Nicola J. Mitchell

Biodiversity redistribution under climate change : Impacts on ecosystems and human well-being

Consequences of shifting species distributions Climate change is causing geographical redistribution of plant and animal species globally. These distributional shifts are leading to new ecosystems and ecological communities, changes that will affect human society. Pecl et al. review these current and future impacts and assess their implications for sustainable development goals. Science, this issue p. eaai9214 BACKGROUND The success of human societies depends intimately on the living components of natural and managed systems. Although the geographical range limits of species are dynamic and fluctuate over time, climate change is impelling a universal redistribution of life on Earth. For marine, freshwater, and terrestrial species alike, the first response to changing climate is often a shift in location, to stay within preferred environmental conditions. At the cooler extremes of their distributions, species are moving poleward, whereas range limits are contracting at the warmer range edge, where temperatures are no longer tolerable. On land, species are also moving to cooler, higher elevations; in the ocean, they are moving to colder water at greater depths. Because different species respond at different rates and to varying degrees, key interactions among species are often disrupted, and new interactions develop. These idiosyncrasies can result in novel biotic communities and rapid changes in ecosystem functioning, with pervasive and sometimes unexpected consequences that propagate through and affect both biological and human communities. ADVANCES At a time when the world is anticipating unprecedented increases in human population growth and demands, the ability of natural ecosystems to deliver ecosystem services is being challenged by the largest climate-driven global redistribution of species since the Last Glacial Maximum. We demonstrate the serious consequences of this species redistribution for economic development, livelihoods, food security, human health, and culture, and we document feedbacks on climate itself. As with other impacts of climate change, species range shifts will leave “winners” and “losers” in their wake, radically reshaping the pattern of human well-being between regions and different sectors and potentially leading to substantial conflict. The pervasive impacts of changes in species distribution transcend single systems or dimensions, with feedbacks and linkages between multiple interacting scales and through whole ecosystems, inclusive of humans. We argue that the negative effects of climate change cannot be adequately anticipated or prepared for unless species responses are explicitly included in decision-making and global strategic frameworks. OUTLOOK Despite mounting evidence for the pervasive and substantial impacts of a climate-driven redistribution of Earth’s species, current global goals, policies, and international agreements fail to account for these effects. With the predicted intensification of species movements and their diverse societal and environmental impacts, awareness of species “on the move” should be incorporated into local, regional, and global assessments as standard practice. This will raise hope that future targets—whether they be global sustainability goals, plans for regional biodiversity maintenance, or local fishing or forestry harvest strategies—can be achievable and that society is prepared for a world of universal ecological change. Human society has yet to appreciate the implications of unprecedented species redistribution for life on Earth, including for human lives. Even if greenhouse gas emissions stopped today, the responses required in human systems to adapt to the most serious effects of climate-driven species redistribution would be massive. Meeting these challenges requires governance that can anticipate and adapt to changing conditions, as well as minimize negative consequences. As the global climate changes, human well-being, ecosystem function, and even climate itself are increasingly affected by the shifting geography of life. Climate-driven changes in species distributions, or range shifts, affect human well-being both directly (for example, through emerging diseases and changes in food supply) and indirectly (by degrading ecosystem health). Some range shifts even create feedbacks (positive or negative) on the climate system, altering the pace of climate change. Distributions of Earth’s species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation’s Sustainable Development Goals.

Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon)

BackgroundThe sex of many reptiles is determined by the temperature an embryo experiences during its development. Three patterns of temperature-dependent sex determination (TSD) have been defined, but one pattern where only males are produced above an upper temperature threshold (Type IB) is controversial. Here we report new data on the relationship between constant temperature incubation and sexual phenotype in two species of tuatara (Sphenodon), archaic reptiles of enormous zoological significance as the sole representatives of a once widespread reptilian order.ResultsIn both species, the pattern observed with constant incubation temperatures from 18 to 23°C (or 24°C) supported a female→male (FM or Type IB) pattern of TSD: in Sphenodon guntheri males were produced above a pivotal temperature of 21.6°C, and in S. punctatus (unnamed subspecies on Stephens Island, Cook Strait), males were produced above a pivotal temperature of 22.0°C. The pivotal temperatures and scaling parameters differed between species (p < 0.001). The thermosensitive period (TSP), where temperature influences gonad morphogenesis, occurs between 0.25 and 0.55 of embryonic development. While it is possible that the more common female→male→female (FMF or Type II) pattern exists, with a second pivotal temperature above 23–24°C, we review several lines of evidence to the contrary. Most notably, we show that in S. punctatus, the warmest natural nests during the TSP produce predominantly males.ConclusionAn FM pattern of TSD could be currently adaptive in promoting sexual size dimorphism in tuatara. However, an FM pattern has particularly serious consequences for S. guntheri because current patterns of global warming could exacerbate the male bias already present in the relic population.

Influence of Environmental Oxygen on Development and Hatching of Aquatic Eggs of the Australian Frog, Crinia georgiana

The effect of oxygen partial pressure (Po2) on development and hatching was investigated in aquatic embryos of the myobatrachid frog, Crinia georgiana, in the field and in the laboratory. Eggs from 29 field nests experienced widely variable Po2 but similar temperatures. Mean Po2 in different nests ranged between 2.9 and 19.3 kPa (grand mean 12.9 kPa), and mean temperature ranged between 11.9° and 16.8°C (grand mean 13.7°C). There was no detectable effect of Po2 or temperature on development rate or hatching time in the field, except in one nest at 2.9 kPa where the embryos died, presumably in association with hypoxia. Laboratory eggs were incubated at 15°C at a range of Po2 between 2 and 25 kPa. Between 5 and 25 kPa, there was almost no effect of Po2 on development rate to stage 26, but the embryos hatched progressively earlier—at earlier stages and lower gut‐free body mass—at lower Po2. At 2 kPa, development was severely delayed, growth of the embryo slowed, and morphological anomalies appeared. A high tolerance to low Po2 may be an adaptation to embryonic development in the potentially hypoxic, aquatic environment.

Detecting extinction risk from climate change by IUCN red list criteria

Anthropogenic climate change is a key threat to global biodiversity. To inform strategic actions aimed at conserving biodiversity as climate changes, conservation planners need early warning of the risks faced by different species. The IUCN Red List criteria for threatened species are widely acknowledged as useful risk assessment tools for informing conservation under constraints imposed by limited data. However, doubts have been expressed about the ability of the criteria to detect risks imposed by potentially slow-acting threats such as climate change, particularly because criteria addressing rates of population decline are assessed over time scales as short as 10 years. We used spatially explicit stochastic population models and dynamic species distribution models projected to future climates to determine how long before extinction a species would become eligible for listing as threatened based on the IUCN Red List criteria. We focused on a short-lived frog species (Assa darlingtoni) chosen specifically to represent potential weaknesses in the criteria to allow detailed consideration of the analytical issues and to develop an approach for wider application. The criteria were more sensitive to climate change than previously anticipated; lead times between initial listing in a threatened category and predicted extinction varied from 40 to 80 years, depending on data availability. We attributed this sensitivity primarily to the ensemble properties of the criteria that assess contrasting symptoms of extinction risk. Nevertheless, we recommend the robustness of the criteria warrants further investigation across species with contrasting life histories and patterns of decline. The adequacy of these lead times for early warning depends on practicalities of environmental policy and management, bureaucratic or political inertia, and the anticipated species response times to management actions.

Linking Eco-Energetics and Eco-Hydrology to Select Sites for the Assisted Colonization of Australia’s Rarest Reptile

Assisted colonization—the deliberate translocation of species from unsuitable to suitable regions—is a controversial management tool that aims to prevent the extinction of populations that are unable to migrate in response to climate change or to survive in situ. The identification of suitable translocation sites is therefore a pressing issue. Correlative species distribution models, which are based on occurrence data, are of limited use for site selection for species with historically restricted distributions. In contrast, mechanistic species distribution models hold considerable promise in selecting translocation sites. Here we integrate ecoenergetic and hydrological models to assess the longer-term suitability of the current habitat of one of the world’s rarest chelonians, the Critically Endangered Western Swamp Tortoise (Psuedemydura umbrina). Our coupled model allows us to understand the interaction between thermal and hydric constraints on the foraging window of tortoises, based on hydrological projections of its current habitat. The process can then be repeated across a range of future climates to identify regions that would fall within the tortoise’s thermodynamic niche. The predictions indicate that climate change will result in reduced hydroperiods for the tortoises. However, under some climate change scenarios, habitat suitability may remain stable or even improve due to increases in the heat budget. We discuss how our predictions can be integrated with energy budget models that can capture the consequences of these biophysical constraints on growth, reproduction and body condition.

How to Decide Whether to Move Species Threatened by Climate Change

Introducing species to areas outside their historical range to secure their future under climate change is a controversial strategy for preventing extinction. While the debate over the wisdom of this strategy continues, such introductions are already taking place. Previous frameworks for analysing the decision to introduce have lacked a quantifiable management objective and mathematically rigorous problem formulation. Here we develop the first rigorous quantitative framework for deciding whether or not a particular introduction should go ahead, which species to prioritize for introduction, and where and how to introduce them. It can also be used to compare introduction with alternative management actions, and to prioritise questions for future research. We apply the framework to a case study of tuatara (Sphenodon punctatus) in New Zealand. While simple and accessible, this framework can accommodate uncertainty in predictions and values. It provides essential support for the existing IUCN guidelines by presenting a quantitative process for better decision-making about conservation introductions.

Sex Ratio Bias and Extinction Risk in an Isolated Population of Tuatara (Sphenodon Punctatus)

Understanding the mechanisms underlying population declines is critical for preventing the extinction of endangered populations. Positive feedbacks can hasten the process of collapse and create an ‘extinction vortex,’ particularly in small, isolated populations. We provide a case study of a male-biased sex ratio creating the conditions for extinction in a natural population of tuatara (Sphenodon punctatus) on North Brother Island in the Cook Strait of New Zealand. We combine data from long term mark-recapture surveys, updated model estimates of hatchling sex ratio, and population viability modeling to measure the impacts of sex ratio skew. Results from the mark-recapture surveys show an increasing decline in the percentage of females in the adult tuatara population. Our monitoring reveals compounding impacts on female fitness through reductions in female body condition, fecundity, and survival as the male-bias in the population has increased. Additionally, we find that current nest temperatures are likely to result in more male than female hatchlings, owing to the pattern of temperature-dependent sex determination in tuatara where males hatch at warmer temperatures. Anthropogenic climate change worsens the situation for this isolated population, as projected temperature increases for New Zealand are expected to further skew the hatchling sex ratio towards males. Population viability models predict that without management intervention or an evolutionary response, the population will ultimately become entirely comprised of males and functionally extinct. Our study demonstrates that sex ratio bias can be an underappreciated threat to population viability, particularly in populations of long-lived organisms that appear numerically stable.

Increased expression of Hsp70 and Hsp90 mRNA as biomarkers of thermal stress in loggerhead turtle embryos (Caretta Caretta).

The survival and viability of sea turtle embryos is dependent upon favourable nest temperatures throughout the incubation period. Consequently, future generations of sea turtles may be at risk from increasing nest temperatures due to climate change, but little is known about how embryos respond to heat stress. Heat shock genes are likely to be important in this process because they code for proteins that prevent cellular damage in response to environmental stressors. This study provides the first evidence of an expression response in the heat shock genes of embryos of loggerhead sea turtles (Caretta caretta) exposed to realistic and near-lethal temperatures (34°C and 36°C) for 1 or 3 hours. We investigated changes in Heat shock protein 60 (Hsp60), Hsp70, and Hsp90 mRNA in heart (n=24) and brain tissue (n=29) in response to heat stress. Under the most extreme treatment (36°C, 3h), Hsp70 increased mRNA expression by a factor of 38.8 in heart tissue and 15.7 in brain tissue, while Hsp90 mRNA expression increased by a factor of 98.3 in heart tissue and 14.7 in brain tissue. Hence, both Hsp70 and Hsp90 are useful biomarkers for assessing heat stress in the late-stage embryos of sea turtles. The method we developed can be used as a platform for future studies on variation in the thermotolerance response from the clutch to population scale, and can help us anticipate the resilience of reptile embryos to extreme heating events.

Securing the Demographic and Genetic Future of Tuatara through Assisted Colonization

Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted-colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long-term sustainable populations capable of persisting during rapid changes in climate.

Effects of Temperature on Energy Cost and Timing of Embryonic and Larval Development of the Terrestrially Breeding Moss Frog, Bryobatrachus nimbus

The Australian moss frog, Bryobatrachus nimbus, oviposits four to 16 large eggs in terrestrial nests constructed in moss or lichen in subalpine regions of southern Tasmania. Nidicolous larvae overwinter beneath snow, reaching metamorphosis without feeding after 395 d, the longest development time known for an endotrophic anuran. However, a few clutches develop more quickly and metamorphose before winter. This study examines the effect of temperature on development time and energy expenditure by measuring temperatures and developmental stages in field nests as well as rates of oxygen consumption (V̇o2), developmental stage, body mass, and energy content in the laboratory at three relevant temperatures (5°, 10°, 15°C). Eggs and larvae reared at 5°C differentiated very slowly, and their development time far exceeded those in natural nests, but development times at 10° and 15°C averaged 277 and 149 d, respectively, and were shorter than field incubation times. Generally, respiration rates of aquatic hatchlings were low in comparison with other species but increased with larval age and jumped about 25% higher near metamorphosis when larvae were able to air breathe. The mean energy density was 26.0 J mg−1 for the dry ova and 20.6 J mg−1 for a dry gut‐free froglet, and total production efficiency was 61.5%. We developed a model based on the relationships between incubation temperature and V̇o2 to estimate the respiratory cost of development to metamorphosis, the first such study for an amphibian. The cost was 177 J at 15°C, 199 J at 10°C, and at least 249 J at 5°C, and we predicted that continual development at 5°C would lead to premature yolk depletion because it equalled the 249 J contained in fresh ova. Continuously logged field‐nest temperatures and interpolation of laboratory data provided estimates of development rates, V̇o2, and respiratory energy costs in field nests. Development to metamorphosis required between 185 and 234 J when larvae overwintered, but completion of metamorphosis before winter saved 123 J. However, the advantage of emergence in warmer months, when conditions are suitable for feeding and growth, may offset the greater energy cost of overwintering.