Interspecific Attraction Research Articles

Mixed-species groups in bats: non-random roost associations and roost selection in neotropical understory bats

BackgroundMixed-species groups in animals have been shown to confer antipredator, foraging and other benefits to their members that may provide selective advantages. In most cases, however, it is unclear whether functional benefits are a principal driver of heterospecific groups, or whether groups simply result from simultaneous exploitation of common resources. Mixed-species groups that form independently of environmental conditions may, however, evidence direct benefits of species associations. Bats are among the most gregarious mammals, with sometimes thousands of individuals of various species roosting communally. Despite numerous potential functional benefits of such mixed-species roosting groups, interspecific attraction has never been shown. To explore alternative explanations for mixed-species roosting, we studied roost selection in a speciose neotropical understory bat community in lowland rainforest in Costa Rica. Long term roost data were recorded over 10 years in a total of 133 roosts comprising both natural roosts and structurally uniform artificial roosts. We modelled bat roost occupancy and abundance in each roost type and in forest and pasture habitats to quantify the effects of roost- and environmental variability.ResultsWe found that bat species presence in natural roosts is predictable from habitat and structural roost parameters, but that the presence and abundance of other bat species further modifies roost choice. One third of the 12 study species were found to actively associate with selected other bat species in roosts (e.g. Glossophaga commissarisi with Carollia sowelli). Other species did not engage in communal roosting, which in some cases indicates a role for negative interspecific interactions, such as roost competition.ConclusionsMixed-species roosting may provide thermoregulatory benefits, reduce intraspecific competition and promote interspecific information transfer, and hence some heterospecific associations may be selected for in bats. Overall, our study contributes to an improved understanding of the array of factors that shape diverse tropical bat communities and drive the dynamics of heterospecific grouping in mammals more generally.

Arboreal monkeys facilitate foraging of terrestrial frugivores

AbstractTerrestrial animals feed on fruit dropped by arboreal frugivores in tropical forests around the world, but it remains unknown whether the resulting spatial associations of these animals are coincidental or intentionally maintained. On Barro Colorado Island, Panama, we used a combination of acoustic playback experiments, remote camera monitoring, and GPS tracking to quantify the frequency of such interactions, determine who initiates and maintains spatial associations, and test whether terrestrial animals adopt a strategy of acoustic eavesdropping to locate fruit patches created by foraging primates. Indeed, 90% of fruits collected in fruit fall traps had tooth marks of arboreal frugivores, and terrestrial frugivores visited fruit trees sooner following visits by GPS‐collared monkeys. While our play back experiments were insufficient to support the hypothesis that terrestrial frugivores use auditory cues to locate food dropped by arboreal primates, analyses of movement paths of capuchin monkeys (Cebus capucinus), spider monkeys (Ateles geoffroyi), and coatis (Nasua narica) reveal that observed patterns of interspecific attraction are not merely a byproduct of mutual attraction to shared resources. Coatis were significantly more likely to initiate close encounters with arboreal primates thanvice versaand maintained these associations by spending significantly longer periods at fruiting trees when collared primates were present. Our results demonstrate that terrestrial frugivores are attracted to arboreal primates, likely because they increase local resource availability. Primates are often among the first species in a habitat to be extirpated by hunting; our results suggest that their loss may have unanticipated consequences for the frugivore community.Abstract in Spanish is available with online material.

Interspecific attraction between ground-nesting songbirds and ants: the role of nest-site selection

BackgroundInterspecific interactions within ecological networks can influence animal fitness and behaviour, including nest-site selection of birds and ants. Previous studies revealed that nesting birds and ants may benefit from cohabitation, with interspecific attraction through their nest-site choice, but mutual interactions have not yet been tested. We explored a previously undescribed ecological link between ground-nesting birds and ants raising their own broods (larvae and pupae) within the birds’ nests in a temperate primeval forest of lowland Europe. We tested whether the occurrence of ant broods within bird nests resulted from a mutual or one-sided interspecific attraction that operated through nest-site choice and was modified by weather conditions.ResultsWe found a non-random occupation of bird nests by ants raising their own broods within them, which indicated interspecific attraction driven solely by the ants. The birds’ preference to nest near tussocks of vegetation showed little overlap with the most frequent placement of ant colonies among fallen deciduous tree-leaves, dead wood and moss. Additionally, birds did not appear to select forest localities with high densities of ant colonies. The occurrence of ant broods within bird nests was also unrelated to bird nest placement near to specific habitat features. The attractiveness of bird nests to ants appeared to increase with the thermal activity of the birds warming their nests, and also during cool and wet weather when the occurrence of ant broods within bird nests was most frequent. Ants often remained in the nests after the birds had vacated them, with only a slight reduction in the probability of ant brood occurrence over time.ConclusionsThe natural patterns of bird nest colonisation by ants support the hypothesis of ants’ attraction to warm nests of birds to raise their broods under advantageous thermal conditions. Similar relationships may occur between other warm-blooded, nest-building vertebrates and nest-dwelling invertebrates, which depend on ambient temperatures. The findings advance our understanding of these poorly recognised interspecific interactions, and can inform future studies of ecological networks.

(S)-Sulcatol Is a Pheromone Component for Two Species of Cerambycid Beetles in the Subfamily Lamiinae.

Males of several species in the large cerambycid beetle subfamily Lamiine, native to South and North America, are known to produce aggregation-sex pheromones composed of three related structures: the sesquiterpene catabolic product geranylacetone, its corresponding alcohol (known as fuscumol), and the acetate ester of the alcohol (fuscumol acetate). Here, we show that males of two lamiine species native to the eastern USA, Astylopsis macula (Say) and Leptostylus transversus (Gyllenhal) (both tribe Acanthocinini), produce pheromones composed of the structurally related (S)-6-methylhept-5-en-2-ol ([S]-sulcatol). Males of both species also produced 6-methylhept-5-en-2-one (sulcatone), and males of A. macula produced trace amounts of (R)-fuscumol acetate. Field experiments demonstrated that both species were attracted by (S)-sulcatol. Sulcatone was not attractive as a single component, nor did it influence attraction of A. macula to (S)-sulcatol, while its effect on L. transversus was unclear. Data from the field experiments, and a separate experiment using traps fitted with a timer mechanism that rotated trap jars, revealed that the two species overlap only slightly in both seasonal and daily flight period, thus minimizing interspecific attraction. Racemic fuscumol acetate and fuscumol antagonized attraction of both species to sulcatol. The identification of sulcatol as a cerambycid pheromone extends the known range of pheromone components in the subfamily Lamiinae.

Tree Regeneration Spatial Patterns in Ponderosa Pine Forests Following Stand-Replacing Fire: Influence of Topography and Neighbors

Shifting fire regimes alter forest structure assembly in ponderosa pine forests and may produce structural heterogeneity following stand-replacing fire due, in part, to fine-scale variability in growing environments. We mapped tree regeneration in eighteen plots 11 to 15 years after stand-replacing fire in Colorado and South Dakota, USA. We used point pattern analyses to examine the spatial pattern of tree locations and heights as well as the influence of tree interactions and topography on tree patterns. In these sparse, early-seral forests, we found that all species were spatially aggregated, partly attributable to the influence of (1) aspect and slope on conifers; (2) topographic position on quaking aspen; and (3) interspecific attraction between ponderosa pine and other species. Specifically, tree interactions were related to finer-scale patterns whereas topographic effects influenced coarse-scale patterns. Spatial structures of heights revealed conspecific size hierarchies with taller trees in denser neighborhoods. Topography and heterospecific tree interactions had nominal effect on tree height spatial structure. Our results demonstrate how stand-replacing fires create heterogeneous forest structures and suggest that scale-dependent, and often facilitatory, rather than competitive, processes act on regenerating trees. These early-seral processes will establish potential pathways of stand development, affecting future forest dynamics and management options.

Synergism between Enantiomers Creates Species-Specific Pheromone Blends and Minimizes Cross-Attraction for Two Species of Cerambycid Beetles.

Research over the last decade has revealed extensive parsimony among pheromones within the large insect family Cerambycidae, with males of many species producing the same, or very similar aggregation pheromones. Among some species in the subfamily Cerambycinae, interspecific attraction is minimized by temporal segregation, and/or by minor pheromone components that synergize attraction of conspecifics or inhibit attraction of heterospecifics. Less is known about pheromone-based mechanisms of reproductive isolation among species in the largest subfamily, the Lamiinae. Here, we present evidence that the pheromone systems of two sympatric lamiine species consist of synergistic blends of enantiomers of (E)-6,10-dimethyl-5,9-undecadien-2-ol (fuscumol) and the structurally related (E)-6,10-dimethyl-5,9-undecadien-2-yl acetate (fuscumol acetate), as a mechanism by which species-specific blends of pheromone components can minimize interspecific attraction. Male Astylidius parvus (LeConte) were found to produce (R)- and (S)-fuscumol + (R)-fuscumol acetate + geranylacetone, whereas males of Lepturges angulatus (LeConte) produced (R)- and (S)-fuscumol acetate + geranylacetone. Field experiments confirmed that adult beetles were attracted only by their species-specific blend of the enantiomers of fuscumol and fuscumol acetate, respectively, and not to the individual enantiomers. Because other lamiine species are known to produce single enantiomers or blends of enantiomers of fuscumol and/or fuscumol acetate, synergism between enantiomers, or inhibition by enantiomers, may be a widespread mechanism for forming species-specific pheromone blends in this subfamily.

State-Space Modelling of the Drivers of Movement Behaviour in Sympatric Species.

Understanding animal movement behaviour is key to furthering our knowledge on intra- and inter-specific competition, group cohesion, energy expenditure, habitat use, the spread of zoonotic diseases or species management. We used a radial basis function surface approximation subject to minimum description length constraint to uncover the state-space dynamical systems from time series data. This approximation allowed us to infer structure from a mathematical model of the movement behaviour of sheep and red deer, and the effect of density, thermal stress and vegetation type. Animal movement was recorded using GPS collars deployed in sheep and deer grazing a large experimental plot in winter and summer. Information on the thermal stress to which animals were exposed was estimated using the power consumption of mechanical heated models and meteorological records of a network of stations in the plot. Thermal stress was higher in deer than in sheep, with less differences between species in summer. Deer travelled more distance than sheep, and both species travelled more in summer than in winter; deer travel distance showed less seasonal differences than sheep. Animal movement was better predicted in deer than in sheep and in winter than in summer; both species showed a swarming behaviour in group cohesion, stronger in deer. At shorter separation distances swarming repulsion was stronger between species than within species. At longer separation distances inter-specific attraction was weaker than intra-specific; there was a positive density-dependent effect on swarming, and stronger in deer than in sheep. There was not clear evidence which species attracted or repelled the other; attraction between deer at long separation distances was stronger when the model accounted for thermal stress, but in general the dynamic movement behaviour was hardly affected by the thermal stress. Vegetation type affected intra-species interactions but had little effect on inter-species interactions. Our modelling approach is useful in interpreting animal interactions, in order to unravel complex cooperative or competitive behaviours, and to the best of our knowledge is the first modelling attempt to make predictions of multi-species animal movement under different habitat mosaics and abiotic environmental conditions.

Intraspecific and interspecific attraction of three Tomicus beetle species during the shoot-feeding phase.

The shoot beetles Tomicus minor, Tomicus yunnanensis, and Tomicus brevipilosus have been decimating Pinus yunnanensis trees for more than 30 years in Southwestern China. To understand the chemical ecological relationship between pines and Tomicus, and among the three beetle species, we compared the attraction of these beetles to damaged shoots, extracts from damaged shoots, and volatiles from damaged shoots collected by the dynamic headspace sampling method. Experiments were performed using a modified open-arena olfactometer. The male T. minor and both sexes of T. brevipilosus were more strongly attracted to damaged shoots than to undamaged shoots and they showed attraction to shoots damaged by the same species. Female T. minor and both sexes of T. yunnanensis were attracted to shoots damaged by female T. brevipilosus. The three beetle species were attracted to shoot extracts and dynamic headspace volatiles from shoots damaged by the same species and sex. Female T. minor and male T. yunnanensis were also attracted to dynamic headspace volatiles from shoots damaged by both sexes of T. brevipilosus. The results suggested that specific semiochemicals that are induced or produced by T. brevipilosus also attract T. minor and T. yunnanensis. The semiochemicals in damaged shoots affect the attraction of the three beetle species and play an important chemical communication role in weakening the host trees during the beetles' shoot-feeding phase.

Inter-specific association and habitat use in a farmland passerine assemblage

We studied the pattern of inter-specific associ- ation of breeding territories in a passerine assemblage of dry cereal farmland in central Spain and evaluated the role of the presence of heterospecifics in the habitat use patterns exhibited by different species. Bird territories showed a non-random inter-specific spatial aggregation pattern. We studied territory abundance variation in the three more abundant species: the corn bunting, the crested lark, and the fan-tailed warbler. Crested lark and fan-tailed warbler territories were more abundant in plots where corn bunting territories were present and vice versa, while their respective abundances did not vary with the breeding presence of the other species. We used landscape and agricultural management variables to analyze the relationships between habitat and each species' breeding territories by means of classification trees. While the corn bunting showed a marked pattern of nesting habitat use, the crested lark and the fan-tailed warbler exhibited a much more generalist one. Corn Bunting presence was affected negatively by intensifica- tion-related variables, such as field size and percent cover of cereal crops. Similarly, the presence of crested larks was negatively related to high yielding areas. However, when the presence of hetero-specific territories was considered, the presence of corn bunting territories was the most important variable explaining the occur- rence of breeding fan-tailed warblers, and the second most important in the case of the crested lark. These results suggest that inter-specific attraction could play a role in the formation of farmland bird assemblages, while adding further evidence for the detrimental effect of agricultural intensification at the community level.

Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species?

When species converge in their colour patterns because of mimicry, and those patterns are also used in mate recognition, there is a probability of conflicting selection pressures. Closely related species that mimic one another are particularly likely to face such confusion because of similarities in their courtship behaviour and ecology. We conducted experiments in greenhouse conditions to study interspecific attraction between two mimetic butterfly species, Heliconius erato and Heliconius melpomene. Both species spent considerable time approaching and courting females of the co-mimic species. Experiments using wing models demonstrated the importance of colour pattern in this interspecific attraction. Although males of H. melpomene were attracted to their co-mimics as much as to their own females, H. erato males were more efficient at distinguishing conspecifics, possibly using wing odours. Although preliminary, these results suggest that the use of additional cues may have evolved in H. erato to reduce the cost of convergence in visual signals with H. melpomene. Overall, our results showed that there might be a cost of mimetic convergence because of a reduction in the efficiency of species recognition. Such cost may contribute to explain the apparently stable diversity in Müllerian mimetic patterns in many tropical butterfly assemblages.

Local Enhancement in Mud-Puddling Swallowtail Butterflies (Battus philenor and Papilio glaucus)

Male butterflies aggregate at moist soil to acquire nutrients, a phenomenon termed “mud-puddling.” We studied the attraction of free-flying Papilio glaucus and Battus philenor swallowtails to dead decoys of those two species at artificial puddles moistened with NaCl solution. Both species landed preferentially at puddles with a decoy present rather than at unbaited puddles, demonstrating very strong local enhancement, a form of social facilitation. Papilio glaucus were attracted only to intraspecific decoys, whereas Battus philenor exhibited both intraspecific and interspecific attraction. Circular discs cut from the hindwings of male Battus were highly attractive to male Battus but completely unattractive to Papilio glaucus. The visual cues attractive to males in their search for salts differ between these two swallowtail species for unexplained reasons.

Polyene hydrocarbons and epoxides: a second major class of lepidopteran sex attractant pheromones.

Polyene hydrocarbons and epoxides are used as pheromone components and sex attractants by four macrolepidopteran families: the Geometridae, Noctuidae, Arctiidae, and Lymantriidae. They constitute a second major class of lepidopteran pheromones, different from the C10-C18 acetates, alcohols, and aldehydes commonly found in other species. They are biosynthesized from diet-derived linoleic or linolenic acids and are characterized by C17-C23 straight chains, 1-3 cis double bonds separated by methylene groups, and 0, 1, or 2 epoxide functions. Pheromone blends are created from components with different chain lengths, numbers of double bonds, and functional groups, or from mixtures of epoxide regioisomers or enantiomers, with several examples of synergism between enantiomers. Behavioral antagonists also limit interspecific attraction, with numerous examples of antagonism by enantiomers. This review summarizes the taxonomic distribution, mechanisms used to generate unique pheromone blends, and the identification, synthesis, and biosynthesis of these compounds.

Interspecific attraction to the mobbing calls of black-capped chickadees ( Parus atricapillus )

The species and number of birds attracted to playbacks of mobbing calls and song of the black-capped chickadee, Parus atricapillus, were compared. The chickadee vocalizations were played at abandoned chickadee nests, and the numbers and species of other birds that approached the speaker were tallied. Few non-chickadees were observed in the area when the song was played. That significantly more birds approached the speaker and displayed mobbing behavior during the mobbing call playback suggests that black-capped chickadee mobbing vocalizations carry meaning for at least ten other avian species. This finding supports the idea that species subjected to the same predators in an area may benefit by recognizing each others’ predator calls. This recognition may be facilitated by the similar structure of different species’ mobbing calls and also a learned association of another species’ call with the presence of a predator.

Interspecific sex attraction in Earias vittella and Earias insulana

Interspecific attraction between Earias vittella and Earias insulana was studied by conducting sex pheromone bioassays and by making visual observations on the behaviour of individual interspecific pairs. Olfactometer bioassays using virgin “calling” females revealed interspecific attraction amongst about 10% males. In bioassays using female sex pheromone, E. insulana did not attract any E. vittella males, but the E. vittella female sex pheromone attracted 8.7% interspecific males. Electroantennogram recordings revealed detection of interspecific sex pheromones by antennae of males of both the species. When kept at a close range and allowed free access to interspecific females, more than 50% of E. insulana males courted and copulated with E. vittella females, but incidence of such courting and copulation was negligible in the reciprocal cross. In both the cases, there was no interspecific insemination. These studies suggested that dissimilarities in: (a) sex pheromone components or their ratio, (b) courtship behaviour and (c) sperm transfer mechanism play a role in the reproductive isolation of these two species.

Aphid semiochemicals ? A review, and recent advances on the sex pheromone

The alarm pheromones are known for many species of aphids, and methods of using the synthetic pheromone to improve control of aphids by contact insecticides and biological agents have been devised. Highly active analogs have been prepared and plant-derived synergists identified. Laboratory studies on compounds obtained by chemical modification of the alarm pheromone and antifeedants derived from non-host plants have led to successful field trials against aphid-borne virus diseases in crops. Strategies for biotechnological production of aphid semiochemicals are described. The sex pheromones for a number of aphids have recently been identified. Further studies on the production, perception, and interspecific attraction of the pheromone components are described and possible uses for the sex pheromone are discussed.

Interspecific attraction to male-produced pheromones of two species ofAmblyomma ticks (Acari: Ixodidae)

Interspecific attraction to male-produced pheromones of two species ofAmblyomma ticks (Acari: Ixodidae)

Intra- and interspecific chemoattraction studies onSchistosoma mansoni, S. japonicum, andS. haematobium in the absence of barriers

Heterosexual intra- and interspecific chemoattraction studies were done in polycarbonate chambers without barriers using 8- to 10-week-oldSchistosoma mansoni from mice, 10-week-oldSchistosoma japonicum from hamsters, and 14-week-oldSchistosoma haematobium from hamsters. Experiments were done for up to 4 hr at 37 °C in a humidified incubator. Single worms were not attracted to decoys or heat-killed worms. Heterosexual intraspecific and interspecific attraction was significant at all time points with all combinations. No clear differences were apparent between intra- and interspecific attraction. Differences between same and differentS. japonicum orS. haematobium pairs were not significant at any time point.

Schistosome behavior in vitro

Schistosome adults attract each other in vitro and the attraction is chemically mediated. InSchistosoma mansoni adults, excretory-secretory (ES) products of worms of one sex attract worms of the opposite sex, and at least the lipophilic fraction is attractive. Intra- and interspecific attraction occurs inSchistosoma mansoni, S. japonicum, andS. haematobium adults. Current knowledge of schistosome behavior in vitro is reviewed.

Cross-attraction of Five Species of Stored-product Phycitinae (Lepidoptera: Pyralidae) in a Wind Tunnel

Sharing of the sex-pheromone communication channel by five species of phycitine moths was measured in a wind tunnel. Overall, male pheromonal response was characterized both by high levels of interspecific attraction and broad overlap in the circadian periods of male response, with attraction to nonconspecific females 75% of that to conspecifics, on average. Cadra cautella (Walker), Plodia interpunctella (Hubner), and Anagasta kuehniella (Zeller) males demonstrated high levels of upwind-flight response throughout an 8-h scotophase. P. interpunctella and A. kuehniella males responded to nonconspecific females at levels that were as high as to conspecifics. Ephestia elutella (H¨bner) males showed the greatest level of response discrimination with the probability of flight to nonconspecific females only 41% of that to conspecific females, although relative importance of pheromonal differences and temporal effects could not be determined. Poor reproductive isolation by long-distance parameters points to a greater reliance on less efficient short-range mechanisms, such as courtship and male pheromones. Significance of these findings to current thought concerning evolution of reproductive isolating mechanisms is considered.

Interspecific attractivity of female sex pheromone components ofPeriplaneta americana

Female sex pheromones ofPeriplaneta americana, P. australasiae, andBlatta orientalis elicit locomotion and upwind orientation in conspecific males. Interspecific attraction between these species was observed in a wind tunnel assay for most species combinations, with the exception ofP. australasiae males not being attracted toP americana females. The role of twoP. americana sex pheromone components, periplanone-A (PA) and periplanone-B (PB) in male attraction was analyzed. PA induced locomotion in males of all three species, with highest threshold concentration inP. americana. PB was effective inP. americana andB. orientalis, but not inP. australasiae. Experiments with mixtures of both components confirmed an inhibitory influence of PB onP. australasiae males when it was added to PA in a ratio of 3∶1 or higher. SinceP. americana andP. australasiae have been found to be syntopous, and their daily mating periods overlap, the female sex pheromone ofP. americana is discussed as an isolating factor between both species.