Resistance and resilience: quantifying relative extinction risk in a diverse assemblage of Australian tropical rainforest vertebrates

Aim Assessing the relative vulnerability of species within an assemblage to extinction is crucial for conservation planning at the regional scale. Here, we quantify relative vulnerability to extinction, in terms of both resistance and resilience to environmental change, in an assemblage of tropical rainforest vertebrates. Location Wet Tropics Bioregion, north Queensland, Australia. Methods We collated data on 163 vertebrates that occur in the Australian Wet Tropics, including 24 frogs, 33 reptiles, 19 mammals and 87 birds. We used the ‘seven forms of rarity’ model to assess relative vulnerability or resistance to environmental change. We then develop a new analogous eight‐celled model to assess relative resilience, or potential to recover from environmental perturbation, based on reproductive output, potential for dispersal and climatic niche marginality. Results In the rarity model, our assemblage had more species very vulnerable and very resistant than expected by chance. There was a more even distribution of species over the categories in the resilience model. The three traits included in each model were not independent of each other; species that were widespread were also habitat generalists, while species with narrow geographical ranges tended to be locally abundant. In the resilience model, species with low reproductive output had a narrow climatic niche and also a low capacity to disperse. Frogs were the most vulnerable taxonomic group overall. The model categories were compared to current IUCN category of listed species, and the product of the two models was best correlated with IUCN listings. Main conclusions The models presented here offer an objective way to predict the resistance of a species to environmental change, and its capacity to recover from disturbance. The new resilience model has similar advantages to the rarity model, in that it uses simple information and is therefore useful for examining patterns in assemblages with many poorly known species.     

The climatic drivers of long-term population changes in rainforest montane birds

Climate-driven biodiversity erosion is escalating at an alarming rate. The pressure imposed by climate change is exceptionally high in tropical ecosystems, where species adapted to narrow environmental ranges exhibit strong physiological constraints. Despite the observed detrimental effect of climate change on ecosystems at a global scale, our understanding of the extent to which multiple climatic drivers affect population dynamics is limited. Here, we disentangle the impact of different climatic stressors on 47 rainforest birds inhabiting the mountains of the Australian Wet Tropics using hierarchical population models. We estimate the effect of spatiotemporal changes in temperature, precipitation, heatwaves, droughts and cyclones on the population dynamics of rainforest birds between 2000 and 2016. We find a strong effect of warming and changes in rainfall patterns across the elevational-segregated bird communities, with lowland populations benefiting from increasing temperature and precipitation, while upland species show an inverse strong negative response to the same drivers. Additionally, we find a negative effect of heatwaves on lowland populations, a pattern associated with the observed distribution of these extreme events across elevations. In contrast, cyclones and droughts have a marginal effect on spatiotemporal changes in rainforest bird communities, suggesting a species-specific response unrelated to the elevational gradient. This study demonstrated the importance of unravelling the drivers of climate change impacts on population changes, providing significant insight into the mechanisms accelerating climate-induced biodiversity degradation.     

Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.     

Evolutionary stasis and lability in thermal physiology in a group of tropical lizards

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.     

New approaches to understanding late Quaternary climate fluctuations and refugial dynamics in Australian wet tropical rain forests

Aim We created spatially explicit models of palaeovegetation stability for the rain forests of the Australia Wet Tropics. We accounted for the climatic fluctuations of the late Quaternary, improving upon previous palaeovegetation modelling for the region in terms of data, approach and coverage of predictions. Location Australian Wet Tropics. Methods We generated climate‐based distribution models for broad rain forest vegetation types using contemporary and reconstructed ‘pre‐clearing’ vegetation data. Models were projected onto previously published palaeoclimate scenarios dating to c. 18 kyr bp . Vegetation stability was estimated as the average likelihood that a location was suitable for rain forest through all climate scenarios. Uncertainty associated with model projections onto novel environmental conditions was also tracked. Results Upland rain forest was found to be the most stable of the wet forest vegetation types examined. We provide evidence that the lowland rain forests were largely extirpated from the region during the last glacial maximum, with only small, marginally suitable fragments persisting in two areas. Models generated using contemporary vegetation data underestimated the area of environmental space suitable for rain forest in historical time periods. Model uncertainty resulting from projection onto novel environmental conditions was low, but generally increased with the number of years before present being modelled. Main conclusions Climate fluctuations of the late Quaternary probably resulted in dramatic change in the extent of rain forest in the region. Pockets of high‐stability upland rain forest were identified, but extreme bottlenecks of area were predicted for lowland rain forest. These factors are expected to have had a dramatic impact on the historical dynamics of population connectivity and patterns of extinction and recolonization of dependent fauna. Finally, we found that models trained on contemporary vegetation data can be problematic for reconstructing vegetation patterns under novel environmental conditions. Climatic tolerances and the historical extent of vegetation may be underestimated when artificial vegetation boundaries imposed by land clearing are not taken into account.     

Thermal tolerance and recovery behaviour of Thorectes lusitanicus (Coleoptera,Geotrupidae)

1. Population differences in physiological responses are examined in Thorectes lusitanicus, an endemic Iberian dung beetle species, by submitting individuals of different populations to the same experimental and acclimation conditions. 2. An infrared thermography protocol was used, consisting of three assays: start of activity, cold response, and heat response. Individuals of 12 populations were studied and the comparative explanatory capacities of several environmental factors in relation to the observed inter‐population differences were examined. 3. The heating rate from chill coma to the beginning of activity was the variable with the highest discrimination power among the studied populations, accounting for 94% of the observed variance. Regarding the heat response, only six of the 16 thermal variables reached significance (inter‐population differences accounted for 52–74% in these six thermal parameters). 4. From the three considered environmental factors (Mediterranean climate, land cover, and trophic characteristics) only land cover characteristics remain statistically significant, affecting the cold response of individuals. 5. Thorectes lusitanicus is a species characterised by a high diversity of thermotolerance and recovery traits across populations with a low degree of association with broad environmental factors. Finally, it is suggested that the apterous character of this species could be a determinant factor explaining the high diversity of ecophysiological traits related to thermal stress tolerance and the recovery time.     

The influence of environment and life-history traits on the distribution of genes and individuals: a comparative study of 11 rainforest trees

This study investigates patterns of genetic connectivity among 11 co-distributed tropical rainforest tree species from the genus Elaeocarpus across a biogeographic barrier, the Black Mountain Corridor (BMC) in the Australian Wet Tropics (AWT). We analysed a combination of allelic and flanking region sequence data from microsatellite markers, and evaluated the relative influence of environmental preferences and functional traits on genetic diversity and gene flow. The results indicate that only in three species geographic structuring of haplotype distribution reflects a north vs. south of the BMC pattern. Environmental factors linked with altitude were recognized as affecting genetic trends, but the selective processes operating on upland species appear to be associated with competitiveness and regeneration opportunities on poor soil types rather than climate variables alone. In contrast to previous observations within southeastern Australian rainforests, genetic differentiation in the AWT appears to be associated with small-fruited rather than large-fruited species, highlighting how external factors can influence the dispersal dimension. Overall, this study emphasizes the importance of considering functional and environmental factors when attempting generalizations on landscape-level patterns of genetic variation. Understanding how plant functional groups respond to environmental and climatic heterogeneity can help us predict responses to future change.     

Rapid evolution of cold tolerance in stickleback

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.     

Flammability dynamics in the Australian Alps

Forests of the Australian Alps (SE Australia) are considered some of the most vulnerable to climate change in the country, with ecosystem collapse considered likely for some due to frequent fire. It is not yet known, however, whether increasing fire frequency may stabilize due to reductions in flammability related to reduced time for fuel accumulation, show no trend, or increase due to positive feedbacks related to vegetation changes. To determine what these trends have been historically, dynamics were measured for 58 years of mapped fire history. The 1.4 million ha forested area was divided into broad formations based on structure and dominant canopy trees, and dynamics were measured for each using flammability ratio, a modification of probability of ignition at a point. Crown fire likelihood was measured for each formation, based on satellite‐derived measurements of the 2003 fire effects across a large part of the area. Contrary to popular perception but consistent with mechanistic expectations, all forests exhibited pronounced positive feedbacks. The strongest response was observed in tall, wet forests dominated by Ash‐type eucalypts, where, despite a short period of low flammability following fire, post‐disturbance stands have been more than eight times as likely to burn than have mature stands. The weakest feedbacks occurred in open forest, although post‐disturbance forests were still 1.5 times as likely to burn as mature forests. Apart from low, dry open woodland where there was insufficient data to detect a trend, all forests were most likely to experience crown fire during their period of regeneration. The implications of this are significant for the Alps, as increasing fire frequency has the potential to accelerate by producing an increasingly flammable landscape. These effects may be semi‐permanent in tall, wet forest, where frequent fire promotes ecosystem collapse into either the more flammable open forest formation, or to heathland.     

Evolutionary potential of thermal preference and heat tolerance in Drosophila subobscura

Evolutionary change of thermal traits (i.e., heat tolerance and behavioural thermoregulation) is one of the most important mechanisms exhibited by organisms to respond to global warming. However, the evolutionary potential of heat tolerance, estimated as narrow‐sense heritability, depends on the methodology employed. An alternative adaptive mechanism to buffer extreme temperatures is behavioural thermoregulation, although the association between heat tolerance and thermal preference is not clearly understood. We suspect that methodological effects associated with the duration of heat stress during thermal tolerance assays are responsible for missing this genetic association. To test this hypothesis, we estimated the heritabilities and genetic correlations for thermal traits in Drosophila subobscura, using high‐temperature static and slow ramping assays. We found that heritability for heat tolerance was higher in static assays (h² = 0.134) than in slow ramping assays (h² = 0.084), suggesting that fast assays may provide a more precise estimation of the genetic variation of heat tolerance. In addition, thermal preference exhibited a low heritability (h² = 0.066), suggesting a reduced evolutionary response for this trait. We also found that the different estimates of heat tolerance and thermal preference were not genetically correlated, regardless of how heat tolerance was estimated. In conclusion, our data suggest that these thermal traits can evolve independently in this species. In agreement with previous evidence, these results indicate that methodology may have an important impact on genetic estimates of heat tolerance and that fast assays are more likely to detect the genetic component of heat tolerance.     

Any which way will do – the pollination biology of a northern Australian rainforest canopy tree (Syzygium sayeri; Myrtaceae)

The pollination biology of Syzygium sayeri was documented using the special capabilities of the Australian Canopy Crane. Syzygium sayeri is a xenogamous species with poor self-compatibility, moderate levels of natural out-crossing, and the producer of copious amounts nectar throughout the day and night. Of a diverse fauna associated with, and visiting the flowers of S. sayeri , larger vertebrates (blossom bats and honeyeaters) account for approximately half its natural pollination rate, while the balance of pollination is attributable to a host of invertebrate visitors (wasps, flies, thrips, butterflies). Day and night pollinators contributed approximately equally to the successful pollination of S. sayeri ; although the number of individuals visiting flowers was greater during the day, further experimentation might reveal night visitors to be more effective pollinators. The co-occurrence of vertebrates and invertebrates, as well as day and night visitors, suggests that S. sayeri has a generalist pollination system, whereby the absence of a discrete set of faunae could be compensated for by the presence of other pollinators. What is not clear is the contribution of different pollinators to the population success (i.e. gene flow) of this species. Further study is needed to determine the contribution of each pollinator group to the flow of genetic material in populations of S. sayeri . © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society , 2005, 149 , 69–84.     

Closing the gap between science and management of cold-water refuges in rivers and streams

Human activities and climate change threaten coldwater organisms in freshwater ecosystems by causing rivers and streams to warm, increasing the intensity and frequency of warm temperature events, and reducing thermal heterogeneity. Cold-water refuges are discrete patches of relatively cool water that are used by coldwater organisms for thermal relief and short-term survival. Globally, cohesive management approaches are needed that consider interlinked physical, biological, and social factors of cold-water refuges. We review current understanding of cold-water refuges, identify gaps between science and management, and evaluate policies aimed at protecting thermally sensitive species. Existing policies include designating cold-water habitats, restricting fishing during warm periods, and implementing threshold temperature standards or guidelines. However, these policies are rare and uncoordinated across spatial scales and often do not consider input from Indigenous peoples. We propose that cold-water refuges be managed as distinct operational landscape units, which provide a social and ecological context that is relevant at the watershed scale. These operational landscape units provide the foundation for an integrated framework that links science and management by (1) mapping and characterizing cold-water refuges to prioritize management and conservation actions, (2) leveraging existing and new policies, (3) improving coordination across jurisdictions, and (4) implementing adaptive management practices across scales. Our findings show that while there are many opportunities for scientific advancement, the current state of the sciences is sufficient to inform policy and management. Our proposed framework provides a path forward for managing and protecting cold-water refuges using existing and new policies to protect coldwater organisms in the face of global change.     

Microclimate of daytime den sites in a tropical possum: implications for the conservation of tropical arboreal marsupials

Tree cavities are an important shelter site for a variety of vertebrate species, including birds, reptiles and mammals. Studies indicate that in most taxa favoured tree hollows are those in larger trees and higher from the ground, generally thought to be related to decreased predation risk and a more optimal thermal environment. However, neither of these ideas has been tested definitively. Here, we investigate the microclimate of daytime den sites in tree hollows of common brushtail possums in tropical northern Australia. We compare tree and hollow characteristics of dens known to be used by possums, and those not known to be used, to determine whether possums choose trees with microhabitats with a more favourable daytime microclimate. Possums chose to den in tree hollows which were on average 1.6 °C cooler during the day, and were more buffered from temperature extremes, than other potential den locations. Important factors explaining daytime temperatures between hollows included height of the hollow, entrance width and tree diameter. Tropical arboreal marsupials have been identified as being particularly vulnerable to climate change and there are calls to identify and preserve natural refuges, such as tree hollows, which could buffer them from extreme temperatures. Our results highlight the value of older, larger hollow-bearing trees as refuges from extreme temperature, the importance of which may become critical for some temperature-sensitive species under the combined effects of continuing habitat loss and climate change.     

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae)

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.     

Comparative experimental evolution reveals species-specific idiosyncrasies in marine phytoplankton adaptation to warming

A number of experimental studies have demonstrated that phytoplankton can display rapid thermal adaptation in response to warmed environments. While these studies provide insight into the evolutionary responses of single species, they tend to employ different experimental techniques. Consequently, our ability to compare the potential for thermal adaptation across different, ecologically relevant, species remains limited. Here, we address this limitation by conducting simultaneous long-term warming experiments with the same experimental design on clonal isolates of three phylogenetically diverse species of marine phytoplankton; the cyanobacterium Synechococcus sp., the prasinophyte Ostreococcus tauri and the diatom Phaeodoactylum tricornutum. Over the same experimental time period, we observed differing levels of thermal adaptation in response to stressful supra-optimal temperatures. Synechococcus sp. displayed the greatest improvement in fitness (i.e., growth rate) and thermal tolerance (i.e., temperature limits of growth). Ostreococcus tauri was able to improve fitness and thermal tolerance, but to a lesser extent. Finally, Phaeodoactylum tricornutum showed no signs of adaptation. These findings could help us understand how the structure of phytoplankton communities may change in response to warming, and possible biogeochemical implications, as some species show relatively more rapid adaptive shifts in their thermal tolerance.     

Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold‐specialized birds in a rapidly warming world

1. Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (T _a) is unknown.
2. Using flow‐through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing T _a and measured body temperature (T _b), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production).
3. Buntings had an average (±SD) T _b of 41.3 ± 0.2°C at thermoneutral T _a and increased T _b to a maximum of 43.5 ± 0.3°C. Buntings started panting at T _a of 33.2 ± 1.7°C, with rapid increases in EWL starting at T _a = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral T _a, a markedly lower increase than seen in more heat‐tolerant arid‐zone species (e.g., ≥4.7× baseline rates). Heat‐stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production.
4. Our results suggest that buntings’ well‐developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment.

     

Improved heat tolerance in air drives the recurrent evolution of air-breathing

The transition to air-breathing by formerly aquatic species has occurred repeatedly and independently in fish, crabs and other animal phyla, but the proximate drivers of this key innovation remain a long-standing puzzle in evolutionary biology. Most studies attribute the onset of air-breathing to the repeated occurrence of aquatic hypoxia; however, this hypothesis leaves the current geographical distribution of the 300 genera of air-breathing crabs unexplained. Here, we show that their occurrence is mainly related to high environmental temperatures in the tropics. We also demonstrate in an amphibious crab that the reduced cost of oxygen supply in air extends aerobic performance to higher temperatures and thus widens the animal''s thermal niche. These findings suggest that high water temperature as a driver consistently explains the numerous times air-breathing has evolved. The data also indicate a central role for oxygen- and capacity-limited thermal tolerance not only in shaping sensitivity to current climate change but also in underpinning the climate-dependent evolution of animals, in this case the evolution of air-breathing.     

The evolution of modern human behavior in East Asia: Current perspectives

Behavioral modernity is considered one of the defining characteristics separating modern humans from earlier hominin lineages. Over the course of the past two decades, the nature and origins of modern human behavior have been among the most debated topics in paleoanthropology. 1 - 7 There are currently two primary competing hypotheses regarding how and when modern human behavior arose. The first one, which we shall term the saltational model, argues that between 50–40 kya modern human behavior appeared suddenly and as a “package”; that is, the entire range of traits appeared more or less simultaneously. The proposed reason most often cited for this sudden change in behavior is a genetic mutation, possibly related to communication, 7 that occurred around 50 kya. The second major hypothesis, which we shall term the gradualistic model, argues that modern human behavior arose slowly and sporadically over the course of the past 150,000 years and may be related to increasing population pressure. 2 In general, many European scholars subscribe to the saltational model, while many Africanists seem to prefer the gradualistic model. As McBrearty and Brooks 2 noted, the disagreement may be related to different developmental histories underlying the research traditions in Europe and Africa.