Pheromonal markers as indicators of parasite load: parasite-mediated behavior in salamanders (Plethodon angusticlavius)

Assessment of parasite load of conspecifics may be important during social interactions such as courtship and aggressive encounters. We used a correlational study to test whether pheromonal markers can be used to assess parasite load of conspecifics, and whether the parasite load of the pheromone receivers affected their responses. We tested the responses of parasitized and nonparasitized Ozark zigzag salamanders, Plethodon angusticlavius, to territorial markers (fecal pellets) from conspecific males. Males and females were simultaneously exposed to fecal pellets placed in front of two artificial burrows located at the opposite ends of their chambers. The treatments were (1) fecal pellet of male with low parasite load versus fecal pellet of male with high parasite load, (2) fecal pellet of male with low parasite load versus control pellet (chemical blank), and (3) fecal pellet of male with high parasite load versus control pellet. Nonparasitized females spent significantly more time near fecal pellets of males with low parasite load in test condition 1, whereas the behavior of parasitized females was not significantly different from random in any test condition. Males responded differently to treatments only in condition 3; males with low parasite loads spent significantly more time near control pellets, whereas males with high parasite loads spent significantly more time near fecal pellets of males with high parasite loads. This study demonstrates that pheromonal markers may be used for assessment of parasite load of conspecifics and that responses by both males and females may be influenced by their own level of infection. Received: 21 January 1999 / Received in revised form: 17 March 2000 / Accepted: 13 November 2000     

Discrimination of chemical stimuli in conspecific fecal pellets by a visually adept iguanid lizard,Crotaphytus collaris

Iguanid lizards are known for visual acuity and a diminished vomeronasal organ, which has led to mixed conclusions on whether iguanids use chemical cues. The collared lizard, Crotaphytus collaris, is a territorial iguanid that lives in open rocky habitats. Fecal pellets placed prominently on open rocky perches may provide an ideal mechanism for intraspecific chemical signaling. In order to determine whether collared lizards can discriminate between chemical stimuli found in conspecific fecal pellets, we collected 24 males and 25 females to analyze sex-specific behavioral responses via tongue-flicks and a newly observed behavior for the species, gular pumps, to cotton swabs containing water, cologne, chemical stimuli from conspecific male and female fecal pellets, and the lizard’s own fecal pellet. Both sexes were able to discriminate chemical stimuli from water via at least one behavior. Male collared lizards exhibited greater rates of response (tongue-flick and gular pumps) toward male fecal pellets when compared to the negative water control. Our results also suggest individuals may be able to discriminate between fecal pellets, as indicated by generally greater (but non-significant) counts of male tongue-flick responses to male fecal pellets when compared to their own. Collared lizard chemical discrimination appears to utilize tongue-flick and gular pump behaviors, possibly associated with distinct chemosensory modes (vomerolfaction and olfaction). Based on this study, we suggest that chemical signals may play a greater role in intraspecific communication than previously thought in this highly visual lizard.     

Faecal pellets as burrow markers: intra- and interspecific odour recognition by western plethodontid salamanders

Chemical communication is widespread among plethodontid salamanders (Caudata: Plethodontidae), but little information exists on the role of odours in interspecific competition in general and among species in western North America in particular. The present study examined the potential of faecal odours for intra- and interspecific communication among sympatric plethodontids in two-choice tests in the laboratory. In experiment 1, Plethodon vehiculum and Aneides ferrus from Vancouver Island, B.C., Canada, were presented with two burrows marked with (1) a faecal pellet of male P. vehiculum versus a control clay pellet, and (2) a faecal pellet of male A. ferreus versus a control pellet. In experiment 2, responses of P. vehiculum, P. dunni and P. vandykei from Washington, U.S.A., were tested towards faecal pellets of conspecific males and females, and towards pellets of congeneric males. Both P. vehiculum and P. dunni distinguished odours of conspecific males and females, based on their behavioural responses towards faecal and control pellets. Only P. dunni, however, avoided burrows marked with faeces of conspecific individuals. In contrast, neither A. ferreus nor P. vandykei appeared to distinguish faecal odours of conspecific salamanders from control pellets. In tests with odours of heterospecific individuals, P. dunni and P. vehiculum distinguished odours of each other, and P. vandykei distinguished odours of P. vehiculum. The data from these two experiments suggest that P. dunni use faecal pellets as territorial markers both in intraspecific communication and in interspecific encounters with P. vehiculum.     

Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp

Among the factors that may contribute to the evolution of social monogamy are selection for extended mate guarding of females and selection for territorial ‘cooperation’. Many socially monogamous taxa are also territorial, with ‘partners’ sharing a single territory, suggesting that one or both partners may benefit by sharing territorial maintenance. Snapping shrimp (genus Alpheus) are socially monogamous and territorial, living in excavated burrows or with host organisms, with females performing all parental care. The territorial cooperation hypothesis predicts that male and female partners share (1) territorial defence, resulting in a reduction in the risk of eviction from the burrow, (2) burrow construction duties, such that individuals in pairs spend less time in burrow construction relative to solitary individuals, and/or (3) foraging duties, by returning food to the burrow, where it is consumed by both partners. UsingA. angulatus as a model species, a territorial defence experiment revealed that females in pairs were significantly less likely than solitary females to be evicted by female intruders, but males in pairs were not significantly less likely than solitary males to be evicted by male intruders. A subsequent experiment revealed that paired males were significantly less likely to be evicted by an intruding male if paired with sexually receptive females than if paired with nonreceptive females. Another experiment revealed that (1) paired females spent significantly more time in burrow construction than paired males, and (2) both males and females consistently returned food items to the burrow, perhaps incidentally provisioning their mates. These data suggest that social monogamy may have been selected for in part because of the advantages of territorial cooperation, as both males and females are likely to benefit by dividing the labour of territorial defence and maintenance. These tests of the territorial cooperation hypothesis are synthesized with data from tests of the extended mate-guarding hypothesis to place snapping shrimp pairing behaviour into a larger construct incorporating both the influence of ecological pressures (territoriality) and mating interactions between the sexes. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Iberian Rock Lizards (Lacerta monticola cyreni) Assess Conspecific Information Using Composite Signals from Faecal Pellets

A field and laboratory study was performed to analyse the role of excrement deposited on the substrate in intraspecific communication of the Iberian rock-lizard (Lacerta monticola cyreni). In the field, lizards selected specific sites on rocks to deposit faecal pellets, probably in order to facilitate visual location of pellets by conspecifics. Differential tongue flick rates to chemicals presented on cotton swabs demonstrated that male lizards can detect and discriminate between self-produced scents from faecal pellets and those of other conspecific males. In a subsequent experiment, male lizards were tested in a chamber with two platforms containing a faecal pellet of other male on one side and a control artificial pellet on the opposite side. Males spent significantly less time on the side containing the faecal pellet, suggesting that the decision of where to stay may depend on the presence of faecal pellets. Smaller males moved less than larger males on the experimental side whereas on the control side body size did not influence the proportion of time moving. The ability to discriminate chemicals from faeces, and the effects of faecal pellets on lizard behaviour, suggests that faeces might act as composite signals (visual and chemical) in the intraspecific communication of this lizard.     

Size-dependent Mating Behaviours of Male Sand-bubbler Crab,Scopimera globosa: Alternative Tactics in the Life History

Factors leading to the separation of mating behaviours were investigated in the sand-bubbler crab, Scopimera globosa. The crabs mated on the surface (surface copulation, SC) and underground (UC). UC males were large (old) whilst SC males were small (young). Burrowless females bred in the UC males' burrows. These females accepted UC in exchange for access to a burrow. UC occurred much more frequently than SC in the burrow area in which females oviposited. Most SC occurred in the water-saturated area affording a rich diet. SC was accepted by most large and small females in both areas and most UC by small females in the burrow area. SC was an alternative to UC for males in that there was a size dependence between types of copulation. These two mating behaviours involved different degrees of interaction with neighbouring males. Males attempting to carry a female to their burrows for UC were more often disturbed by other males than were males attempting SC. In the interaction for both UC and SC, larger males were likely to resist the disturbances. UC males needed their own burrows, but these burrows were not enlarged before mating. UC males have a higher paternity of eggs than SC males, because SC males' sperm is often displaced by other males. Thus, UC was a behaviour with relatively higher costs and benefits for male crabs than SC behaviour. Alternative mating behaviours in male S. globosa are conditional, and explained by intrasexual interactions and a male life history strategy with a trade-off between growth and reproduction. It is not likely that the size dependence of male mating behaviour is caused by mate preference of females for UC males in the burrow area.     

Courtship Activity of Wandering and Burrow-holding Male Uca arcuata

The male of Uca (Deltuca) arcuata, a vertical claw-waving fiddler in the Indo-Pacific, is used to court females by approaching them from his burrow or while wandering. Differences in the rate of encounters with females between burrow-holding males and burrowless wandering males are found not to be significant. Burrow-holding males less often cause displacement of wandering by females than wandering males do. Wandering of females caused by wandering males occurs as often as wandering of males caused by other males. Thus, burrow-holding males tend not to reduce the number of their potential mates in the neighborhood. Burrow dwelling males are apt to start wandering after decreased encounters with females. Wandering males experience more interactions with other males than burrow-holding males do. Most wandering males that displace burrow owners descend the burrows one or more times after displacing the owners. The extra fighting for temporary burrows is responsible for no increase of the encounter rate with females during wandering.     

The Role of Chemical Cues in Host and Mate Location in the Pear Psylla Cacopsylla bidens (Homoptera: Psyllidae)

Chemical communication was shown to play a role in the pear psylla, Cacopsylla bidens. Electrophysiological (EAG) and behavioral responses were investigated in males and females pear psylla . Males were found to be attracted to females, and especially to those on host plants, but not to males, uninfested host plants, or plants infested with conspecific larvae. On the other hand, females were not attracted to males or females but displayed some attraction to host plants. Furthermore, females showed a preference for uninfested pear versus plants infested with conspecific larvae. The antennae of males gave highest electroantenographic response to volatiles from pears infested with females but not males, while females, responded also toward the volatiles of pear alone. These results indicate that females of C. bidens emit sex pheromones that are attractive to the males and suggest that, host volatiles may play a role in host selection by pear psylla females.     

Resource attractiveness of the male beaugregory damselfish and his decision to court or defend

We examined the decisions territorial male beaugregory damselfish (Stegastes leucostictus) make when presented with mating and aggressive situations simultaneously. Specifically, we testedhow males responded to simultaneous and consecutive presentationsof conspecific males and females in bottles. We hypothesizedthat (1) territorial males would show lower levels of courtshiptoward females when a competing male is also present comparedto when only the female is present and (2) territorial maleswould show higher levels of aggression toward intruding maleswhen a female is also present on their territories than whenonly the intruder is present. We predicted that males withhigh-quality breeding sites would court females and attackcompetitors more vigorously than males with low-quality breedingsites. Males on low-quality breeding sites exhibited fewerconspicuous courtship displays toward bottled females and alower bite rate toward bottled males than did the males onhigh-quality breeding sites. We concluded that poor breeding-sitequality was responsible for the decline in the most conspicuous aspects of both courtship and aggression. When presented simultaneouslywith a bottled male and a bottled female, defenders of bothbreeding-site types drastically reduced the number of courtshipdisplays and the amount of time they spent near the female.Thus, all aspects of courtship were reduced in the presenceof a male intruder. Time spent near the bottled male also decreased in these simultaneous presentations; however, this decreasewas less dramatic than the reduction in time spent near bottledfemales. Habitat quality did not affect these trade-off decisions,but the bite rate exhibited toward the bottled male increasedin the simultaneous presentations compared to the single presentations.Due to this increase in a territorial male's defensive behaviorwhen a female is present, we conclude that the presence of afemale temporarily increased the value of a territory. We suggestthat the possible loss of a territory to an intruding maletakes priority over the potential benefits of successfullycourting a single female and that it is a male's future reproduction,as well as his current reproduction, by which he assesses hisbenefits.     

高原鼠兔领域行为时间分配格局及其对风险环境适应的探讨

采用直接观察法测定了高原鼠兔地面、洞道活动时间及进、出洞频率。结果表明,在07：00-18：00,雄性和雌性高原鼠兔平均地面活动时间分别占总活动时间比例的87．09％和85．22％。地面活动时间具有明显的季节性,但两性个体间无显著的差异。繁殖早期,成年雌体地面活动时问显著高于繁殖后期,第2胎幼体地面活动时间显著低于第1胎幼体。不同年龄和性别的高原鼠兔进洞频率存在极显著差异,5月成年雌体进洞频率最高,而成年雄体在4月进洞频率最低。研究结果验证了捕食风险可制约鼠兔属动物领域活动时间分配,高风险环境能增加其利用洞道的时间及频率的特定假设。     

Spawning synchrony in Arenicola marina: evidence for sex pheromonal control

Chemical communication systems controlling reproductive behaviour have been shown in a number of marine polychaetes. This study investigated the use of sex pheromones to coordinate spawning behaviour in gravid lugworms (Arenicola marina). Lugworms typically reproduce in the autumn, during low water of spring tides, and often exhibit epidemic spawning. Females release gametes within the burrow whereas males deposit spermatozoa on to the beach surface. The incoming tide dilutes the spermatozoa and transports them to the females'' burrows. Sperm is diluted rapidly and sperm concentrations fall below the minimum required for fertilization within a few minutes. The present investigation establishes the existence of chemical signals synchronizing spawning for the first time in an iteroparous polychaete. The process can be divided into two steps, the induction of gamete release by waterborne chemical cues and burrow irrigation behaviour in females: burrow irrigation representing the means by which spermatozoa are carried to the eggs. In both sexes, the release of gametes can be induced by exposure to sea water into which other individuals had previously spawned. Males also respond to odour compounds from other males. The overall effect of the chemical signals results in synchronized, mass spawning of a population.     

Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders

Jumping spiders (Salticidae) are renowned for their exceptional vision, but this does not preclude use of other senses. Here we provide evidence that olfactory pheromones are widespread in the Spartaeinae and Lyssomaninae, two subfamilies regarded as basal clades within the Salticidae. Pheromone use by salticids was tested in a series of experiments: males were tested with the odour of conspecific females, heterospecific females, and conspecific males, and females were tested with the odour of conspecific males. With seven of the 29 species tested, we also tested males using the draglines of conspecific females (spider absent) as the odour source. Males of all species tested were attracted to the odour of conspecific females and to the odour of the draglines of conspecific females. There was no evidence of males responding to the odour of heterospecific females or conspecific males, or of females responding to the odour of conspecific males. These findings suggest that it is primarily males that respond to olfactory sex pheromones, consistent with the apparent trend within spiders of males more actively searching for females and females placing greater emphasis on mate‐choice decisions. Compared with most salticid groups, lyssomanines and spartaeines are unusually sedentary and this lifestyle may favour olfactory mate searching. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 664–677.     

Detection of the Sexual Identity of Conspecifics through Volatile Chemical Signals in a Territorial Salamander

Territorial red‐backed salamanders (Plethodon cinereus) have been shown to use nonvolatile chemical signals in both territorial defense and to convey a variety of information to conspecifics. We investigated whether or not red‐backed salamanders could determine the sexual identity of conspecifics through volatile chemical signals, and we explored their use in the context of territorial defense. We exposed male and female red‐backed salamanders to four experimental treatments (i.e. filter papers that had been scent marked by male or female conspecifics for 1 and 5 d) and two control treatments (i.e. unscented filter papers for 1 and 5 d tests). The focal salamanders were prevented from physically accessing the scent marked filter papers and, presumably, some of the substrate scent marks had volatile components that were detected and interpreted by the focal salamanders. Both male and female red‐backed salamanders spent significantly more time in threat displays when they were exposed to volatile chemical signals from same‐sex conspecifics than they did toward similar signals from opposite‐sex conspecifics. A similar statistical pattern was observed for the amount of chemosensory sampling exhibited by focal red‐backed salamanders. From these results, we infer that red‐backed salamanders can determine the sexual identity of conspecifics through volatile chemical signals, some of which may be used in territorial defense. Further, such airborne pheromones may influence the spatial organization of salamander territories on the forest floor.     

Monogamous Mating System and Spawning Cycle in the Gobiid Fish, Amblygobius phalaena (Gobiidae)

Reproductive ecology and mating system of the gobiid fish, Amblygobius phalaena, were studied on the coral reef at Sesoko Island, Okinawa, Japan. This goby usually lives in pairs, and maintains territories with several burrows for shelter and spawning. Although a few paired individuals changed partners, most pairs remained together over successive rounds of reproduction. Mate guarding by females appeared to prevent males from mating with other females. Spawnings were synchronous with semilunar periods. Several expected spawnings failed to occur (12%). These may have been caused by the delays in spawning preparation of the paired females or by the disturbance caused by a typhoon. A pair spawned in one of the several burrows within their home ranges. Eggs were deposited on the ceiling of the burrow, and were tended by the paired male for 3–4 days until embryos hatched. The males tended eggs at the expense of their feeding. Aggression toward fishes approaching their burrows were exhibited by the males as well as the females. Because of its low frequency in females, this behavior did not limit their ability to feed.     

Courtship tactics by male Ilyoplax pusilla (Brachyura, Dotillidae)

Mating in the dotillid crab Ilyoplax pusilla occurs after the female enters the male’s burrow in the tidal flat. Males use two tactics to cause females to enter their burrows for mating: the male either directs claw waving to the female (courting-wave display), to which the females responds by following the male to his burrow, or the male runs rapidly away from, then back toward, his burrow (dash-out-back display), which startles the female into his burrow. Males more often used the courting-wave than the dash-out-back display, but mating success did not differ between the two tactics. Male use of either tactic was influenced by date, female density and male size; the courting-wave display was used by larger males, later in the breeding period, and under higher female density.     

Burrow ornamentation in the fiddler crab (Uca leptodactyla): female mate choice and male–male competition

Non-biological ornamentation is found in the nests and burrows of different kinds of animals. We evaluated here whether sand hoods constructed by male fiddler crabs (Uca leptodactyla) are one of the signals used by males to attract females during courtship. We observed females when they were walking among the males, and we quantified the proportion of females that visited male burrows with and without ornamentation and the choice to stay in a male’s burrow. Females visited more burrows with hoods than burrows without hoods, and they chose significantly more builder males. Male investment in ornamentation nevertheless decreased when the proportion of females increased in the area. Male investment was not correlated with the proportion of non-builder males nearby, but was positively correlated with overall density. The density sex ratio, however, was more male-biased in high-density than in low-density areas suggesting that even if building attracts females, the function could be related to male competition for mates.     

高原鼠兔种群恢复过程中的洞穴分布动态

高原鼠兔洞穴系统的恢复是其种群恢复的关键指标之一,洞穴分布的变化可以反映种群的动态。本研究于2014-2016年在青海省祁连县对2.79 hm2高寒草甸内高原鼠兔(Ochotona curzoniae)种群密度、洞穴密度和洞穴的相对位置进行跟踪观测。其中包括6个50m×50m 的灭鼠堵洞处理、6个30m×30m 的灭鼠处理和3个50m×50m的对照处理。分别采用平均最近邻指数和平均拥挤度指数分析洞穴系统中有效洞、弃洞、粪坑和嬉戏坑的分布模式及洞系表现面积,并对各参数进行描述性和相关性分析。结果显示：高原鼠兔种群密度恢复过程中（1）有效洞的空间格局由随机向离散分布转变,弃洞由随机向聚集分布转变,粪坑和嬉戏坑无明显变化趋势;有效洞和弃洞分布格局的恢复都朝向灭鼠前状态,但恢复的都不充分;（2）有效洞最近邻指数与其自身密度正相关;弃洞最邻近指数与其自身密度负相关;粪坑、嬉戏坑最近邻指数与其自身密度无显著相关性;其中,仅粪坑的分布最近邻指数与高原鼠兔种群密度呈显著负相关;（3）有效洞与粪坑、嬉戏坑表现面积的变化情况较为一致,与弃洞呈互补态势;洞系表现面积的变异性远小于洞穴密度。结果说明：（1）高原鼠兔洞穴分布格局和洞穴密度的恢复具有滞后性;（2）有效洞、弃洞的分布格局主要受洞穴密度的影响;（3）高原鼠兔种群的恢复过程中对洞系面积的需求优先于洞口数量。     

Individual recognition in salamanders: Cloacal odours

Male red-backed salamanders (Plethodon cinereus) were studied to determine the origin of the chemical cues allowing for individual odour recognition between conspecifics. Individual males showed a preference for substrates with their own faecal and cloacal odours rather than those marked by unfamiliar conspecific males. This discriminatory ability did not depend on recent differences in food consumed. These scent marks might be used to define breeding territories in the field.     

Male orientation to trail sex pheromones in parasitoid wasps: does the spatial distribution of virgin females matter?

We studied male locomotory response to trails and patches of sex pheromone (left respectively by free-ranging females and females constrained to stay on a small area) in the two parasitoids Aphelinus asychis (Hymenoptera: Aphelinidae) and Trichogramma brassicae (Hymenoptera: Trichogrammatidae). Under the hypothesis that the spatial distribution of virgin females differs between these species (scattered among host plants in A. asychis, gregarious at emergence sites in T. brassicae), we predicted that male locomotory response to their sex pheromones should also differ: A. asychis males should follow pheromone trails on plants in order to encounter the females along these trails, whereas T. brassicae males should stay on pheromone patches, at emergence sites, and mate the females on these patches. Using an improved video-tracking system, we found that males of both species respond to conspecific sex pheromone trails and patches, but that the response does not differ much between species. Males released on marked substrates walked in a more convoluted pattern (i.e. higher path fractal dimension and higher number of crossings within tracks) than males released on unmarked substrates. On pheromone patches, males turned persistently in the same direction when leaving the patch, which explains a higher number of visits on marked patches than on unmarked patches, and possibly, higher track convolution on pheromone trails. Contrary to our hypothesis, male A. asychis did not follow female trails more accurately than male T. brassicae, and male T. brassicae did not stay longer on pheromone patches than male A. asychis. We argue that these discrepancies between our predictions and the observed responses originates from discrepancies between the assumed spatial distribution of virgin females and their actual distribution in the wild.     

Does time until mating affect progeny sex ratio? A manipulative experiment with the parasitoid wasp Aphelinus asychis

In haplodiploid organisms, unmated or sperm depleted females are “constrained” to produce only male progeny. If such constrained females reproduce, the population sex ratio will shift toward males and unconstrained females will be selected to produce more females. Assuming that a female's own time spent constrained is an index of the population-wide level of constrained oviposition, and that constrained and unconstrained females reproduce at the same rate, the proportion of sons that females produce when unconstrained should decrease with increasing time spent constrained. Alternatively, if females cannot measure time spent constrained or if time spent constrained is not an index to the level of constrained oviposition in the population, the proportion of sons among progeny produced when unconstrained should not depend upon time spent constrained and should be female biased to an extent depending upon the average time spent constrained over evolutionary time. To test these predictions, we manipulated the amount of time spent virgin in the parasitoid wasp Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and measured the number of males and females among progeny produced before and after mating. First, we found no interaction between age and age at mating in their effect on fecundity, which suggests that mating does not change fecundity. Second, we found that females mated at 8 days and 15 days produced equal sex ratios after mating but these were slightly more female biased than the sex ratios of females mated at 1 day. This observed “step response” suggests that females may perceive time from emergence to mating as a discrete rather than a continuous variable (i.e., short versus long), or that females do not perceive time per se but assess their age class (i.e., young versus old) at the time of mating.