Paternal investment in Poecilimon veluchianus bushcrickets: beneficial effects of nuptial feeding on offspring viability

In most bushcrickets, males transfer a large spermatophore during copulation that is afterwards consumed by the female. In some species this nuptial gift enhances offspring fitness and is therefore believed to function as paternal investment. To determine whether this is the case, I examined whether a male's own offspring benefit from spermatophore consumption in the bushcricket Poecilimon veluchianus. Females that consumed a spermatophore produced offspring with increased residuals of dry weight compared to females that were prevented from feeding on the spermatophore. This beneficial effect of spermatophore consumption occurred within the first 4 days after copulation. An increased dry weight indicates higher energy reserves because offspring dry weight correlates significantly with the lifespan of starved larvae and because spermatophore consumption increased the lifespan of starved offspring. During egg-laying, females apply a liquid substance to the soil that hardens and probably serves as protection for the egg clutch. The amount of this substance correlated with the number of eggs laid but did not differ between spermatophore treatments. In P. veluchianus, females mate frequently and there is last-male sperm precedence. The spermatophore thus only constitutes paternal investment when offspring produced before female remating benefit from spermatophore consumption. The dry weight of offspring increased during the first 4 days after spermatophore consumption and thus within the natural remating interval. This shows that the spermatophore has a paternal investment function in addition to its already known sperm protection function. Received: 15 May 1998 / Accepted after revision: 11 October 1998     

Biased primary sex ratio in the bushcricket Poecilimon veluchianus,an insect with sex chromosomes

Offspring sex ratio at hatching was examined in the bushcricket Poecilimon veluchianus. Offspring sex ratios varied significantly between females (Fig. 1). Low mortality prior to sex determination established that this heterogeneity was already present in the primary offspring sex ratio. Sperm age and female age had no influence on offspring sex ratio (Fig. 2). Male age at copulation, however, correlated significantly with offspring sex ratio (Fig. 3). There were two types of males: one type produced predominantly daughters when young and an increasing proportion of sons with age. The other type produced, independent of age, 1:1 offspring sex ratios (Fig. 4). The two types of males seem to occur in approximately equal numbers. Sex ratio variation (1) may adaptively compensate for local sex ratio biases caused by sex-specific motility, or (2) it may be adaptive if there is a sex-differential effect of laying date on offspring fitness. Received: 14 March 1996/Accepted after revision: 24 June 1996     

Some costs of reproduction for male bushcrickets,Requena verticalis (Orthoptera : Tettigoniidae) allocating resources to mate attraction and nuptial feeding

Summary The cost of reproductive effort is known to result in a trade-off between current and future reproduction. Similarly, trade-offs in energy allocation may occur between components of reproductive effort, mating and parental effort, within a single reproductive episode. We investigated the energy allocated to mating effort (calling to attract females) and parental effort (donation of spermatophore nutrients at mating) by male bushcrickets, Requena verticalis, under two dietary regimes. Males provided with a low quality diet reduced the daily energy allocated to calling activity while maintaining their investment in spermatophores. Males provided with a high quality diet did not allocate more resources per day to their spermatophores but stored excess energy for future reproduction. Thus, on a per day basis, males appear to hold constant their investment in the spermatophore at the cost of reduced mating effort when resources are limited. Males on both diets, however, increased the size of their spermatophore donations when the interval between female encounters was increased. One explanation for this pattern could be a frequency-dependent optimization of spermatophore size. Correspondence to: L.W. Simmons     

Protandry and mate assessment in the wartbiter Decticus verrucivorus (Orthoptera : Tettigoniidae)

Summary Protandry, or early male emergence, is prevalent in the majority of insects. There are several explanations, both adaptive and incidental for this widespread phenomenon. Here I report the occurrence of protandry in the wartbiter, Decticus verrucivorus, and argue that the explanation for the evolution of protandry in this species is the result of selection acting on males in relation to sperm competition. It has previously been shown that sperm mixing occurs in this species, leading to a reduction in confidence of paternity with number of matings. Emerging early and thereby having a higher probability of mating with virgin females benefits males in two ways: both through a 100% assurance of paternity and because female egglaying rate decreases over time. A singly mated female can lay up to 30% of her lifetime egg production during her first refractory period, during which time the eggs are exclusively fertilized by the first male. Wartbiter males seem also to be able to assess female mating status and transfer larger spermatophores when mating with virgin females than when mating with already mated females. This holds true both for previously mated and virgin males. Thus, it seems that male wartbiters allocate their resources differentially depending on female quality.     

The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae,Decticus verrucivorus)

Summary Male wartbiters Decticus verrucivorus transfer elaborate spermatophores to females during copulation. The spermatophore is attached externally to the female's genitalia and consists of two parts: a large, gelatinous, sperm-free portion, the spermatophylax, eaten by the female after mating; and a sperm-containing ampulla, eaten after the spermatophylax has been consumed. Since females take longer to eat larger spermatophylaxes, the duration of ampulla attachment is positively correlated with spermatophylax size. Two series of experiments were carried out, one in which the size of the spermatophylax consumed by females and the duration of ampulla attachment were manipulated in concert and another in which they were manipulated independently. Some females were also maintained on a protein-free diet and either supplied with or deprived of spermatophylax material. The amount of protein in the diet, but not the amount of spermatophylax material consumed, influenced female longevity, lifetime fecundity, and egg weight. When females were deprived of the spermatophylax, an experimental increase in the duration of ampulla attachment induced longer periods of unreceptivity in females after mating, a more rapid onset of oviposition, and an increased oviposition rate. Consequently, the number of eggs laid by females during their nonreceptive refractory periods increased significantly with increasing duration of ampulla attachment up to 180 min; however, there was no significant increase in the number of eggs laid beyond 180 min of ampulla attachment. This closely corresponds to an ampulla attachment duration of 188 min expected when a male transfers a natural spermatophylax of mean size to the female. These results suggest that the amount of ejaculate transferred to the female, and not the amount of spermatophylax material per se, is the factor controlling female receptivity and oviposition behavior. Since we did not detect any effect of spermatophylax consumption on female fecundity or egg weight, we conclude that the spermatophylax of D. verrucivorus functions primarily as a sperm protection device rather than as a form of male parental investment.     

Pre-mating sperm removal in the bushcricket Metaplastes ornatus Ramme 1931 (Orthoptera, Tettigonoidea, Phaneropteridae)

Summary Mating in the bushcricket Metaplastes ornatus Ramme 1931 entails a number of peculiar genital couplings that precede the transfer of the large spermatophore. During these phase-I couplings, the male introduces his specially structured subgenital plate into the female's genital chamber, performs back-and-forth movements, and turns her genital chamber inside out when he withdraws, whereupon the female carefully cleans her everted genital chamber with her mouthparts. During the last coupling (phase II) the male's subgenital plate is not introduced but the large spermatophore, which averages 22% of a male's body weight, is transferred. Counts of sperm in the spermathecae of females suggested that the phase-I couplings, which occur prior to spermatophore transfer, function to remove, or at least to reduce, the sperm of a female's previous mates. The form of the keel of the male's subgenital plate, its position within the female's genital tract during phase-I couplings, and the back-and-forth movements suggest that the male may stimulate release of sperm from the female's spermatheca by a mechanism similar to fertilization as eggs pass through the genital chamber during oviposition.     

Geometrical Factors and Metapopulation Dynamics of the Bush Cricket, Metrioptera bicolor Philippi (Orthoptera: Tettigoniidae)

This paper presents a metapopulation study of the bush cricket, Metrioptera bicolor , living in a recently fragmented landscape. The species inhabits grass and heathland patches of varying area and isolation. Analyses are made of how these geometrical factors affect local population size and density, distribution pattern, and the probability of local extinction and colonization. The proportion of available patches occupied varied between 72 and 79% during 1985–1990. Unoccupied patches were smaller and more isolated than those that were occupied. Patches where populations became extinct during this period were smaller than those with persisting populations. Since local population size was well correlated with patch area, it was clear that stochastic extinctions only occurred in small populations. Critical patch size for population extinction was approximately half a hectare. Colonized patches were less isolated than those that had not been colonized. Critical inter-patch distance for colonization was about 100 meters. The turnover was restricted to an identifiable share of the available patches. Only 33% of the patches were so small that extinction due to stochastic causes could be considered highly probable. This metapopulation will therefore most likely persist over a considerable period in its present spatial structure. There are apparent threats of further fragmentation, however, and nothing is known about the likelihood of large-scale extinctions resulting from extremely unfavorable weather conditions. Nevertheless, our results show that it is appropriate to include geometrical factors in metapopulation models.     

Sperm competition and the level of polyandry in a bushcricket with large nuptial gifts

Variation in paternity due to sperm competition or post-copulatory female choice has a major influence on animal mating system evolution and on the levels of genetic variability in natural populations. However, there are relatively few studies comparing the outcome of sperm-competition experiments in the laboratory with natural variation in polyandry among families from the field. In the bushcricket Ephippiger ephippiger, females mate multiply, and the males provide them with a large, nutritious, and probably expensive, donation at mating. We examined paternity in a series of laboratory matings, where females mated with two males, and amongst a series of families collected from a natural population. In the laboratory, paternity was highly bimodally distributed: 24% of families had offspring fathered by the first male to mate, 68% by the second male (in only 8% was paternity shared). In the field, paternity was more mixed: only 27% of families had a single father, 14% had more than two fathers, whilst 59% had two fathers. While unsuccessful matings may contribute to the highly biased paternity in the laboratory, they cannot fully explain the high incidence of complete P2 families. Nonrandom sperm utilisation is therefore likely. Greater sperm mixing in the field probably results from females mating with more males, but the distribution of paternity also reflects an active process of nonrandom sperm utilisation. Confidence of paternity due to last male advantage may be relatively high in this species, and therefore may have facilitated the evolution of the large spermatophore in E. ephippiger.Communicated by D. Gwynne     

Female encounter rate and the calling behavior and mating propensity of male Requena verticalis (Orthoptera: Tettigoniidae)

Mating effort, the energy exerted in finding and persuading a member of the opposite sex to mate, may be influenced by how frequently potential mates are encountered. Specifically, males that frequently encounter females may reduce calling effort and be less eager to mate than males that infrequently encounter females. An experiment was set up to test this hypothesis, using the tettigoniid Requena verticalis. We examined the song structure, calling activity and mating propensity of individual males exposed to one of five different encounter rates with virgin females. Song structure and calling effort were significantly altered by an encounter with a female. After an encounter, males significantly increased chirp rate and decreased variability in interchirp interval. Encounters also stimulated a male to call and to continue to call for up to two hours. The elapsed time since mating affected mating propensity but not calling activity. Mating propensity asymptotically increased to reach a maximum by day 17 since last mating. However, neither the frequency of encounters, nor the number of previous encounters experienced by a male, influenced calling activity or the propensity of a male to mate. The significance of changes in song structure and calling activity following an encounter, and of increasing male mating propensity over time, are discussed. Correspondence to: G.R. Allen     

Role-reversal in katydids: Habitat influences reproductive behaviour (Orthoptera: Tettigoniidae,Metaballus sp.)

Summary Mating behaviour of the katydid Metaballus sp. varies. At sites QS and DB (in 1982) females competed for access to calling males and males chose mates by mating with heavier, more fecund females. At another site (BR) there was no evidence of role-reversal in reproductive behaviour, and males were observed to compete for mates. This species has a large spermatophore, a product of male reproductive glands, that is eaten by the female after mating. Males at the DB site had small reproductive glands. This suggests that some aspect of the QS and DB environments decreases spermatophore production; spermatophores become a limiting resource for females resulting in the reversal in reproductive roles observed at these sites. A field experiment that involved moving individuals from site BR to QS in 1983 determined that mating system was influerced by site (Table 1). At BR, males produced a continuous calling song, a third of the males observed attracted mates, and called for about 30 min before the female arrived; courtship duration was short. Males that were moved from BR to QS encountered a higher density of receptive females as all males attracted females after an average of just 3 min of calling. They changed their behaviour by producing short periodic bursts of song (zipping), and by courting females for long periods of time. The long courtship period may function as as a mate-assessment period for males. The reproductive behaviour of BR males moved to QS differed from that of native QS males only in the length of time spent in copula.     

The sex in short supply for matings varies over small spatial scales in a katydid (Kawanaphilanartee, Orthoptera: Tettigoniidae)

In katydids such as Kawanaphilanartee, a female bias in the operational sex ratio (OSR) results in female competition for mates and male choice of mates. Previous work showed that the excess of sexually active females occurs when food availability is low, in part because less food increases the propensity of females to mate as they forage for the large edible spermatophores produced by males. In this study with K.nartee, a pollen-feeding species, we estimate natural variation in numbers of sexually active males and females by assessing male calling activity and the propensity of females to respond to experimental calling males. We found an excess of sexually active males at a site with many flowers and an excess of sexually active females at a site with few flowers about 900 m away. Between-site differences in gut masses of calling males were consistent with the hypothesis that pollen availability controls OSR. Finally, at a third site where flowers were at first scarce, we found that the initial excess in sexually active females changed to an excess of sexually active males after a clump of grass-trees flowered. The mean gut mass of all sampled males from this site increased after flowering. The large variation in OSR that we document for K. nartee highlights the importance of identifying the appropriate spatial and temporal scales over which OSRs are measured in studies of factors controlling sexual selection. Received: 13 May 1997 / Accepted after revision: 27 October 1997     

Some constraints on reproduction for male bushcrickets,Requena verticalis (Orthoptera : Tettigoniidae) diet,size and parasite load

Summary Reproduction for male bushcrickets is energetically expensive. Male Requena verticalis invest 70% of their daily energy reserves in calling to attract a female and providing her with a nutritious spermatophore. Males are thereby likely to be constrained in their mating frequency. I investigated constraints on reproduction imposed by body size and the levels of a protozoan gut parasite when males were fed diets that differed in their nutritional value. Males suffered a cost of reproduction in terms of an increasing interval between matings that was independent of diet and parasitic infection. After three successive matings, males decreased the magnitude of investment in courtship feeding when fed a diet poor in protein. Furthermore, these males suffered a reduction in the number of times they were capable of mating relative to males fed a diet rich in protein. Male size constrained mating frequency on both rich and poor diets; small males were able to mate less frequently than large males. There was an interaction between the effects of diet and parasitic infection on male mating frequency. Heavily infected males mated less frequently than uninfected individuals when fed the poor diet. However, males fed the rich diet were able to overcome the constraints imposed by parasitic infection. Reproductive constraints are discussed in relation to the costs of reproduction and their effects on courtship roles.     

The evolution of empty nuptial gifts in a dance fly, Empis snoddyi (Diptera: Empididae): bigger isn't always better

Adaptive female choice is thought to have led to the evolution of nutritionally valuable nuptial gifts in many insect species. However, in several dance fly species, males offer and females accept “empty gifts” with no nutritional value. In the species studied here, Empis snoddyi Steyskal, males produce empty balloons comprised of hundreds of silk bubbles and form mating swarms that females approach to investigate males. Males within the swarm engage in agonistic interactions. The empty balloon has been hypothesized to be an indicator of male condition such that males with larger balloons are predicted to have higher mating success and be more successful in male-male interactions than males with smaller balloons. We examined the role of male body size and balloon size in the context of intersexual and intrasexual selection. We found that neither male body size nor balloon size affected the outcome of pairwise male-male interactions. Using multiple-regression techniques, we found significant linear selection for increasing male body size and decreasing balloon size associated with mating success, a surprising result given a positive relationship between male body size and balloon size. A visualization of selection showed the highest peak of male mating success for larger males with intermediate-size balloons. These results can be explained by a trade-off between long-range attraction of females using large balloons and close-range attraction of females via improved flying efficiency associated with smaller balloons. Both male body size and balloon size are important components in determining male mating success; however, the empty balloon does not appear to play a typical role as a sexually selected ornament. Received: 29 December 1997 / Accepted after revision: 7 October 1998     

Studies on the maturation-accelerating pheromone of the desert locustSchistocerca gregaria (Orthoptera: Acrididae)

Summary The accelerating effect of mature males of the desert locust,Schistocerca gregaria, on the maturation of immature male and female conspecifics was confirmed. The onset of sexual activity was found to correlate with yellowing of the male insects. Using the colour as an indicator of maturation, the maturation-hastening effect of an hexane extract from mature males was also confirmed. Likewise, volatiles from mature males placed in the upper storey of a two-chamber bioassay system (no visual or tactile contact possible) and charcoal-trapped volatiles from the mature males also induced accelerated maturation in recipient males placed in the lower storey. GC and GC-MS analysis of volatiles collected from 4-week-old mature males showed the presence of anisole, benzaldehyde, veratrole, phenylacetonitrile and 4-vinylveratrole, roughly at the ratio 4.8:7.0:3.3:79.8:5.0. In addition, guaiacol, phenol, benzoylnitrile, benzyl alcohol and 2-benzoyloxyphenylacetonitrile were present in smaller amounts. These compounds were either absent or found only in trace amounts in the female volatiles. Earlier, we had shown that essentially the same blend collected from younger males (10–20 d old, not yet demonstrating signs of maturation) induced strong aggregation of both sexes of adult desert locusts, suggesting a parsimonious role for the pheromone system: as an adult aggregation signal and as a maturation accelerant in young adults.     

On the feeding of Branchiostoma senegalense (Acrania: Branchiostomidae)

The feeding biology of Branchiostoma senegalense Webb from the North-West African shelf region off Mauritania was investigated. The hindgut contained almost exclusively seston components, ranging in size from less than 1 m (bacteria size) to 300 m. Numerous chloroplasts of ingested phytoplankton appeared to be undigested. Dunaliella salina was still alive when leaving the anus after 1 to 2 h. Detritus formed the greater part of the gut contents. The authors conclude that the lancelets feed mainly on detritus and thus are indiscriminate suspension feeders.     

The boll weevil (Coleoptera: Curculionidae) feeding process: A simulation model

A model is presented for predicting boll weevil, Anthonomus grandis Boheman, feeding damage to cotton. The model uses appropriate probability theory based on behavioral components of male and nonreproducing female boll weevils and includes the effects of (1) differential feeding site preferences, (2) previous damage to the sites, and (3) individual insect behavior extended to feeding damage caused by a population of insects. The model is sensitive to both crop and insect parameters. An example of how this model can be used in an insect-crop ecosystem simulation is offered.     

Field observations on the feeding behavior of salps (Tunicata: Thaliacea)

Observations of living salps by SCUBA diving in the Florida Current and Gulf of California (Mexico) indicate that they filter feed with a continuously renewed mucus net. Ninety-one percent of 1420 salps (6 species) examined were feeding in this manner. Particles collected range from about 1 mm to less than 1 μm. Compact fecal pellets appear to contain much undigested material and may carry significant amounts of carbon out of surface waters.     

The effects of early experience on subsequent feeding responses in the Tegu,Tupinambis teguixin (Squamata : Teiidae)

The purpose of this study was to assess the effects of early feeding experiences on subsequent responses to prey in the tegu, Tupinambis teguixin. Five-day old lizards were exposed to the odors of various prey and control substances on cotton-tipped applicators with the tongue-flick attack score (TFAS) chosen as the dependent variable. Each lizard was exposed to four stimuli: two controls (deionised water and cologne), and extracts from a mouse Mus musculus, and a lizard Ameiva ameiva, in a repeated measures, randomized block design, receiving one stimulus training session / day over a 40-day period. Tongue-flicks directed toward the applicator were counted over a 1 min period as well as the amount of time that elapsed from the first tongue flick to any bite that may have occurred. Live neonatal mice (but not A. ameiva), offered on a weekly basis, were used as a food source for tegus over a 10-month period. After 10 months, tegus were exposed to applicators containing control odors as well as those containing extracts from mice and lizards (A. ameiva). Mouse extracts elicited significantly higher TFAS as compared to those elicited by A. ameiva or control odors, suggesting that prey odors encountered in the environment shortly after hatching can influence prey preferences by these lizards later in life. These results also indicate that tegu lizards can learn to use specific odor cues associated with naturally occurring prey as releasers for subsequent hunting behaviors.     

Digestive mechanics and gluttonous feeding in the feather starOligometra serripinna (Echinodermata: Crinoidea)

The movement and digestion of food in the gut ofOligometra serripinna (Carpenter) were studied at Lizard Island (14°3842S; 145°2710E) in the austral winter of 1986. Feather stars in the laboratory were fed a brief, small meal of brine shrimp nauplii and killed at increasing time intervals thereafter. Histological reconstructions showed that the ingested nauplii progressed along the digestive tract surprisingly quickly. Some nauplii were found in the mid and hind intestine in only 30 min, and all of the nauplii had reached the hind intestine and rectum in 1 h. Digestion of the nauplii had started at 1 h, and only a few fragments of naupliar exoskeleton remained in the hind intestine and rectum 5 h after the start of feeding. Videotape analysis showed that no fecal pellets were released during this experiment. In the natural environment ofO. serripinna, ingested particles may similarly be transported quickly to the hind part of the gut and digested there — when feather stars were fixed in the field, most of the gut contents were found in the hind intestine and rectum.O. serripinna, which efficiently rejects inert particles before they are ingested, usually defecates infrequently (probably not more than once over a span of many hours) and differs from some other feather stars that ingest numerous inert particles and defecate much more frequently. When specimens ofO. serripinna were fed continuously on brine shrimp nauplii,Artemia sp. (San Francisco strain), in the laboratory, the feather stars fed gluttonously, packing their guts with several hundred nauplii in 1 to 2 h. Thereafter, superfluous feeding began (i.e., further ingestions appeared to force undigested nauplii, some of them still living, out of the anus). These observations suggest thatO. serripinna usually feeds at relatively modest rates in its natural habitat, but can feed gluttonously to take advantage of infrequent patches of highly concentrated, nutritious particles (e.g. copepod swarms, migrating demersal zooplankton, and invertebrate gametes from mass spawnings). It is likely that such patches of nutritious particles are usually small enough to drift out of reach of the feather stars before gluttonous feeding proceeds to superfluous feeding. Opportunities for superfluous feeding in nature are probably very infrequent (e.g. ingestion of coral gametes and embryos after a mass spawning), and the feather stars evidently have no behavior that stops further ingestions after the gut becomes filled to capacity.     

The role of helpers in feeding chicks in cooperatively breeding green (red-billed) woodhoopoes

Summary Observations were made of ten green (red-billed) woodhoopoe Phoeniculus purpureus flocks during the breeding season in order to quantify the relationship between flock size and the amount of food delivered to chicks. The study period was kept short specifically to minimize the effects of environmental stochasticity. Neither woodhoopoe feeding visit rates nor the total amount of food brought to chicks increased with flock size. Although nonbreeders did not increase the net rate of food provisioning to chicks, they reduced parental input in chick rearing, and hence energy expenditure by the breeding pair. However, over an 8-year study period, which includes data for 144 flock years, this did not result in increased breeding frequency or enhanced survival of breeders. There is thus no evidence that helpers' feeding contributions to young per se influence the indirect fitness of helpers.