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Random Mating by Size in the Simultaneously Hermaphroditic Land Snail Arianta Arbustorum: Experiments and an Explanation

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Random Mating by Size in the Simultaneously Hermaphroditic Land Snail Arianta Arbustorum: Experiments and an Explanation Anita. Behav., 1992, 43, 511-518 Random mating by size in the simultaneously hermaphroditic land snail Arianta arbustorum: experiments and an explanation BRUNO BAUR Institute of Zoology, University of Basel, Rheinsprung 9, CH-4051 Basel, Switzerland (Received 7 March 1991; initial acceptance 4 April 1991; final acceptance 23 August 1991; MS. number: 3737) Abstract. It has been proposed that size-assortative mating should occur in simultaneous hermaphrodites with reciprocal fertilization and size-related fecundity because all individuals invest substantially in mating. Mating patterns were recorded in two species of simultaneously hermaphroditic land snails. In a natural population of Helix pomatia, snails showed a slight (but non-significant) tendency towards size- assortative mating, whereas mating in a population ofA rianta arbustorum was random with respect to size. Laboratory experiments were conducted to test (1) whether individuals of A. arbustorum discriminate between mating partners of different size, and (2) whether a large shell might be of advantage during courtship to increase mating success. In mate-choice tests with individuals of different shell size, pairs formed randomly with respect to size. Courtship was neither hindered nor prolonged in pairs with large size differences. In the second experiment, a large snail was placed close to two courting conspecifics (both smaller). The larger snail interfered with the courting snails, but in general did not displace one of them. Courtship progressed to copulation only if one of the three snails ceased to court; this was independent of the size of that individual. Thus, a large shell did not increase mating success. It is suggested that time- constraints of locomotory activity and high costs of searching for a mate can explain the prevalence of random mating patterns in simultaneously hermaphroditic land snails. Size-assortative mating is a common mating Ridley (1983) proposed that three conditions are pattern in natural populations of many inverte- necessary and sufficient for the development of brate and vertebrate species (e.g. Bateson 1983; size-assortative mating in natural populations. Ridley 1983; Crespi 1989). Among molluscs, size- These factors are (1) a correlation between male assortative mating has been observed in marine size and success in competition for mates (intra- gastropods (Crozier 1918; Edwards 1968). In sexual selection), (2) a correlation between female simultaneously hermaphroditic terrestrial gastro- size and fecundity, and (3) prolonged pairing. pods, however, mating has been reported to be Ridley (1983) suggested that size-assortative random with respect to shell size (Cepaea mating should also occur in simultaneous nemoralis: Wolda 1963), shell colour and banding hermaphrodites with reciprocal fertilization and pattern (C. nemoralis: Schilder 1950; Schnetter size-related female fecundity. He argued that all 1950; Lamotte 1951; Wolda 1963), as well as individuals invest substantially (all their eggs) in between resident and introduced individuals (Helix mating, so there will be selection for careful mate pomatia: Woyciechowski & Lomnicki 1977). An choice. Specifically, a land snail should choose a exception is Partula suturalis, in which assortative mate as large as possible. mating with respect to dextral and sinistral shell In another approach, Parker (1983) proposed a coiling has been observed in the wild (copulation is model for indiscriminate mate choice (random hindered but not prohibited by opposite coil in this mating). This should occur when there is little vari- species; Clarke & Murray 1969; Johnson 1982). ance in mate quality in both sexes, and/or when Hermaphroditic land snails would greatly enhance search costs for mates are high (e.g. low encounter their reproductive success by choosing large mates rates due to low population densities or low since female fecundity (number of clutches, clutch mobility). size and egg size) is positivelycorrelated with shell size Here I present data on mating patterns in natural (Wolda 1963; Baur 1988a; Baur & Raboud 1988). populations of two species of hermaphroditic land 0003 3472/92/030511 +08 $03.00/0 1992 The Association for the Study of Animal Behaviour 511 512 Animal Behaviour, 43, 3 snails. I also present experiments designed to test MATING PATTERNS IN NATURAL whether courting individuals of the land snail POPULATIONS Arianta arbustorum discriminate between potential mates of different size and whether large individ- Observations on mating A. arbustorum were made uals have any way of increasing mating success in a natural population in a subalpine forest near during courtship. Based on field observations and Gurnigel, 30km south of Bern, Switzerland experimental results, I propose a hypothesis to (46~ 7~ altitude 1430 m above sea level). explain the absence of size-assortative mating in Snails were abundant on the embankment of a simultaneously hermaphroditic land snails. track (population size approximately 300 sexually mature individuals). On 3 May 1990, snails were creeping in patches free of snow. Thirty-five mating STUDY ANIMALS pairs were found between 1200 and 1400 hours. I measured the size (shell breadth and height) of Arianta arbustorum is a simultaneously herma- mating and non-mating snails to the nearest phroditic, self-incompatible helicid land snail, 0.1 mm using a vernier caliper and calculated which is common in moist habitats of north- shell volume following Rensch (1932): shell western and central Europe. Individuals become volume = (breadth) 2 x (height/2). Shell volume is a sexually mature at an age of 2-4 years. Adult snails more reliable measurement of snail size than live on average 3-4 years (maximum 14 years; Baur weight, because weight depends on the state of & Raboud 1988). In the field, snails deposit one to hydration and thus is highly variable in terrestrial three clutches each consisting of 20 50 eggs in each gastropods. reproductive season (Baur & Raboud 1988; Baur Mating patterns are usually quantified by the 1990). product-moment correlation coefficient (r) for Mating behaviour in A. arbustorum includes in- the sizes of mating pairs (Ridley 1983). In troductory behaviour (foreplay) with reciprocal simultaneously hermaphroditic animals r can be tactile and oral contacts, and curving turns to reach distorted by the way the animals' sizes are assigned an optimal position with respect to the genital to the axes. To overcome this problem, I used a opening of the partner (Hofmann 1923; B. Baur, randomizing method to assign the larger or smaller unpublished data). This is followed by dart individual of a mating pair first to the X-axis, shooting, the pushing of a calcareous dart into the the other to the Y-axis. Having calculated the cor- mating partner's body, which is assumed to facili- relation coefficient r, the individuals of each mating tate mating by increasing behavioural synchrony pair were again randomly assigned to the axes. This (Adamo & Chase 1988). Finally, the copulation is procedure was repeated 100 times and r is presented reciprocal; spermatophores are transferred after as the mean value of 100 runs. Correlations are simultaneous intromission. Arianta arbustorum presented for shell volume; body size expressed mates repeatedly in the course of a reproductive by linear dimensions (shell breadth and height) season and viable sperm can be stored for more yielded lower r-values throughout. Deviations than a year (Baur 1988b). from random mating (r= 0) were tested using a Helix pomatia, also a simultaneously reciprocal two-sided t-test (Sokal & Rohlf 1981). hermaphrodite, has elaborate mating behaviour Mating and non-mating snails did not differ in (for detailed descriptions see Meisenheimer 1907; size (,g+SD; shell volume of mating snails: Lind 1976). Mating is followed by an obligatory 2.28 + 0-31 cm 3, N= 70; non-mating snails: 2.30 + post-copulatory pause which lasts up to 8 h and is 0'33cm 3, N=188; t=0.397, P>0.7). Mating essential for the internal transport of the spermato- A. arbustorum varied in shell volume from 1'65 to phore (Lind 1973, 1976). In the field, mating can 2.96 cm 3, but pairs were formed randomly with last up to 36 h (Tischler 1973; Lind 1988). Periods respect to size (r = 0'245, N= 35, P = 0' 16; range ofr of mating activity alternate with periods without in the 100 runs: 0.2284).305). None of the 100 ran- mating activity. In the latter phase a snail will not domized runs revealed any significant correlation mate even in the company of a sexually active snail coefficient (for dr= 33 the critical value of r is 0"334 (Jeppesen 1976). Individuals mate two to six times at the 5% level). per year, and viable sperm are stored for up to Observations on mating H. pomatia were made 4 years (Tischler 1973; Duncan 1975; Lind 1988). in a natural population near Uppsala, central Baur: Mating patterns in land snails 513 Sweden (59~ 17~ in the late afternoon of photoperiod) for at least 2 weeks before being used 10 June 1988. This population lives on the northern in the tests. Based on their shell size (measured as periphery of the species distribution (H, pomatia described above), the individuals were divided was originally brought to Sweden during medieval into three groups: small snails (shell volume times; Kerney & Cameron 1979). The snails were 1-60-2.10 cm 3, N= 61); medium-sized snails (2.11- abundant (700-1000 sexually mature individuals) 2"45 cm 3, N=62) and large snails (2.46-3.50 cm 3, in a clearing of a pine-dominated forest. The tem- N= 65). Hereafter these groups are referred to as perature was 18~ and the vegetation was drying small, medium and large snails. Half of the snails up after a rain shower the previous night. Many of each group were used in the size-discrimination snails were active, most of them grazing. Approxi- experiment, the other half in the size-advantage mately 20% of the active snails were courting or experiment (see below).
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