Sei. Symp., 199 (1995) Depensatory mechanisms and reproductive output in gonochoristic molluscs 1 7

buffer against recruitment overfishing is an open question; that these populations are declining rapidly is not. In many estuarine bivalves, dense populations can be found in polluted areas closed to fishing. These areas cn may also act as refuges if the pollution is non-toxic. In other instances, attempts have been made to create erZ> spawner sanctuaries by transplanting clams into pro­ o tected areas (Carter et al., 1984; McCay, 1988). The LU overall importance of maintaining populations of high CC density cannot yet be determined, but the arguments given above indicate that density could be significant in maintaining the reproductive potential of a stock.

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