Development of microsatellite loci from a reference genome for the Neotropical butterfly Heliconius numata and its close relatives

The Neotropical butterfly Heliconius numata (Lepidoptera: Nymphalidae: Heliconiinae) is known for its striking diversity of wing color patterns driven by the Müllerian mimicry of multiple local models and controlled by a single supergene locus. Such fine‐scale variation of traits under strong selection offers a unique opportunity for the study of the ecology and genetics of adaptation. However, little is still known of the population processes driving geographical variation in wing‐pattern phenotypes. We report the characterization of 26 microsatellite markers for the butterfly H. numata, including six located inside the wing color‐pattern supergene region. All markers are polymorphic, with allele numbers ranging from 2 to 21 per locus, an observed heterozygosity of 0.111 to 0.848 and an expected heterozygosity of 0.126 to 0.942. A subset of 18 of these markers was tested on five closely related sympatric Heliconius species with an amplification success ranging from 88% to 94%. The obtained set of microsatellite markers provides a new and useful set of tools to investigate patterns of differentiation and selection in populations of mimetic Heliconius butterflies. Moreover, markers developed within the color‐pattern supergene will facilitate characterization of the association between the genetic architecture and the functional diversity of wing patterns. Finally, the cross‐species amplification success of the described markers extends their utility to also encompass comparative population genetic studies of closely related species within a clade of rapidly diversifying species.     

Sex-linked hybrid sterility in a butterfly

Recent studies, primarily in Drosophila, have greatly advanced our understanding of Haldane's rule, the tendency for hybrid sterility or inviability to affect primarily the heterogametic sex (Haldane 1922). Although dominance theory (Turelli and Orr 1995) has been proposed as a general explanation of Haldane's rule, this remains to be tested in female-heterogametic taxa, such as the Lepidoptera. Here we describe a novel example of Haldane's rule in Heliconius melpomene (Lepidoptera; Nymphalidae). Female F1 offspring are sterile when a male from French Guiana is crossed to a female from Panama, but fertile in the reciprocal cross. Male F1s are fertile in both directions. Similar female F1 sterility occurs in crosses between French Guiana and eastern Colombian populations. Backcrosses and linkage analysis show that sterility results from an interaction between gene(s) on the Z chromosome of the Guiana race with autosomal factors in the Panama genome. Large X (or Z) effects are commonly observed in Drosophila, but to our knowledge have not been previously demonstrated for hybrid sterility in Lepidoptera. Differences in the abundance of male versus female or Z-linked versus autosomal sterility factors cannot be ruled out in our crosses as causes of Haldane's rule. Nonetheless, the demonstration that recessive Z-linked loci cause hybrid sterility in a female heterogametic species supports the contention that dominance theory provides a general explanation of Haldane's rule (Turelli and Orr 2000).     

Effects of an ENSO-related fire on birds of a lowland tropical forest in Sumatra

Comparisons of bird community composition in burned and unburned areas of a lowland tropical rainforest in Sumatra, Indonesia indicated the following during the first 5 years after burning: (1) original burn severity strongly affected bird community composition at both the genus and family levels; (2) bird community composition continued to change progressively away from immediate post-burn composition in medium and severely burned forest as well as adjacent unburned forest; and (3) the degree of impact was both taxon and guild specific, with understory insectivores most detrimentally affected. Although species richness may temporarily increase in burned areas, this study suggests that multiple wildfires will lead to a decline in diversity over a large scale as birds of open fields replace interior forest specialists.     

Does prey dispersion affect frequency-dependent predation by wild birds?

Despite the fact that the vast majority of natural prey items are dispersed in a non-random manner, few studies of frequency-dependent selective predation have explicitly examined the effect of prey dispersion on selectivity. We examined the effect of prey dispersion on the direction and strength of frequency-dependent selection by wild birds feeding on artificial prey (green or brown pastry baits). In a series of four experimental manipulations, we tested for the occurrence of frequency dependence with two different dispersion patterns (random or clumped). Manipulations were carried out at one of two absolute densities (25 prey m⁻² or 100 prey m⁻²), and were repeated at different sites in Southampton, England and Aljarafe, Spain. Our results suggest that prey dispersion has no effect on either frequency-dependent or -independent preferences. One possible explanation for this is that the birds had virtually complete information about prey frequencies at the relatively high densities used and based their preferences on their overall perception of availability. However, we cannot rule out the possibility that dispersion may influence selectivity when prey are cryptic or available at lower absolute densities. Although there was no effect of dispersion, frequency-dependent selection was, overall, significantly anti-apostatic (i.e. rare baits were more preferred than common baits). This anti-apostatic effect was stronger in Southampton than Aljarafe and stronger at 100 prey m⁻² than 25 prey m⁻². The differences in the strength of selection between the two locations was interpreted in terms of (i) whether the avian predators foraged in flocks or not, and (ii) the number of different species present (and, consequently, the variation in preference among individual birds). Received: 21 December 1996 / Accepted: 26 February 1997     

Species traits help explain butterfly habitat use in a tropical forest

1. When species can access all parts of the landscape, species-sorting metacommunity theory predicts that community composition depends on habitat choice and interactions with other species and the environment. These filtering processes can also depend on species' traits.
2. The authors investigated how traits mediate a species-sorting process in determining butterfly community composition in a naturally patchy landscape in the tropical Western Ghats, India. The authors asked, do traits mediate access to certain habitats and does seasonality affect these patterns? The authors surveyed 56 habitat patches in three habitat types: laterite plateau grasslands, ridge grassland, and moist-deciduous forest, in a 65-km² landscape.
3. Non-palatable butterflies showed similar occurrences across seasons and habitats, but palatable butterflies were less commonly encountered in open habitats in the dry season. Polyphagous butterflies occurred infrequently in the dry season in laterite habitats, potentially indicating emigration or diapause patterns are linked to diet breadth.
4. All species were present in all habitats, implying dispersal does not limit access to different habitat patches, consistent with the species-sorting metacommunity concept. Nevertheless, butterfly occurrence was strongly influenced by the interaction of mobility and habitat type with sedentary species occurring less often in low-resource open laterite patches than mobile species.
5. Species sorting is typically regarded as occurring directly through environmental filters, but here the authors suggest that the environmental filter acts through movement limitations. Studies integrating landscape heterogeneity and species characteristics will help us better understand metacommunities and species distributions in nature.

     

Conservation of tropical forest birds in countryside habitats

The pressing need to increase agricultural production often seems at odds with conserving biodiversity. We find that if managed properly, the tropical countryside may provide a substantial opportunity for tropical bird conservation. We detected 144 bird species from 29 families in agricultural areas outside of extensive native forest in southern Costa Rica. The majority of the species detected were observed foraging, often kilometres from extensive native forest. We estimate that 46% of those native to this region (excluding nocturnal species and waterfowl) are utilizing the countryside in some manner. Forecasts of biodiversity change under various land-use scenarios indicate that policies that affect habitat composition could greatly impact the persistence of these species in the countryside. In particular, if tall trees and edge habitats were removed from this landscape, we predict that bird richness in the countryside would decline by approximately 40%.     

Lekking birds in a tropical forest forego sex for migration

Facultative, partially migratory animals provide a contemporary window into the evolution of migration, offering rare opportunities to examine the life-history trade-offs associated with migration. For the first time, to our knowledge, we describe the nature of these trade-offs, using a lek-breeding tropical bird, the white-ruffed manakin (Corapipo altera). Previous evidence indicated that weather drives post-breeding migration to lower elevations bringing condition-related benefits. Using elevation-sensitive stable isotope measurements and more than 1200 h of behavioural observations, we show that male manakins which migrate incur costs of diminished social status and matings with females the following breeding season. Because migratory tendency depends on inter-annual variation in weather, physical costs of displays and breeding prospects the following year, migratory decisions are subject to both natural and sexual selection, with the outcome of such decisions linked to changing climatic regimes.     

Rapid colonization and turnover of birds in a tropical forest treefall gap

Ecological disturbance is an important factor that influences the abundance and distribution of species. Treefalls are a prominent source of disturbance in tropical forests, but robust characterization of community change after treefalls requires baseline data that are often not available. We capitalized on 25 yr of avian mark–recapture data from a lowland moist forest in central Panama to investigate the timescale of colonization and persistence of birds in a newly formed treefall gap. We compared bird species assemblages pre- and post-treefall to explore how the disturbance affected specific foraging guilds and overall assemblage structure (abundance and alpha diversity). We documented rapid colonization (i.e., within five months post-treefall) of the treefall gap by birds. Abundance and alpha diversity increased following the treefall, but both remained relatively constant in a nearby control plot. At the guild level, frugivores spiked in abundance and nectarivores (i.e., hummingbirds) increased in alpha diversity following the treefall. These results are in agreement with those of previous spatial studies of gap dynamics and suggest that certain tropical frugivores and nectarivores have a remarkable ability to rapidly find and exploit preferred resources and microhabitats embedded in a landscape matrix. Assemblage abundance and alpha diversity decreased back to pre-treefall levels within 1 and 4 yr of the treefall, respectively. Thus, even large gaps may provide only ephemeral benefits, highlighting the importance of periodic disturbance for landscape-level persistence of species that use gaps.     

Factors affecting post-dispersal seed survival in a tropical forest

Summary Using the subcanopy tree Faramea occidentalis in Panama, I studied post-dispersal seed survival as a function of five characteristics describing seed locations. By simultaneously considering distance from a conspecific adult, size of the nearest conspecific adult, leaf litter quantity, proximity to logs or tree trunks, and whether or not the seed was in a gap, I was able to analyze the influences of individual factors, as well as the interactions among factors. Seed survival was significantly less in treefall gaps than in the forest understory. Seed survival was also influenced by the size of the nearest adult but in a complex interaction with distance to an adult. For seeds beneath adults, survival decreased with increasing tree size, while for seeds away from adults, survival was independent of the size of the nearest conspecific adult. Distance did not directly affect seed survival, nor did the quantity of leaf litter or the proximity to a tree trunk or a log. In a separate analysis, the relationship between distance and seed survival was consistent over four years, suggesting that single cohort studies may provide accurate insights into the consequences of dispersal. In contrast, the spatial locations of surviving seeds were not consistent over the four-year period. Transects with high survival one year did not tend to have high survival in other years, and the locations of surviving seeds in any particular year could not be predicted from the knowledge of where seeds survived in other years. While survival is patchy within a year, the locations of patches shift from year to year.     

Functional traits determine heterospecific use of risk‐related social information in forest birds of tropical South‐East Asia

In birds and mammals, mobbing calls constitute an important form of social information that can attract numerous sympatric species to localized mobbing aggregations. While such a response is thought to reduce the future predation risk for responding species, there is surprisingly little empirical evidence to support this hypothesis. One way to test the link between predation risk reduction and mobbing attraction involves testing the relationship between species’ attraction to mobbing calls and the functional traits that define their vulnerability to predation risk. Two important traits known to influence prey vulnerability include relative prey‐to‐predator body size ratio and the overlap in space use between predator and prey; in combination, these measures strongly influence prey accessibility, and therefore their vulnerability, to predators. Here, we combine community surveys with behavioral experiments of a diverse bird assemblage in the lowland rainforest of Sumatra to test whether the functional traits of body mass (representing body size) and foraging height (representing space use) can predict species’ attraction to heterospecific mobbing calls. At four forest sites along a gradient of forest degradation, we characterized the resident bird communities using point count and mist‐netting surveys, and determined the species groups attracted to standardized playbacks of mobbing calls produced by five resident bird species of roughly similar body size and foraging height. We found that (1) a large, diverse subcommunity of bird species was attracted to the mobbing calls and (2) responding species (especially the most vigorous respondents) tended to be (a) small (b) mid‐storey foragers (c) with similar trait values as the species producing the mobbing calls. Our findings from the relatively lesser known bird assemblages of tropical Asia add to the growing evidence for the ubiquity of heterospecific information networks in animal communities, and provide empirical support for the long‐standing hypothesis that predation risk reduction is a major benefit of mobbing information networks.     

Dummy birds in artificial nest studies: an experiment with Red-backed Shrike Lanius collurio

Capsule Dummy birds placed on artificial nests increase nest survival, and their use should be considered in future studies of nest predation.     

Nest position and type affect predation rates of artificial avian nests in the tropical lowland forest on Mount Cameroon

Nest predation is the leading cause of reproductive failure in birds and thus it shapes their life history strategies. Intensities of nest predation appear to differ among nest locations and types in both temperate and tropical regions. However, there is limited knowledge of factors influencing susceptibility of avian nests to predation in Africa. The aim of our study was to investigate artificial nest predation rates of different ground and shrub nests located at different heights in the rainforest undergrowth. We placed artificial avian nests within a homogeneous lowland forest interior with sparse forest undergrowth in the Mount Cameroon National Park, Cameroon. We exposed three sets of nests: 50 bare-ground, 50 cup-ground and 50 cup-shrub nests, for 10 d. Predation was higher for cup-ground nests compared to cup-shrub nests, and bare-ground nests were more depredated than cup-ground nests. We concluded that the presence of a cup as well as higher nest position significantly increased probability of artificial nest survival. The results of this study suggest a potential selection pressure on nest type and placement in lowland forest birds for a poorly known tropical region.     

Behaviour and ecology of birds in tropical rain forest canopies

The canopy of rain forests exhibits several distinct features that determine avian adaptations. Light intensity and colour, wind, and temperature are the most important components of the physical environment. Tree architecture poses many challenges for the evolution of avian morphological features, and resource availability varies greatly. The canopy is easily accessible for birds that are equipped to travel over considerable distances. Given these conditions, high behavioural flexibility, and adaptations in behaviour and morphology related to a nomadic life-style, should prevail among canopy birds. The easy access for certain groups of birds also has consequences for the historical processes that shape canopy bird communities. Birds may contribute greatly to forest dynamics and composition, mainly due to their role as seed dispersers. We elaborate on these points with behavioural, morphological, and ecological data collected at our Neotropical study site in southern Venezuela (Surumoni Canopy Crane Project). We discuss how behaviour and morphological features reflect the ecological demands in the canopy. We contrast the specific behavioural and ecological characteristics of canopy birds with those of species found in the other tiers of the rain forest. It is pointed out that much of our knowledge is biased towards the Neotropics, and that better knowledge of the larger canopy species is needed for conservation.     

Community seed rain patterns and a comparison to adult community structure in a West African tropical forest

We examined the seed rain throughout a twelve month period in a lowlandtropical forest in Cameroon, West Africa, 1996–97. Traps (0.5m², n = 216) were erected throughout a 25km² area in 24 randomly placed clusters of nine trapseach. Fruits and seeds that landed in traps were collected every 7–10daysand classified by species and dispersal type. More than 32,000 seeds fromapproximately 200 species fell into the traps, an average of 297 seedsm^–2 yr^–1 Thirty species represent 82%of the total seed rain while an additional 175 species comprise the remaining18%. When we compared the adult community to the seed rain community within thesame plots, we found no apparent correlation between seed rain patterns andadult community structure for this year of study. Furthermore, only 49% of theadult tree community produced and dispersed seed into traps in this year. Morethan 100 species (52%) found in the seed rain represented long-distanceimmigrant seed rain. Seed rain was highly variable at several scales, bothspatially and seasonally, although seeds arrived in traps during eachcollectionperiod. Cluster analyses showed that traps within plots were seldom moresimilarto one another than traps between plots. While 82% of the tree species in thecommunity are thought to be animal dispersed, only 28% of all seeds that fellinto traps had been obviously handled (bitten, chewed, or passed)by animals. Tests for fruit and seed removal by predators or dispersers found5%or less removal rate from traps.     

Provision of supplementary food for wild birds may increase the risk of local nest predation

In countries such as the UK, USA and Australia, approximately half of all households provide supplementary food for wild birds, making this the public's most common form of active engagement with nature. Year‐round supplementary feeding is currently encouraged by major conservation charities in the UK as it is thought to be of benefit to bird conservation. However, little is understood about how the provision of supplementary food affects the behaviour and ecology of target and non‐target species. Given the scale of supplementary feeding, any negative effects may have important implications for conservation. Potential nest predators are abundant in urban areas and some species frequently visit supplementary feeding stations. We assess whether providing supplementary food affects the likelihood of nest predation in the vicinity of the feeder, by acting as a point attractant for potential nest predators. We provided feeding stations (empty, peanut feeder, peanut feeder with guard to exclude potential nest predators) in an area of suburban parkland in the UK and monitored the predation rate of eggs placed in artificial nests located at distances that replicated the size of typical suburban gardens. Nest predators (Magpies Pica pica, Grey Squirrels Sciurus carolinensis) were frequent visitors to filled feeders, and predation caused by Magpies, European Jays Garrulus glandarius and Grey Squirrels was significantly higher when nests were adjacent to filled feeders. The presence of a feeder guard did not significantly reduce nest predation. As supplementary feeding is becoming increasingly common during the breeding season in suburban habitats, we suggest that providing point attractants to nest predators at this time may have previously unconsidered consequences for the breeding success of urban birds.     

Constrained camouflage facilitates the evolution of conspicuous warning coloration

The initial evolution of aposematic and mimetic antipredator signals is thought to be paradoxical because such coloration is expected to increase the risk of predation before reaching a stage when predators associate it effectively with a defense. We propose, however, that constraints associated with the alternative strategy, cryptic coloration, may facilitate the evolution of antipredator signals and thus provide a solution for the apparent paradox. We tested this hypothesis first using an evolutionary simulation to study the effect of a constraint due to habitat heterogeneity, and second using a phylogenetic comparison of the Lepidoptera to investigate the effect of a constraint due to prey motility. In the evolutionary simulation, antipredator warning coloration had an increased probability to invade the prey population when the evolution of camouflage was constrained by visual difference between microhabitats. The comparative study was done between day-active lepidopteran taxa, in which camouflage is constrained by motility, and night-active taxa, which rest during the day and are thus able to rely on camouflage. We compared each of seven phylogenetically independent day-active groups with a closely related nocturnal group and found that antipredator signals have evolved at least once in all the diurnal groups but in none of their nocturnal matches. Both studies lend support to our idea that constraints on crypsis may favor the evolution of antipredator warning signals.     

Seedling interactions in a tropical forest in Panama

Competition is believed to be a central force limiting local diversity and controlling the structure of plant communities. However, it has been proposed that the stressed understory environment limits total understory plant density to such low levels that competitive exclusion cannot be an important factor limiting the local diversity of understory plants. To evaluate the importance of inter-seedling competition, we performed a seedling competition experiment with five shade-tolerant species in a tropical moist forest in Panama. Three-month-old seedlings were transplanted into the forest singly or with their roots intertwined with a single conspecific or heterospecific seedling in all pairwise species combinations. If competition is important, performance (survival, stem height, and number of leaves after one and six years) would be expected to be lowest with a conspecific neighbor and greatest without a neighbor. The experiment was replicated in five 0.24-m² plots at each of 20 sites in tall secondary forest. To test whether seedling performance differed among treatments we fitted linear mixed models (LMM) and generalized linear mixed models (GLMM), treating species identity and microsite (site and plot) as random effects. The five shade-tolerant study species all experienced good establishment with relatively high survival and growth rates. The neighbor treatment consistently affected seedling performance, but the effect was always very small, both in absolute terms and relative to the much stronger species and microsite effects. Seedlings with a conspecific neighbor consistently performed worse than seedlings with a heterospecific neighbor, but having no neighbor generally did not cause superior performance relative to the other treatments. We conclude that direct competitive interactions are relatively unimportant among understory plants in humid tropical forests.     

Experimental evidence for extreme dispersal limitation in tropical forest birds

Movements of organisms between habitat remnants can affect metapopulation structure, community assembly dynamics, gene flow and conservation strategy. In the tropical landscapes that support the majority of global biodiversity and where forest fragmentation is accelerating, there is particular urgency to understand how dispersal across habitats mediates the demography, distribution and differentiation of organisms. By employing unique dispersal challenge experiments coupled with exhaustive inventories of birds in a Panamanian lacustrine archipelago, we show that the ability to fly even short distances (< 100 m) between habitat fragments varies dramatically and consistently among species of forest birds, and that this variation correlates strongly with species' extinction histories and current distributions across the archipelago. This extreme variation in flight capability indicates that species' persistence in isolated forest remnants will be differentially mediated by their respective dispersal abilities, and that corridors connecting such fragments will be essential for the maintenance of avian diversity in fragmented tropical landscapes.