Divergence of thermal physiological traits in terrestrial breeding frogs along a tropical elevational gradient

Critical thermal limits are thought to be correlated with the elevational distribution of species living in tropical montane regions, but with upper limits being relatively invariant compared to lower limits. To test this hypothesis, we examined the variation of thermal physiological traits in a group of terrestrial breeding frogs (Craugastoridae) distributed along a tropical elevational gradient. We measured the critical thermal maximum (CT_max; n = 22 species) and critical thermal minimum (CT_min; n = 14 species) of frogs captured between the Amazon floodplain (250 m asl) and the high Andes (3,800 m asl). After inferring a multilocus species tree, we conducted a phylogenetically informed test of whether body size, body mass, and elevation contributed to the observed variation in CT_max and CT_min along the gradient. We also tested whether CT_max and CT_min exhibit different rates of change given that critical thermal limits (and their plasticity) may have evolved differently in response to different temperature constraints along the gradient. Variation of critical thermal traits was significantly correlated with species’ elevational midpoint, their maximum and minimum elevations, as well as the maximum air temperature and the maximum operative temperature as measured across this gradient. Both thermal limits showed substantial variation, but CT_min exhibited relatively faster rates of change than CT_max, as observed in other taxa. Nonetheless, our findings call for caution in assuming inflexibility of upper thermal limits and underscore the value of collecting additional empirical data on species’ thermal physiology across elevational gradients.     

Adaptive plasticity in wing melanisation of a montane butterfly across a Himalayan elevational gradient

1. Traits that are significant to the thermal ecology of temperate or montane species are expected to prominently co-vary with the thermal environment experienced by an organism. The Himalayan Pieris canidia butterfly exhibits considerable variation in wing melanisation. We investigated: (i) whether variation in wing melanisation and (ii) activity period of this montane butterfly was influenced by the seasonally and elevationally changing thermal landscape.
2. We discovered that wing melanisation varied across elevation, seasons, sex, and wing surfaces, with the variation strongly structured in space and time: colder seasons and higher elevations produced more melanic individuals. Notably, melanisation did not vary uniformly across all wing surfaces: (i) melanisation of the ventral hindwing co-varied much more prominently with elevation, but (ii) melanisation on all other surfaces varied with seasonal changes in the thermal environment.
3. Observed wing surface-specific patterns indicated thermoregulatory function for this variation in melanisation. Such wing surface-specific responses to seasonal and elevational variation in temperature have rarely been reported in montane insects.
4. Moreover, daily and seasonal thermal cycles were found to strongly influence activity periods of this species, suggesting the potential limits to wing melanisation plasticity.
5. Overall, these results showed that the seasonal and elevational gradients in temperature influence the thermal phenotype as well as activity periods of this Himalayan butterfly. It will be critical to study the phenotypic evolution of such montane insects in response to the ongoing climate change, which is already showing significant signs in this iconic mountain range.

     

Thermal ecology and baseline energetic requirements of a large‐bodied ectotherm suggest resilience to climate change

1. Most studies on how rising temperatures will impact terrestrial ectotherms have focused on single populations or multiple sympatric species. Addressing the thermal and energetic implications of climatic variation on multiple allopatric populations of a species will help us better understand how a species may be impacted by altered climates.
2. We used eight years of thermal and behavioral data collected from four populations of Pacific rattlesnakes (Crotalus oreganus) living in climatically distinct habitat types (inland and coastal) to determine the field‐active and laboratory‐preferred body temperatures, thermoregulatory metrics, and maintenance energetic requirements of snakes from each population.
3. Physical models showed that thermal quality was best at coastal sites, but inland snakes thermoregulated more accurately despite being in more thermally constrained environments. Projected increases of 1 and 2°C in ambient temperature result in an increase in overall thermal quality at both coastal and inland sites.
4. Population differences in modeled standard metabolic rate estimates were driven by body size and not field‐active body temperature, with inland snakes requiring 1.6× more food annually than coastal snakes.
5. All snakes thermoregulated with high accuracy, suggesting that small increases in ambient temperature are unlikely to impact the maintenance energetic requirements of individual snakes and that some species of large‐bodied reptiles may be robust to modest thermal perturbations under conservative climate change predictions.

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Functional diversity decreases with temperature in high elevation ant fauna

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Thermal physiology explains the elevational range for a lizard,Eutropis longicaudata,in Taiwan

1The decrease of temperatures along an elevation gradient imposes physiological constraints on reptiles that ultimately determine their distribution ranges. Forest patterns are likely to interact with this process, but very few studies have examined their contribution in determining distribution limits.2We examined the role played by thermal physiology and forest cover in determining the elevational ranges of a lizard, Eutropis longicaudata. We integrated this species’ thermal traits in simulating its maximum activity time under different conditions of forest cover and elevation using a NicheMapR model. In addition, we evaluated the influence of winter temperatures on the range limit by examining the simulated soil temperatures at the occurrence sites.3Laboratory experiments showed that E. longicaudata has a high preferred body temperature and low cold tolerance. The model predicts that maximum activity time decreases with elevation and forest cover. Although unforested areas may provide longer active time in all simulated elevations, mountain areas in Taiwan are heavily forested and are predicted to allow only a very short period of activity above 1000 m elevation.4All sightings were indeed located in areas below 1000 m elevation, in which the predicted average soil temperature is above 10 °C in January in cold years.5Our results show that reptile physiological response does respond strongly to the change of microclimate induced by forest cover and elevation. Overall, this suggests that forest cover is a major determinant of some reptiles’ elevational range.     

Elevation provenance affects photosynthesis and its acclimation to temperature in the high-Andes alpine herb Phacelia secunda

• We analysed whether Phacelia secunda populations from different elevations exhibit intrinsic traits associated with diffusive and biochemical components of photosynthesis, and if they differ in acclimation of photosynthesis to warmer temperatures. We hypothesized that P. secunda will have similar photosynthetic performance regardless of altitudinal provenance and that plants from high elevations will have a lower photosynthetic acclimation capacity to higher temperature than plants from low elevations.
• Plants from 1600, 2800 and 3600 m a.s.l. in the central Chilean Andes were collected and grown under two temperature regimes (20/16 °C and 30/26 °C day/night). The following photosynthetic traits were measured in each plant for the two temperature regimes: A_N, g_s, g_m, J_max, V_cmax, Rubisco carboxylation k_cat^c.
• Under a common growth environment, plants from the highest elevation had slightly lower CO₂ assimilation rates compared to lower elevation plants. While diffusive components of photosynthesis increased with elevation provenance, the biochemical component decreased, suggesting compensation that explains the similar rates of photosynthesis among elevation provenances. Plants from high elevations had lower photosynthetic acclimation to warmer temperatures compared to plants from lower elevations, and these responses were related to elevational changes in diffusional and biochemical components of photosynthesis.
• Plants of P. secunda from different elevations maintain photosynthetic traits when grown in a common environment, suggesting low plasticity to respond to future climate changes. The fact that high elevation plants had lower photosynthetic acclimation to warmer temperature suggests higher susceptibility to increases in temperature associated with global warming.

     

Weather variation affects the dispersal of grasshoppers beyond their elevational ranges

1. Understanding how abiotic conditions influence dispersal patterns of organisms is important for understanding the degree to which species can track and persist in the face of changing climate.
2. The goal of this study was to understand how weather conditions influence the dispersal pattern of multiple nonmigratory grasshopper species from lower elevation grassland habitats in which they complete their life‐cycles to higher elevations that extend beyond their range limits.
3. Using over a decade of weekly spring to late‐summer field survey data along an elevational gradient, we explored how abundance and richness of dispersing grasshoppers were influenced by temperature, precipitation, and wind speed and direction. We also examined how changes in population sizes at lower elevations might influence these patterns.
4. We observed that the abundance of dispersing grasshoppers along the gradient declined 4‐fold from the foothills to the subalpine and increased with warmer conditions and when wind flow patterns were mild or in the downslope direction. Thirty‐eight unique grasshopper species from lowland sites were detected as dispersers across the survey years, and warmer years and weak upslope wind conditions also increased the richness of these grasshoppers. The pattern of grasshoppers along the gradient was not sex biased. The positive effect of temperature on dispersal rates was likely explained by an increase in dispersal propensity rather than by an increase in the density of grasshoppers at low elevation sites.
5. The results of this study support the hypothesis that the dispersal patterns of organisms are influenced by changing climatic conditions themselves and as such, that this context‐dependent dispersal response should be considered when modeling and forecasting the ability of species to respond to climate change.

     

Elevation gradients of lemur abundance emphasise the importance of Madagascar’s lowland rainforest for the conservation of endemic taxa

1. Elevation gradients correlate with changes in several environmental conditions and are known to be related to animal abundance. Animals in regions with a naturally limited extent of lowland rainforest are expected to have evolved adaptations to intermediate elevations that provided a stable environment during their evolution.
2. Since the lowland rainforest of Madagascar has a limited extent and suffers from increasing anthropogenic pressure, it is essential to understand how well species tolerate intermediate and high elevations. In this study, we aim to quantify the relationship between lemur abundance and elevation in the eastern rainforest of Madagascar.
3. We correlated abundance data on 26 lemur species (10 genera), including 492 records from 26 studies, with elevation. We analysed the consistency of correlations across species with a meta-analytical approach. We controlled for species’ body mass, elevational range and median elevation. We then ran generalised linear mixed models to determine whether lemur abundance was related to elevation, body mass, plant productivity and anthropogenic disturbance.
4. Overall, the abundance of lemur species in Malagasy rainforests was negatively correlated with elevation, and species occupying broader elevational ranges showed stronger correlations. Body mass was not related to species’ tolerance of high elevations. Even though several lemur species are able to occupy the entire elevation gradient, the few remaining patches of lowland rainforests host lemur species at greater abundances than other sites. Abundance across species was negatively related to body mass, elevation and seasonality in plant productivity and positively related to plant productivity.
5. Despite the ecological flexibility of many lemur species, the remnant patches of lowland rainforests host the highest levels of lemur abundance and are key to lemur conservation. It is crucial to preserve this priority habitat both for biodiversity conservation and for our understanding of lemur adaptations.

     

Oxygen-dependence of upper thermal limits in crustaceans from different thermal habitats

The critical thermal maximum (CT_MAX) is the temperature at which animals exhibit loss of motor response because of a temperature-induced collapse of vital physiological systems. A central mechanism hypothesised to underlie the CT_MAX of water-breathing ectotherms is insufficient tissue oxygen supply for vital maintenance functions because of a temperature-induced collapse of the cardiorespiratory system. The CT_MAX of species conforming to this hypothesis should decrease with declining water oxygen tension (PO₂) because they have oxygen-dependent upper thermal limits. However, recent studies have identified a number of fishes and crustaceans with oxygen-independent upper thermal limits, their CT_MAX unchanged in progressive aquatic hypoxia. The previous studies, which were performed separately on cold-water, temperate and tropical species, suggest the oxygen-dependence of upper thermal limits and the acute thermal sensitivity of the cardiorespiratory system increases with decreasing habitat temperature. Here we directly test this hypothesis by assessing the oxygen-dependence of CT_MAX in the polar Antarctic krill (Euphausia superba), as well as the temperate Baltic prawn (Palaemon adspersus) and brown shrimp (Crangon crangon). We found that P. adspersus and C. crangon maintain CT_MAX in progressive hypoxia down to 40 mmHg, and that only E. superba have oxygen-dependent upper thermal limits at normoxia. In E. superba, the observed decline in CT_MAX with water PO₂ is further supported by heart-rate measurements showing a plateauing, and subsequent decline and collapse of heart performance at CT_MAX. Our results support the hypothesis that the oxygen-dependence of upper thermal limits in water-breathing ectotherms and the acute thermal sensitivity of their cardiorespiratory system increases with decreasing habitat temperature.     

Seasonal changes in arthropod diversity patterns along an Alpine elevation gradient

1. Deciphering patterns in species distributions and species interactions along ecological gradients are fundamental topics in ecology. Theory holds that species diversity is greater and interactions are stronger under warmer and more stable environments, such as low elevations and latitudes. However, recent findings have shown conflicting evidence, potentially due to seasonal effects.
2. We aimed to address this gap by studying seasonal changes in arthropod communities over an elevation gradient in the Swiss Alps, as well as herbivore-predator interactions and their resulting consequences on plant herbivory levels.
3. Overall, we found hump-shaped patterns in arthropod abundance, richness and diversity with increasing elevation, with all factors peaking below the tree line. However, these patterns varied seasonally, with strong mid-elevation peaks at the beginning of the summer, shifting to a pattern of linear decrease at the beginning of the fall. In searching for mechanisms explaining these changes, we found that shifts in arthropod communities over elevation and seasons usually followed shifts in vegetation productivity estimates. Other factors, such as top-down control by natural enemies, which was generally stronger at low elevations, and plant species-specific resistance rates along elevation gradients were also implicated as drivers of diversity and herbivory rates.
4. These results highlight the complexity of arthropod communities' responses to environmental gradients, which vary during the season in response to relative changes in both bottom-up and top-down forces.

     

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.

     

A metabolic syndrome in terrestrial ectotherms with different elevational and distribution patterns

The metabolic performance of ectotherms is expected to be driven by the environment in which they live. Ecologically similar species with contrasting elevation distributions occurring in sympatry at mid‐elevations, provide good models for studying how physiological responses to temperature vary as a function of adaptation to different elevations. Under sympatry, at middle elevations, where divergent species ranges overlap, sympatric populations are expected to have similar thermal responses, suggesting similar local acclimation or adaptation, while observed differences would suggest adaptation to each species’ core range. We analysed the metabolic traits of sympatric species pairs from three ectotherm groups: reptiles (Reptilia: Lacertidae), amphibians (Amphibia: Salamandridae) and beetles (Coleoptera: Carabidae), living at different elevations, in order to test how adaptation to different elevations affects metabolic responses to temperature. We experimentally tested the thermal response of respiration rate (RR) and estimated potential metabolic activity (PMA) at three temperature regimes surrounding the groups’ optimal activity body temperatures. RR was relatively similar among groups and showed a positive response to increasing temperature, which was more pronounced in the high‐elevation species of reptiles and beetles. Relative to RR, PMA displayed a stronger and more consistent positive response to increased temperature in all three groups. For all three groups, the average biochemical capacity for metabolism (PMA) was higher in the range‐restricted, high‐elevation species, and this difference increased at higher temperatures in a consistent manner. These results, indicating consistent pattern in three independently evolved animal groups, suggest a ubiquitous adaptive syndrome and represent a novel understanding of the mechanisms shaping spatial biodiversity patterns. Our results also highlight the importance of geographic patterns for the mechanistic understanding of adaptations in physiological traits, including species’ potential to respond/adapt to global climate changes.     

Streams in an uninhabited watershed have predictably different thermal sensitivities to variable summer air temperatures

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Changes in seed dormancy of Rosa multibracteata Hemsl. & E. H. Wilson with increasing elevation in an arid valley in the eastern Tibetan Plateau

Variations in levels of seed dormancy among conspecific populations are poorly understood. We aim to determine the variations in the level of dormancy in Rosa multibracteata along an elevational gradient, and to analyze the mechanisms underlying seed dormancy. The study was conducted in an arid valley in the eastern Tibetan Plateau at five elevations: 1700, 1900, 2100, 2300 and 2500 m. Achene traits were measured and physiological levels of dormancy were determined by measuring germination percentages of achenes treated with H₂SO₄ scarification, warm stratification and cold stratification and combinations of those treatments. Achene size, mass and pericarp thickness increased with increasing elevation, but embryo width decreased with increasing in the arid valley. The level of dormancy generally increased with increasing elevation. The level of dormancy of the rose achenes is intermediate from sites at elevations of 1700, 1900 and 2100 m and deep at elevations of 2300 and 2500 m. Comprehensive analysis suggests that the elevational pattern of level of seed dormancy could be ascribed to intrinsically thicker pericarp and deeper physiological dormancy in the embryo, and extrinsically decreased temperature, increased precipitation and soil moisture at the higher elevations. The great variations of achene traits and levels of seed dormancy across elevations suggest a phenotypic differentiation exists within this rose species. Thus, habitat conditions and achene traits should be considered when selecting roses as materials used to propagate seedlings for ornamental purposes or plant restoration.     

Variations in fecundity over catchment scales: Implications for caddisfly populations spanning a thermal gradient

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Restriction of sexual reproduction in the moss Racomitrium lanuginosum along an elevational gradient

1. Terrestrial plant populations located at the margins of species’ distributions often display reduced sexual reproduction and an increased reliance on asexual reproduction. One hypothesis to explain this phenomenon is that the decline is associated with environmental effects on the energetic costs to produce reproductive organs.
2. In order to clarify the changing processes of sexual reproduction along an elevational gradient, we investigated the sexual reproductive parameters, such as the number of sporophytes and gametangia, in Racomitrium lanuginosum, a dioicous moss found on Mt. Fuji.
3. Matured sporophytes were present only below 3,000 m, and the number of sporophytes per shoot tended to be lower at higher elevation habitats. The numbers of male inflorescences per shoot and antheridia per inflorescence and shoot significantly decreased with increasing elevation. In contrast, the numbers of female inflorescences per shoot and archegonia per inflorescence and shoot varied little across elevations.
4. Synthesis. Our results suggest that the reasons for this limitation are assumed to be limitations in sporophyte development that result in abortion, and the spatial segregation between males and females. Possible reasons for the abortion of sporophytes are the inhibitory effects of low air temperature, a shortened growth period, and winter environmental conditions at higher elevations. Remarkable differences between male and female on various reproductive parameters found in this study are thought to affect the mode of sexual reproduction under the harsh environment. These differences between males and females may be caused by differences in the costs of production and development of gametangia, sensitivity to environmental stressors, and phenological patterns.

     

Investigating the abundance and flight period of bark beetles (Coleoptera: Curculionidae: Scolytinae) over elevational gradients in Sitka spruce forests

1. A warming climate, as predicted under current climate change projections, is likely to influence the population dynamics of many forest insect species. Numerous bark beetle species in both Europe and North America have already responded to a warming climate by significantly expanding their geographical ranges.
2. The aim of the current study was to investigate how populations of bark beetles within stands of Sitka spruce, a widely planted non-native commercial plantation tree species in the U.K., were likely to respond to a warming climate. Experimental plots were established in stands of Sitka spruce over elevational gradients in two commercial forest plantations, and the abundance and emergence times of key bark beetle species were assessed over a 3-year period using flight interception traps. The air temperature difference between the lowest and highest experimental plot in each forest was consistently >1°C throughout the 3-year period.
3. In general, the abundance of the most dominant bark beetle species (e.g. Trypodendron, Dryocoetes, Hylastes spp.) was higher, and emergence times tended to be earlier in the year at the lower elevation plots, where temperatures were higher, although not all bark beetle species responded in the same manner.
4. The results of the study indicated that, under the projected future climate warming scenarios, monoculture Sitka spruce stands at low elevations may potentially be more vulnerable to significant outbreak events from existing or invasive bark beetle species. Hence, consideration of establishing more resilient forests of Sitka spruce by diversifying the species composition and structure of Sitka spruce stands is discussed.

     

Seed germination and dormancy traits of forbs and shrubs important for restoration of North American dryland ecosystems

• In degraded dryland systems, native plant community re‐establishment following disturbance is almost exclusively carried out using seeds, but these efforts commonly fail. Much of this failure can be attributed to the limited understanding of seed dormancy and germination traits.
• We undertook a systematic classification of seed dormancy of 26 species of annual and perennial forbs and shrubs that represent key, dominant genera used in restoration of the Great Basin ecosystem in the western United States. We examined germination across a wide thermal profile to depict species‐specific characteristics and assessed the potential of gibberellic acid (GA₃) and karrikinolide (KAR₁) to expand the thermal germination envelope of fresh seeds.
• Of the tested species, 81% produce seeds that are dormant at maturity. The largest proportion (62%) exhibited physiological (PD), followed by physical (PY, 8%), combinational (PY + PD, 8%) and morphophysiological (MPD, 4%) dormancy classes. The effects of chemical stimulants were temperature‐ and species‐mediated. In general, mean germination across the thermal profile was improved by GA₃ and KAR₁ for 11 and five species, respectively. We detected a strong germination response to temperature in freshly collected seeds of 20 species. Temperatures below 10 °C limited the germination of all except Agoseris heterophylla, suggesting that in their dormant state, the majority of these species are thermally restricted.
• Our findings demonstrate the utility of dormancy classification as a foundation for understanding the critical regenerative traits in these ecologically important species and highlight its importance in restoration planning.

     

Critical thermal maxima of early life stages of three tropical fishes: Effects of rearing temperature and experimental heating rate

Marine ectotherms are often sensitive to thermal stress, and certain life stages can be particularly vulnerable (e.g., larvae or spawners). In this study, we investigated the critical thermal maxima (CT_max) of larval and early juvenile life stages of three tropical marine fishes (Acanthochromis polyacanthus, Amphiprion melanopus, and Lates calcarifer). We tested for potential effects of developmental acclimation, life stage, and experimental heating rates, and we measured metabolic enzyme activities from aerobic (citrate synthase, CS) and anaerobic pathways (lactate dehydrogenase, LDH). A slightly elevated rearing temperature neither influenced CT_max nor CS activity, which otherwise could have indicated thermal acclimation. However, we found CT_max to either remain stable (Acanthrochromis polyacanthus) or increase with body mass during early ontogeny (Amphiprion melanopus and Lates calcarifer). In all three species, faster heating rates lead to higher CT_max. Acute temperature stress did not change CS or LDH activities, suggesting that overall aerobic and anaerobic metabolism remained stable. Lates calcarifer, a catadromous species that migrates from oceanic to riverine habitats upon metamorphosis, had higher CT_max than the two coral reef fish species. We highlight that, for obtaining conservative estimates of a fish species’ upper thermal limits, several developmental stages and body mass ranges should be examined. Moreover, upper thermal limits should be assessed using standardized heating rates. This will not only benefit comparative approaches but also aid in assessing geographic (re-) distributions and climate change sensitivity of marine fishes.