Is there a fish alarm cue? Affirming evidence from a wild study

Chemical alarm cues released from injured tissue are not released under any other context and therefore reliably inform nearby prey of the presence of a predator. Laboratory and field studies have demonstrated that most aquatic taxa show antipredator responses to chemical alarm cues. Ostariophysan fish (e.g. minnows) possess specialized skin cells that contain an alarm chemical. Magurran et al. (1996, Proceedings of the Royal Society of London, Series B,263, 1551-1556) were the first to use underwater video to carefully document the behavioural response of free-ranging wild populations of minnows to minnow alarm cues. They found no evidence of an antipredator response, and challenged the assumption that the contents of these cells indicate risk in the field. They proposed that alarm responses are context dependent in that they are an artefact of enclosed environments such as laboratory aquaria and field traps. Here, we repeat their experiment on free-swimming field populations of littoral fish and report a significant decrease in the number of fish in areas where chemical alarm cues of blacknose shiners, Notropis heterolepis (Ostariophysi: Cyprinidae) were released. The effect of these chemical cues was equal in magnitude to the effect of the presentation of a model predator. The response to the approach of a model predator (visual cue) was intensified by pre-exposure to chemical alarm cues. We corroborated this interaction between chemical and visual indicators of predation risk in a laboratory study using glowlight tetras, Hemigrammus erythrozonus (Ostariophysi: Characidae). Response to the visual stimulus of a predator was significantly intensified by previous exposure to conspecific chemical alarm cues. We conclude that ostariophysan skin indeed contains an alarm cue that (1) informs nearby prey of imminent predation risk, (2) induces some form of antipredator behaviour in most contexts, and (3) affects subsequent behavioural responses to stimuli in other sensory modalities.     

Stability of within-host–parasite communities in a wild mammal system

Simultaneous infection by multiple parasite species is ubiquitous in nature. Interactions among co-infecting parasites may have important consequences for disease severity, transmission and community-level responses to perturbations. However, our current view of parasite interactions in nature comes primarily from observational studies, which may be unreliable at detecting interactions. We performed a perturbation experiment in wild mice, by using an anthelminthic to suppress nematodes, and monitored the consequences for other parasite species. Overall, these parasite communities were remarkably stable to perturbation. Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition. These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.     

Can overmarking be considered as a means of chemical mate guarding in a wild callitrichid?

Mate guarding is a male strategy to monopolize matings and thus to ensure paternity. Since in callitrichids female reproductive status is advertised by scent marks, one may expect mate guarding by chemical means. We addressed this question during an episode of consortship observed in a polyandrous trio of wild saddleback tamarins (Saguinus fuscicollis). During consortship, the consort male was the only one to allomark the female. Scent marking frequency decreased for all individuals, although the consort male marked more than the other male during consortship, while there was no difference in the previous period. During consortship, almost 50% of female scents were overmarked by the consort, and more than 56% of the consort's scent marks were employed to overmark the female's scents. Therefore, the other male had limited access to female scent marks. Mate guarding may thus have a chemical component in tamarins, and olfactory communication may play an important role in mating competition.     

Host-pathogen diversity in a wild system: Chondrilla juncea–Puccinia chondrillina

The resistance structure of a Turkish population of the clonal, apomictic composite Chondrilla juncea and the pathotypic structure of a co-occurring population of its obligate rust pathogen, Puccinia chondrillina, was determined by sequential inoculation of 19 host lines with 15 pathogen isolates each derived from single pustules collected from separate plants among the host population. The resultant matrix of resistant and susceptible reactions provides strong circumstantial evidence for a gene-for-gene interaction. Seven distinct pathotypes were detected in the pathogen population. One of these comprised 53% of the population, a second comprised 13%, while the remaining five pathotypes were each detected only once. The host population was similarly diverse, being composed of eight resistance phenotypes, only two of which were represented by more than one host line. Although C. juncea is apomictic, there was only 58% congruence between host resistance and multi-locus isozyme phenotype categories within this population. Pathotypic phenotypes of 13 other isolates of P. chondrillina collected from ten other Turkish and three more distant populations of C. juncea were markedly different from those found in the population studied in detail. There was no obvious relationship between the degree of geographic separation of pathotypes and their ability to attack particular C. juncea lines in this or three other populations represented by single host lines. Received: 10 March 1997 / Accepted: 4 August 1997     

The BOS™ as a species-specific method to deliver baits to wild boar in a Mediterranean area

The impact of wild boar Sus scrofa and feral pigs on ecosystems and human activities is of interest worldwide. Bait-delivered pharmaceuticals such as contraceptives or disease vaccines are increasingly advocated to assist the management of such impacts. We evaluated the Boar-Operated-System (BOS?) to deliver baits to wild boar in a Mediterranean area with a large community of potential nontarget species. In a pre-trial phase (BOS? open), both wild boar and 12 nontarget species (wildlife and livestock) visited the BOS? and eight species consumed the baits. In the trial phase, when the BOS? were closed, only wild boar consumed baits. From pre-trial to trial, the rate of visits by nontarget species to the BOS? decreased significantly, but that of wild boar did not change. We observed that crested porcupines Hystrix cristata prevented the wild boar from using BOS?. We confirmed the effectiveness of BOS? to deliver baits selectively to wild boar in a Mediterranean area.     

Can we stop transgenes from taking a walk on the wild side?

Whether the potential costs associated with broad‐scale use of genetically modified organisms (GMOs) outweigh possible benefits is highly contentious, including within the scientific community. Even among those generally in favour of commercialization of GM crops, there is nonetheless broad recognition that transgene escape into the wild should be minimized. But is it possible to achieve containment of engineered genetic elements in the context of large scale agricultural production? In a previous study, Warwick et al. (2003) documented transgene escape via gene flow from herbicide resistant (HR) canola (Brassica napus) into neighbouring weedy B. rapa populations ( Fig. 1 ) in two agricultural fields in Quebec, Canada. In a follow‐up study in this issue of Molecular Ecology, Warwick et al. (2008) show that the transgene has persisted and spread within the weedy population in the absence of selection for herbicide resistance. Certainly a trait like herbicide resistance is expected to spread when selected through the use of the herbicide, despite potentially negative epistatic effects on fitness. However, Warwick et al.'s findings suggest that direct selection favouring the transgene is not required for its persistence. So is there any hope of preventing transgene escape into the wild?

Figure 1 Open in figure viewer PowerPoint Weedy Brassica rapa (orange flags) growing in a B. napus field. (Photo: MJ Simard)     

The helminth fauna of wild and domestic ruminants in Mongolia—a review

The helminth fauna of eight species of wild ruminants and five species of domestic ruminants sharing common grassland in Mongolia was reviewed. A total of 108 species of helminths, belonging to 40 genera, 23 families, 11 superfamilies, 6 orders and 3 classes were reported in wild and domestic ruminants in Mongolia. Several new host–helminth associations have been recorded. Twenty seven helminth species have been found in certain host species for the first time in Mongolia. These included 2 species of trematodes, 2 species of cestodes and 23 species of nematodes. Helminths that are specific for some of the examined ruminant species were determined. However, wild animals may serve as a reservoir of helminth infections for domestic animals when sharing grassland in Mongolia. The helminth fauna of the ruminants with respect to occurrence, distribution, prevalence and intensity of infection was considered for six geographic regions of Mongolia.     

Is telomere length a molecular marker of past thermal stress in wild fish?

Telomeres protect eukaryotic chromosomes; variation in telomere length has been linked (primarily in homoeothermic animals) to variation in stress, cellular ageing and disease risk. Moreover, telomeres have been suggested to function as biomarker for quantifying past environmental stress, but studies in wild animals remain rare. Environmental stress, such as extreme environmental temperatures in poikilothermic animals, may result in oxidative stress that accelerates telomere attrition. However, growth, which may depend on temperature, can also contribute to telomere attrition. To test for associations between multitissue telomere length and past water temperature while accounting for the previous individual growth, we used quantitative PCR to analyse samples from 112 young‐of‐the‐year brown trout from 10 natural rivers with average water temperature differences of up to 6°C (and an absolute maximum of 23°C). We found negative associations between relative telomere length (RTL) and both average river temperature and individual body size. We found no indication of RTL–temperature association differences among six tissues, but we did find indications for differences among the tissues for associations between RTL and body size; size trends, albeit nonsignificant in their differences, were strongest in muscle and weakest in fin. Although causal relationships among temperature, growth, oxidative stress, and cross‐sectional telomere length remain largely unknown, our results indicate that telomere‐length variation in a poikilothermic wild animal is associated with both past temperature and growth.     

Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation?

Culture has long been assumed to be uniquely human but recent studies, in particular on great apes, have suggested that cultures also occur in non-human primates. The most apparent cultural behaviours in great apes involve tools in the subsistence context where they are clearly functional to obtain valued food. On the other hand, tool-use to modify acoustic communication has been reported only once and its function has not been investigated. Thus, the question whether this is an adaptive behaviour remains open, even though evidence indicates that it is socially transmitted (i.e. cultural). Here we report on wild orang-utans using tools to modulate the maximum frequency of one of their sounds, the kiss squeak, emitted in distress. In this variant, orang-utans strip leaves off a twig and hold them to their mouth while producing a kiss squeak. Using leaves as a tool lowers the frequency of the call compared to a kiss squeak without leaves or with only a hand to the mouth. If the lowering of the maximum frequency functions in orang-utans as it does in other animals, two predictions follow: (i) kiss squeak frequency is related to body size and (ii) the use of leaves will occur in situations of most acute danger. Supporting these predictions, kiss squeaks without tools decreased with body size and kiss squeaks with leaves were only emitted by highly distressed individuals. Moreover, we found indications that the calls were under volitional control. This finding is significant for at least two reasons. First, although few animal species are known to deceptively lower the maximum frequency of their calls to exaggerate their perceived size to the listener (e.g. vocal tract elongation in male deer) it has never been reported that animals may use tools to achieve this, or that they are primates. Second, it shows that the orang-utan culture extends into the communicative domain, thus challenging the traditional assumption that primate calling behaviour is overall purely emotional.     

Opportunistic or selective? Stage-dependent feeding behavior in a wild vector of Chagas disease

The composition and contribution of different host species in the dynamics of vector-borne zoonotic parasites are particularly relevant for public health. Hence, the study of host selection by vectors is fundamental. Developmental stage and infection status are factors that may modulate vector feeding behavior. In the semi-arid Mediterranean ecosystem of South America, the transmission of Trypanosoma cruzi, the protozoan causing Chagas disease, includes the triatomine vector Mepraia spinolai and several vertebrate species. In this field study, we examined whether M. spinolai exhibits an opportunistic feeding behavior dependent upon developmental stage and/or infection status. We found that M. spinolai does not feed according to the relative availability of vertebrate species. In addition, early stage nymphs (first/second instars) fed on twice as many different species as middle (third/fourth instars) and late (fifth instars and adults) M. spinolai, with the former feeding on native rodents and lizards and the latter mostly on rabbits. Infected and uninfected M. spinolai showed similar feeding profiles. Wild triatomine species might be described as stage-dependent selective blood feeders, as a consequence of the temporal and spatial scale at which host-vector interactions occur, highlighting that all developmental stages might be infected and capable of transmitting T. cruzi.     

Are flower-visiting ants mutualists or antagonists? A study in a gynodioecious wild strawberry

Ants are common flower visitors, but their effects on plant reproductive fitness have not often been assessed. Flower-visiting ants were studied to determine whether they are antagonists or mutualists and whether they could influence floral or breeding system evolution in gynodioecious wild strawberry (Fragaria virginiana). Ant and flying pollinator (bees/flies) access to plants was manipulated, and visitation, fruit, and seed set were assessed. Ants visited flowers of hermaphrodites more often than those of females when bees and flies were excluded, but visited the sex morphs equally when they were present. Insect class did not influence fruit or seed set of hermaphrodites. In contrast, ants had both positive and negative effects on seed set in females. Females visited only by ants had 90% of the seed set of those visited only by bees/flies, and their seed set increased with ant visitation. The spatial pattern of seed set, however, suggests that ants may also damage pistils. Lastly, in contrast to bees and flies, ants failed to increase visitation with floral display size, suggesting that ant presence at flowers could reduce selection on this attractive trait. Findings suggest that when in high abundance, flower-visiting ants could affect breeding system and floral evolution in this gynodioecious plant.     

Is polyandry a common event among wild populations of the pest Ceratitis capitata?

In many insect species, females can mate more than once and store sperm from more than one male. An assessment and understanding of polyandry in the field can be important for pest species with a high colonization potential, such as the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), which is also highly polyphagous and among the most destructive agricultural insects. The use of polymorphic microsatellite markers, combined with different statistical approaches, provides evidence that polyandry occurs in two C. capitata natural populations, one population from the Greek island of Chios and one population from Rehovot, in Israel. The observed different level of polyandry is discussed in relation to the genetic diversity, seasonality, and demography of the two populations. When polyandry is present, paternity analysis also indicates that one male, presumably the last, tends to sire most of the progeny. Polyandry and paternity skew may have important implications for the evolution of the species, in terms of maintenance of the genetic variability. Moreover, these aspects of the mating behavior, i.e., remating frequency and paternity skew, may locally affect the sterile insect technique, the most commonly applied control strategy against C. capitata.     

Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.     

Father–offspring phenotypic correlations suggest intralocus sexual conflict for a fitness-linked trait in a wild sexually dimorphic mammal

In sexually dimorphic and polygynous mammals, sexual selection often favours large males with well-developed weaponry, as these secondary sexual characters confer advantages in intrasexual competition and are often preferred by females. Little is known, however, about the effects of sexually selected paternal traits on offspring phenotype in wild mammals, especially when considering that shared phenotypic traits and selection can also differ greatly between genders. Here, we conducted molecular parentage analyses in a long-term study population of mountain goats (Oreamnos americanus), an ungulate exhibiting high sexual dimorphism in mass, to first assess the determinants of yearly reproductive success (YRS) in males. We then examined the effects of paternal characteristics on offspring mass at 1 year of age. Paternity was highly skewed, with 9 per cent of 57 males siring 51 per cent of 96 offspring assigned over 12 years. Male YRS increased with age until apparent reproductive senescence at 9 years, but mass was a stronger determinant of siring success than age, horn length or social rank. Mass of sons increased with paternal mass, but the mass of daughters was negatively related to that of their father, a finding consistent with recent theory on intralocus sexual conflict. Because early differences in mass persisted to early adulthood, sex-specific effects of paternal mass can have important fitness consequences, as adult mass is positively linked with reproduction in both sexes. Divergent father–offspring phenotypic correlations may partly explain the maintenance of sexual dimorphism in mountain goats and the large variance observed for this homologous trait within each gender in polygynous mammals.     

Epichloë endophyte affects the root colonization pattern of belowground symbionts in a wild grass

Plants host multiple symbionts that interact with each other affecting plant performance and regulating their establishment. Here, we analyzed how the association with Epichloë endophytes affects belowground colonization by Dark Septate Endophytes (DSE) and arbuscular mycorrhizal fungi (AMF) in the grass Bromus auleticus. Epichloë-symbiotic (E+) and Epichloë-non symbiotic (E−) plants were sampled from a long-term experimental plot and colonization structures were analyzed in the roots. We also examined the influence of Epichloë exudates on the in vitro growth of DSE Microdochium bolleyi isolated from roots. Epichloë symbiosis increased AMF colonization, although differences were not significant. Despite the lack of differences in total DSE colonization, in concordance with in vitro findings, a higher significant abundance of microsclerotia was observed in E+ plants. A negative correlation between total mycorrhizal and DSE was found. Our findings show a more uniform root colonization pattern in E+ plants, suggesting a root symbiosis modulating role.     

Use of leaves to inspect ectoparasites in wild chimpanzees: a third cultural variant?

We report 26 cases of using leaves as tools with which wild chimpanzees (Pan troglodytes schweinfurthii) in the Sonso community, Budongo Forest, Uganda, appeared to inspect objects removed during grooming. Careful removal of potential ectoparasites and delicate lip or manual placement on leaves followed by intense visual examination characterised this behaviour. It appears to be done to judge whether either ingestion or discarding is most appropriate, the former occurring in most cases. This behaviour may represent a third variant of ectoparasite handling, different from those described at Taï and Gombe, yet sharing features with the latter. These two East African techniques may thus have evolved from leaf grooming.     

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

Hosts have evolved two distinct defence strategies against parasites: resistance (which prevents infection or limit parasite growth) and tolerance (which alleviates the fitness consequences of infection). However, heritable variation in resistance and tolerance and the genetic correlation between these two traits have rarely been characterized in wild host populations. Here, we estimate these parameters for both traits in Leuciscus burdigalensis, a freshwater fish parasitized by Tracheliastes polycolpus. We used a genetic database to construct a full-sib pedigree in a wild L. burdigalensis population. We then used univariate animal models to estimate inclusive heritability (i.e. all forms of genetic and non-genetic inheritance) in resistance and tolerance. Finally, we assessed the genetic correlation between these two traits using a bivariate animal model. We found significant heritability for resistance (H = 17.6%; 95% CI: 7.2–32.2%) and tolerance (H = 18.8%; 95% CI: 4.4–36.1%), whereas we found no evidence for the existence of a genetic correlation between these traits. Furthermore, we confirm that resistance and tolerance are strongly affected by environmental effects. Our results demonstrate that (i) heritable variation exists for parasite resistance and tolerance in wild host populations, and (ii) these traits can evolve independently in populations.     

A plethora of Plasmodium species in wild apes: a source of human infection?

Recent studies of captive and wild-living apes in Africa have uncovered evidence of numerous new Plasmodium species, one of which was identified as the immediate precursor of human Plasmodium falciparum. These findings raise the question whether wild apes could be a recurrent source of Plasmodium infections in humans. This question is not new, but was the subject of intense investigation by researchers in the first half of the last century. Re-examination of their work in the context of recent molecular findings provides a new framework to understand the diversity of Plasmodium species and to assess the risk of future cross-species transmissions to humans in the context of proposed malaria eradication programs.     

Symbolic communication in wild chimpanzees?

The language abilities of captive chimpanzees give rise to the question of the existence and use of similar capabilities in wild chimpanzees. In Taï forest, wild chimpanzees seem to use drumming on buttressed trees to convey information an changes of travel direction, resting periods or both information combined. This communication system is iconic and relies on some arbitrariness. Emergence of symbol-like communication in wild chimpanzees seems mainly dependent on a low visibility environment, a high predation pressure and a large group of males.