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      The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy

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          Abstract

          Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the hypothesis that thermal limits are reduced under low oxygen availability – such as might happen when key life-stages reside within plants – but also extend this test to attempt to explain that the magnitude of the effect of hypoxia depends on variation in key respiration-related parameters such as aerobic scope and respiratory morphology. Using two life-stages of a xylophagous cerambycid beetle, Cacosceles ( Zelogenes) newmannii we assessed oxygen-limitation effects on metabolic performance and thermal limits. We complement these physiological assessments with high-resolution 3D (micro-computed tomography scan) morphometry in both life-stages. Results showed that although larvae and adults have similar critical thermal maxima (CT max) under normoxia, hypoxia reduces metabolic rate in adults to a greater extent than it does in larvae, thus reducing aerobic scope in the former far more markedly. In separate experiments, we also show that adults defend a tracheal oxygen (critical) setpoint more consistently than do larvae, indicated by switching between discontinuous gas exchange cycles (DGC) and continuous respiratory patterns under experimentally manipulated oxygen levels. These effects can be explained by the fact that the volume of respiratory anatomy is positively correlated with body mass in adults but is apparently size-invariant in larvae. Thus, the two life-stages of C. newmannii display key differences in respiratory structure and function that can explain the magnitude of the effect of hypoxia on upper thermal limits.

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          Attributing physical and biological impacts to anthropogenic climate change.

          Significant changes in physical and biological systems are occurring on all continents and in most oceans, with a concentration of available data in Europe and North America. Most of these changes are in the direction expected with warming temperature. Here we show that these changes in natural systems since at least 1970 are occurring in regions of observed temperature increases, and that these temperature increases at continental scales cannot be explained by natural climate variations alone. Given the conclusions from the Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report that most of the observed increase in global average temperatures since the mid-twentieth century is very likely to be due to the observed increase in anthropogenic greenhouse gas concentrations, and furthermore that it is likely that there has been significant anthropogenic warming over the past 50 years averaged over each continent except Antarctica, we conclude that anthropogenic climate change is having a significant impact on physical and biological systems globally and in some continents.
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            Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?

            Temperature has dramatic evolutionary fitness consequences and is therefore a major factor determining the geographic distribution and abundance of ectotherms. However, the role that age might have on insect thermal tolerance is often overlooked in studies of behaviour, ecology, physiology and evolutionary biology. Here, we review the evidence for ontogenetic and ageing effects on traits of high- and low-temperature tolerance in insects and show that these effects are typically pronounced for most taxa in which data are available. We therefore argue that basal thermal tolerance and acclimation responses (i.e. phenotypic plasticity) are strongly influenced by age and/or ontogeny and may confound studies of temperature responses if unaccounted for. We outline three alternative hypotheses which can be distinguished to propose why development affects thermal tolerance in insects. At present no studies have been undertaken to directly address these options. The implications of these age-related changes in thermal biology are discussed and, most significantly, suggest that the temperature tolerance of insects should be defined within the age-demographics of a particular population or species. Although we conclude that age is a source of variation that should be carefully controlled for in thermal biology, we also suggest that it can be used as a valuable tool for testing evolutionary theories of ageing and the cellular and genetic basis of thermal tolerance.
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              Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction.

              The critical thermal maximum (CTmax), the temperature at which motor control is lost in animals, has the potential to determine if species will tolerate global warming. For insects, tolerance to high temperatures decreases with latitude, suggesting that similar patterns may exist along elevational gradients as well. This study explored how CTmax varies among species and populations of a group of diverse tropical insect herbivores, the rolled-leaf beetles, across both broad and narrow elevational gradients. Data from 6,948 field observations and 8,700 museum specimens were used to map the elevational distributions of rolled-leaf beetles on two mountains in Costa Rica. CTmax was determined for 1,252 individual beetles representing all populations across the gradients. Initial morphological identifications suggested a total of 26 species with populations at different elevations displaying contrasting upper thermal limits. However, compared with morphological identifications, DNA barcodes (cytochrome oxidase I) revealed significant cryptic species diversity. DNA barcodes identified 42 species and haplotypes across 11 species complexes. These 42 species displayed much narrower elevational distributions and values of CTmax than the 26 morphologically defined species. In general, species found at middle elevations and on mountaintops are less tolerant to high temperatures than species restricted to lowland habitats. Species with broad elevational distributions display high CTmax throughout their ranges. We found no significant phylogenetic signal in CTmax, geography, or elevational range. The narrow variance in CTmax values for most rolled-leaf beetles, especially high-elevation species, suggests that the risk of extinction of insects may be substantial under some projected rates of global warming.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                20 November 2019
                2019
                : 10
                : 1426
                Affiliations
                [1] 1Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University , Stellenbosch, South Africa
                [2] 2Department of Zoology, Stockholm University , Stockholm, Sweden
                [3] 3South African Sugarcane Research Institute , Mount Edgecombe, South Africa
                [4] 4CT Scanner Facility, Central Analytical Facilities, Stellenbosch University , Stellenbosch, South Africa
                [5] 5Physics Department, Stellenbosch University , Stellenbosch, South Africa
                Author notes

                Edited by: Fernando Ariel Genta, Oswaldo Cruz Foundation (FIOCRUZ), Brazil

                Reviewed by: Jake Socha, Virginia Tech, United States; John M. VandenBrooks, Arizona State University, United States

                *Correspondence: Marion Javal, mjaval@ 123456sun.ac.za

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2019.01426
                6879455
                31824337
                f0c5fcf5-3c0f-49da-8c6e-802574b4645c
                Copyright © 2019 Javal, Thomas, Lehmann, Barton, Conlong, Du Plessis and Terblanche.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 July 2019
                : 04 November 2019
                Page count
                Figures: 4, Tables: 3, Equations: 0, References: 87, Pages: 11, Words: 0
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                cacosceles newmannii,thermolimit respirometry,critical temperature,tracheal system,hypoxia

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