Alpine Grasshopper Research Articles

Food plant odor perception in three sympatric alpine grasshopper species (Orthoptera: Acrididae: Catantopinae) in Aotearoa New Zealand

The alpine grasshoppers Sigaus nivalis, Sigaus australis and Sigaus nitidus are sympatric in the central mountains of South Island, Aotearoa New Zealand. These grasshoppers feed on a range of alpine plants but show preference towards dicots over monocots. Because herbivorous insects often use smell and taste to locate and recognize food plants it was expected that these grasshoppers would show sensitivity to their favorite foods and potential sensitivity to nonhost plants. Here, we determined feeding preference in captivity allowing each of these three sympatric grasshoppers the same choice of six native alpine plant species. We analyzed the chemical compositions of the plants used in these experiments using gas-chromatograph coupled with mass-spectrometry (GC-MS) and then recorded olfactory responses in the grasshoppers to plant-derived smells (with synthetic compounds) using electroantennogram (EAG). The grasshoppers were able to distinguish between the potential food plants and ate the shrub Coriaria sarmentosa but not the grass Chionochloa pallens, however, the chemicals we detected in the six plant species were very similar. High sensitivity to fatty acid derived aldehydes (decanal, (E,Z)-2,6-nonadienal, hexanal) and a 6-carbon alcohol ((Z)-2-hexen-1-ol) compared to terpenoids (α-phellandrene, β-myrcene, β-ocimene, eucalyptol, (S)-(-)-limonene, (1S)-(-)-α-pinene) or an aromatic compound (2-phenylethanol) was recorded in the antennae of all three grasshopper species and no species- or sex-specific sensitivity to particular compounds was observed. As aldehydes and alcohols are emitted upon plant damage, it is possible that these generalist grasshoppers are sensitive to the smells of damaged plants rather than species-specific plant smells.

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets.

Bacteria colonize the body of macroorganisms to form associations ranging from parasitic to mutualistic. Endosymbiont and gut symbiont communities are distinct microbiomes whose compositions are influenced by host ecology and evolution. Although the composition of horizontally acquired symbiont communities can correlate to host species identity (i.e. harbor host specificity) and host phylogeny (i.e. harbor phylosymbiosis), we hypothesize that the microbiota structure of vertically inherited symbionts (e.g. endosymbionts like Wolbachia) is more strongly associated with the host species identity and phylogeny than horizontally acquired symbionts (e.g. most gut symbionts). Here, using 16S metabarcoding on 336 guts from 24 orthopteran species (grasshoppers and crickets) in the Alps, we observed that microbiota correlated to host species identity, i.e. hosts from the same species had more similar microbiota than hosts from different species. This effect was ~5 times stronger for endosymbionts than for putative gut symbionts. Although elevation correlated with microbiome composition, we did not detect phylosymbiosis for endosymbionts and putative gut symbionts: closely related host species did not harbor more similar microbiota than distantly related species. Our findings indicate that gut microbiota of studied orthopteran species is more correlated to host identity and habitat than to the host phylogeny. The higher host specificity in endosymbionts corroborates the idea that-everything else being equal-vertically transmitted microbes harbor stronger host specificity signal, but the absence of phylosymbiosis suggests that host specificity changes quickly on evolutionary time scales.

Mwhitiwhiti Aotearoa: Phylogeny and synonymy of the silent alpine grasshopper radiation of New Zealand (Orthoptera: Acrididae).

Aotearoa New Zealand has a fauna of endemic alpine grasshoppers, consisting of thirteen species distributed among four genera. The many re-classifications of species within this group and the presence of species complexes highlight the uncertainty that surrounds relationships within and between these genera. High-throughput Next Generation Sequencing was used to assemble the complete mitochondrial genomes, 45S ribosomal cassettes and histone sequences of New Zealands four endemic alpine genera: Alpinacris, Brachaspis, Paprides and Sigaus. Phylogenetic analysis of these molecular datasets, as individual genes, partitions and combinations returned a consistent topology that is incompatible with the current classification. The genera Sigaus, Alpinacris, and Paprides all exhibit paraphyly. A consideration of the pronotum, epiphallus and terminalia of adult specimens reveals species-specific differences, but fails to provide compelling evidence for species groups justifying distinct genera. In combination with phylogenetic, morphological and spatial evidence we propose a simplified taxonomy consisting of a single genus for the mwhitiwhiti Aotearoa species radiation.

Puke or poop? Comparison of regurgitate and faecal samples to infer alpine grasshopper (Paprides nitidus Hutton) diet in experimental plant communities.

Characterising plant-herbivore interactions is important to understanding the processes that influence community structure and ecosystem functioning. Traditional methods used to identify plant-herbivore interactions are being superseded by non-destructive molecular approaches that can infer interactions with greater resolution and accuracy from environmental DNA (e.g. faeces and regurgitate). However, few studies have compared the success of using different sample types and whether they provide similar or contrasting information about species' diet. Here we compared the success of DNA amplification and host plant species identification using restriction fragment length polymorphism (RFLP) applied to faecal and regurgitate samples collected from alpine grasshoppers Paprides nitidus Hutton during a grassland community mesocosm experiment. We found that DNA amplification success was 23% and 86% higher for faecal than regurgitate samples from female and male grasshoppers, respectively. In contrast, successful host plant identification using RFLP was 9% higher for regurgitate than faecal samples. The mean number of host plant species identified per sample (1.40) did not differ between sample types or grasshopper sexes. Of the 136 paired faecal-regurgitate samples, just 41% and 74% produced exactly or partially matching host plant identifications, respectively, indicating that different sample types provided complementary information about herbivore diet. Some plant species were more likely to be identified from faecal samples than expected by chance, and we found that this identification bias skewed towards plant species with higher investment in leaf tissue. We conclude that multiple sample types may be required to fully characterise an invertebrate herbivore species' diet.

Abundance and distribution of antennal sensilla on males and females of three sympatric species of alpine grasshopper (Orthoptera: Acrididae: Catantopinae) in Aotearoa New Zealand

Brachaspis nivalis, Sigaus australis and Paprides nitidus are grasshopper species endemic to Aotearoa, New Zealand where they are sympatric in several regions of South Island. On mountains of Kā Tiritiri o te Moana (Southern Alps), B. nivalis is more abundant on scree/rock habitat, whereas S. australis and P. nitidus are prevalent in alpine tussock and herbfields. It is expected, therefore, that these species have different sensory needs that are likely to be apparent in the type, abundance, and distribution of chemo-sensilla on their antennae. It is also likely that natural selection has resulted in sexual differences in sensilla. To test these hypotheses, abundance and distribution of the chemo-sensilla on the dorsal and ventral surfaces of their antennae were characterized in adult males and females of the three species. Five types of chemo-sensilla were identified on the distal portion of their antenna: chaetica, basiconica, trichoidea, coeloconica, and cavity. All species had significantly more chemo-sensilla on the ventral than the dorsal surface of antennae and a similar distribution pattern of chemo-sensilla. Despite having relatively short antenna, B. nivalis had the largest number of olfactory sensilla, but the fewest chaetica of the three species studied. A plausible explanation is that B. nivalis is abundant on less vegetated habitats compared to the other species, and therefore may rely more on olfaction (distance) than gustatory (contact) reception for finding food. No significant differences were observed between the sexes of B. nivalis and P. nitidus, however, S. australis males had significantly more basiconica sensilla than females.

Population dynamics of an alpine grasshopper (Orthoptera) community over 30 years and the effects of climate warming and grazing

Population dynamics of an alpine grasshopper (Orthoptera) community over 30 years and the effects of climate warming and grazing

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic-based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.

Digest: Dispersal reduction drives rapid diversification in alpine grasshoppers.

Dispersal-associated traits -such as flight ability- influence how species move across the landscape, and can dramatically impact their distributions and patterns of genetic structure. Ortego etal. examine genomic data from two recently diverged alpine grasshopper lineages with distinct wing sizes to assess the demographic impacts of flight loss. The authors showed that flight loss may lead to asymmetric introgression during speciation, and can significantly increase rates of intraspecific diversification.

Climate and ice in the last glacial maximum explain patterns of isolation by distance inferred for alpine grasshoppers

Abstract Cold‐adapted species are likely to have had more widespread ranges and greater population connectivity during the last glacial period than is the case today. This contrasts with the trend in many species for range and population size to increase during interglacials. We examined the pattern of genetic and morphological variation within an endemic, wingless, alpine grasshopper Sigaus australis (Orthoptera: Acrididae) in the Southern Alps of New Zealand, testing for isolation by distance using geometric morphometric and mitochondrial ND2 sequences to document variation. Presence/absence data were analysed to estimate the environmental envelope (niche) of Sigaus australis and the resulting model used to infer the extent of available habitat for the species during the last glacial maximum. Estimates of past range size were modified using models of montane ice extent during the LGM. Clinal patterns of pronotum shape variation and signatures of isolation by distance support the hypothesis of a formerly more connected species. A north/south division was observed in pronotum shape, but the phenotypic variation was not diagnostic, as one would expect within a single species. Although the current habitat area occupied by Sigaus australis is much smaller than estimates for the LGM from our climate model, we show that realised area differed less due to the extension of valley glaciers. However, the current distribution of S. australis is more fragmented than in the past. This and other flightless alpine species currently restricted to fragmented high elevation habitat demonstrate genetic lag but are subject to loss of diversity as anthropogenic climate warming proceeds.

Elevational partitioning in species distribution, abundance and body size of Australian alpine grasshoppers (Kosciuscola)

AbstractChanges in the physical environment with elevation can influence species distributions and their morphological traits. In mountainous regions, steep temperature gradients can result in patterns of ecological partitioning among species that potentially increases their vulnerability to climate change. We collected data on species distributions, relative abundance and body size for three grasshopper species of the genus Kosciuscola (K. usitatus, K. tristis and K. cognatus) at three locations within the mountainous Kosciuszko National Park in Australia (Thredbo, Guthega and Jagungal). All three species showed differences in their distributions according to elevation, with K. usitatus ranging from 1400 to 2000 m asl, K. tristis from 1600 to 2000 m asl and K. cognatus from 1550 to 1900 m asl. Decreasing relative abundance with increasing elevation was found for K. usitatus, but the opposite pattern was found for K. tristis. The relative abundance of K. cognatus did not change with elevation but was negatively correlated with foliage cover. Body size decreased with elevation in both male and female K. usitatus, which was similarly observed in female K. tristis and male K. cognatus. Our results demonstrate spatial partitioning of species distributions and clines in body size in relation to elevational gradients. Species‐specific sensitivities to climatic gradients may help to predict the persistence of this grasshopper assemblage under climate change.

An alpine grasshopper radiation older than the mountains, on Kā Tiritiri o te Moana (Southern Alps) of Aotearoa (New Zealand)

In New Zealand, 13 flightless species of endemic grasshopper are associated with alpine habitats and freeze tolerance. We examined the phylogenetic relationships of the New Zealand species and a subset of Australian alpine grasshoppers using DNA sequences from the entire mitochondrial genome, nuclear 45S rRNA and Histone H3 and H4 loci. Within our sampling, the New Zealand alpine taxa are monophyletic and sister to a pair of alpine Tasmanian grasshoppers. We used six Orthopteran fossils to calibrate a molecular clock analysis to infer that the most recent common ancestor of New Zealand and Tasmanian grasshoppers existed about 20 million years ago, before alpine habitat was available in New Zealand. We inferred a radiation of New Zealand grasshoppers ~13–15 Mya, suggesting alpine species diversification occurred in New Zealand well before the Southern Alps were formed by the mountain building events of the Kaikoura Orogeny 2–5 Mya. This would suggest that either the ancestors of today’s New Zealand grasshoppers were not dependent on living in the alpine zone, or they diversified outside of New Zealand.

Green-brown polymorphism in alpine grasshoppers affects body temperature.

Ectothermic animals depend on external heat sources for pursuing their daily activities. However, reaching sufficiently high temperature can be limiting at high altitudes, where nights are cold and seasons short. We focus on the role of a green‐brown color polymorphism in grasshoppers from alpine habitats. The green‐brown polymorphism is phylogenetically and spatially widespread among Orthopterans and the eco‐evolutionary processes that contribute to its maintenance have not yet been identified.We here test whether green and brown individuals heat up to different temperatures under field conditions. If they do, this would suggest that thermoregulatory capacity might contribute to the maintenance of the green‐brown polymorphism.We recorded thorax temperatures of individuals sampled and measured under field conditions. Overall, thorax temperatures ranged 1.7–42.1°C. Heat up during morning hours was particularly rapid, and temperatures stabilized between 31 and 36°C during the warm parts of the day. Female body temperatures were significantly higher than body temperatures of males by an average of 2.4°C. We also found that brown morphs were warmer by 1.5°C on average, a pattern that was particularly supported in the polymorphic club‐legged grasshopper Gomphocerus sibiricus and the meadow grasshopper Pseudochorthippus parallelus.The difference in body temperature between morphs might lead to fitness differences that can contribute to the maintenance of the color polymorphism in combination with other components, such as crypsis, that functionally trade‐off with the ability to heat up. The data may be of more general relevance to the maintenance of a high prevalence polymorphism in Orthopteran insects.

Gradual Distance Dispersal Shapes the Genetic Structure in an Alpine Grasshopper.

The location of the high mountains of southern Europe has been crucial in the phylogeography of most European species, but how extrinsic (topography of sky islands) and intrinsic features (dispersal dynamics) have interacted to shape the genetic structure in alpine restricted species is still poorly known. Here we investigated the mechanisms explaining the colonisation of Cantabrian sky islands in an endemic flightless grasshopper. We scrutinised the maternal genetic variability and haplotype structure, and we evaluated the fitting of two migration models to understand the extant genetic structure in these populations: Long-distance dispersal (LDD) and gradual distance dispersal (GDD). We found that GDD fits the real data better than the LDD model, with an onset of the expansion matching postglacial expansions after the retreat of the ice sheets. Our findings suggest a scenario with small carrying capacity, migration rates, and population growth rates, being compatible with a slow dispersal process. The gradual expansion process along the Cantabrian sky islands found here seems to be conditioned by the suitability of habitats and the presence of alpine corridors. Our findings shed light on our understanding about how organisms which have adapted to live in alpine habitats with limited dispersal abilities have faced new and suitable environmental conditions.

Male mate choice in the chameleon grasshopper (Kosciuscola tristis)

AbstractIn many species, males can increase their fitness by mating with the highest quality females. Female quality can be indicated by cues, such as body size, age and mating status. In the alpine grasshopper Kosciuscola tristis, males can be found riding on subadult females early in the season, and as the season progresses, males engage in fights over ovipositing females. These observations suggest that males may be competing for females that are either unmated (early season) or sperm‐depleted (late season). We thus hypothesised that male K. tristis may be choosy in relation to female mating status, and specifically, we predicted that males prefer females that are unmated. We conducted behavioural experiments in which males were given the choice of two females, one mated and one unmated. Contrary to our prediction, males did not mate preferentially with unmated females. However, copulation duration with unmated females was, on average, 24 times the length of copulation with mated females. While female K. tristis can reject mates, we did not observe any evidence of overt female choice during our trials. Females may gain additional benefits from mating multiply and may therefore not readily reject males. While our experiment cannot definitively disentangle female from male control over copulation duration, we suggest that males choose to invest more time in copula with unmated females, perhaps for paternity assurance, and that male mate assessment occurs during copulation rather than beforehand.

Spatial analyses of two color polymorphisms in an alpine grasshopper reveal a role of small-scale heterogeneity.

Discrete color polymorphisms represent a fascinating aspect of intraspecific diversity. Color morph ratios often vary clinally, but in some cases, there are no marked clines and mixes of different morphs occur at appreciable frequencies in most populations. This poses the questions of how polymorphisms are maintained. We here study the spatial and temporal distribution of a very conspicuous color polymorphism in the club‐legged grasshopper Gomphocerus sibiricus. The species occurs in a green and a nongreen (predominately brown) morph, a green–brown polymorphism that is common among Orthopteran insects. We sampled color morph ratios at 42 sites across the alpine range of the species and related color morph ratios to local habitat parameters and climatic conditions. Green morphs occurred in both sexes, and their morph ratios were highly correlated among sites, suggesting shared control of the polymorphism in females and males. We found that in at least 40 of 42 sites green and brown morphs co‐occurred with proportions of green ranging from 0% to 70% with significant spatial heterogeneity. The proportion of green individuals tended to increase with decreasing summer and winter precipitations. Nongreen individuals can be further distinguished into brown and pied individuals, and again, this polymorphism is shared with other grasshopper species. We found pied individuals at all sites with proportions ranging from 3% to 75%, with slight, but significant variation between years. Pied morphs show a clinal increase in frequency from east to west and decreased with altitude and lower temperatures and were more common on grazed sites. The results suggest that both small‐scale and large‐scale spatial heterogeneity affects color morph ratios. The almost universal co‐occurrence of all three color morphs argues against strong effects of genetic drift. Instead, the data suggest that small‐scale migration–selection balance and/or local balancing selection maintain populations polymorphic.

Within-season variability of fighting behaviour in an Australian alpine grasshopper.

Throughout the breeding season, changing environmental and biological conditions can lead to variation in the reproductive landscape of many species. In alpine environments temperature is a key driver of behaviour for small ectotherms such as insects, but variable biotic factors such as mate quality and availability can also influence behaviour. Kosicuscola tristis is a small semelparous grasshopper of the Australian alpine region. In a rare behaviour among grasshoppers, K. tristis males engage in vigorous fights over access to females, involving mandible displays, kicking, biting and grappling. In this study we describe the variation in fighting behaviour of K. tristis throughout the breeding season and test several hypotheses related to temperature, body size, mating behaviour, and female quality. We show that K. tristis males are more aggressive toward each other at the end of the breeding season than at the beginning. This increased aggression is associated with decreased daily average temperatures (from ~20°C to ~9°C), decreased mating activity, increased female fecundity, and an unexpected trend toward an increase in female-to-male aggression. These results suggest that K. tristis is likely under increased selective pressure to time key life cycle events with favourable biological and climatic conditions. The stochastic nature of alpine environments combined with a relatively short life span and breeding season, as well as limited mating opportunities toward the end of the season may have contributed to the evolution of this extraordinary mating system.

MicroRNAs of the mesothorax in Qinlingacris elaeodes, an alpine grasshopper showing a wing polymorphism with unilateral wing form.

MicroRNAs (miRNAs) are now recognized as key post-transcriptional regulators in regulation of phenotypic diversity. Qinlingacris elaeodes is a species of the alpine grasshopper, which is endemic to China. Adult individuals have three wing forms: wingless, unilateral-winged and short-winged. This is an ideal species to investigate the phenotypic plasticity, development and evolution of insect wings because of its case of unilateral wing form in both the sexes. We sequenced a small RNA library prepared from mesothoraxes of the adult grasshoppers using the Illumina deep sequencing technology. Approximately 12,792,458 raw reads were generated, of which the 854,580 high-quality reads were used only for miRNA identification. In this study, we identified 49 conserved miRNAs belonging to 41 families and 69 species-specific miRNAs. Moreover, seven miRNA*s were detected both for conserved miRNAs and species-specific miRNAs, which were supported by hairpin forming precursors based on polymerase chain reaction. This is the first description of miRNAs in alpine grasshoppers. The results provide a useful resource for further studies on molecular regulation and evolution of miRNAs in grasshoppers. These findings not only enrich the miRNAs for insects but also lay the groundwork for the study of post-transcriptional regulation of wing forms.

What triggers colour change? Effects of background colour and temperature on the development of an alpine grasshopper.

BackgroundColour polymorphisms are a fascinating facet of many natural populations of plants and animals, and the selective processes that maintain such variation are as relevant as the processes which promote their development. Orthoptera, the insect group that encompasses grasshoppers and bush crickets, includes a particularly large number of species that are colour polymorphic with a marked green-brown polymorphism being particularly widespread. Colour polymorphism has been associated with the need for crypsis and background matching and background-dependent homochromy has been described in a few species. However, when and how different environmental conditions influence variation in colour remains poorly understood. Here we test for effects of background colour and ambient temperature on the occurrence of colour morph switches (green to brown or brown to green) and developmental darkening in the alpine dwelling club-legged grasshopper Gomphocerus sibiricus.ResultsWe monitored individually housed nymphae across three of their four developmental stages and into the first week after final ecdysis. Our data show an absence of colour morph switches in G. sibiricus, without a single switch observed in our sample. Furthermore, we test for an effect of temperature on colouration by manipulating radiant heat, a limiting factor in alpine habitats. Radiant heat had a significant effect on developmental darkening: individuals under low radiant heat tended to darken, while individuals under high radiant heat tended to lighten within nymphal stages. Young imagoes darkened under either condition.ConclusionsOur results indicate a plastic response to a variable temperature and indicate that melanin, a multipurpose pigment responsible for dark colouration and presumed to be costly, seems to be strategically allocated according to the current environmental conditions. Unlike other orthopterans, the species is apparently unable to switch colour morphs (green/brown) during development, suggesting that colour morphs are determined genetically (or very early during development) and that other processes have to contribute to crypsis and homochromy in this species.

Plastic Responses to Temperature Versus Local Adaptation at the Cold Extreme of the Climate Gradient

Climate is a strong selection agent at high elevations, but experimental examinations of how animals exclusive of highlands cope with its variation are scarce. We analysed temperature-induced variation of early ontogenetic traits in the alpine grasshopper Chorthippus cazurroi, and compared populations from the elevational extremes of the species distribution under laboratory conditions spanning natural temperature ranges. Neither elevation of origin, nor different growing temperatures, had a direct effect on nymph body size, but both factors contributed to size at hatching indirectly, via their effect on the duration of embryo development. Large emerging nymphs had a consistently greater survival, although small and fast-developing nymphs from highlands also performed well at low temperatures. Viability selection favoured fast-developing phenotypes in conditions in which plasticity delayed development, in a typical countergradient pattern. Growth in the successive stage did not compensate for slow development at hatching, thus responses at this early stage have potential long-lasting consequences. Although phenotypic selection during early development certifies the strength of selection imposed by cold temperatures in the laboratory, elevation clines of body size did not emerge in either nymphs or the wild parental generation. Differentiation in the wild may be levelled out by fecundity selection for large sizes, drift and gene flow resulting from the fragmentation and proximity of populations, or by micro-climatic differences that reduce the likelihood of directional selection. There is therefore potential for local adaptation to temperature, but a series of conditions typical of alpine environments and ectotherms may impair, confound or constrain full differentiation along the gradient.

Canalization of freeze tolerance in an alpine grasshopper

In the Rock and Pillar Range, New Zealand, the alpine grasshopper, Sigaus australis Hutton, survives equilibrium freezing (EF) all-year round. A comparison of freeze tolerance (FT) in grasshoppers over four austral seasons for a 1year period finds that: (a) the majority (>70%) of the sample population of grasshoppers survive single freeze-stress throughout the year; (b) exposure to increased freeze stress (multiple freeze-stress events) does not lead to a loss of freeze tolerance; and (c) responses to increased freeze stress reveal seasonal tuning of the FT adaptation to environmental temperatures. The Rock and Pillar sample population provides a clear example of the canalization of the FT adaptation. Seasonal variability in the extent of tolerance of multiple freezing events indicates that physiology is modulated to environmental temperatures by phenotypic plasticity – i.e. the FT adaptation is permanent and adjustable.