Post-Copulatory Mate Guarding in Decorated Crickets
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Anim. Behav., 1991, 41, 207-216 Post-copulatory mate guarding in decorated crickets SCOTT K. SAKALUK Ecology Group, Department of Biological Sciences, Illinois State University, Normal, IL 61761, U.S.A. (Received 8 February 1990; initial acceptance 27 April 1990; final acceptance 20 June 1990; MS. number: A5733) Abstract. Although post-copulatory mate guarding occurs in a variety of crickets, its adaptive significance remains largely unknown. Mate guarding may function to prevent females from prematurely removing the externally attached sperm ampulla, thereby ensuring maximum insemination. This hypothesis was tested in decorated crickets, Gryllodes supplicans, by comparing ampulla retention times of females guarded by their mates with those of unguarded females. There was no difference in ampulla attachment duration between the two groups, thus falsifying the 'ampulla-retention assurance' hypothesis. Two additional hypotheses related to the function of mate guarding were also tested: (I) mate guarding allows a male to remain in close proximity to his mate during the time it takes to produce a new spermatophore and (2) guarding functions to deter rivals from courting the recently mated female. The 'spermatophore renewal' hypothesis was rejected because the average inter-copulatory interval of males greatly exceeded the aver- age guarding duration. The 'courtship reduction' hypothesis was supported by four lines of evidence: (1) guarded females were less likely to be courted by intruders than were females whose mates had been removed, (2) unguarded females mounted intruders significantly more often than guarded females, (3) the ampullae of unguarded females were more likely to be partially dislodged by the copulatory attempts of intruding males than were those of guarded females, and (4) guarded females were more likely to be maximally inseminated than were unguarded females. In various insect species, males guard females after disposes of the spermatophore by consuming it mating and such behaviour usually functions to (Loher & Renee 1978; Sakaluk &Cade 1980, 1983), deter the female from remating with other males and often does so before the spermatophore has (Thornhill & Alcock 1983). Guarding serves to been emptied of sperm (Sakaluk 1984, 1987; increase a male's fitness by reducing the probability Simmons 1986). Male crickets initiate guarding that his sperm will have to compete with the sperm behaviour immediately after copulation and of his rivals for the fertilization of a female's eggs attempt to remain in close proximity to their mates (Parker 1970, 1984). Post-copulatory mate guard- by employing a variety of tactics, including: (1) ing occurs in crickets (Orthoptera: Gryllidae; passively standing immediately adjacent to the Khalifa 1950; Alexander & Otte 1967), but its func- female, (2) frequently antennating the female, (3) tion remains unclear. This study was designed to searching rapidly whenever the female wanders determine the adaptive significance of post- out of range of the male's antennae, (4) producing copulatory mate guarding in the decorated cricket, aggressive chirps upon any movement by the Gryllodes supplicans (Orthoptera: Gryllidae), a female or upon intrusion by another male and (5) species for which other aspects of copulatory behav- physically attacking males that intrude (Khalifa iour have been examined in some detail (Sakaluk 1950; Alexander & Otte 1967). 1984, 1985). There are at least three hypotheses that could In crickets, copulation is completed when the account for the post-copulatory guarding behav- male transfers a spermatophore, which usually con- iour of male crickets. First, mate guarding may sists of a small sperm-containing ampulla that hangs function to prevent the early removal of sperrnato- outside the female's body after mating (Alexander & phores by females, thus ensuring that females are Otte 1967). The spermatophore is drained as sperm maximally inseminated (Alexander 1961, 1962; enter the female's genital tract through a narrow Loher & Rence 1978; Zuk 1987). In support of this spermatophore tube inserted in the female's bursa hypothesis, a correlation between guarding time copulatrix. In most species, the female eventually and the duration of spermatophore attachment has 0003-3472/91/020207 + 10 $03.00/0 1991 The Association for the Study of Animal Behaviour 207 208 Animal Behaviour , 41, 2 been shown for a variety of species (Loher & Rence dislodge the ampulla of the female's previous mate 1978 and references; Graham 1982). Although such (Spann 1934; Loher & Rence 1978; Sakaluk 1987). a correlation is consistent with the hypothesis, it (2) Even if the ampulla is not dislodged, a female does not directly demonstrate that male guarding often removes the ampulla of her previous mate controls the ampulla-removal behaviour of after an unsuccessful mating with another male females. For example, ampulla removal might be (personal observations). (3) A mated female that is entirely under female control, with females leaving left unprotected may have her ampulla stolen and their mates shortly before or immediately after consumed by a conspecific of either sex (Sakaluk consuming the sperm ampulla. 1987). Thus, the 'rival exclusion' hypothesis This 'ampulla-retention assurance' hypothesis suggests that mate guarding may prevent prema- also poses an apparent theoretical difficulty, at least ture removal of a male's ampulla, not through as it applies to G. supplicans. In this species, the direct control of a female's behaviour, but rather male provides the female with a courtship food gift, through exclusion of competitors. the spermatophylax, a specialized portion of the I conducted experiments to determine the func- spermatophore that the female consumes after tion of post-copulatory mate guarding under two mating (Alexander & Otte 1967). This gift func- conditions: (1) in the presence of rival males and (2) tions to keep the female preoccupied while sperm in the absence of rival males. The three hypotheses drain from the remaining portion of the spermato- and their attendant predictions under the two phore (i.e. the sperm ampulla) into her body experimental conditions are summarized in Table I. (Sakaluk 1984, 1987). However, the provision of a spermatophylax does not rule out the possibility METHODS that guarding functions in a similar manner. Should the female discard the spermatophylax or Collection and Rearing Procedures consume it quickly (as often happens; Sakaluk Experimental subjects were descendants (Fs) of 1984, 1987), it may be that mate guarding acts as a approximately 60 adult G. supplicans collected at form of insurance, deterring a female that is no various locations in Tucson, Arizona, in May 1987. longer preoccupied with consuming the spermato- Captive crickets were housed in a glass terrarium phylax from prematurely removing the sperm and provisioned with Purina Cat Chow and water ampulla. in vials plugged with cotton wicks. The effective A second hypothesis is that guarding allows a surface area of the terrarium was increased by the male to maintain close physical proximity to his addition of several egg cartons as a form of shelter. mate during the time it takes to manufacture a Eggs were obtained by allowing adult females to new spermatophore, thus permitting repeated oviposit in 0' 1-1itre plastic weighing dishes filled copulations with the same female (Khalifa 1950; with a mixture of equal amounts of moistened sand Alexander & Meral 1967; Loher & Rence 1978). and vermiculite. Offspring were reared in plastic This 'spermatophore renewal' hypothesis assumes shoe boxes measuring 16.5 • 30.5 • 8.5 cm, pro- that multiple matings with the same female are visioned in the same manner as the adults, and held adaptive. In support of this assumption, Sakaluk in environmental chambers maintained at 30 + 1~ (1986) and Simmons (1987) have shown that on a 12:12 h light:dark cycle. Two holes, each 5 cm the fertilization success of a male's sperm, rela- in diameter, were drilled in the cover of each cage tive to that of rivals' sperm, depends partly on and covered with metal screen to permit adequate their numerical representation in the female's ventilation. To ensure the production of robust spermatheca. adult stock, densities in rearing cages were main- A third hypothesis is that mate guarding func- tained at low levels, ranging from five to 12 crickets tions to deter other males from courting the female, per cage. Individuals of known age and mating thereby reducing the probability of the females' status were obtained by isolating crickets by sex in remating and the concomitant risk of sperm com- separate cages immediately after the imaginal petition. Failure to prevent access of rivals to the moult. female can be costly to a male in several other respects. (1) A recently mated female will often General Methods mount another courting male, and the thrusting All matings were staged in plastic shoe boxes actions involved in an attempted copulation may during the dark portion of the photoperiod within Sakaluk: Mate guarding in crickets 209 Table I. Hypotheses concerning the function of post-copulatory mate guarding in crickets and their attendant predictions Predictions Male/female pairs Male/female pairs Hypothesis no rivals present rivals present (1) Ampulla-retention a>b a>b assurance e = f g=h (2) Spermatophore-renewal c>~d c~>d (3) Rival exclusion a=b a>b e<f g<h a: Ampulla attachment times of guarded females. b: Ampulla attachment times of unguarded females. c: Guarding times of males. d: Spermatophore replacement times of males. e: Courtship attempts by rivals when guard present. f: Courtship attempts by rivals when no guard present. g: Remounting frequencies of guarded females. h: Remounting frequencies of unguarded females. 4-10h of 'lights off', the period during which male was removed from the mating cage immedi- decorated crickets are most active (Sakaluk 1987). ately after mating. Group 3 consisted of 15 pairs in Observations were made under the illumination which the male was removed immediately after provided by a 25-W incandescent red light. No food mating, but then immediately placed back with the or water was provided during experimental trials female.