Identification of sex and parasitism via pheromones by the Ozark zigzag salamander

Chemical communication appears to be the primary mode of information transfer among woodland salamanders of the genus Plethodon. These pheromones have been shown to convey a wide variety of information, and are used to establish territorial boundaries. Responses to pheromones can include changes in both behavior and energy consumption. The ability of Ozark zigzag salamanders, Plethodon angusticlavius, to detect the sex of a conspecific through chemical substrate markings has not been assessed. In addition, some populations of P. angusticlavius are naturally infected with the ectoparasitic mite Hannemania eltoni. Parasitism can impact both the behavior and metabolism of the host as well as the behavior of others towards the parasitized individual. We examined whether sex and parasitism of the pheromone donor and receiver influenced behavioral and metabolic responses in P. angusticlavius. In laboratory trials, behavior of P. angusticlavius was influenced by the sex and parasite load of the pheromone donors and receivers. Behavioral responses were also influenced by whether the receiver was in its own territory or in the territory of the pheromone donor. Metabolic responses were not affected by the sex or parasite load of the pheromone donor, but males had higher metabolic rates than females, even after adjusting for differences in body size. Overall, our study indicates that both sex and parasitism can be detected via pheromones in this species, and the nature of the response depends on residency status, sex, and parasite load of the receiver.     

Aggressive male mating behavior depends on female maturity in Octopus bimaculoides

This laboratory study examined the combined effects of male and female behaviors on the outcome of mating encounters in Octopus bimaculoides. We found that male–male competition for mating opportunities depends on female maturity; the presence of immature females elicited significantly higher levels of aggression between competing males. We conclude that males are able to assess the reproductive status of females. The study also found that immature and mature females resisted male mating attempts to a similar extent but that males that showed more aggression toward male competitors were able to spend more time in contact with females. We suggest that the lack of prominent visual displays in these mating trials indicates the importance of chemical cues in Octopus mating systems, as has been demonstrated for other cephalopods. This study contributes to the growing research on cephalopod mating systems and in particular shows that Octopus mating dynamics may be more behaviorally complex than initially assumed.     

Reproductive isolation between populations from Northern and Central Europe of the leaf beetle Chrysomela lapponica L.

Summary. Allopatric populations of the leaf beetle Chrysomela lapponica are known to feed upon either willow (Salicaceae) or birch (Betulaceae). This study aimed to elucidate the differentiation process of these allopatric populations. We investigated whether these allopatric populations specialized on different host plants are still able to produce fertile offspring when interbreeding. Individuals from a population in Finland (willow specialists) and one in the Czech Republic (birch specialists) were crossed in laboratory. Hybrid formation succeeded only between females from the Czech, birch specialized population and males from the Finnish, willow specialized population, while no eggs were produced by females of the willow specialists having mated males of the birch specialists. Behavioral, morphological, physiological, and chemical features of the F₁ hybrids were studied. The chemical composition of larval defensive secretion and feeding preferences of the resulting F₁ hybrids mainly showed similarities with the paternal phenotype, while the area of black coloring on the offspring’s elytra was intermediate between those of the parental elytra. F₁ hybrids did not accept the host plant (birch) of their mothers for feeding and only survived on willow. Thus, since mothers only lay eggs on birch, we found evidence for a postzygotic isolation mechanism between the individuals of the two investigated populations: when having been mated with willow specialized Finnish males, the birch specialized Czech mothers place the hybrid eggs on a plant species (birch), on which the hatching larvae cannot survive.     

Kin-based male mating preferences in two species of halictine bee

Summary In both of the social bee species Lasioglossum (Dialictus) zephyrum and Lasioglossum (Evylaeus) malachurum (Hymenoptera: Halictidae), males are shown to be attracted to females in field experiments by a pheromone which covaries among female relatives. Females sampled from a nesting aggregation other than the one in which the tested males occur are slightly more attractive than females from the males' own aggregation, and always significantly more attractive than females whose pheromones have been extracted. Furthermore, in L. malachurum experience with a female alters the response of the males towards that female and towards her nestmates (most probably close relatives) in further encounters, but does not alter the males' responses towards females who were non-nestmates of the experienced one. These data indicate that some form of learning of female kin-identity takes place in adult males, and influences the mating system. How males may integrate kinship information into a mating strategy is discussed.     

Chemical ornaments of male lizards <Emphasis Type="Italic">Psammodromus algirus</Emphasis> may reveal their parasite load and health state to females

Evidence for parasite-mediated sexual selection has been found in many species that use visual ornaments to attract females. However, in many animals, variation in female responses to scents of parasitized males suggests that parasitic infections might also affect information conveyed by pheromones (i.e., chemical ornaments). Thus, pheromones might also function in parasite-mediated sexual selection. We show here that female lizards Psammodromus algirus responded differently to femoral gland secretions of males according to the parasite load and health of these males. Scents of healthier males elicited more tongue flicks (a chemosensory behavior) by females, suggesting that these scents were more attractive. Chemical analyses showed that parasite load and the T-cell-mediated immune response were related to the variability in the proportions of some lipids in secretions of males. Further trials testing the chemosensory responses of females to chemical standards indicated that females actually discriminated the chemicals related to males’ health from other chemicals found in secretions. We suggest that these chemical ornaments may provide reliable information on the health and degree of parasitic infection of a male.     

Chemosensory and behavioural responses of the turnip sawfly, Athalia rosae, to glucosinolates and isothiocyanates

Summary. The turnip sawfly Athalia rosae sequesters glucosinolates from its cruciferous host plants in the larval stage. Investigation of the chemosensory and behavioural responses of adult A. rosae to glucosinolates and their volatile hydrolysis products, isothiocyanates, revealed that females detect glucosinolates by contact chemoreception and isothiocyanates by antennal olfaction. In electroantennogram recordings, four isothiocyanates (allyl [2-propenyl] isothiocyanate, benzyl isothiocyanate, butyl isothiocyanate and iberverin [3-methylthiopropyl isothiocyanate]) were active at all doses presented, including the lowest (0.1 μg), whilst the threshold for detection of three others, iberin [3-methylsulphinylpropyl isothiocyanate], methyl isothiocyanate, and sulforaphane [4-methylsulphinylbutyl isothiocyanate], was higher, at between 1 and 10 μg (source concentration of volatiles). Allyl isothiocyanate attracted experienced females in a four-chambered olfactometer, whilst na?ve females showed no response. Allyl isothiocyanate also attracted mature females to baited yellow water traps in field trials, although immature females were repelled at high isothiocyanate concentrations. In laboratory behavioural bioassays the glucosinolates sinigrin (allyl [2-propenyl] glucosinolate) and sinalbin (p-hydroxybenzyl glucosinolate), stimulated ovipositor probing in mature female A. rosae to an extent comparable to hot-water extracts of their host plants. These responses show that glucosinolates and isothiocyanates play an important role in host finding and host recognition in A. rosae.     

The scent of dominance: female field crickets use odour to predict the outcome of male competition

Pheromones may convey information about mate quality and social status. In the field cricket Gryllus integer, females mount the males for copulation, such that males cannot coerce females to mate. We examined whether virgin G. integer females preferred the scent of potentially dominant males to that of subordinate males. First, we collected pheromones by confining males on filter paper. Next, we offered filter paper from each of two size-matched males and control paper to females that had never been exposed to males, and measured the time spent by the female on each kind of paper. Finally, dominance status of the males in each size-matched pair was determined by pitting the two males against one another in agonistic contests. When offered filter paper from subsequently dominant versus subsequently subordinate males, females spent more time on the paper from the dominant male than the subordinate male, and much less time on control paper. Thus, pheromones may inform female G. integer about a male's potential to achieve dominant social status. Male pheromones were also associated with the female's tendency to mount a male. In contrast to cockroaches, where females prefer the scent of subordinate males (presumably to avoid risk of injury), female crickets prefer the scent of potentially dominant males and are more likely than males to wound their mating partners.     

New repellent semiochemicals for three species of <Emphasis Type="Italic">Dendroctonus</Emphasis> (Coleoptera: Scolytidae)

Summary. Nine compounds identified from captured volatiles of the Douglas-fir beetle, Dendroctonus pseudotsugae, the mountain pine beetle, D. ponderosae, and the spruce beetle, D. rufipennis, that elicited antennal responses in males and females of one or more of these species were tested in the field to determine behavioural activity. 1-Octen-3-ol, found in the volatiles of females of all three species decreased the response of male and female coastal and male interior D. pseudotsugae and both sexes of D. ponderosae to their aggregation pheromones. Acetophenone, identified in the volatiles of females of all three species, significantly decreased the response of interior female D. pseudotsugae. trans-Verbenol, a potent aggregation pheromone of D. ponderosae, decreased the response of both sexes of D. pseudotsugae, while 3-methyl-2-cyclohexen-1- one (MCH), the antiaggregation pheromone of D. pseudotsugae and D. rufipennis decreased the response of both sexes of D. ponderosae. While it has been demonstrated that semiochemical mediated interspecific communication occurs among bark beetles infesting the same host, this study demonstrates that beetles can perceive signals emitted by heterospecifics attacking nonhosts and can potentially use them to avoid attacking the wrong species of conifer.     

Attraction and learning in mate-finding by solitary bees,Lasioglossum (Dialictus) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera : Halictidae)

Summary Males of the solitary sweat bee, Nomia triangulifera, patrol over large areas where thousands of females emerge, searching for receptive females. The daily operational sex ratio is strongly male-biased. Males contact dead, frozen (untreated) females more frequently than they contact females which were washed in hexane, showing that olfactory cues are utilized in mate-finding. A major source of female sex pheromone is in the head. Male pouncing on females is temporally non-random, indicative of group stimulation. Bioassays show that newly emerged females are more attractive to males than are older pollen-collecting females. Female odors are individually distinctive, based on male responses, and there is much variation among females in their attractive properties. Male responses to female odors suggest that learning is important for mating in natural populations. In contrast, the following hypotheses are unlikely to account for the observed behavior: (1) dissipation of female odors; (2) site learning and avoidance behavior by males; (3) decay of male motivation; or (4) male-produced repellents effective against other males. Laboratory and field studies show that female Lasioglossum figueresi produce individually-distinctive odors, which are attractive to males. There is considerable inter-individual variation among females in their attractiveness to males among sexually immature females. Male responses to female odors decay over the course of the presentation, suggesting the importance of learning in natural populations, although several alternatives could not be tested.     

Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis

Carotenoid- and melanin-based colors are valuable indicators of quality in many vertebrates, but their signaling role in invertebrates remains relatively unexplored. The Asian ladybird beetle Harmonia axyridis is an ideal organism for studies of this nature because males and females exhibit highly variable red and black colors on their elytra and are chemically defended with an alkaloid (harmonine). We used digital photography to quantify elytra coloration and absorbance spectrophotometry and gas chromatography mass spectrometry analyses to quantify pigment and alkaloid concentrations, respectively, in wild-caught male and female H. axyridis. We predicted that extensive or intense coloration would be an aposematic signal of high-alkaloid stores. We found that carotenoid pigments largely controlled variation in red elytra coloration. There was no relationship between alkaloid content and either elytra redness or carotenoid pigment concentration in either sex. However, we found a positive correlation between the extent of elytra coloration and alkaloid content. Animals with proportionally more red (or less black) on the elytra were more alkaloid-rich; this relationship was particularly strong in females. We also found that females with lighter black spots had greater amounts of harmonine than those with darker spots. These results suggest that elytra color patterns have the potential to reveal information about chemical defensiveness to mates or predators. Prior studies in this species show that nonmelanic forms are typically less active and yet more sexually attractive than melanic forms, and both results may be explained by the fact that nonmelanics are better chemically defended.     

Temporal life history plasticity of the Southern Ocean squid <Emphasis Type="Italic">Todarodes filippovae</Emphasis> from waters off Tasmania,Australia

Population dynamics and maturity parameters were analysed for seasonal samples of the oceanic ommastrephid squid Todarodes filippovae from off the coast of Tasmania Australia from 2002 to 2004. Based on assumed daily periodicity in statolith increments, T. filippovae had a life cycle of about a year with the sexually dimorphic females reaching their larger size by predominantly growing faster than males. Due to the small sample size of males, analysis was undertaken on female individuals only. Growth in all samples was best described by a power curve and varied annually, with significantly faster growth in 2001 compared to the subsequent 2 years. Seasonal growth rates also varied with autumn- and winter-hatched squid significantly faster than summer-hatched squid. Spring growth rates were intermediate but not significantly different to the other three seasons. Peak hatching periods occurred in late autumn and early winter. ANOVA revealed a season × year interaction for mantle length and total body weight. Pairwise comparisons showed that the annual differences were likely driven by smaller squid in autumn 2002 compared to autumn samples in the other 2 years. Pairwise comparisons also revealed seasonal differences with winter-caught squid smaller than those from the majority of other samples. There were no seasonal effects on mature female gonad weights but females caught in 2002 had significantly lighter gonad weights than females from the following 2 years. There were no consistent trends among seasons or years in the age structure of mature females. This study revealed the plasticity and flexibility in growth and maturity parameters in this species, with a preference for faster growth during cooler periods.     

Pheromones and colonization: reassessment of the milkweed bug migration model (Heteroptera: Lygaeidae: Lygaeinae)

Summary. Research on insect migration has justifiably emphasized females – the so-called “oogenesis-flight syndrome”– since it is the females that place the eggs into new habitats. The large and small milkweed bugs, Oncopeltus fasciatus and Lygaeus kalmii, respectively, have featured prominently in studies of insect migration and sequestration of host plant toxins for chemical defense. Here we report that males of these species, and males of another well-studied lygaeine (Neacoryphus bicrucis), produce pheromones in glands usually considered to serve only a defensive role in Heteroptera (the metathoracic scent glands), and that these pheromones are exploited by a tachinid parasitoid as a host-finding kairomone. The pheromones are mixtures of C₆ and C₈ saturated and unsaturated esters reminiscent of lepidopteran pheromones, and the key compound of the O. fasciatus pheromone has now been correctly identified as (E)-2,7-octadienyl acetate. It is proposed that the concept of the oogenesis-flight syndrome for these kinds of insects should accommodate the role of males in the migration process. The hypothesis is presented that male-produced pheromones play a significant role in guiding colonization of new habitats in many heteropteran species. In addition, data are presented suggesting that there is a trade-off between the amount of pheromone produced by colonizing males and the host breadth of the species. Received 21 December 1998; accepted 15 February 1999.     

Operational sex ratios and sperm limitation in populations of Drosophila pachea

Males of the cactophilic fruitfly, Drosophila pachea, produce relatively few but very large sperm, and partition their limited gamete numbers among successive mates. The present study found that males take 10 days longer than females, post-eclosion, to become sexually mature. The pattern of testes development suggests that the need to produce testes long enough to manufacture the giant sperm is the cause of the delayed male maturity. These findings generate the prediction that the operational sex ratio (OSR) of populations will be female-biased. The size, sex ratio, and OSR of natural populations were examined. In general, local populations tended to be small and sex ratios tended to be slightly male-biased. However, as predicted, the OSR of populations, at least in one season, tended to be female-biased, with an average of 2.3 receptive females for each sexually active male. Results of laboratory experiments to determine the relationship between female remating frequency and fitness, and between population OSR and productivity, suggest that natural populations with female-biased OSRs are sperm-limited. The origin and maintenance of sperm gigantism and the unusual sperm-partitioning behavior of males are discussed with respect to population structure.     

Sexual maturity and hermaphroditism of the red porgy Pagrus pagrus (Teleostei: Sparidae)

Gonadal changes related to sexual maturity were examined by histology in reared populations of the red porgy Pagrus pagrus L., aged 0.5 to 6.5 years. More than 50% of red porgies were mature at the age of 4 years although some individuals were already mature at the age of 3, as indicated by changes in the gonadosomatic index, plasma levels of vitellogenin, 17β-estradiol and testosterone in females and males. Sex frequency distribution analysis in relation to the age and histological analysis of the gonads indicated the presence of males originated from the sex change of adult functional females. P. pagrus is a protogynous species. Some females had not changed sex up to the age of 6.5 years. Received: 16 July 1998 / Accepted: 29 April 1999     

Spatial and temporal variation in the size at maturity of the western rock lobster Panulirus cygnus George

The sizes at which female and male western rock lobster Panulirus cygnus become mature were examined over 32 years from records at six localities along the coast of Western Australia. The size of males at maturity was estimated from a subset of these data by a morphometric and a physiological method, with both producing statistically similar results. Males were larger at first maturity than females at the same sites. For both sexes, the sizes at first maturity at each location correlated (P<0.05) with the mean annual water temperature at that location, decreasing from south to north along the mainland coast and being smallest at the offshore Abrolhos Islands. Smaller sizes at maturity were recorded for both sexes than have been published previously. One certain explanation for these differences is that management measures protecting females with ovigerous setae have distorted size compositions and the ratio of immature to mature females, thereby increasing the likelihood of capturing small mature females. However, these fishing effects cannot fully account for the progressive decline in CL₅₀ observed over the past 20 years. Other possible hypotheses considered include increases in water temperature over this period, as well as whether this change could be consistent with a genotypic response caused by the selective removal of large lobsters combined with high exploitation rates.     

Behavioral consequences of exotic host plant adoption and the differing roles of male harassment on female movement in two checkerspot butterflies

Herbivorous insects may evolve convergent behaviors when independent adoption of a shared novel host plant places populations in environmental conditions that diverge from the ancestral state. We investigated the behavioral consequences of adopting Plantago lanceolata, an exotic species to North America, in populations of Euphydryas p. phaeton and Euphydryas editha taylori, on the east and west coasts of North America. Activity budgets and short-term movements suggested that innate species tendencies exert a greater impact on behavior than adoption of the same exotic host plant. However, female E. phaeton from a Plantago-dependent population spent more time inspecting host plants than females from a population dependent on the native host plant, Chelone glabra. Both checkerspot species had similar diffusion coefficients (D) regardless of host plant association. But, E. e. taylori step-lengths appeared bimodal and power law distributed while E. phaeton step-lengths were unimodal and best fit by an exponential distribution. We attribute this bimodal step-length distribution to the persistent harassment of courting males which induces a “long-distance” evasive flight in otherwise sedentary E. e. taylori females. In contrast, the longer distance step-lengths of E. phaeton were associated with the inspection of oviposition plants. These two checkerspot species appear to move greater distances across the reproductive landscape with contrasting motivational states that could lead to either intimate mapping (E. phaeton) or coarse mapping (E. e. taylori) of host resources.     

Behavioural and electrophysiological responses of the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), to male- and female-borne sex attractants

In the olive fruit fly, Bactrocera oleae, females attract males by producing 1,7-dioxaspiro[5.5]undecane (olean), the main component of the sex pheromone secreted by rectal glands. It has been recently demonstrated that males are able to produce (Z)-9-tricosene (muscalure) in rectal glands, a compound that selectively attracts females. In this study, a male grooming reaction that may transfer the male-borne compounds from rectal to urotergal glands was observed, suggesting that urotergal glands could be involved in B. oleae sexual communication. GC/MS, EAG, GC/EAD analyses and behavioural assays were carried out to compare the role of male rectal and urotergal glands during courtship. In both male glands, olean and muscalure amounts were age dependent. Extracts of rectal glands contained higher amounts of olean and/or muscalure than urotergal ones. Extracts of rectal and urotergal glands of males and females elicited EAG responses in both sexes. GC/EAD showed that female EAG response to male rectal extracts was mainly due to olean and muscalure. Synthetic compounds evoked EAG dose-dependent responses in both sexes, and the EAG response to muscalure was higher as compared to olean. Rectal and urotergal glands from old males were able to attract females, while urotergal glands from young males attracted only males. Overall, our results add knowledge to the mating system of B. oleae, giving first evidences on the electrophysiological activity of muscalure towards both sexes, as well as on the involvement of male urotergal glands in the chemical sexual communication of this pest.     

Moult in relation to some aspects of reproduction and growth in swarms of Antarctic krill,Euphausia superba

In a 14-d period 38 swarms of Antarctic krill,Euphausia superba Dana, were sampled in an area 55.5 x 55.5 km to the southwest of Elephant Island, at the north of the South Shetland Islands. Moult stage, maturity stage, and size of ca. 100 krill from each swarm were measured. Each of the characteristics varied greatly between swarms. Moulting krill were found in most swarms, but in one swarm all of the krill were just about to moult. Ways in which moulting may act as a possible sorting mechanism are discussed. Data for all the analysed krill (ca. 3000 specimens) were used to investigate the interdependence of moult rate, sexual maturation and growth. While all immature krill moulted at approximately the saine rate in the study, there were significant differences in the moulting rates of mature male and female krill. Gravid female krill continued to moult, although less frequently than mature males. As a consequence males had to attach spermatophores to females after each moult. It is likely that variation in moult rate of females and males was related to the energy expenditure required for ovary development in females and spermatophore production and searching behaviour in males. Spawning and moulting were only partly coupled in gravid females. Spawning appeared to take place predominantly during Moult Stage D₂. There was no evidence of intermoult growth by intersegmental dilation.     

The role of sexual harassment in cave and surface dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei)

Sexual coercion is a common behaviour for males trying to compensate for being inferior in male competition and/or female choice. We measured the cost of male sexual harassment for females as reduced feeding time in three populations of the Atlantic molly (Poecilia mexicana). Of these populations, one originated from a typical river habitat, another from a lightless cave chamber and the third one from a small, milky creek outside the cave. We gave hungry females an opportunity to feed in the presence of either another female or a male. We found the following: (1) male sexual harassment represents a cost in the river dwelling population and both small and large males significantly reduce female feeding time; and (2) sexual harassment was not detected in the other two populations (cave and cave entrance). In the cave molly, small males are at a disadvantage in female choice, but predation by an aquatic heteropteran selects against large male body size.     

Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice

There is accumulating evidence that females may preferentially select parasite-free or -resistant males. Minimal attention has, however, been paid to the mate preferences and responses of the parasitized male hosts themselves. Here, we considered the effects of parasitic infection on male host mate responses, the neuromodulatory correlates of these responses, and the relations of these responses to female mate choice. Using an odor “preference” test, we examined the effects of different stages of an acute, sub-clinical infection with the naturally occurring, enteric, single host, protozoan parasite, Eimeria vermiformis, on the responses of male mice, Mus musculus domesticus, to the odors of estrous females along with the responses of uninfected females to the parasitized males. At 4 days post-infection (non-infective, pre-patent stage) E. vermiformis-infected male mice showed a significantly decreased preference for the odors of estrous females, whereas at 10 days post-infection (infective, patent stage) infected males showed a significantly increased preference for the odors of estrous females. Parasitized males displayed no significant changes in their responses to the odors of non-estrous females, supporting effects on the reproductively related responses of the host. In parallel, estrous females displayed a reduced interest in the odors of infected males. Least interest was expressed in the odors of the patent, infective males, consistent with the avoidance of contagion. Using selective opioid peptide receptor agonists and antagonists we found evidence that enhanced kappa opioid peptide (e.g., dynorphin) activity was related to the decreased sexual interest of the pre-infective males, while augmented delta opioid peptide (e.g., enkephalin) activity was associated with the enhanced responses of the infective males to females. We further showed that acute kappa opiate administration reduced the responses of uninfected males to females and that uninfected females displayed modified responses to the odors of uninfected males subject to acute modifications of opioid activity. We suggest that these differential shifts in endogenous opioid activity in the parasitized males are associated with and, or related to alterations in neuro-immune and endocrine functions. These findings show that parasitic infection can have, depending on the stage of infection and associated neuromodulatory changes, either significant facilitatory or inhibitory effects on male host preferences for and responses to females. Received: 22 April 1996 / Accepted after revision: 15 March 1997