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Insects are mass-reared for release for biocontrol including the sterile insect technique. Insects are usually reared at temperatures that maximize the number of animals produced, are chilled for handling and transport, and released into the field, where temperatures may be considerably different to those experienced previously. Insect thermal biology is phenotypically plastic (i.e. flexible), which means that there may exist opportunities to increase the performance of these programmes by modifying the temperature regimes during rearing, handling, and release. Here we synthesize the literature on thermal plasticity in relation to the opportunities to reduce temperature-related damage and increase the performance of released insects. We summarize how and why temperature affects insect biology, and the types of plasticity shown by insects. We specifically identify aspects of the production chain that might lead to mismatches between the thermal acclimation of the insect and the temperatures it is exposed to, and identify ways to harness physiological plasticity to reduce that potential mismatch. We address some of the practical (especially engineering) challenges to implementing some of the best-supported thermal regimes to maximize performance (e.g. fluctuating thermal regimes), and acknowledge that a focus only on thermal performance may lead to unwanted trade-offs with other traits that contribute to the success of the programme. Together, it appears that thermal physiological plasticity is well-enough understood to allow its implementation in release programmes.
Pseudoscorpions are microarthropods that are distributed from the equator to beyond the Arctic circle. Wyochernes asiaticus (Arachnida: Pseudoscorpiones: Chernetidae) is the northernmost species of pseudoscorpion and is broadly distributed in Beringia, an Arctic and sub-Arctic region that remained unglaciated during the last glacial maximum. Wyochernes asiaticus is anoxia tolerant and has moderate cold tolerance, but nothing is known about the molecular basis of their survival in Canadian polar environments. We de novo assembled and characterised the transcriptome of W. asiaticus collected from the Yukon Territory in northwestern Canada. We assembled an approximately 62.6-million base-pair transcriptome with a mean contig length of 1277, which was 76% complete, according to a benchmark universal single copy orthologue (BUSCO) analysis. We identified 1100 transcripts encoding proteins associated with stress tolerance in these pseudoscorpions, including heat shock proteins, antioxidants, ubiquitination and proteosomal proteins, and sirtuins. We also identified transcripts encoding putative venom proteins. We highlight eight transcripts with high sequence similarity to sequences of venom proteins (ctenitoxins and agatoxins) described from other pseudoscorpions. Our study yields the first transcriptome of a Beringian arthropod, providing important sequence information that will allow future investigation of how W. asiaticus survives in Canadian polar environments.
Drosophila suzukii Matsumura (Diptera: Drosophilidae) is a cosmopolitan polyphagous pest on unripe soft-skinned fruits. We sought to determine (1) temperature treatments that could be used to kill immature D. suzukii in fruit or packaging and (2) whether development on different fruits led to differences in cold tolerance of immature D. suzukii. We reared animals from egg on a banana-based laboratory diet and diets made of apple (Malus domestica Borkhausen; Rosaceae), blueberry (Vaccinium Linnaeus; Ericaceae), cherry (Prunus avium Linnaeus; Rosaceae), grape (Vitis Linnaeus; Vitaceae), orange (Citrus × sinensis (Linnaeus) Osbeck; Rutaceae), raspberry (Rubus Linnaeus; Rosaceae), or strawberry (Fragaria × ananassa Duchesne; Rosaceae) homogenate in agar and measured development time, adult body size, and cold tolerance. Diet type had complex effects on development time; in particular, D. suzukii reared on apple-based or blueberry-based diets developed more slowly to a smaller adult body size than those on other diets. Cold exposure killed eggs and both first and second instars. Survival of 24 hours at +4 °C by feeding third instars was lowest in blueberry and cherry. Five days at +0.6 °C killed all feeding third instars; this treatment is likely sufficient for targeting D. suzukii in fruit. Two hours at −5 °C or −6 °C killed all wandering third instars and pupae; this exposure could be sufficient for sanitation of packaging.
The insect commensal microbiota consists of prokaryotes and eukaryotes. We explored the effect of diet and the persistence of the gut microbiota across generations in Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). We transferred subsets of a single population of D. suzukii to different fruit-based diets (blueberry (Vaccinium Linnaeus; Ericaceae), raspberry (Rubus Linnaeus; Rosaceae), and strawberry (Fragaria × ananassa Duchesne; Rosaceae)) for three generations and then returned them to a common, banana-based, diet. We used 16S rDNA (Bacteria) and ITS (internal transcribed spacer; Fungi) sequencing of female endosymbiont-free flies to identify the microbiota. We identified 2700 bacterial and 350 fungal operational taxonomic units (OTUs); there was no correlation between the number of bacterial and fungal OTUs in a sample. Bacterial communities were dominated by Proteobacteria (especially Acetobacteraceae); Ascomycota dominated the fungal communities. Species diversity of both bacteria and fungi differed among diets, but there were no differences in species-level diversity when these D. suzukii were returned to a control diet. A principle coordinates analysis revealed no differences in the bacterial or fungal community in the first generation on fruit diets, but that the communities diverged over the next two generations; neither fungal and bacterial communities converged after one generation on control food. We conclude that diet changes the D. suzukii microbiota, and that these changes persist for more than one generation.
Many biological processes are partitioned among organs and tissues, necessitating tissue-specific or organ-specific analysis (particularly for comparative -omics studies). Standardised techniques for tissue identification and dissection are therefore imperative for comparing among studies. Here we describe dissection protocols for isolating six key tissues/organs from larvae of the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae): the supraoesophageal ganglion, posterior midgut, hindgut, Malpighian tubules, fat body, and thoracic muscle. We also describe how to extract haemolymph and preserve whole larvae for measurements such as protein, lipid, and carbohydrate content. We include dissection protocols for both fresh-killed and previously frozen specimens. Although this protocol is developed for A. glabripennis, it should allow standardised tissue collection from larvae of other cerambycids and be readily transferrable to other beetle taxa with similar larval morphology.
The great grig, Cyphoderris monstrosa Uhler (Orthoptera: Prophalangopsidae), is a large (20–30 mm, >1 g), nocturnal ensiferan that inhabits montane coniferous forests in northwestern North America. Cyphoderris monstrosa overwinters as a late instar nymphs, but its cold tolerance strategy has not previously been reported. We collected nymphs from near Kamloops, British Columbia, Canada in late spring to determine their cold tolerance strategy. Cyphoderris monstrosa nymphs were active at low temperatures until they froze at −4.6±0.3 °C. The nymphs survived internal ice formation (i.e., are freeze tolerant), had a lethal temperature between −9 °C and −12 °C, and could survive for between five and 10 days at −6 °C. Isolated C. monstrosa gut, Malpighian tubules, and metafemur muscle tissues froze at temperatures similar to whole nymphs, and likely inoculate freezing in vivo. Hemolymph osmolality was 358±51 mOsm, with trehalose and proline comprising ~10% of that total. Glycerol was not detectable in hemolymph from field-fresh nymphs, but accumulated after freezing and thawing. The control of ice formation and presence of hemolymph cryoprotectants may contribute to C. monstrosa freeze tolerance and overwintering survival.
On sub-Antarctic Marion Island, wandering albatross (Diomedea exulans) nests support high abundances of tineid moth, Pringleophaga marioni, caterpillars. Previous work proposed that the birds serve as thermal ecosystem engineers by elevating nest temperatures relative to ambient, thereby promoting growth and survival of the caterpillars. However, only 17 days of temperature data were presented previously, despite year-long nest occupation by birds. Previous sampling was also restricted to old and recently failed nests, though nests from which chicks have recently fledged are key to understanding how the engineering effect is realized. Here we build on previous work by providing nest temperature data for a full year and by sampling all three nest types. For the full duration of nest occupancy, temperatures within occupied nests are significantly higher, consistently by c. 7°C, than those in surrounding soils and abandoned nests, declining noticeably when chicks fledge. Caterpillar abundance is significantly higher in new nests compared to nests from which chicks have fledged, which in turn have higher caterpillar abundances than old nests. Combined with recent information on the life history of P. marioni, our data suggest that caterpillars are incidentally added to the nests during nest construction, and subsequently benefit from an engineering effect.
We tested the hypothesis that slow rewarming would improve the ability of Drosophila melanogaster Meigen (Diptera: Drosophilidae) larvae to survive acute low-temperature exposure. Four larval stages (1st, 2nd, and 3rd instars, including wandering-stage 3rd instars) of four wild-type strains were exposed to –7 °C for periods of time expected to result in 90% mortality. Larvae were then directly transferred to their rearing temperature (21 °C) or returned to this temperature either in a stepwise fashion (pausing at 0 and 15 °C) or by slow warming at 1 or 0.1 °C/min. We observed a reduced rapid cold-hardening effect and no general increase in survival of acute chilling in larvae rewarmed in a stepwise or slow fashion, and we hypothesize that slow rewarming may result in accumulation of chill injuries.
During the early part of the twentieth century, comparative physiological studies were as much at home in ecological journals as they were in those devoted to physiology. Indeed, Shelford (1913) considered ecology to be a “branch of general physiology which deals with the organism as a whole…and which also considers the organism with particular reference to its usual environment”. For reasons that have been discussed elsewhere (e.g. Huey, 1991; Spicer and Gaston, 1999; Chown et al., 2004) ecology and physiology subsequently parted ways with both increasing their focus on smaller-scale questions. Although large-scale ecological and biogeographic work continued, interest in physiological mechanisms waned (see e.g. Myers and Giller, 1988; Lomolino and Heaney, 2004). In much the same way, large-scale comparative physiological ecology dwindled in significance, making studies such as those by Scholander et al. (1953) and Brattstrom (1968) milestones along an increasingly deserted road. Clearly, investigations of animal responses to the environment continued (the work of Bartholomew stands out especially (Dawson, 2005) (see also reviews in Prosser, 1986; Angilletta et al., 2002; Hoffmann et al., 2003), and the development of methods to correct for phylogenetic non-independence prompted a resurgence of interest in understanding the evolution of physiological traits and their variation among species and higher taxa (Feder et al., 2000). However, by the late 1980s, the subject of organismal physiological diversity was in several ways thought to be a dead end.
The distribution and abundance of free-living arthropods from soil and under stones were surveyed at the Cape Hallett ice-free area (ASPA No. 106), North Victoria Land, Antarctica. A total of 327 samples from 67 plots yielded 11 species of arthropods comprised of three Collembola: Cryptopygus cisantarcticus, Friesea grisea and Isotoma klovstadi and eight mites: Coccorhagidia gressitti, Eupodes wisei, Maudheimia petronia, Nanorchestes sp., Stereotydeus belli, S. punctatus, Tydeus setsukoae and T. wadei. Arthropods were absent from areas occupied by the large Adélie penguin colony. There was some distinction among arthropod communities of different habitats, with water and a lichen species (indicative of scree slope habitats) ranking as significant community predictors alongside spatial variables in a Canonical Correspondence Analysis. Recent changes to the management plan for ASPA No. 106 may need to be revisited as the recommended campsite is close to the area of greatest arthropod diversity.
Cold tolerance of the springtail Gomphiocephalus hodgsoni Carpenter (Collembola: Hypogastruridae) was studied at Cape Bird, Ross Island, Antarctica (77°13′S, 166°26′E). Microclimate temperatures indicate a highly seasonal thermal environment, with winter minima <–39°C. Snow cover significantly buffers both minimum temperatures and cooling rates. Gomphiocephalus hodgsoni survives low temperatures by avoiding freezing. Mean low group supercooling points (SCPs) ranged from –35.4°C in October to –28.3°C in January. The lowest SCP measured was –38.0°C. The high SCP group was very small, making up only 18% of the population in January. In October, G. hodgsoni had a very high glycerol content (>80 μg mg−1 dry weight), although this declined rapidly to low levels (c. 7–10 μg mg−1 dry weight) in January. Quantities of glucose and trehalose were low during October, but steadily increased throughout the summer. Haemolymph osmolality was exceptionally high (up to 1755 mOsm kg−1) at the end of November, but this rapidly declined to c. 500 mOsm kg−1 by late December. The presence of thermal hystersis proteins was indicated by both osmometry on haemolymph samples and recrystallization inhibition studies of springtail homogenates. There was a strong relationship between glycerol content and SCP, but the relationship between haemolymph osmolality, SCP and carbohydrates is uncertain.
Insects may survive subzero temperatures by two general strategies: Freeze-tolerant insects withstand the formation of internal ice, while freeze-avoiding insects die upon freezing. While it is widely recognized that these represent alternative strategies to survive low temperatures, and mechanistic understanding of the physical and molecular process of cold tolerance are becoming well elucidated, the reasons why one strategy or the other is adopted remain unclear. Freeze avoidance is clearly basal within the arthropod lineages, and it seems that freeze tolerance has evolved convergently at least six times among the insects (in the Blattaria, Orthoptera, Coleoptera, Hymenoptera, Diptera and Lepidoptera). Of the pterygote insect species whose cold-tolerance strategy has been reported in the literature, 29% (69 of 241 species studied) of those in the Northern Hemisphere, whereas 85% (11 of 13 species) in the Southern Hemisphere exhibit freeze tolerance. A randomization test indicates that this predominance of freeze tolerance in the Southern Hemisphere is too great to be due to chance, and there is no evidence of a recent publication bias in favour of new reports of freeze-tolerant species. We conclude from this that the specific nature of cold insect habitats in the Southern Hemisphere, which are characterized by oceanic influence and climate variability must lead to strong selection in favour of freeze tolerance in this hemisphere. We envisage two main scenarios where it would prove advantageous for insects to be freeze tolerant. In the first, characteristic of cold continental habitats of the Northern Hemisphere, freeze tolerance allows insects to survive very low temperatures for long periods of time, and to avoid desiccation. These responses tend to be strongly seasonal, and insects in these habitats are only freeze tolerant for the overwintering period. By contrast, in mild and unpredictable environments, characteristic of habitats influenced by the Southern Ocean, freeze tolerance allows insects which habitually have ice nucleators in their guts to survive summer cold snaps, and to take advantage of mild winter periods without the need for extensive seasonal cold hardening. Thus, we conclude that the climates of the two hemispheres have led to the parallel evolution of freeze tolerance for very different reasons, and that this hemispheric difference is symptomatic of many wide-scale disparities in Northern and Southern ecological processes.
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