Life history costs of olfactory status signalling in mice

Large body size confers a competitive advantage in animal contests but does not always determine the outcome. Here we explore the trade-off between short-term achievement of high social status and longer-term life history costs in animals which vary in competitive ability. Using laboratory mice, Mus musculus, as a model system, we show that small competitors can initially maintain dominance over larger males by increasing investment in olfactory status signalling (scent-marking), but only at the cost of reduced growth rate and body size. As a result they become more vulnerable to dominance reversals later in life. Our results also provide the first empirical information about life history costs of olfactory status signals. Received: 15 December 1999 / Revised: 6 June 2000 / Accepted: 24 June 2000     

A new challenge—development of test systems for the infochemical effect

Background, aim, and scope

Many—if not all—organisms depend on so-called infochemicals, chemical substances in their surroundings which inform the receivers about their biotic and abiotic environment and which allow them to react adequately to these signals. Anthropogenic substances can interfere with this complex chemical communication system. This finding is called infochemical effect. So far, it is not known to what extent anthropogenic discharges act as infochemicals and influence life and reproduction of organisms in the environment because adequate testing methods to identify chemicals which show the infochemical effect and to quantify their effects have not been developed yet. The purpose of this article is to help and find suitable test designs.

Main features

Test systems used in basic research to elucidate the olfactory cascade and the communication of environmental organisms by infochemicals are plentiful. Some of them might be the basis for a quantified ecotoxicological analysis of the infochemical effect. In principle, test systems for the infochemical effect could be developed at each step of the chemosensory signal transduction and processing cascade.

Results

Experimental set-ups were compiled systematically under the aspect whether they might be usable for testing the infochemical effect of single chemicals in standardized quantifying laboratory experiments. For an appropriate ecotoxicological assessment of the infochemical effect, experimental studies of many disciplines, such as molecular biology, neurobiology, physiology, chemical ecology, and population dynamics, should be evaluated in detail before a decision can be made which test system, respectively which test battery, might be suited best. The test systems presented here are based on the knowledge of the genetic sequences for olfactory receptors, binding studies of odorants, signal transmission, and reactions of the receivers on the level of the organisms or the populations. The following basic approaches are conceivable to identify the role of an infochemical: binding studies to the odorant-binding protein or to the odorant receptor binding protein (e.g., by in situ hybridization and immunohistochemical studies), measurement of electrical signals of the receptor cells in the tissue (e.g., electroolfactograms, electroantennograms), registration of phenotypic changes (e.g., observation under the microscope), behavioral tests (e.g., in situ online biomonitoring, use of T-shaped olfactometers, tests of avoidance responses), measurement of population changes (e.g., cell density or turbidity measurements), and multispecies tests with observation of community structure and community function. The main focus of this study is on aquatic organisms.

Discussion

It is evident that the infochemical effect is a very complex sublethal endpoint, and it needs further studies with standardized quantitative methods to elucidate whether and to what extent the ecosystem is affected. The collection of approaches presented here is far from being complete but should serve as a point of depart for further experimental research.

Conclusions

This article is the first to compare various approaches for testing the infochemical effect. The development of a suitable test system will not be easy as there are a multitude of relevant chemicals, a multitude of relevant receptors, and a multitude of relevant reactions, and it must be expected that the effective concentrations are very low. The chemical communication is of utmost importance for the ecosystem and justifies great endeavors to find solutions to these technical problems.

Recommendations and perspectives

The infochemical effect is a new chapter in ecotoxicology. Will a new endpoint, the so-called infochemical effect, be required in addition to the actual standard test battery of Annex 5 to Commission Directive 92/69/EEC (EC 1992)? Finding the answer to this question is a big challenge that could be met by a comprehensive research project.     

Insecticide resistance may enhance the response to a host-plant volatile kairomone for the codling moth, <Emphasis Type="Italic">Cydia pomonella</Emphasis> (L.)

The behavioral and electroantennographic responses of Cydia pomonella (L.) to the ripe pear volatile ethyl (2E,4Z)-2,4-decadienoate (Et-E,Z-DD), were compared in insecticide-susceptible and -resistant populations originating from southern France. A dose–response relationship to this kairomonal attractant was established for antennal activity and did not reveal differences between susceptible and resistant strains. Conversely, males of the laboratory strains expressing metabolic [cytochrome P450-dependent mixed-function oxidases (mfo)] or physiological (kdr-type mutation of the sodium-channel gene) resistance mechanisms exhibited a significantly higher response to Et-E,Z-DD than those of the susceptible strain in a wind tunnel experiment. No response of the females to this kairomone could be obtained in our wind-tunnel conditions. In apple orchards, mfo-resistant male moths were captured at significantly higher rates in kairomone-baited traps than in traps baited with the sex pheromone of C. pomonella. Such a differential phenomenon was not verified for the kdr-resistant insects, which exhibited a similar response to both the sex pheromone and the kairomonal attractant in apple orchards. Considering the widespread distribution of metabolic resistance in European populations of C. pomonella and the enhanced behavioral response to Et-E,Z-DD in resistant moths, the development of control measures based on this kairomonal compound would be of great interest for the management of insecticide resistance in this species.     

Atypical homing or self-odour avoidance? Blue petrels (Halobaena caerulea) are attracted to their mate’s odour but avoid their own

Among procellariiform seabirds, many burrowing petrels show good olfactory abilities especially in recognising their nest. In particular, it has been reported that Antarctic prions (Pachyptila desolata) discriminate their own and their mate’s odours and, in Y-maze experiments, prefer the odour of a conspecific bird to their own. While traditionally examined from the perspective of homing mechanisms, these recent results have drawn attention to the possible use of chemical signals in birds’ social behaviours. Indeed, the life history of petrels suggests that a mate choice mediated by olfactory mechanisms may have evolved in this group to ensure genetic compatibility. This study was undertaken to validate and extend results obtained on petrels’ olfactory discrimination capabilities. Following the Y-maze experiment protocol, blue petrels (Halobaena caerulea) were offered three different choices: (1) mate versus conspecific’s odour, (2) own versus mate’s odour and (3) own versus conspecific’s odour. We discovered that birds prefer the odour of their mate not only when presented against conspecific’s odour but also against their own. We further verified that blue petrels also avoid their own odour when presented against conspecific’s odour. Our results confirm that olfactory discrimination in burrowing petrels goes beyond self-recognition and that self-odour avoidance may be widespread. We use two mutually non-exclusive behavioural frameworks for the interpretation of our results, homing and mate choice, and explain why homing mechanisms cannot account for all of our observations. This study opens the door to further research on olfactory mechanisms that, in petrels, might mediate individual recognition and mate choice.     

Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants

The controversy concerning the extent to which the organization of division of labor in social insects is a developmental process or is based on task allocation dynamics that emerge from colony need independent of worker age and endocrine or neural state has yet to be resolved. We present a novel analysis of temporal polyethism in the ant Pheidole dentata, demonstrating that task attendance by minor workers does not shift among spatially associated sets of behaviors that minimally overlap but rather expands with age. Our results show that the number of tasks performed by older minors increases through the addition and retention of behaviors, with up to a sixfold increase in repertoire size from day 1 to day 20 of adult life. We also show that older minors respond to colony needs by performing significantly more brood care as its demand increases, indicating that they can quickly upregulate nursing according to labor requirements. This level of plasticity was absent in younger siblings. The breadth of responsiveness to task-related olfactory stimuli increased with age. In a binary choice test in which young and old minor workers could orient toward odorants from brood or food, older workers responded to both brood and food, whereas young workers responded only to brood. These dissimilar responses to stimuli associated with nursing and foraging indicate age-related differences in sensory ability and provide a physiological basis for the age-related repertoire expansion model. We discuss repertoire expansion in P. dentata in light of behavioral development and caste flexibility in ants.     

Social recognition in sticklebacks: the role of direct experience and habitat cues

The social organisation of animals relies on recognition. However, there are many means by which animals may recognise one another and a variety of cues are available to any individual at any one time. We tested the effects of cues based on direct experience and of cues based on habitat and diet on association decisions in the three-spined stickleback (Gasterosteus aculeatus). Our results show that sticklebacks rapidly acquire association preferences for novel con- and heterospecifics (nine-spined sticklebacks, Pungitius pungitius) which had experienced the same habitat and diet conditioning as themselves over novel con- and heterospecifics which had experienced a different habitat and diet conditioning, a preference which may be based on self-referent matching. Association preferences were observed after only 24 h and were independent of the number of tank mates (treatments with 20 and 100 fish). Evidence for the influence of direct social experience on association preferences was weak and may be confounded by other factors.Communicated by K. Lindström     

Schooling decisions in guppies (Poecilia reticulata) are based on familiarity rather than kin recognition by phenotype matching

Evidence from a number of freshwater species indicates that fish prefer to school with familiar individuals. Do they also choose to associate with kin? Our experiment tested this idea using the Trinidadian guppy, Poecilia reticulata, a species whose reproductive biology favours the association of kin groups. Juveniles reared together were able to recognise one another on the basis of either visual or chemical cues, but showed no preference for schooling with unfamiliar kin. We therefore conclude that any naturally occurring kin groups in this species will occur as a result of familiarity rather than as a consequence of kin recognition based on phenotype matching.     

Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus)

In monogamous species, females often choose between males according to the quality of the territories they defend, but the extent to which females themselves contribute to territory defence is frequently underestimated. Here we test for differences in male and female roles during paired scent-marking bouts, a key component of territorial defence, in a monogamous antelope. In two populations (Kenya, Zimbabwe) of klipspringer, Oreotragus oreotragus, both males and females usually scent-marked at the same site, but there were significant differences between sexes in terms of investment within bouts. Females initiated most bouts, thus dictating the marking strategy of the pair. Males initiated relatively few bouts, but deposited more scent marks per bout than females and were usually the last to scent-mark before leaving the site; they marked on the same branches as the female and thus overmarked her scent. Both sexes deposited more marks during paired than solo visits. Immediately preceding and following scent-marking bouts, males approached females and females left males more often than expected. Female scent-marking rates were higher when they were receptive than at other times, and this increase was matched by elevated marking rates of males. Females may increase marking rates when they are receptive in order to test the quality of their mate or to incite male competition. However, these ideas are unlikely to explain female scent-marking behaviour outside the mating season, which appears to be related primarily to territorial defence. We suggest that these differences in investment in scent-marking bouts are consistent with predictions that females may be autonomously territorial and that overmarking of female scent by males is a form of mate-guarding. Received: 17 November 1999 / Received in revised form: 24 February 2000 / Accepted: 13 March 2000     

Sexual contact influences orientation to plant attractant in Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae)

Chemical signals emitted by insects and their hosts are important for sexual communication and host selection. Plant volatiles facilitate the location of suitable hosts for feeding and oviposition, and may moderate responses to sex and aggregation pheromones. While mating has been shown to moderate behavioral responses to pheromones in a number of insects, little is known about the effects of mating on behavioral responses of insects to plant attractants, and even less is known about the mechanisms involved. In this study, mating was shown to decrease behavioral responses of the Colorado potato beetle to a host kairomone within 24 h, and attraction to the kairomone recovers only after 72 h. This decrease in responsiveness also occurs when only contact with the opposite sex is allowed; the effect is not observed with contact among individuals of the same sex. Peripheral olfactory responses to a component of the kairomone correlate with the observed behavioral responses and suggest involvement of antennal receptors in the behavioral change.     

To whom it may concern: the transmission and function of chemical signals in Lemur catta

The goals of this study were to investigate the transmission and possible functions of chemical signals in intragroup communication among ring-tailed lemurs, Lemur catta. In particular, I examined the effects of sex on these processes because sexual selection theory predicts specific functions for chemical signals. I recorded all interactions with 214 scent marks of 11 male and 9 female ring-tailed lemurs during the first 10 min following their deposition. I found that 62% of these scent marks were investigated with a median latency of 30 s and that 89% of investigated scents were also counter-marked by the receiver. The type of focal scent mark (male or female anogenital and male antebrachial mark) had a significant effect on both the timing and type of response. Males investigated and counter-marked female scents more often than vice versa, but significant second-order transitions suggested that the behavior of an animal was not only influenced by the immediately preceding scent mark and that a scent is not completely masked by a counter-mark. There was no evidence for an audience effect, and only social rank of female senders had an effect on receivers. Variation in the response of receivers across reproductive seasons as a function of senders' sex indicated that female scents may function in mate attraction and competition among females, whereas male scents may be primarily used in intrasexual competition. Three main conclusions emerged. First, the exchange of olfactory signals within groups was highly structured and surprisingly efficient. Second, olfactory signals may constitute general mesasages whose transfer is partly controlled by the receiver. Finally, sexual selection theory provides a useful theoretical framework for functional examinations of mammalian olfactory communication. Received: 13 June 1997 / Accepted after revision: 20 March 1998