Genes and song : genetic and social connections in fragmented habitat in a woodland bird with limited dispersal

Understanding the processes leading to population declines in fragmented landscapes is essential for successful conservation management. However, isolating the influence of disparate processes, and dispersal in particular, is challenging. The Grey Shrike-thrush, Colluricincla harmonica, is a sedentary woodland-dependent songbird, with learned vocalizations whose incidence in suitable habitat patches falls disproportionally with decline in tree cover in the landscape. Although it has been suggested that gaps in tree cover might act as barriers to its dispersal, the species remains in many remnants of native vegetation in agricultural landscapes, suggesting that it may have responded to habitat removal and fragmentation by maintaining or even increasing dispersal distances. We quantified population connectivity of the Grey Shrike-thrush in a system fragmented over more than 120 years using genetic (microsatellites) and acoustic (song types) data. First, we tested for population genetic and acoustic structure at regional and local scales in search of barriers to dispersal or gene flow and signals of local spatial structuring indicative of restricted dispersal or localized acoustic similarity. Then we tested for effects of habitat loss and fragmentation on genetic and acoustic connectivity by fitting alternative models of mobility (isolation-by-distance [the null model] and reduced and increased movement models) across treeless vs. treed areas. Birds within 5 km of each other had more similar genotypes and song types than those farther away, suggesting that dispersal and song matching are limited in the region. Despite restricted dispersal detected for females (but not males), populations appeared to be connected by gene flow and displayed some cultural (acoustic) connectivity across the region. Fragmentation did not appear to impact greatly the dispersal of the Grey Shrike-thrush: none of the mobility models fit the genetic distances of males, whereas for females, an isolation-by-distance model could not be rejected in favor of the models of reduced or increased movement through treeless gaps. However, dissimilarities of the song types were more consistent with the model of reduced cultural connectivity through treeless areas, suggesting that fragmentation impedes song type sharing in the Grey Shrike-thrush. Our paper demonstrates that habitat fragmentation hinders important population processes in an Australian woodland bird even though its dispersal is not detectably impacted.

How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species

1. How species reach and persist in isolated habitats remains an open question in many cases, especially for rapidly spreading invasive species. This is particularly true for temporary freshwater ponds, which can be remote and may dry out annually, but may still harbour high biodiversity. Persistence in such habitats depends on recurrent colonisation or species survival capacity, and ponds therefore provide an ideal system to investigate dispersal and connectivity. 2. Here, we test the hypothesis that the wide distributions and invasive potential of aquatic snails is due to their ability to exploit several dispersal vectors in different landscapes. We explored the population structure of Physa acuta (recent synonyms: Haitia acuta, Physella acuta, Pulmonata: Gastropoda), an invasive aquatic snail originating from North America, but established in temporary ponds in Doñana National Park, southern Spain. In this area, snails face land barriers when attempting to colonise other suitable habitat. 3. Genetic analyses using six microsatellite loci from 271 snails in 21 sites indicated that (i) geographically and hydrologically isolated snail populations in the park were genetically similar to a large snail population in rice fields more than 15 km away; (ii) these isolated ponds showed an isolation-by-distance pattern. This pattern broke down, however, for those ponds visited frequently by large mammals such as cattle, deer and wild boar; (iii) snail populations were panmictic in flooded and hydrologically connected rice fields. 4. These results support the notion that aquatic snails disperse readily by direct water connections in the flooded rice fields, can be carried by waterbirds flying between the rice fields and the park and may disperse between ponds within the park by attaching to large mammals. 5. The potential for aquatic snails such as Physa acuta to exploit several dispersal vectors may contribute to their wide distribution on various continents and their success as invasive species. We suggest that the interaction between different dispersal vectors, their relation to specific habitats and consequences at different geographic scales should be considered both when attempting to control invasive freshwater species and when protecting endangered species.

Gut travellers : internal dispersal of aquatic organisms by waterfowl

Aim: Patterns of high biodiversity among less mobile organisms throughout isolated locations suggest that passive dispersal importantly contributes to biodiversity. We examined the contribution of waterbirds to the dispersal of plant seeds and macroinvert

Subfossils of extinct and extant species of Simuliidae (Diptera) from Austral and Cook Islands (Polynesia): anthropogenic extirpation of an aquatic insect?

Subfossil head capsules of Simuliidae larvae have been recovered from swamps on Tubuai and Raivavae of the Austral Islands, and Atiu and Mangaia of the southern Cook Islands. For Tubuai and Raivavae it is likely that the simuliids are extinct, but a single simuliid species is extant on nearby Rurutu. For Atiu and Mangaia, extant simuliids have not been reported, but are known on Rarotonga. Well-preserved head capsules indicate that the Cook Islands subfossils are those of Simulium (Inseliellum) teruamanga Craig and Craig, 1986. For the Austral Islands, the simuliid from Tubuai is considered a variant of Simulium (Inseliellum) rurutuense Craig and Joy, 2000. That from Raivavae is morphologically distinct and is described here as a new species, Simulium (Inseliellum) raivavaense Craig and Porch. Humans arrived in Eastern Polynesia ca. 1,000 years ago resulting in the widespread destruction of lowland forest and conversion of wetlands to agriculture with implied consequences for the indigenous biota of these habitats. Here we consider that one such result was loss of freshwater aquatic biodiversity.

Satellite tracking large numbers of individuals to infer population level dispersal and core areas for the protection of an endangered species

Aim: Tracking the dispersal patterns and habitat use of migratory species is necessary to delineate optimal areas for protection, with large sample sizes being more representative of the population. Here, we examine the dispersal patterns of a key Mediterranean loggerhead turtle (Caretta caretta) breeding population to identify priority foraging sites for protection. Location: Zakynthos Island, Greece and the wider Mediterranean. Method: We examined the dispersal patterns and foraging sites of 75 adult loggerheads (n = 38 males and 37 females) tracked from the breeding area of Zakynthos Island (Greece) from 2004 to 2011. We then combined our data with published sea turtle literature to identify key foraging sites for protection. Results: While both males and females exhibited similar dispersal patterns, about 25% males remained < 100 km of Zakynthos, whereas all females (except one) migrated > 200 km. Integration of our data with the wider literature isolated 10 core sites in proximity to existing protected areas, which could potentially protect 64% of the Zakynthos population, while five sites support individuals from at least 10 other loggerhead breeding populations. Main conclusions: Due to the widespread availability of neritic foraging grounds across the Mediterranean, sea turtles from Zakynthos exhibit disparate dispersal patterns. However, protecting only a few objectively defined important sites can encompass a large proportion of the foraging areas used and hence have considerable conservation benefit.

Sex differences in insect immune function : a consequence of diet choice?

Males often have reduced immune function compared to females but the proximate mechanisms underlying this taxonomically widespread pattern are unclear. Because immune function is resource-dependent and sexes may have different nutritional requirements, we hypothesized that sexual dimorphism in immune function may arise from differential nutrient intake (acquisition hypothesis). To test this hypothesis, we examined patterns of phenoloxidase (PO) activity in relation to nutrient consumption in Queensland fruit flies (Q-flies). In the first experiment, flies were allowed to choose their preferred nutrient intake. Compared with males, female Q-flies had higher PO activity, consumed more calories, and preferred a higher protein:carbohydrate (P:C) diet, suggesting that differential acquisition could explain sex differences. In the second experiment, we restricted flies to one of 12 diets varying in protein and carbohydrate concentrations and mapped PO activity for each sex onto a nutritional landscape. Counter to our hypothesis, females had higher PO activity than males at any given level of nutrient intake. Both carbohydrate and protein intake affected PO activity in females but only protein affected PO activity in males. Our results indicate that sex differences in Q-fly immune function are not solely explained by sex differences in nutrient intake, although nutrition does contribute to the magnitude of these sex differences.

Lost at sea: genetic, oceanographic and meteorological evidence for storm-forced dispersal

For many species, there is broad-scale dispersal of juvenile stages and/or long-distance migration of individuals and hence the processes that drive these various wide-ranging movements have important life-history consequences. Sea turtles are one of these paradigmatic long-distance travellers, with hatchlings thought to be dispersed by ocean currents and adults often shuttling between distant breeding and foraging grounds. Here, we use multi-disciplinary oceanographic, atmospheric and genetic mixed stock analyses to show that juvenile turtles are encountered ‘downstream’ at sites predicted by currents. However, in some cases, unusual occurrences of juveniles are more readily explained by storm events and we show that juvenile turtles may be displaced thousands of kilometres from their expected dispersal based on prevailing ocean currents. As such, storms may be a route by which unexpected areas are encountered by juveniles which may in turn shape adult migrations. Increased stormy weather predicted under climate change scenarios suggests an increasing role of storms in dispersal of sea turtles and other marine groups with life-stages near the ocean surface.

Seasonal- and sex-specific correlations between dispersal and exploratory behaviour in the great tit

While the importance of personality in explaining individual dispersal strategies is increasingly recognized, limited information is still available on how patterns of personality-dependent dispersal may develop, hampering our understanding of the ecological significance of behavioural dispersal syndromes. Here, we examine the relative importance of personality at different stages of dispersal in the great tit, by analysing the sex-specific relationship between exploratory behaviour (EB; quantified in a novel environment) and dispersal distances in different seasons over the course of the first year of life (summer, autumn, winter, and until the first breeding attempt). In females, we found that EB was an important predictor of dispersal distances in summer and autumn, but only a weak to moderate correlation remained for females captured in winter or for natal dispersal distances based on first breeding records. We obtained a contrasting pattern at the population level, whereby male (but not female) immigrants captured in summer and autumn had higher EB scores than locally born birds, while this was not the case in birds captured in winter and those recruited as breeders into the population. In addition to providing further evidence for the existence of a behaviour dispersal syndrome in birds, our results show that correlations between EB and dispersal appear strongest at the early stages of the dispersal process, rather than being developed gradually. These findings show the importance of analysing the effect of phenotypic attributes on dispersal across different stages of the dispersal phenomenon and in each sex separately.

Population genetic structure, gene flow and sex-biased dispersal in frillneck lizards (Chlamydosaurus kingii)

By using both mitochondrial and nuclear multiloci markers, we explored population genetic structure, gene flow and sex-specific dispersal of frillneck lizards (Chlamydosaurus kingii) sampled at three locations, separated by 10 to 50 km, in a homogenous savannah woodland in tropical Australia. Apart from a recombinant lizard, the mitochondrial analyses revealed two nonoverlapping haplotypes/populations, while the nuclear markers showed that the frillneck lizards represented three separate clusters/populations. Due to the small population size of the mtDNA, fixation may occur via founder effects and/or drift. We therefore suggest that either of these two processes, or a combination of the two, are the most likely causes of the discordant results obtained from the mitochondrial and the nuclear markers. In contrast to the nonoverlapping mitochondrial haplotypes, in 12 out of 74 lizards, mixed nuclear genotypes were observed, hence revealing a limited nuclear gene flow. Although gene flow should ultimately result in a blending of the populations, we propose that the distinct nuclear population structure is maintained by frequent fires resulting in local bottlenecks, and concomitant spatial separation of the frillneck lizard populations. Limited mark-recapture data and the difference in distribution of the mitochondrial and nuclear markers suggest that the mixed nuclear genotypes were caused by juvenile male-biased dispersal.

Simplification of arboreal marsupial assemblages in response to increasing urbanization

Arboreal marsupials play an essential role in ecosystem function including regulating insect and plant populations, facilitating pollen and seed dispersal and acting as a prey source for higher-order carnivores in Australian environments. Primarily, research has focused on their biology, ecology and response to disturbance in forested and urban environments. We used presence-only species distribution modelling to understand the relationship between occurrences of arboreal marsupials and eco-geographical variables, and to infer habitat suitability across an urban gradient. We used post-proportional analysis to determine whether increasing urbanization affected potential habitat for arboreal marsupials. The key eco-geographical variables that influenced disturbance intolerant species and those with moderate tolerance to disturbance were natural features such as tree cover and proximity to rivers and to riparian vegetation, whereas variables for disturbance tolerant species were anthropogenic-based (e.g., road density) but also included some natural characteristics such as proximity to riparian vegetation, elevation and tree cover. Arboreal marsupial diversity was subject to substantial change along the gradient, with potential habitat for disturbance-tolerant marsupials distributed across the complete gradient and potential habitat for less tolerant species being restricted to the natural portion of the gradient. This resulted in highly-urbanized environments being inhabited by a few generalist arboreal marsupial species. Increasing urbanization therefore leads to functional simplification of arboreal marsupial assemblages, thus impacting on the ecosystem services they provide.

Insights into the evolution of a cryptic radiation of bats: dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae)

The past decade has seen a proliferation of new species of Miniopterus bats (family Miniopteridae) recognized from Madagascar and the neighboring Comoros archipelago. The interspecific relationships of these taxa, their colonization history, and the evolution of this presumed adaptive radiation have not been sufficiently explored. Using the mitochondrial cytochrome-b gene, we present a phylogeny of the Malagasy members of this widespread Old World genus, based on 218 sequences, of which 82 are new and 136 derived from previous studies. Phylogenetic analyses recovered 18 clades, which divide into five primary lineages: (1) M. griveaudi; (2) M. mahafaliensis, M. sororculus and X3; (3) M. majori, M. gleni and M. griffithsi; (4) M. brachytragos; M. aelleniA, and M. aelleniB; and (5) M. manavi and M. petersoni recovered as sister species, which were in turn linked to a group comprising M. egeri and five genetically distinct populations referred to herein as P3, P4, P5, P6 and P7. Beast analysis indicated that the initial divergence within the Malagasy Miniopterus radiation took place 4.5 Myr; most species diverged between 4 and 2.5 Myr, and a secondary period was between 1.25 and 1 Myr. DNA K2P-distances between recognized taxa ranged from 12.9% to 2.5% and intraspecific variation was less than 1.8%. Of the 18 identified clades, Latin binomials are only associated with 11, which indicates much greater differentiation than currently recognized for Malagasy Miniopterus. These data are placed in a context of the dispersal history of this genus on the island and patterns of ecological diversity.

Evaluating irradiation dose for sterility induction and quality control of mass-produced fruit fly Bactrocera tryoni (Diptera : Tephritidae)

The sterile insect technique has been routinely used to eradicate fruit fly Bactrocera tryoni (Froggatt) incursions. This study considers whether fly quality in a mass-rearing facility can be improved by reducing irradiation doses, without sacrificing reproductive sterility. Pupae were exposed to one of five target irradiation dose ranges: 0, 40-45, 50-55, 60-65, and 70-75 Gy. Pupae were then assessed using routine quality control measures: flight ability, sex ratio, longevity under nutritional stress, emergence, and reproductive sterility. Irradiation did not have a significant effect on flight ability or sex ratio tests. Longevity under nutritional stress was significantly increased at 70-75 Gy, but no other doses differed from 0 Gy. Emergence was slightly reduced in the 50-55, 60-65, and 70-75 Gy treatments, but 40-45 Gy treatments did not differ from 0 Gy, though confounding temporal factors complicate interpretation. Reproductive sterility remained acceptable (> 99.5%) for all doses--40-45 Gy (99.78%), 50-55 Gy (100%), 60-65 Gy (100%), and 70-75 Gy (99.99%). We recommend that B. tryoni used in sterile insect technique releases be irradiated at a target dose of 50-55 Gy, providing improved quality and undiminished sterility in comparison with the current 70-75 Gy standard while also providing a substantial buffer against risk of under dosing.