David T. Bilton

Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization

There is a general perception that central and northern Europe were colonized by range expansion from Mediterranean refugia at the end of the last glaciation. Data from various species support this scenario, but we question its universality. Our mitochondrial DNA studies on three widespread species of small mammal suggest that colonization may have occurred from glacial refugia in central Europe–western Asia. The haplotypes on the Mediterranean peninsulae are distinctive from those found elsewhere. Rather than contributing to the postglacial colonization of Europe, Mediterranean populations of widespread small mammals may represent long–term isolates undergoing allopatric speciation. This could explain the high endemism of small mammals associated with the Mediterranean peninsulae.

The Effect of Geographical Scale of Sampling on DNA Barcoding

Abstract Eight years after DNA barcoding was formally proposed on a large scale, CO1 sequences are rapidly accumulating from around the world. While studies to date have mostly targeted local or regional species assemblages, the recent launch of the global iBOL project (International Barcode of Life), highlights the need to understand the effects of geographical scale on Barcodings goals. Sampling has been central in the debate on DNA Barcoding, but the effect of the geographical scale of sampling has not yet been thoroughly and explicitly tested with empirical data. Here, we present a CO1 data set of aquatic predaceous diving beetles of the tribe Agabini, sampled throughout Europe, and use it to investigate how the geographic scale of sampling affects 1) the estimated intraspecific variation of species, 2) the genetic distance to the most closely related heterospecific, 3) the ratio of intraspecific and interspecific variation, 4) the frequency of taxonomically recognized species found to be monophyletic, and 5) query identification performance based on 6 different species assignment methods. Intraspecific variation was significantly correlated with the geographical scale of sampling (R-square = 0.7), and more than half of the species with 10 or more sampled individuals (N = 29) showed higher intraspecific variation than 1% sequence divergence. In contrast, the distance to the closest heterospecific showed a significant decrease with increasing geographical scale of sampling. The average genetic distance dropped from > 7% for samples within 1 km, to < 3.5% for samples up to > 6000 km apart. Over a third of the species were not monophyletic, and the proportion increased through locally, nationally, regionally, and continentally restricted subsets of the data. The success of identifying queries decreased with increasing spatial scale of sampling; liberal methods declined from 100% to around 90%, whereas strict methods dropped to below 50% at continental scales. The proportion of query identifications considered uncertain (more than one species < 1% distance from query) escalated from zero at local, to 50% at continental scale. Finally, by resampling the most widely sampled species we show that even if samples are collected to maximize the geographical coverage, up to 70 individuals are required to sample 95% of intraspecific variation. The results show that the geographical scale of sampling has a critical impact on the global application of DNA barcoding. Scale-effects result from the relative importance of different processes determining the composition of regional species assemblages (dispersal and ecological assembly) and global clades (demography, speciation, and extinction). The incorporation of geographical information, where available, will be required to obtain identification rates at global scales equivalent to those in regional barcoding studies. Our result hence provides an impetus for both smarter barcoding tools and sprouting national barcoding initiatives—smaller geographical scales deliver higher accuracy.

Macrophysiology: A Conceptual Reunification

Widespread recognition of the importance of biological studies at large spatial and temporal scales, particularly in the face of many of the most pressing issues facing humanity, has fueled the argument that there is a need to reinvigorate such studies in physiological ecology through the establishment of a macrophysiology. Following a period when the fields of ecology and physiological ecology had been regarded as largely synonymous, studies of this kind were relatively commonplace in the first half of the twentieth century. However, such large‐scale work subsequently became rather scarce as physiological studies concentrated on the biochemical and molecular mechanisms underlying the capacities and tolerances of species. In some sense, macrophysiology is thus an attempt at a conceptual reunification. In this article, we provide a conceptual framework for the continued development of macrophysiology. We subdivide this framework into three major components: the establishment of macrophysiological patterns, determining the form of those patterns (the very general ways in which they are shaped), and understanding the mechanisms that give rise to them. We suggest ways in which each of these components could be developed usefully.

Oxygen supply in aquatic ectotherms: Partial pressure and solubility together explain biodiversity and size patterns

Aquatic ectotherms face the continuous challenge of capturing sufficient oxygen from their environment as the diffusion rate of oxygen in water is 3 x 10(5) times lower than in air. Despite the recognized importance of oxygen in shaping aquatic communities, consensus on what drives environmental oxygen availability is lacking. Physiologists emphasize oxygen partial pressure, while ecologists emphasize oxygen solubility, traditionally expressing oxygen in terms of concentrations. To resolve the question of whether partial pressure or solubility limits oxygen supply in nature, we return to first principles and derive an index of oxygen supply from Ficks classic first law of diffusion. This oxygen supply index (OSI) incorporates both partial pressure and solubility. Our OSI successfully explains published patterns in body size and species across environmental clines linked to differences in oxygen partial pressure (altitude, organic pollution) or oxygen solubility (temperature and salinity). Moreover, the OSI was more accurately and consistently related to these ecological patterns than other measures of oxygen (oxygen saturation, dissolved oxygen concentration, biochemical oxygen demand concentrations) and similarly outperformed temperature and altitude, which covaried with these environmental clines. Intriguingly, by incorporating gas diffusion rates, it becomes clear that actually more oxygen is available to an organism in warmer habitats where lower oxygen concentrations would suggest the reverse. Under our model, the observed reductions in aerobic performance in warmer habitats do not arise from lower oxygen concentrations, but instead through organismal oxygen demand exceeding supply. This reappraisal of how organismal thermal physiology and oxygen demands together shape aerobic performance in aquatic ectotherms and the new insight of how these components change with temperature have broad implications for predicting the responses of aquatic communities to ongoing global climate shifts.

Can oxygen set thermal limits in an insect and drive gigantism

Background Thermal limits may arise through a mismatch between oxygen supply and demand in a range of animal taxa. Whilst this oxygen limitation hypothesis is supported by data from a range of marine fish and invertebrates, its generality remains contentious. In particular, it is unclear whether oxygen limitation determines thermal extremes in tracheated arthropods, where oxygen limitation may be unlikely due to the efficiency and plasticity of tracheal systems in supplying oxygen directly to metabolically active tissues. Although terrestrial taxa with open tracheal systems may not be prone to oxygen limitation, species may be affected during other life-history stages, particularly if these rely on diffusion into closed tracheal systems. Furthermore, a central role for oxygen limitation in insects is envisaged within a parallel line of research focussing on insect gigantism in the late Palaeozoic. Methodology/Principal Findings Here we examine thermal maxima in the aquatic life stages of an insect at normoxia, hypoxia (14 kPa) and hyperoxia (36 kPa). We demonstrate that upper thermal limits do indeed respond to external oxygen supply in the aquatic life stages of the stonefly Dinocras cephalotes, suggesting that the critical thermal limits of such aquatic larvae are set by oxygen limitation. This could result from impeded oxygen delivery, or limited oxygen regulatory capacity, both of which have implications for our understanding of the limits to insect body size and how these are influenced by atmospheric oxygen levels. Conclusions/Significance These findings extend the generality of the hypothesis of oxygen limitation of thermal tolerance, suggest that oxygen constraints on body size may be stronger in aquatic environments, and that oxygen toxicity may have actively selected for gigantism in the aquatic stages of Carboniferous arthropods.

Respiratory control in aquatic insects dictates their vulnerability to global warming

Forecasting species responses to climatic warming requires knowledge of how temperature impacts may be exacerbated by other environmental stressors, hypoxia being a principal example in aquatic systems. Both stressors could interact directly as temperature affects both oxygen bioavailability and ectotherm oxygen demand. Insufficient oxygen has been shown to limit thermal tolerance in several aquatic ectotherms, although, the generality of this mechanism has been challenged for tracheated arthropods. Comparing species pairs spanning four different insect orders, we demonstrate that oxygen can indeed limit thermal tolerance in tracheates. Species that were poor at regulating oxygen uptake were consistently more vulnerable to the synergistic effects of warming and hypoxia, demonstrating the importance of respiratory control in setting thermal tolerance limits.

Mitochondrial DNA phylogeography and population history of Meladema diving beetles on the Atlantic Islands and in the Mediterranean basin (Coleoptera, Dytiscidae)

The phylogeny and population history of Meladema diving beetles (Coleoptera, Dytiscidae) were examined using mitochondrial DNA sequence from 16S ribosomal RNA and cytochrome oxidase I genes in 51 individuals from 22 populations of the three extant species (M. imbricata endemic to the western Canary Islands, M. lanio endemic to Madeira and M. coriacea widespread in the Western Mediterranean and on the western Canaries), using a combination of phylogenetic and nested clade analyses. Four main lineages are observed within Meladema, representing the three recognized species plus Corsican populations of M. coriacea. Phylogenetic analyses demonstrate the sister relationship of the two Atlantic Island taxa, and suggest the possible paraphyly of M. coriacea. A molecular clock approach reveals that speciation within the genus occurred in the Early Pleistocene, indicating that the Atlantic Island endemics are not Tertiary relict taxa as had been proposed previously. Our results point to past population bottlenecks in all four lineages, with recent (Late‐Middle Pleistocene) range expansion in non‐Corsican M. coriacea and M. imbricata. Within the Canary Islands, M. imbricata seems to have independently colonized La Gomera and La Palma from Tenerife (although a colonization of La Palma from La Gomera cannot be discarded), and M. coriacea has independently colonized Tenerife and Gran Canaria from separate mainland lineages. In the Mediterranean basin this species apparently colonized Corsica on a single occasion, relatively early in its evolutionary history (Early Pleistocene), and has colonized Mallorca recently on multiple occasions. On the only island where M. coriacea and M. imbricata are broadly sympatric (Tenerife), we report evidence of bidirectional hybridization between the two species.

Population structure and dispersal in the Canary Island caddisfly Mesophylax aspersus (Trichoptera, Limnephilidae)

Population genetic structure of the circum-Mediterranean caddisfly Mesophylax aspersus (Trichoptera, Limnephilidae) on the Canary Islands was investigated by studying allozyme variation at nine putative loci in five populations. Genetic variability, population structure and gene flow were compared with data in the literature for continental taxa to assess the effect of isolation of island populations on the genetic structure. Larvae were collected from streams on the islands of Tenerife (one population), La Gomera (two populations in the same catchment) and La Palma (two populations in different catchments). Genetic variability within populations was high relative to that recorded previously for continental Trichoptera, e.g. mean heterozygosity was 0.119–0.336 (0.035–0.15 in continental taxa). Highly significant population structuring was observed (mean F ST=0.250), and there was significant within-population structuring (mean F IS = 0.098). Populations from the same catchment or island were no more similar than populations from different islands, which suggests that occasional long-distance dispersal, both between and within islands, is the predominant influence on the population structure. This dispersal ability has contributed to the colonization of most permanent streams on the Canary Islands by M. aspersus.

The impact of encroachment and bankside development on the habitat complexity and supralittoral invertebrate communities of the Thames Estuary foreshore

1. The Thames Estuary has a long history of human habitation and industrial development, which has resulted in dramatic losses of foreshore habitat; those fragments of fringing habitats that remain are also under threat from potential encroachment onto the foreshore. This paper describes a survey that set out to document the structural complexity and invertebrate communities of 21 supralittoral sites along a 65 km section of the Thames foreshore, and to assess their conservation value. This is the first extensive survey of supralittoral habitats in an urbanized estuary. 2. Invertebrates were sampled from the supralittoral at each site and the habitat types and their structural complexity (including numbers of plant species) at each site were also documented. The relationships between habitat complexity and invertebrate communities were investigated by linear correlation and multivariate analyses. 3. There were significant positive correlations between the number of supralittoral invertebrate species, habitat complexity (measured as the number of complex habitats present) and the number of plant species at each site. 4. The community composition of supralittoral invertebrates was also related to habitat complexity, although this trend was only evident for species data aggregated to higher taxonomic groups, suggesting that chance may play a key role in the colonization of these fragmented habitats. 5. Based on species recorded, the conservation value of supralittoral sites was low; most taxa were widespread eurytopics and only one supralittoral site (Syon Park) contained a threatened species, the snail Perforatella rubiginosa. Copyright

Population genetic structure and long‐distance dispersal among seabird populations: Implications for colony persistence

Dramatic local population decline brought about by anthropogenic‐driven change is an increasingly common threat to biodiversity. Seabird life history traits make them particularly vulnerable to such change; therefore, understanding population connectivity and dispersal dynamics is vital for successful management. Our study used a 357‐base pair mitochondrial control region locus sequenced for 103 individuals and 18 nuclear microsatellite loci genotyped for 245 individuals to investigate population structure in the Atlantic and Pacific populations of the pelagic seabird, Leach’s storm‐petrel Oceanodroma leucorhoa leucorhoa. This species is under intense predation pressure at one regionally important colony on St Kilda, Scotland, where a disparity between population decline and predation rates hints at immigration from other large colonies. amova, FST,ΦST and Bayesian cluster analyses revealed no genetic structure among Atlantic colonies (Global ΦST = −0.02 P > 0.05, Global FST = 0.003, P > 0.05, structureK = 1), consistent with either contemporary gene flow or strong historical association within the ocean basin. The Pacific and Atlantic populations are genetically distinct (Global ΦST = 0.32 P < 0.0001, Global FST = 0.04, P < 0.0001, structureK = 2), but evidence for interocean exchange was found with individual exclusion/assignment and population coalescent analyses. These findings highlight the importance of conserving multiple colonies at a number of different sites and suggest that management of this seabird may be best viewed at an oceanic scale. Moreover, our study provides an illustration of how long‐distance movement may ameliorate the potentially deleterious impacts of localized environmental change, although direct measures of dispersal are still required to better understand this process.