Unpacking the mechanisms captured by a correlative species distribution model to improve predictions of climate refugia

Climate refugia are regions that animals can retreat to, persist in and potentially then expand from under changing environmental conditions. Most forecasts of climate change refugia for species are based on correlative species distribution models (SDMs) using long‐term climate averages, projected to future climate scenarios. Limitations of such methods include the need to extrapolate into novel environments and uncertainty regarding the extent to which proximate variables included in the model capture processes driving distribution limits (and thus can be assumed to provide reliable predictions under new conditions). These limitations are well documented; however, their impact on the quality of climate refugia predictions is difficult to quantify. Here, we develop a detailed bioenergetics model for the koala. It indicates that range limits are driven by heat‐induced water stress, with the timing of rainfall and heat waves limiting the koala in the warmer parts of its range. We compare refugia predictions from the bioenergetics model with predictions from a suite of competing correlative SDMs under a range of future climate scenarios. SDMs were fitted using combinations of long‐term climate and weather extremes variables, to test how well each set of predictions captures the knowledge embedded in the bioenergetics model. Correlative models produced broadly similar predictions to the bioenergetics model across much of the species' current range – with SDMs that included weather extremes showing highest congruence. However, predictions in some regions diverged significantly when projecting to future climates due to the breakdown in correlation between climate variables. We provide unique insight into the mechanisms driving koala distribution and illustrate the importance of subtle relationships between the timing of weather events, particularly rain relative to hot‐spells, in driving species–climate relationships and distributions. By unpacking the mechanisms captured by correlative SDMs, we can increase our certainty in forecasts of climate change impacts on species.     

Mutualism influences species distribution predictions for a bromeliad‐breeding anuran under climate change

Ecological niche models, or species distribution models, have been widely used to identify potentially suitable areas for species in future climate change scenarios. However, there are inherent errors to these models due to their inability to evaluate species occurrence influenced by non‐climatic factors. With the intuit to improve the modelling predictions for a bromeliad‐breeding treefrog (Phyllodytes melanomystax, Hylidae), we investigate how the climatic suitability of bromeliads influences the distribution model for the treefrog in the context of baseline and 2050 climate change scenarios. We used point occurrence data on the frog and the bromeliad (Vriesea procera, Bromeliaceae) to generate their predicted distributions based on baseline and 2050 climates. Using a consensus of five algorithms, we compared the accuracy of the models and the geographic predictions for the frog generated from two modelling procedures: (i) a climate‐only model for P. melanomystax and V. procera; and (ii) a climate‐biotic model for P. melanomystax, in which the climatic suitability of the bromeliad was jointly considered with the climatic variables. Both modelling approaches generated strong and similar predictive power for P. melanomystax, yet climate‐biotic modelling generated more concise predictions, particularly for the year 2050. Specifically, because the predicted area of the bromeliad overlaps with the predictions for the treefrog in the baseline climate, both modelling approaches produce reasonable similar predicted areas for the anuran. Alternatively, due to the predicted loss of northern climatically suitable areas for the bromeliad by 2050, only the climate‐biotic models provide evidence that northern populations of P. melanomystax will likely be negatively affected by 2050.     

Efficient distinction of invasive aquatic plant species from non‐invasive related species using DNA barcoding

Biological invasions are regarded as threats to global biodiversity. Among invasive aliens, a number of plant species belonging to the genera Myriophyllum, Ludwigia and Cabomba, and to the Hydrocharitaceae family pose a particular ecological threat to water bodies. Therefore, one would try to prevent them from entering a country. However, many related species are commercially traded, and distinguishing invasive from non‐invasive species based on morphology alone is often difficult for plants in a vegetative stage. In this regard, DNA barcoding could become a good alternative. In this study, 242 samples belonging to 26 species from 10 genera of aquatic plants were assessed using the chloroplast loci trnH‐psbA, matK and rbcL. Despite testing a large number of primer sets and several PCR protocols, the matK locus could not be amplified or sequenced reliably and therefore was left out of the analysis. Using the other two loci, eight invasive species could be distinguished from their respective related species, a ninth one failed to produce sequences of sufficient quality. Based on the criteria of universal application, high sequence divergence and level of species discrimination, the trnH‐psbA noncoding spacer was the best performing barcode in the aquatic plant species studied. Thus, DNA barcoding may be helpful with enforcing a ban on trade of such invasive species, such as is already in place in the Netherlands. This will become even more so once DNA barcoding would be turned into machinery routinely operable by a nonspecialist in botany and molecular genetics.     

Dietary specialization and the effects of plant species on potential multitrophic interactions of three species of nymphaline caterpillars

The diet breadth of insect herbivores influences their response to variation in plant quality, and these bitrophic interactions have implications for the higher‐level trophic interactions between herbivores and their natural enemies. In this comparative study, we examined the role of host plant species and plant secondary chemistry on the potential interactions between three species of nymphaline caterpillars and their natural enemies. The caterpillar species (all Lepidoptera: Nymphalidae) varied in their degree of specialization: the buckeye, Junonia coenia Hübner, is a specialist on plants that contain iridoid glycosides (IGs); the white peacock, Anartia jatrophae L., feeds on plants in five families, some of which contain IGs and some of which do not; and the painted lady, Vanessa cardui L., is a generalist, feeding on plants in at least 15 families. Each species was reared on leaves of an introduced host plant, Plantago lanceolata L. (Plantaginaceae), which produces two IGs, aucubin and catalpol, and on another plant species that is a common host plant. These alternate host plants were Plantago major L. (Plantaginaceae) for J. coenia, Bacopa monnieri (L.) Pennell (Plantaginaceae) for A. jatrophae, and Malva parviflora L. (Malvaceae) for V. cardui. We examined growth, sequestration, and immune response of these caterpillars on the different host plant species. Junonia coenia developed more rapidly and sequestered higher IG concentrations when reared on P. lanceolata, whereas both other species grew more slowly on P. lanceolata. Host plant did not influence immune response of J. coenia or A. jatrophae, whereas V. cardui immune response was weaker when reared on P. lanceolata. Junonia coenia was most efficient at IG sequestration and A. jatrophae was least efficient, when all three species were reared on P. lanceolata. These results indicate that diet breadth may play an important role in structuring tritrophic interactions, and this role should be further explored.     

Coexistence of two Cyclotella diatom species in the plankton of Lake Baikal

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Pathogens of Ips amitinus: new species and comparison with Ips typographus

Ips amitinus and I. typographus are two serious pests of spruce in Europe, have similar bionomics and are likely to occur and meet on the same host trees. We therefore hypothesized that the two species support similar levels of similar pathogens. To test this hypothesis, we collected mature beetles from three trap trees at each of eight study sites and determined beetle numbers and pathogen infection levels. In total, 938 mature I. amitinus beetles and 3435 of I. typographus were dissected; five pathogens, as well as intestinal nematodes and endoparasitoids, were detected. The neogregarine Mattesia schwenkei is reported here for the first time as a new pathogen in 9.4% of I. amitinus individuals at one site. Average infection levels of most pathogens (Chytridiopsis typographi, Gregarina typographi, Mattesia schwenkei and parasitoids) were significantly higher in I. typographus than in I. amitinus. Metschnikowia typographi was confirmed only in Ips amitinus, while the microsporidium of Nosema typographi occurred only in I. typographus. Within‐season increases in G. typographi infection levels were documented in Ips amitinus.     

Concordance of bacterial communities of two tick species and blood of their shared rodent host

High‐throughput sequencing is revealing that most macro‐organisms house diverse microbial communities. Of particular interest are disease vectors whose microbiome could potentially affect pathogen transmission and vector competence. We investigated bacterial community composition and diversity of the ticks Dermacentor variabilis (n = 68) and Ixodes scapularis (n = 15) and blood of their shared rodent host, Peromyscus leucopus (n = 45) to quantify bacterial diversity and concordance. The 16S rRNA gene was amplified from genomic DNA from field‐collected tick and rodent blood samples, and 454 pyrosequencing was used to elucidate their bacterial communities. After quality control, over 300 000 sequences were obtained and classified into 118 operational taxonomic units (OTUs, clustered at 97% similarity). Analysis of rarefied communities revealed that the most abundant OTUs were tick species‐specific endosymbionts, Francisella and Rickettsia, and the commonly flea‐associated bacterium Bartonella in rodent blood. An Arsenophonus and additional Francisella endosymbiont were also present in D. variabilis samples. Rickettsia was found in both tick species but not in rodent blood, suggesting that it is not transmitted during feeding. Bartonella was present in larvae and nymphs of both tick species, even those scored as unengorged. Relatively, few OTUs (e.g. Bartonella, Lactobacillus) were found in all sample types. Overall, bacterial communities from each sample type were significantly different and highly structured, independent of their dominant OTUs. Our results point to complex microbial assemblages inhabiting ticks and host blood including infectious agents, tick‐specific endosymbionts and environmental bacteria that could potentially affect arthropod‐vectored disease dynamics.     

Penetration by Botryosphaeriaceae species in avocado,guava and persimmon fruit during postharvest

Botryosphaeriaceae species have a wide host range and a worldwide distribution. These fungal species can colonize several plant organs, such as the trunk, leaves and fruit. Some Botryosphaeriaceae species cause important diseases on persimmon, avocado and guava fruit. However, there is a lack of information regarding the mechanisms of penetration by Botryosphaeriaceae species on these tropical and subtropical fruits. This study aimed to better understand the mechanisms involved in fungal penetration, host specificity and aggressiveness of Botryosphaeria dothidea, Lasiodiplodia pseudotheobromae and Neofusicoccum parvum on avocado (Persea americana), guava (Psidium guajava) and persimmon (Diospyros kaki) fruit. Scanning electron microscopy (SEM) image analysis showed that in avocado fruit, the three studied Botryosphaeriaceae species penetrated through lenticels. In guava fruit, penetration through stomata was verified for Botryosphaeria dothidea and Neofusicoccum parvum. In persimmon fruit, an appressoria-like structure was observed for B. dothidea, which suggests direct penetration. Disease incidence in wounded fruit was 24% higher than in non-wounded fruit. L. pseudotheobromae and N. parvum showed differences in aggressiveness in guava fruit. The longest incubation period was observed for N. parvum inoculated on guava, with an average of 4.5 days, and the shortest incubation period was verified for B. dothidea inoculated on avocado, with an average of 2.8 days. The area under the disease progress curve (AUDPC) did not differ between Botryosphaeriaceae species on avocado, whereas on guava and persimmon fruit, the AUDPC was lower for B. dothidea. The information regarding penetration mechanisms and aggressiveness is important to improve postharvest disease control strategies.     

Projecting future expansion of invasive species: comparing and improving methodologies for species distribution modeling

Modeling the distributions of species, especially of invasive species in non‐native ranges, involves multiple challenges. Here, we developed some novel approaches to species distribution modeling aimed at reducing the influences of such challenges and improving the realism of projections. We estimated species–environment relationships for Parthenium hysterophorus L. (Asteraceae) with four modeling methods run with multiple scenarios of (i) sources of occurrences and geographically isolated background ranges for absences, (ii) approaches to drawing background (absence) points, and (iii) alternate sets of predictor variables. We further tested various quantitative metrics of model evaluation against biological insight. Model projections were very sensitive to the choice of training dataset. Model accuracy was much improved using a global dataset for model training, rather than restricting data input to the species’ native range. AUC score was a poor metric for model evaluation and, if used alone, was not a useful criterion for assessing model performance. Projections away from the sampled space (i.e., into areas of potential future invasion) were very different depending on the modeling methods used, raising questions about the reliability of ensemble projections. Generalized linear models gave very unrealistic projections far away from the training region. Models that efficiently fit the dominant pattern, but exclude highly local patterns in the dataset and capture interactions as they appear in data (e.g., boosted regression trees), improved generalization of the models. Biological knowledge of the species and its distribution was important in refining choices about the best set of projections. A post hoc test conducted on a new Parthenium dataset from Nepal validated excellent predictive performance of our ‘best’ model. We showed that vast stretches of currently uninvaded geographic areas on multiple continents harbor highly suitable habitats for parthenium. However, discrepancies between model predictions and parthenium invasion in Australia indicate successful management for this globally significant weed.     

Evaluating the capacity of plant DNA barcodes to discriminate species of cotton (Gossypium: Malvaceae)

Although two plastid regions have been adopted as the standard markers for plant DNA barcoding, their limited resolution has provoked the consideration of other gene regions, especially in taxonomically diverse genera. The genus Gossypium (cotton) includes eight diploid genome groups (A–G, and K) and five allotetraploid species which are difficult to discriminate morphologically. In this study, we tested the effectiveness of three widely used markers (matK, rbcL, and ITS2) in the discrimination of 20 diploid and five tetraploid species of cotton. Sequences were analysed locus‐wise and in combinations to determine the most effective strategy for species identification. Sequence recovery was high, ranging from 92% to 100% with mean pairwise interspecific distance highest for ITS2 (3.68%) and lowest for rbcL (0.43%). At a 0.5% threshold, the combination of matK+ITS2 produced the greatest number of species clusters. Based on ‘best match’ analysis, the combination of matK+ITS2 was best, while based on ‘all species barcodes’ analysis, ITS2 gave the highest percentage of correct species identifications (98.93%). The combination of sequences for all three markers produced the best resolved tree. The disparity index test based on matK+rbcL+ITS2 was significant (P < 0.05) for a higher number of species pairs than the individual gene sequences. Although all three barcodes separated the species with respect to their genome type, no single combination of barcodes could differentiate all the Gossypium species, and tetraploid species were particularly difficult.     

Quantifying the effects of drought on abrupt growth decreases of major tree species in Switzerland

Drought entails important effects on tree physiology, which may result in short‐ to long‐term radial growth decreases. While the majority of studies have focused on annual drought‐related variability of growth, relatively little is known about sustained growth decreases following drought years. We apply a statistical framework to identify climatic factors that induce abrupt growth decreases and may eventually result in tree mortality. We used tree‐ring data from almost 500 standing dead trees and 200 living trees in eight sites of the Swiss network of strict forest reserves, including four of the most important Central European tree species (Abies alba, Picea abies, Fagus sylvatica and Quercus spp.). First, to assess short‐term growth responses to drought under various climate and site conditions, we calculated correlations and linear mixed‐effects models between ring‐width indices (RWIs) and drought based on the Standardized Precipitation Evapotranspiration Index (SPEI). Second, to quantify drought effects on abrupt growth decreases, we applied distributed lag nonlinear models (DLNMs), which account for both delayed effects and the nonlinear relationship between the SPEI and the occurrence of abrupt growth decreases. Positive correlations between RWIs and the SPEI indicated short‐term growth responses of all species, particularly at arid sites. Results of the DLNMs revealed species‐specific growth responses to drought. For Quercus spp., abrupt growth decreases were more likely to occur several years following severe drought, whereas for P. abies, A. alba, and F. sylvatica abrupt growth decreases started frequently immediately in the drought year. We conclude that the statistical framework allows for quantifying the effects of drought intensity on the probability of abrupt growth decreases, which ultimately contributes to an improved understanding of climate impacts on forest community dynamics.     

An amphibian species pushed out of Britain by a moving hybrid zone

Classical theory states that hybrid zones will be stable in troughs of low population density where dispersal is hampered. Yet, evidence for moving hybrid zones is mounting. One possible reason that moving zones have been underappreciated is that they may drive themselves into oblivion and with just the superseding species remaining, morphological and genetic signals of past species replacement may be difficult to appreciate. Using genetic data (32 diagnostic single nucleotide polymorphisms) from a clinal hybrid zone of the common toad (Bufo bufo) and the spined toad (Bufo spinosus) in France for comparison, alleles of the latter species were documented in common toads in the south of Great Britain, at frequencies in excess of 10%. Because long distance dispersal across the Channel is unlikely, the conclusion reached was that the continental toad hybrid zone which previously extended into Britain, moved southwards and extirpated B. spinosus. Species distribution models for the mid‐Holocene and the present support that climate has locally changed in favour of B. bufo. The system bears resemblance with the demise of Homo neanderthalensis and the rise of Homo sapiens and provides an example that some paleoanthropologists demanded in support of a hominin “leaky replacement” scenario. The toad example is informative just because surviving pure B. spinosus and an extant slowly moving interspecific hybrid zone are available for comparison.     

Five species of passerine bird differ in their ability to detect Batesian mimics

Multiple predators affect the evolution of aposematic signals in nature and these predators may substantially differ in terms of ecological and cognitive parameters. However, most experimental studies testing the evolution of Batesian mimics use only a single species of predator (usually the great tit or a domestic chick). Therefore, in the present study, we experimentally tested the responses of five passerine predators to an artificially made Batesian mimic (a cockroach equipped with the warning pattern of the red firebug) with respect to their dietary ecology. Half of the individuals of each species were fed on unmodified roaches before the experiment, whereas the other half were fed with mealworms and thus had no previous experience with roaches. We found that Batesian mimics were better protected than inconspicuous prey against inexperienced great tits and robins alone. The other three bird species showed high level of neophobia; therefore, the effect of warning coloration could not be assessed. We also found that experienced birds attacked a greater number of Batesian mimics compared to inexperienced individuals of all tested species, with the exception of blackcaps. In the great tits, robins, and blue tits, a significant number of experienced birds attacked the Batesian mimic, which was possibly the result of a learned search image for a roach. Our results suggest that using a limited array of predators to describe evolutionary processes forming the diversity of antipredatory strategies of the prey may be biased and need not describe the situation occurring in nature.     

Comparative phylogeography and asymmetric hybridization between cryptic bat species

Cryptic speciation and hybridization are two key processes that affect the origin and maintenance of biodiversity and our ability to understand and estimate it. To determine how these two processes interact, we studied allopatric and sympatric colonies of two cryptic bat species (Eptesicus serotinus and Eptesicus isabellinus) with parapatric distribution in the Iberian Peninsula. These species are the main reservoir for the most commonly rabies virus found in bats in Europe: the European bat Lyssavirus type 1 (EBLV‐1). We used mtDNA and nuclear microsatellite markers to confirm the taxonomic status of both species and to show a more pronounced and geographically based genetic structure in E. isabellinus than in its sibling E. serotinus. Using approximate Bayesian computation (ABC), we inferred rapid range expansion in both species after the Last Glacial Maximum until reaching their present distributions. ABC analysis also supported interspecific differences in genetic diversity and structure, pointing to an earlier expansion of E. isabellinus northward. We found no evidence of mitochondrial introgression between species, but nuclear markers identified a male‐mediated ongoing asymmetric hybridization from E. isabellinus to E. serotinus (28% hybrids in E. serotinus and 5% in E. isabellinus) in the contact zone. Although none of the bats studied tested positive for Lyssavirus RNA, the asymmetric hybridization supports the potential for the recently suggested interspecific transmission of EBLV‐1 from E. isabellinus into E. serotinus.     

Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co‐occurring host species

Understanding the ecology and evolution of parasites is contingent on identifying the selection pressures they face across their infection landscape. Such a task is made challenging by the fact that these pressures will likely vary across time and space, as a result of seasonal and geographical differences in host susceptibility or transmission opportunities. Avian haemosporidian blood parasites are capable of infecting multiple co‐occurring hosts within their ranges, yet whether their distribution across time and space varies similarly in their different host species remains unclear. Here, we applied a new PCR method to detect avian haemosporidia (genera Haemoproteus, Leucocytozoon, and Plasmodium) and to determine parasite prevalence in two closely related and co‐occurring host species, blue tits (Cyanistes caeruleus, N = 529) and great tits (Parus major, N = 443). Our samples were collected between autumn and spring, along an elevational gradient in the French Pyrenees and over a three‐year period. Most parasites were found to infect both host species, and while these generalist parasites displayed similar elevational patterns of prevalence in the two host species, this was not always the case for seasonal prevalence patterns. For example, Leucocytozoon group A parasites showed inverse seasonal prevalence when comparing between the two host species, being highest in winter and spring in blue tits but higher in autumn in great tits. While Plasmodium relictum prevalence was overall lower in spring relative to winter or autumn in both species, spring prevalence was also lower in blue tits than in great tits. Together, these results reveal how generalist parasites can exhibit host‐specific epidemiology, which is likely to complicate predictions of host–parasite co‐evolution.     

Population genetics of four heavily exploited shark species around the Arabian Peninsula

The northwestern Indian Ocean harbors a number of larger marine vertebrate taxa that warrant the investigation of genetic population structure given remarkable spatial heterogeneity in biological characteristics such as distribution, behavior, and morphology. Here, we investigate the genetic population structure of four commercially exploited shark species with different biological characteristics (Carcharhinus limbatus, Carcharhinus sorrah, Rhizoprionodon acutus, and Sphyrna lewini) between the Red Sea and all other water bodies surrounding the Arabian Peninsula. To assess intraspecific patterns of connectivity, we constructed statistical parsimony networks among haplotypes and estimated (1) population structure; and (2) time of most recent population expansion, based on mitochondrial control region DNA and a total of 20 microsatellites. Our analysis indicates that, even in smaller, less vagile shark species, there are no contemporary barriers to gene flow across the study region, while historical events, for example, Pleistocene glacial cycles, may have affected connectivity in C. sorrah and R. acutus. A parsimony network analysis provided evidence that Arabian S. lewini may represent a population segment that is distinct from other known stocks in the Indian Ocean, raising a new layer of conservation concern. Our results call for urgent regional cooperation to ensure the sustainable exploitation of sharks in the Arabian region.