The geographic selection mosaic for squirrels, crossbills and Aleppo pine

The interactions between many species are structured in a geographic mosaic of populations among which selection is divergent. Here we tested the hypothesis that such a geographic selection mosaic arises for common crossbills (Loxia curvirostra) feeding on seeds in the cones of Aleppo pine (Pinus halepensis) because of geographic variation in the occurrence of European red squirrels (Sciurus vulgaris). On the Iberian Peninsula, Sciurus exerted directional selection favouring larger cones with larger scales, which has caused cones there to be larger than in the Balearic Islands where Sciurus are absent. Moreover, cones on the Iberian Peninsula are so large that they are apparently little used by the relatively small-billed crossbills on the Peninsula; selection by Sciurus seems to have made the cones so difficult to feed on that crossbills rely mostly on the seeds of other conifers. Where crossbills are present but Sciurus are absent (Mallorca Island), cones were smaller as a result of relaxation of selection by Sciurus. However, cones on Mallorca had proportionally thicker scales in comparison to where both Sciurus and crossbills are absent (Ibiza Island), presumably as an adaptation against crossbill predation. Here crossbills specialize on Aleppo pine, have relatively large bills and have apparently coevolved in an arms race with Aleppo pine. These results suggest that Sciurus has influenced both the geographic selection mosaics for crossbills and conifers and the adaptive radiation of crossbills in Eurasia much like Tamiasciurus has done in the North America.     

The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.     

When directional selection reduces geographic variation in traits mediating species interactions

Although we often focus on the causes of geographic variation, understanding processes that act to reduce geographic variation is also important. Here, we consider a process whereby adaptive foraging across the landscape and directional selection exerted by a conifer seed predator, the common crossbill (Loxia curvirostra), potentially act to homogenize geographic variation in the defensive traits of its prey. We measured seed predation and phenotypic selection exerted by crossbills on black pine (Pinus nigra) at two sites in the Pindos Mountains, Greece. Seed predation by crossbills was over an order of magnitude higher at the site where cone scale thickness was significantly thinner, which was also the cone trait that was the target of selection at the high predation site. Additional comparisons of selection differentials demonstrate that crossbills exert selection on black pine that is consistent in form across space and time, and increases in strength with increasing seed predation. If predators distribute themselves in relation to the defensive traits of their prey and the strength of selection predators exert is proportional to the amount of predation, then predators may act to homogenize trait variation among populations of their prey in a process analogous to coevolutionary alternation with escalation.     

The geographic selection mosaic for ponderosa pine and crossbills: a tale of two squirrels

Recent research demonstrates how the occurrence of a preemptive competitor (Tamiasciurus) gives rise to a geographic mosaic of coevolution for crossbills (Loxia) and conifers. We extend these studies by examining ponderosa pine (Pinus ponderosa), which produces more variable annual seed crops than the conifers in previous studies and often cooccurs with tree squirrels in the genus Sciurus that are less specialized than Tamiasciurus on conifer seed. We found no evidence of seed defenses evolving in response to selection exerted by S. aberti, which was apparently overwhelmed by selection resulting from inner bark feeding that caused many developing cones to be destroyed. In the absence of S. aberti, defenses directed at crossbills increased, favoring larger-billed crossbills and causing stronger reciprocal selection between crossbills and ponderosa pine. However, crossbill nomadism in response to cone crop fluctuations prevents localized reciprocal adaptation by crossbills. In contrast, evolution in response to S. griseus has incidentally defended cones against crossbills, limiting the geographic range of the interaction between crossbills and ponderosa pine. Our results suggest that annual resource variation does not prevent competitors from shaping selection mosaics, although such fluctuations likely prevent fine-scale geographic differentiation in predators that are nomadic in response to resource variability.     

The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).     

The geographic mosaic in predispersal interactions and selection on Helleborus foetidus (Ranunculaceae)

We examine the hierarchical geographic structure of the interaction between a plant, Helleborus foetidus, and its floral herbivores and pollinators (interactors). Six populations from three distant regions of the Iberian Peninsula were used to examine intra- and inter-regional variation in plant traits, interactors and plant fecundity, and to compare, through selection gradient and path analyses, which traits were under selection, and which interactors were responsible for differential selection. Geographic and temporal congruency in interactor-mediated selection was further tested using a recent analytical approach based on multi-group comparison in Structural Equation Models. Most plant traits, interactors and fecundity differed among regions but not between populations. Similarly, the identity of the traits under selection, the selection gradients (strength and/or the direction of the selection) and the path coefficients (identifying the ecological basis for selection) varied inter- but not intra-regionally. Results show a selection mosaic at the broad scale and, for some traits, a link of differential selection to trait differentiation.     

COEVOLUTION BETWEEN HISPANIOLAN CROSSBILLS AND PINE: DOES MORE TIME ALLOW FOR GREATER PHENOTYPIC ESCALATION AT LOWER LATITUDE?

Crossbills (Aves: Loxia) and several conifers have coevolved in predator-prey arms races over the last 10,000 years. However, the extent to which coevolutionary arms races have contributed to the adaptive radiation of crossbills or to any other adaptive radiation is largely unknown. Here we extend our previous studies of geographically structured coevolution by considering a crossbill-conifer interaction that has persisted for a much longer time period and involves a conifer with more variable annual seed production. We examined geographic variation in the cone and seed traits of two sister species of pines, Pinus occidentalis and P. cubensis, on the islands of Hispaniola and Cuba, respectively. We also compared the Hispaniolan crossbill (Loxia megaplaga) to its sister taxa the North American white-winged crossbill (Loxia leucoptera leucoptera). The Hispaniolan crossbill is endemic to Hispaniola whereas Cuba lacks crossbills. In addition and in contrast to previous studies, the variation in selection experienced by these pines due to crossbills is not confounded by the occurrence of selection by tree squirrels (Tamiasciurus and Sciurus). As predicted if P. occidentalis has evolved defenses in response to selection exerted by crossbills, cones of P. occidentalis have scales that are 53% thicker than those of P. cubensis. Cones of P. occidentalis, but not P. cubensis, also have well-developed spines, a known defense against vertebrate seed predators. Consistent with patterns of divergence seen in crossbills coevolving locally with other conifers, the Hispaniolan crossbill has evolved a bill that is 25% deeper than the white-winged crossbill. Together with phylogenetic analyses, our results suggest that predator-prey coevolution between Hispaniolan crossbills and P. occidentalis over approximately 600,000 years has caused substantial morphological evolution in both the crossbill and pine. This also indicates that cone crop fluctuations do not prevent crossbills and conifers from coevolving. Furthermore, because the traits at the phenotypic interface of the interaction apparently remain the same over at least several hundred thousand years, divergence as a result of coevolution is greater at lower latitude where crossbill-conifer interactions have been less interrupted by Pleistocene events.     

Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic

Repeated patterns among biological communities suggest similar evolutionary and ecological forces are acting on the communities. Conversely, the lack of such patterns suggests that similar forces are absent or additional ones are present. Coevolution between a seed predator, the red crossbill (Loxia curvirostra complex), and lodgepole pine (Pinus contorta var. latifolia) exemplifies the ecological and evolutionary predictions for coevolving systems. In the absence of another seed predator and preemptive competitor (pine squirrels Tamiasciurus hudsonicus), natural selection by crossbills results in the evolution of larger cones with thicker distal scales, while relaxation of selection by squirrels results in the evolution of cones with more seeds and a greater ratio of seed mass to cone mass. However, in one range, the Little Rocky Mountains, distal scale thickness has diverged as expected but cone size has not. In these mountains seed predation by lodgepole pine cone borer moths (Eucosma recissoriana) was about 10 times greater than in other ranges lacking squirrels. We quantified moth predation and cone traits and found that moths select for smaller cones with fewer seeds. Thus, selection by moths in the Little Rocky Mountains counters both selection by crossbills for large cone size and relaxation of selection by squirrels favoring more seeds per cone and accounts for the relatively small and few-seeded cones in these mountains. It is also apparent that selection by crossbills changes seed defenses in a manner that favors seed predation by moths, whereas selection by squirrels likely reduces such predation. These results demonstrate the importance of considering the evolutionary consequences of community context in locally evolved (coevolved) traits and interactions.     

Influence of voltine ecotype and geographic distance on genetic and haplotype variation in the Asian corn borer

Diapause is an adaptive dormancy strategy by which arthropods endure extended periods of adverse climatic conditions. Seasonal variation in larval diapause initiation and duration in Ostrinia furnacalis may influence adult mating generation number (voltinism) across different local environments. The degree to which voltine ecotype, geographic distance, or other ecological factors influence O. furnacalis population genetic structure remains uncertain. Genetic differentiation was estimated between voltine ecotypes collected from 8 locations. Mitochondrial haplotypes were significantly different between historically allopatric univoltine and bivoltine locations, but confounded by a strong correlation with geographic distance. In contrast, single nucleotide polymorphism (SNP) genotypes show low but significant levels of variation and a lack of influence of geographic distance between allopatric voltine locations. Regardless, 11 of 257 SNP loci were predicted to be under selection, suggesting population genetic homogenization except at loci proximal to factors putatively under selection. These findings provide evidence of haplotype divergent voltine ecotypes that may be maintained in allopatric and sympatric areas despite relatively high rates of nuclear gene flow, yet influence of voltinism on maintenance of observed haplotype divergence remains unresolved.     

A geographic mosaic of trophic interactions and selection: trees, aphids and birds

Genetic variation in plants is known to influence arthropod assemblages and species interactions. However, these influences may be contingent upon local environmental conditions. Here, we examine how plant genotype-based trophic interactions and patterns of natural selection change across environments. Studying the cottonwood tree, Populus angustifolia, the galling aphid, Pemphigus betae and its avian predators, we used three common gardens across an environmental gradient to examine the effects of plant genotype on gall abundance, gall size, aphid fecundity and predation rate on galls. Three patterns emerged: (i) plant genotype explained variation in gall abundance and predation, (ii) G×E explained variation in aphid fecundity, and environment explained variation in gall abundance and gall size, (iii) natural selection on gall size changed from directional to stabilizing across environments.     

A role for habitat area in the geographic mosaic of coevolution between red crossbills and lodgepole pine

Understanding how resource abundance limits adaptive evolution and influences species interactions is an important step towards developing insight into the role of microevolutionary processes in establishing macroevolutionary patterns. We examined how variation in resource abundance (forest area of lodgepole pine Pinus contorta ssp. latifolia) influenced patterns of co-adaptation and coevolution between red crossbill (Loxia curvirostra complex) and lodgepole pine populations. First, we found that crossbill abundance increased logarithmically as forest area increased in mountain ranges lacking a preemptive competitor (pine squirrels Tamiasciurus hudsonicus). Second, seed defences against predation by crossbills increased with increases in crossbill density, suggesting that seed defences have likely evolved in proportion to the intensity of selection that crossbills exert. Third, the average bill size of crossbill populations increased with increasing seed defences, which implies that crossbill offenses increased with increases in seed defences. The large bill size on the largest range is the result of coevolution with lodgepole pine with this crossbill population perhaps speciating. Local adaptation of crossbill populations on smaller ranges, however, is more likely the result of resident crossbills representing a subset of the potential colonists (phenotypic sorting) than of local evolution. In the smallest range, migration and possibly more frequent extinction likely impede local adaptation and may result in maladaptation.     

On the relative importance of ecology and geographic isolation as drivers for differentiation of call types of red crossbill Loxia curvirostra in the Palearctic

Efforts to understand the process of speciation have been central to the research of biologists since the origin of evolutionary biology as a discipline. While it is well established that geographic isolation has played a key role in many speciation events, particularly in birds, there is ongoing debate about how frequent speciation is in the partial or complete absence of geographical isolation. In the red crossbill Loxia curvirostra, good arguments do exist for sympatric speciation processes. In this species, several classes of calls are clustered in distinct groups, so-called ‘call types', which mate assortatively. Often, several call types can be found at a single site, breeding and feeding next to each other. It has been hypothesized that red crossbill call types evolved by specialising in extracting seeds from cones of different conifer species. Alternatively, call types might have evolved in temporal geographic isolation. Within Europe, little is known about the distribution of the various call types and preferences for distinct food resources. In this study, we analysed the temporal and spatial occurrence of red crossbill call types in the Palearctic, investigated potential reasons for call-type composition at a site, and compared the occurrence of call types with the fructification of conifers. Call-type composition changed with site and season but hardly with conifer species. With our data, we could localise range areas of twelve different call types, which cannot be explained by conifer species occurrence. Therefore, we suggest that call types evolved in parapatry in most of the northern Palearctic region, and, although contradictory results exist from Iberia, we argue that differentiation might be driven by the same drivers there as well. Additionally, we discuss the potential influence of anthropogenic changes of forest composition and distribution on call types, which offers a unique possibility for future studies.     

The spatial analysis of biological interactions: morphological variation responding to the co‐occurrence of competitors and resources

By sharing geographic space, species are forced to interact with one another and the contribution of this process to evolutionary and ecological patterns of individual species is not fully understood. At the same time, species turnover makes that species composition varies from one area to another, so the analysis of biological interaction cannot be uncoupled from the spatial context. This is particularly important for clades that show high degree of specialization such as hummingbirds, where any variation in biotic pressures might lead to changes in morphology. Here, we describe the influence of biological interactions on the morphology of Hylocharis leucotis by simultaneously considering potential competition and diet resources. We characterized the extent of local potential competition and local available floral resources by correlating two measurements of hummingbird diversity, floral resources and the size of morphological space of H. leucotis along its geographic distribution. We found that H. leucotis shows an important morphological variability across its range and two groups can be recognized. Surprisingly, morphological variation is not always linked to local hummingbird richness or the phylogenetic similarity of. Only in the southern part of its distribution, H. leucotis is morphologically more variable in those communities where it coexist with closely related hummingbird species. We also found that morphological variation in H. leucotis is independent from the availability of floral resources. Our results suggest that abiotic factors might be responsible for morphological differences across populations in Hylocharis leucotis being biological interactions of minor importance.     

The effect of the taxon and geographic range size of host eucalypt species on the species richness of gall-forming insects

Abstract This field study was designed to test whether the taxonomic group and geographic range size of a host plant species, usually found to influence insect species richness in other parts of the world, affected the number of gall species on Australian eucalypts. We assessed the local and regional species richness of gall-forming insects on five pairs of closely related eucalypt species. One pair belonged to the subgenus Corymbia, one to Monocalyptus, and three to different sections of Symphyomyrtus. Each eucalypt pair comprised a large and a small geographic range species. Species pairs were from coastal or inland regions of eastern Australia. The total number of gall species on eucalypt species with large geographic ranges was greater than on eucalypt species with small ranges, but only after the strong effect of eucalypt taxonomic grouping was taken into account. There was no relationship between the geographic range size of eucalypt species and the size of local assemblages of gall species, but the variation in insect species composition between local sites was higher on eucalypt species with large ranges than on those with small ranges. Thus the effect of host plant range size on insect species richness was due to greater differentiation between more widespread locations, rather than to greater local species richness. This study confirms the role of the geographic range size of a host plant in the determination of insect species richness and provides evidence for the importance of the taxon of a host plant.     

The performance of range maps and species distribution models representing the geographic variation of species richness at different resolutions

Aim The method used to generate hypotheses about species distributions, in addition to spatial scale, may affect the biodiversity patterns that are then observed. We compared the performance of range maps and MaxEnt species distribution models at different spatial resolutions by examining the degree of similarity between predicted species richness and composition against observed values from well‐surveyed cells (WSCs). Location Mexico. Methods We estimated amphibian richness distributions at five spatial resolutions (from 0.083° to 2°) by overlaying 370 individual range maps or MaxEnt predictions, comparing the similarity of the spatial patterns and correlating predicted values with the observed values for WSCs. Additionally, we looked at species composition and assessed commission and omission errors associated with each method. Results MaxEnt predictions reveal greater geographic differences in richness between species rich and species poor regions than the range maps did at the five resolutions assessed. Correlations between species richness values estimated by either of the two procedures and the observed values from the WSCs increased with decreasing resolution. The slopes of the regressions between the predicted and observed values indicate that MaxEnt overpredicts observed species richness at all of the resolutions used, while range maps underpredict them, except at the finest resolution. Prediction errors did not vary significantly between methods at any resolution and tended to decrease with decreasing resolution. The accuracy of both procedures was clearly different when commission and omission errors were examined separately. Main conclusions Despite the congruent increase in the geographic richness patterns obtained from both procedures as resolution decreases, the maps created with these methods cannot be used interchangeably because of notable differences in the species compositions they report.     

The relationship between geographic area and the latitudinal gradient in species richness in New World birds

One hypothesis for the latitudinal gradient in species richness observed in most animal taxa is that the richness of a region is determined by its geographic area. However, the relationship between geographic area and species richness across regions is generally weak. It has been suggested that this is because species from the tropics spill out of this region of high richness, artificially inflating the richness of other regions. This generates the interesting prediction that the area and richness of extra-tropical regions should be more strongly correlated if tropical species are excluded. We test this prediction using the avifauna of the New World. We find that there is indeed a relationship between the land area and species richness of a region once tropical species are excluded. This relationship is independent of the latitude and productivity of regions. Both latitude and productivity can explain variance in richness unexplained by land area. There is no relationship between land area and species richness if tropical species are not excluded from the analysis, suggesting that tropical species do indeed mask the relationship between richness and area. We conclude that our results generally support the geographic area hypothesis, although tests of its other predictions and on other land masses are required.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.     

Phenotypic variation of an alien species in a new environment: the body size and diet of American mink over time and at local and continental scales

Introduced species must adapt their ecology, behaviour, and morphological traits to new conditions. The successful introduction and invasive potential of a species are related to its levels of phenotypic plasticity and genetic polymorphism. We analysed changes in the body mass and length of American mink (Neovison vison) since its introduction into the Warta Mouth National Park, western Poland, in relation to diet composition and colonization progress from 1996 to 2004. Mink body mass decreased significantly during the period of population establishment within the study area, with an average decrease of 13% from 1.36 to 1.18 kg in males and of 16% from 0.83 to 0.70 kg in females. Diet composition varied seasonally and between consecutive years. The main prey items were mammals and fish in the cold season and birds and fish in the warm season. During the study period the proportion of mammals preyed upon increased in the cold season and decreased in the warm season. The proportion of birds preyed upon decreased over the study period, whereas the proportion of fish increased. Following introduction, the strictly aquatic portion of mink diet (fish and frogs) increased over time, whereas the proportion of large prey (large birds, muskrats, and water voles) decreased. The average yearly proportion of large prey and average‐sized prey in the mink diet was significantly correlated with the mean body masses of males and females. Biogeographical variation in the body mass and length of mink was best explained by the percentage of large prey in the mink diet in both sexes, and by latitude for females. Together these results demonstrate that American mink rapidly changed their body mass in relation to local conditions. This phenotypic variability may be underpinned by phenotypic plasticity and/or by adaptation of quantitative genetic variation. The potential to rapidly change phenotypic variation in this manner is an important factor determining the negative ecological impacts of invasive species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 681–693.     

The evolution of trade-offs: geographic variation in call duration and flight ability in the sand cricket, Gryllus firmus

Quantitative genetic theory assumes that trade-offs are best represented by bivariate normal distributions. This theory predicts that selection will shift the trade-off function itself and not just move the mean trait values along a fixed trade-off line, as is generally assumed in optimality models. As a consequence, quantitative genetic theory predicts that the trade-off function will vary among populations in which at least one of the component traits itself varies. This prediction is tested using the trade-off between call duration and flight capability, as indexed by the mass of the dorsolateral flight muscles, in the macropterous morph of the sand cricket. We use four different populations of crickets that vary in the proportion of macropterous males (Lab = 33%, Florida = 29%, Bermuda = 72%, South Carolina = 80%). We find, as predicted, that there is significant variation in the intercept of the trade-off function but not the slope, supporting the hypothesis that trade-off functions are better represented as bivariate normal distributions rather than single lines. We also test the prediction from a quantitative genetical model of the evolution of wing dimorphism that the mean call duration of macropterous males will increase with the percentage of macropterous males in the population. This prediction is also supported. Finally, we estimate the probability of a macropterous male attracting a female, P, as a function of the relative time spent calling (P = time spent calling by macropterous male/(total time spent calling by both micropterous and macropterous male). We find that in the Lab and Florida populations the probability of a female selecting the macropterous male is equal to P, indicating that preference is due simply to relative call duration. But in the Bermuda and South Carolina populations the probability of a female selecting a macropterous male is less than P, indicating a preference for the micropterous male even after differences in call duration are accounted for.