Physiological responses to temperature in Merizodus soledadinus (Col., Carabidae), a subpolar carabid beetle invading sub-Antarctic islands

Recent human activities and rising air temperature have increased the vulnerability of sub-Antarctic islands to alien species. At the Kerguelen Islands, the predaceous ground beetle Merizodus soledadinus is the only invasive insect originating from the southern cold temperate area (native from Patagonia, Tierra del Fuego and Falkland Islands). This austral origin raises the question of the limits of its physiological tolerance and capability to withstand (1) global change and (2) warmer climates of archipelagos where its accidental transportation could be facilitated from the Kerguelen Islands (namely Amsterdam and Saint Paul). Using gas chromatography/mass spectrometry metabolomics, we compared metabotypes of adults exposed to different temperatures (0, 4, 8, 12, 16, 20 °C). All individuals survived after 2 weeks regardless of the temperature they were exposed to. The physiological changes observed were consistent with increased metabolic rate at increased temperatures, without extreme metabotypes that are characteristic of acute stress. First cues of sublethal stress were observed after prolonged exposure to 20 °C, a warm regime unrealistic for such duration in sub-Antarctic Islands. Overall, M. soledadinus’ thermal tolerance exceeded temperatures currently experienced in nature, suggesting that climate warming may boost its invasion by eliciting its activity and broadening habitat suitability in both invaded and still pristine islands. This thermal tolerance may allow survival aboard ships and development in sub-Antarctic islands with conditions warmer than the Kerguelen Islands, such as Amsterdam and St Paul. Stringent biosecurity measures are thus needed to prevent transfer from Kerguelen to these islands. The native range of this predaceous beetle limited to the Falkland Islands and southernmost South America may be partly constrained by factors other than temperature, such as desiccation, predation or competition.     

Sea water transport and submersion tolerance as dispersal strategies for the invasive ground beetle Merizodus soledadinus (Carabidae)

The alien ground beetle Merizodus soledadinus was introduced to the sub-Antarctic Kerguelen Islands in 1913. It colonized several small islands and islets of this archipelago, without any apparent human assistance in some locations, and crossed several large rivers and alluvial plains. As aggregations of this species on the tidal drift line are common at the Kerguelen Islands, the present work examined whether adult individuals of M. soledadinus could disperse by flotation on the sea. Different sample sizes of ground beetles (from 1 to 10) were placed on sea water at 8°C in plastic vials. Survival (50% lethal times) significantly increased from 2.1 ± 0.2 days for single beetles to 6.5 ± 0.3 days for groups of 10 beetles per vial, with there being no difference in the survival duration for groups of 2, 5, and 10 beetles per vial. Similar survival durations were found for beetles in vials with artificially agitated water and controls. In addition, the duration of survival was twice as high under freshwater versus sea water conditions, when groups of 10 adults were used. Finally, the survival to total submersion in freshwater was evaluated, and ranged from 3 to 4 days. This ability to survive extended periods both floating on and/or submerged beneath salt and freshwater conditions, indicates the presence of a successful dispersal mechanism, which may facilitate the dispersal range of M. soledadinus across the Kerguelen Islands, comprising over 300 islands and islets in total.     

The importance of relative humidity and trophic resources in governing ecological niche of the invasive carabid beetle Merizodus soledadinus in the Kerguelen archipelago

Comprehensive studies to identify species-specific drivers of survival to environmental stress, reproduction, growth, and recruitment are vital to gaining a better understanding of the main ecological factors shaping species habitat distribution and dispersal routes. The present study performed a field-based assessment of habitat distribution in the invasive carabid beetle Merizodus soledadinus for the Kerguelen archipelago. The results emphasised humid habitats as a key element of the insect’s realised niche. In addition, insects faced food and water stress during dispersal events. We evaluated quantitatively how water availability and trophic resources governed the spatial distribution of this invasive predatory insect at Îles Kerguelen. Food and water stress survival durations [in 100%, 70%, and 30% relative humidity (RH) conditions] and changes in a set of primary metabolic compounds (metabolomics) were determined. Adult M. soledadinus supplied with water ad libitum were highly tolerant to prolonged starvation (LT₅₀ = 51.7 ± 6.2 d). However, food-deprived insect survival decreased rapidly in moderate (70% RH, LT₅₀ = 30.37 ± 1.39 h) and low (30% RH, LT₅₀ = 13.03 ± 0.48 h) RH conditions. Consistently, body water content decreased rapidly in insects exposed to 70% and 30% RH. Metabolic variation evidenced the effects of food deprivation in control insects (exposed to 100% RH), which exhibited a progressive decline of most glycolytic sugars and tricarboxylic acid cycle intermediates. Most metabolite levels were elevated levels during the first few hours of exposure to 30% and 70% RH. Augmented alanine and lactate levels suggested a shift to anaerobic metabolism. Simultaneously, peaks in threonine and glycolytic sugars pointed to metabolic disruption and a progressive physiological breakdown in dehydrating individuals. Overall, the results of our study indicate that the geographic distribution of M. soledadinus populations is highly dependent on habitat RH and water accessibility.     

Thermal biology of the alien ground beetle <Emphasis Type="Italic">Merizodus soledadinus</Emphasis> introduced to the Kerguelen Islands

Thermal tolerance is one of the major determinants of successful establishment and spread of invasive aliens. Merizodus soledadinus (Coleoptera, Carabidae) was accidentally introduced to Kerguelen from the Falkland Islands in 1913. On Kerguelen, the climate is cooler than the Falklands Islands but has been getting warmer since the 1990s, in synchrony with the rapid expansion of M. soledadinus. We aimed to investigate the thermal sensitivity in adults of M. soledadinus and hypothesised that climate warming has assisted the colonisation process of M. soledadinus. We examined (1) survival of constant low temperatures and at fluctuating thermal regimes, (2) the critical thermal limits (CT_min and CT_max) of acclimated individuals (4, 8 and 16°C), (3) the metabolic rates of acclimated adults at temperatures from 0 to 16°C. The FTRs moderately increased the duration of survival compared to constant cold exposure. M. soledadinus exhibited an activity window ranged from −5.5 ± 0.3 to 38 ± 0.5°C. The Q ₁₀ after acclimation to temperatures ranging from 0 to 16°C was 2.49. Our work shows that this species is only moderately cold tolerant with little thermal plasticity. The CT_min of M. soledadinus are close to the low temperatures experienced in winter on Kerguelen Islands, but the CT_max are well above summer conditions, suggesting that this species has abundant scope to deal with current climate change.     

Starvation resistance and effects of diet on energy reserves in a predatory ground beetle (Merizodus soledadinus; Carabidae) invading the Kerguelen Islands

The relationship between nutritional requirements and the availability or quality of food is a prime parameter in determining the geographical expansion of invasive insects. At the sub-Antarctic Kerguelen Islands, the invasive ground beetle Merizodus soledadinus becomes the main invertebrate predator when it colonizes new habitats, leading to the local extinction of native fly species. Such changes in the structure of prey communities may alter the energy management (storage and expenditure) of this predator. In this species, we monitored survival and body mass during food deprivation, in addition to evaluating the effects of two distinct diets (maggots versus enchytraeids) on the consumption and restoration of body reserves (sugars and triglycerides). We found that adults can starve for more than 60 days, and feed every 3.76 days on average when food is available. We recorded higher predation rates on maggots, associated with steeper body mass variations, compared to enchytraeids. Sugars and triglycerides were significantly consumed during food deprivation and restored after refeeding, but varied similarly among individuals supplied on the distinct diets. Other parameters may determine the food preferences observed, such as salt content in prey tissues, because M. soledadinus mainly feeds in hypersaline foreshore habitats, and may limit the consumption of osmotic conformers.     

Comparative salinity tolerance in native flies from the subantarctic Kerguelen Islands: a metabolomic approach

The quasi-extirpation of the cabbage Pringlea antiscorbutica in some locations at the Kerguelen Islands has large impacts on the distribution of the native fly Calycopteryx moseleyi. This insect has long been supposed as being subordinant to P. antiscorbutica until both larvae and adults were observed under seaweed in littoral margins. Physiological plasticity to saline conditions is expected in C. moseleyi, and metabolic rearrangements in salt-exposed specimens should thus be similar between individuals from cabbages and seaweeds. Individuals of C. moseleyi from non-saline (cabbages) and saline (seaweeds) habitats were experimentally subjected to different salinities (0, 35, 70 practical salinity units) and compared to the widely distributed native Anatalanta aptera flies that coexist with C. moseleyi under the seaweeds. A progressive drop of the survival and body water content was observed in C. moseleyi from cabbages exposed to increasing saline conditions. Body water contents remained similar at 35 and 70 practical salinity units in C. moseleyi from seaweeds, while it did not change over the whole saline gradient in A. aptera. Metabolic profiles revealed that both fly populations from the seaweeds accumulated compatible solutes in the form of alanine or glutamic acid when they were exposed to salinity. A distinct pattern was observed in C. moseleyi specimens from cabbages, whose metabolic profiles revealed a progressive loss of metabolic homoeostasis. We conclude that the C. moseleyi specimens from the cabbages and seaweeds differentiated, as also supported by their contrasted morphotypes, and that the limited salinity tolerance of individuals from cabbages may hinder their future expansion to seaweeds.     

Variation of morphometric traits in populations of an invasive carabid predator (<Emphasis Type="Italic">Merizodus soledadinus</Emphasis>) within a sub-Antarctic island

Invasive predators may change their own trophic conditions by progressively displacing or reducing diversity and abundance of native prey. As food quality and quantity are two main factors determining adult body size in arthropods, alteration of the available resources may thus affect predators’ morphology. The flightless carabid beetle Merizodus soledadinus was accidentally introduced to Iles Kerguelen in a single site in 1913. Its successful spreading process has been monitored over the long term, providing an exceptional research opportunity with multiple snapshots of similar colonized sites mostly differing by the residence time of M. soledadinus. To test if M. soledadinus’ morphology is correlated with its residence time in each habitat, we measured nine morphometric traits in five populations. We detected significant morphological differences: individuals from the first colonized site were the smallest, whereas individuals from the most recently colonized site were the largest. Our study also highlighted among-site variation in sexual dimorphism of the last abdominal sternite: its length differed between sites for females, but not for males. We discuss this diminution of M. soledadinus’ size in the light of both a priori (development under diet restriction, survival) and a posteriori (intrapopulation competition, cannibalism) effects on growth and development.     

The significance of the sub-Antarctic Kerguelen Islands for the assessment of the vulnerability of native communities to climate change,alien insect invasions and plant viruses

The suite of environments and anthropogenic modifications of sub-Antarctic islands provide key opportunities to improve our understanding of the potential consequences of climate change and biological species invasions on terrestrial ecosystems. The profound impact of human introduced invasive species on indigenous biota, and the facilitation of establishment as a result of changing thermal conditions, has been well documented on the French sub-Antarctic Kerguelen Islands (South Indian Ocean). The present study provides an overview of the vulnerability of sub-Antarctic terrestrial communities with respect to two interacting factors, namely climate change and alien insects. We present datasets assimilated by our teams on the Kerguelen Islands since 1974, coupled with a review of the literature, to evaluate the mechanism and impact of biological invasions in this region. First, we consider recent climatic trends of the Antarctic region, and its potential influence on the establishment, distribution and abundance of alien insects, using as examples one fly and one beetle species. Second, we consider to what extent limited gene pools may restrict alien species’ colonisations. Finally, we consider the vulnerability of native communities to aliens using the examples of one beetle, one fly, and five aphid species taking into consideration their additional impact as plant virus vectors. We conclude that the evidence assimilated from the sub-Antarctic islands can be applied to more complex temperate continental systems as well as further developing international guidelines to minimise the impact of alien species.     

Breeding system of the subantarctic plant species Pringlea antiscorbutica R. Br. and search for potential insect pollinators in the Kerguelen Islands

The reproductive biology of Pringlea antiscorbutica R. Br. (Brassicaceae), an endemic species from the southern Indian Ocean islands, is investigated here. Controlled crosses were performed between plants grown in a common garden on the Kerguelen Islands. Searching for potential insect pollinators, we investigated the flying ability of all insects known from the Kerguelen Islands. We showed evidence for self-compatibility, low pollen limitation in the absence of a biotic pollen vector and slight selfing depression in P. antiscorbutica. The insects present on the islands are mostly wingless and are not likely to be efficient pollinators of this species. Since P. antiscorbutica shows morphological adaptations to insect pollination despite the absence of pollinators in its present range, we conclude that this species recently evolved from insect pollination to wind and/or autonomous pollination.     

Habitat phenotyping of two sub-Antarctic flies by metabolic fingerprinting: evidence for a species outside its home?

Metabolic fingerprinting can elucidate rearrangements of metabolic networks in organisms exposed to various environmental conditions. Maintenance of organismal performance occurs by alterations in metabolic fluxes and pathways, resulting in habitat-specific metabolic signatures. Several insects of sub-Antarctic Islands, including the wingless flies Anatalanta aptera and Calycopteryx moseleyi, are exposed to saline organic matter accumulated along littoral margins. However, C. moseleyi has long been considered restricted to a habitat of lower salinity, the Kerguelen cabbage. High C. moseleyi densities identified in saline decaying seaweeds are intriguing, and may involve osmoregulatory adjustments including accumulation of osmoprotectants. In the present work, we examined quantitative metabotypes (metabolic phenotypes) among wild C. moseleyi individuals from seaweeds versus non-saline Kerguelen cabbages. They were compared to metabotypes from wild A. aptera, a common fly on seaweed. Statistical procedures designed to magnify between-class differences failed to clearly separate C. moseleyi metabotypes from cabbage and seaweed, despite contrasted morphotypes, diets, and salinities. A. aptera exhibited higher glycerol, inositol, trehalose, and other osmoprotectants concentrations that may enhance its performance under saline environments. Seaweed may represent a secondary niche in C. moseleyi, promoted by the marked reduction in Kerguelen cabbage frequency subsequent to climate change, and herbivorous pressures caused by rabbit invasion.     

Accumulation of organic and inorganic solutes in the subantarctic cruciferous species Pringlea antiscorbutica in response to saline and cold stresses

Pringlea antiscorbutica R. Br., a subantarctic endemic cruciferous species, is endangered in its natural sites by several ecological changes. This species is tolerant to salinity and a permanent cold temperature on Kerguelen and Crozet Islands. We attempted the investigation of regulating mechanisms of osmotic adjustment in this species. ¹³C NMR analyses of water-soluble compounds from leaves collected from the field revealed glucose and proline to be the main accumulated organic solutes. Colorimetric determinations in these samples showed that proline and soluble carbohydrates were present at remarkably high levels. When young plants were cultivated in growth chambers they showed a good resistance to cold and medium resistance to saline conditions. High levels of soluble carbohydrates were present in all situations. Proline was accumulated in response to a saline and a cold treatment. The quantitative variations of the pool of proline in response to saline treatments were rapid and important. The adaptive value of these responses of organic solutes in the tolerance of Pringlea antiscorbutica to various stresses is discussed. Received: 16 June 1997 / Accepted: 5 May 1998     

Wing morphology of the active flyer Calliphora vicina (Diptera: Calliphoridae) during its invasion of a sub‐Antarctic archipelago where insect flightlessness is the rule

The cosmopolitan blowfly Calliphora vicina became established in the sub‐Antarctic Kerguelen Islands in the late 1970s, following a warming period that allowed its full development. Although temperature and wind may limit flight activity, the fly invaded the archipelago, reaching sites remote from the introduction point. Most native competitors have converged to flightlessness as a response to stringent environmental conditions and therefore the flight strategy of C. vicina might be either a handicap or a competitive advantage under ongoing climate change. Using geometric morphometrics, we investigated whether the wing had changed over time in C. vicina within the archipelago (1998 vs. 2009) and compared its morphology with that of a continental population from a temperate area (1983 vs. 2009). Wing shape plasticity to temperature was also experimentally investigated. We found no clues of relaxed selection on flight morphology in the range invaded. However, rapid changes of wing shape occurred over time in females from the Kerguelen Islands compared with both males and females of the continental population, despite a shorter time‐lag between samples in the former. The thermal reaction norms for wing shape found for C. vicina from Kerguelen were also different from those of the continental population, but it remains unknown whether this resulted from or preceded the introduction. These combined findings are consistent with a fingerprint of local adaptation in the invasive population. However, the adaptive significance of the changes, in terms of their aerodynamic consequences and the future evolution of C. vicina in the Kerguelen Islands, requires further investigation. From an evolutionary standpoint, sustaining flight capability under the novel sub‐Antarctic conditions might be critical to the invasive success of C. vicina as most competitors are flightless.     

Genetic differences and environments of mussel populations in Kerguelen Islands

Summary Samples of subantarctic mussels, Mytilus desolationis, from 12 locations in the Kerguelen Islands (South Indian Ocean) were analysed electrophoretically at 5 polymorphic loci to study correlations between genotype frequencies and environmental factors. Thirty-one out 48 pairs (population-locus) were not in Hardy-Weinberg equilibrium proportions, and 41 out 60 showed heterozygote deficiency. Spatial heterogeneity analysed with correspondence analysis was observed at 3 loci (Lap2, Pgd and Pgm). The genetic differentiation of M. desolationis could be explained through both geographical origin of populations and adaptation to environmental conditions. Within each geographical group, the first parameter influencing spatial structure is salinity. Additional differentiation is related to a factor linked to maximal size and to a lesser extent to shore exposure. The higher genetic differentiation occurring within the Kerguelen populations than among continental populations could correspond to incomplete panmixia due to a reduced gene flow versus constant external immigration in continental populations.     

Attraction of the predator,Harmonia axyridis (Coleoptera: Coccinellidae), to its prey,Myzus persicae (Hemiptera: Aphididae), feeding on Chinese cabbage

The predatory multicolored Asian lady beetle, Harmonia axyridis, was attracted to volatiles released from Chinese cabbage infested by the green peach aphid, Myzus persicae, in T-tube olfactometer choice tests. However, lady beetle adults and larvae did not respond to clean air, Chinese cabbage alone or green peach aphid alone. Of different prey densities, H. axyridis adults were most attracted to Chinese cabbage infested by 60 M. persicae adults after 24 h. However, H. axyridis larvae were not attracted to Chinese cabbage infested by M. persicae. Mechanically damaged Chinese cabbage attracted neither lady beetle adults nor larvae. Predatory adults were attracted to 60 M. persicae adults after 24 and 48 h, and to 90 M. persicae adults after 12 h, suggesting that the predatory response depends on the prey density. Lady adult beetles did not prefer the volatiles induced by Diamondback moth, Plutella xylostella, indicating that specific host insect specificity attracts respective natural enemies. It can be explained that the volatile compounds emitted from the host plant as a result of herbivore attack preferred by the specific insect species.     

The Implications of Habitat Management on the Population Viability of the Endangered Ohlone Tiger Beetle (Cicindela ohlone) Metapopulation

Despite their role in providing ecosystem services, insects remain overlooked in conservation planning, and insect management approaches often lack a rigorous scientific basis. The endangered Ohlone tiger beetle (Cicindela ohlone) occurs in a 24-km² area in Santa Cruz County, California. The once larger metapopulation now consists of subpopulations inhabiting five patches of coastal prairie where it depends on bare ground for mating, foraging, and oviposition. Human activities have eliminated natural disturbances and spread invasive grasses, reducing C. ohlone''s bare-ground habitat. Management actions to restore critical beetle habitat consist of cattle and horse grazing, maintaining slow bicycle speeds on occupied public trails, and artificial creation of bare-ground plots. Recreational biking trails help maintain bare ground, but can cause beetle mortality if left unregulated. We tracked C. ohlone survivorship and estimated fecundity for three years. We then constructed a stage-structured population projection matrix model to estimate population viability among the five patches, and to evaluate the success of management interventions. We demonstrate that habitat creation, regulation of bicycle speed, and migration between patches increase C. ohlone survival and population viability. Our results can be directly applied to management actions for conservation outcomes that will reduce species extinction risk and promote recolonization of extirpated patches.     

Fish Heat Shock Cognate 70 Derived AMPs <Emphasis Type="Italic">Cs</Emphasis>HSC70 A1 and <Emphasis Type="Italic">Cs</Emphasis>HSC70 A2

Heat shock cognate 70 (HSC70) is an important evolutionary conserved protein that plays a major role in maintaining the homeostasis and immunity of many organisms. In this study, a HSC70 from Channa striatus was identified from its cDNA library and characterized using bioinformatics and molecular biology tools. CsHSC70 cDNA was 1953 base pair (bp) in length along with an open reading frame which encoded a polypeptide of 650 amino acid residues. Tissue distribution results showed that CsHSC70 was considerably expressed in gill, to a lesser extent in head kidney, blood, spleen and liver and at low level in other tissues. Using C. striatus gill as cell model, effects of fungal, bacterial and poly I:C stimulant on the mRNA levels of CsHSC70 was examined. We also described the antimicrobial features of two peptides namely CsHSC70 A1and CsHSC70 A2 derived from the N-terminal of CsHSC70 protein. CsHSC70 A1 peptide (40 µg/ml) exhibited potent bactericidal activity against Micrococcus luteus cells. Flow cytometric analysis revealed that the M. luteus cells stained with propidium iodide, upon treated with CsHSC70 A1 at the concentration of 40 µM/ml showed 38% survival compared to its control (99.6%). It seems that CsHSC70 A1 peptide shows antimicrobial activity against M. luteus through membrane disruption. Additionally, scanning electron microscope (SEM) observation confirmed that CsHSC70 A1 peptide treatment completely damaged and destructed the M. luteus cells. Taken together, these findings suggest that CsHSC70 A1 peptide could be a safe and potential therapeutic molecule substitute to antibiotics in various clinical fields.     

Behavioral interactions under multiple stressors: temperature and salinity mediate aggression between an invasive and a native fish

Interspecific aggression is a critical determinant of the success and competitive superiority of many invasive over native species. While single abiotic stressors can alter aggression levels, the manner in which multiple stressors may alter the strength and outcome of interspecific interactions and hence the invasion potential of a species is still poorly understood, even though multiple stressors are prevalent in many ecosystems. Furthermore, multiple stressors may interact to produce synergistic or antagonistic effects on individual level behaviors, thereby modulating invasive-native species interactions in unexpected ways. Here we examined the effect of two key abiotic stressors in freshwater ecosystems-temperature and salinity-on interspecific aggression between the invasive eastern mosquito fish (Gambusia holbrooki) and juveniles of the native Australian bass (Macquaria novemaculeata). Under controlled laboratory conditions, individuals were exposed to low or high salinity levels (15 and 35‰), and low or high temperatures (21 and 28 °C), and the frequency of interspecific aggressive behaviors was scored. The effect of temperature and salinity on interspecific aggression was antagonistic for both M. novemaculeata and G. holbrooki. While elevated temperature promoted aggression, elevated salinity partially or entirely negated this effect. Moreover, regardless of temperature, M. novemaculeata was more aggressive than G. holbrooki under elevated salinity. In addition to this, the native displayed more aggression to smaller than larger heterospecifics when exposed to elevated salinity alone, while G. holbrooki showed no such preference. These results highlight the importance of considering the interplay between multiple abiotic stressors and behavioral interactions between invasive and native species, combined with the modulating effect of species-specific and size based responses to those stressors.     

Saline stress tolerance partly matches with habitat preference in ground‐living wolf spiders

Salinity interacts with many physiological functions and therefore probably influences the distribution of terrestrial fauna in tidal flooded salt marshes. The present study tests the hypothesis that the physiological tolerance of stenotopic wolf spiders for saline conditions at least partially determines their occurrence throughout salt‐marsh and nonsaline habitats. The duration of survival of three stenotopic wolf spider species (Araneae: Lycosidae) with different habitat preferences is compared in a controlled laboratory experiment. The forest‐dwelling Pardosa saltans, the salt‐marsh resident Pardosa purbeckensis and its sister species the inland‐living Pardosa agrestis are exposed to experimental conditions with different levels of salinity. Individuals (45 males and 20–45 females per treatment) are placed in individual air‐tight boxes filled with water‐saturated sand. Three levels of salinity are tested: nonsaline (0‰), medium saline (33–35‰) and highly saline (66–70‰). Contents of carbon, hydrogen and nitrogen and the molar ration carbon/nitrogen remain constant over time and do not differ among salinity treatments, indicating that starvation effects on survival, if any, are similar for all treatments. Conversely, body water significantly decreases over time and differs among salinity treatments, in accordance with patterns of survival. Conforming to their habitat preference, the survival of P. saltans and P. agrestis decreases quickly under highly saline conditions. Pardosa purbeckensis, however, has a high survival under both saline and nonsaline conditions. The duration of survival of females is significantly lower than that of males of P. saltans and P. purbeckensis. Durations of survival of ground‐living wolf spiders exposed to salinity partly match their habitat distribution but do not explain the restriction of salt‐marsh species to saline habitats.