Printer Friendly

Ground dwelling pygmy grasshoppers (Orthoptera: Tetrigidae) in Southeast Asian tropical freshwater swamp forest prefer wet microhabitats.

Abstract

Tetrigidae are an ancient group of grasshoppers and, similar to many other insects, have associations and preferences for specific microhabitats and habitats. The ecology of pygmy grasshoppers in Southeast Asia is generally under studied, especially in threatened habitats such as freshwater swamp forests. A study in Nee Soon Swamp forest, Singapore, was conducted to investigate association of limno-terrestrial pygmy grasshoppers with waterbodies and microhabitat. Specifically, we looked at the abundance and species assemblage of all pygmy grasshoppers. We correlated the abundance with major gradients of variation summarizing substrate and vegetation types along belt transects where sampling was performed. We found that pygmy grasshoppers in general are associated with wetter microhabitat conditions rather than the main streams in the swamp forest (i.e., water bodies). This is despite differences in microhabitat conditions of belt transects nearer to and further away from the main streams. We also found that pygmy grasshopper abundance is associated with the wetness of dicot leaf litter. We inferred that the abundance of food resources and suitability for egg development may explain their preference for wet microhabitats. We also found that the same patterns applied for adults and juveniles, suggesting that there is no demographic difference or ontogenetic shift in microhabitat association. Lastly, the adult assemblage can also be correlated to microhabitats. Based on our findings, we propose that pygmy grasshoppers can also be suitable bioindicators for the freshwater swamp forest, owing to their sensitivity to microhabitat conditions.

Key words

abundance, ecology, limno-terrestrial, microhabitat association, Singapore

Introduction

Insects are highly dependent on their environment. Plant communities within an area can vary in diversity assemblage and productivity and such heterogeneity can drive dynamics among arthropod communities and influence arthropod-plant interactions (e.g. Knops et al. 1999, Schaffers et al. 2008, Haddad et al. 2009). At a smaller scale, insects are also known to have preference for specific microhabitat conditions (e.g. Wardhaugh et al. 2013, 2014, Pincebourde and Casas 2015, Thorn and Daniels 2017). Likewise, orthopterans have associations with vegetation and microhabitat conditions (Joern 1982, Badenhausser et al. 2015).

Orthoptera (grasshoppers, crickets and katydids) are among the largest group of terrestrial insects, comprising more than 27,000 described species (Cigliano et al. 2017). The Tetrigidae, or pygmy grasshoppers, are a monophyletic clade and forms a unique lineage among the Caelifera (grasshoppers) (Song et al. 2015). These grasshoppers are known to prefer moist areas and semi-aquatic habitats like marshes, margins of waterbodies and floodplains. Amedegnato and Devriese (2008) considered most species of pygmy grasshoppers as limno-terrestrial that require an aqueous matrix (moist areas) in strictly terrestrial habitats while some are more dependent on water (such as for egg laying and nymphal development). They appear to be good swimmers and/or divers (Paranjape et al. 1987, Groning et al. 2007, Amedegnato and Devriese 2008). Different levels of dependency on water correspond to varying degrees of adaptations to swimming, including expanded hind tibia with reduced spines in more water dependent species (Amedegnato and Devriese 2008). Being a group of terrestrial invertebrates which are associated with water, they thus provide an important trophic exchange between aquatic and terrestrial food webs (Bastow et al. 2002, Balian et al. 2008).

However, there is still a dearth of information on the pygmy grasshoppers from Southeast Asia. This is made worse with the taxonomy being particularly problematic, rendering accurate species identification difficult (Tumbrinck 2014). Most of our current understanding of the ecology of pygmy grasshoppers is limited to their diet, ranging from observational (e.g. Paranjape and Bhalerao 1985, Blackith and Blackith 1987, Reynolds et al. 1988) to quantitative data (eg. Kuravova et al. 2017b). Quantitative studies on the habitat/micro-habitat association of pygmy grasshoppers are rare and restricted to a few species (eg. Hochkirch et al. 2000, Groning et al. 2007, Kuravova and Kocarek 2015, Musiolek and Kocarek 2016), and even fewer in Southeast Asia. Southeast Asia consists of three biodiversity hotspots (Myers et al. 2000), and is threatened by large-scale deforestation and land use conversion (Brooks et al. 2002, Sodhi et al. 2010, Wilcove et al. 2013). At the same time, Southeast Asia is also rich in orthopterans, possibly equally affected by the crisis as are other organisms (Tan et al. 2017a). Along with fragmentary understanding of the orthopteran diversity in Southeast Asia (Tan et al. 2017a), there is a pressing need to study the ecology of Southeast Asian orthopterans.

Here, an attempt was made to investigate the association of the Southeast Asian pygmy grasshoppers with microhabitats and proximity to water bodies. Specifically such ecological association of the pygmy grasshoppers from freshwater swamp forest were examined for the first time. Studies on pygmy grasshoppers in aquatic habitats focus mostly on species occurring in salt marshes, ponds and rivers (eg. Hochkirch et al. 2000, Groning et al. 2007, Amedegnato and Devriese 2008). There has not been a study on species from a tropical region and hence tropical freshwater swamp forests up to now. Our study of the water association of the pygmy grasshoppers can provide us with a better understanding of the ecological preferences and association of these tropical orthopterans.

To investigate the association of the pygmy grasshoppers with the microhabitats in the freshwater swamp forests, two hypotheses were tested. Firstly, we investigated if the pygmy grasshoppers in freshwater swamp forest were associated with the water body by comparing the abundance of pygmy grasshoppers near vs. further away from the main streams. If the unique semi-aquatic lifestyle of the pygmy grasshoppers required a close association with existing waterbodies in the swamp forest, this would suggest they may tend to concentrate near streams. Secondly, we also aimed to investigate if the pygmy grasshoppers preferred specific microhabitat conditions. The microhabitats were quantified by a series of vegetation and surface types, as well as surface temperature and relative humidity. Nee Soon Swamp Forest (NSSF), Singapore, was used as the study site. NSSF is the last remnant of freshwater swamp forest in Singapore but remains ecologically significant (Ng and Lim 1992, O'Dempsey and Chew 2013). It also holds unique and endemic biodiversity (eg. Gorochov and Tan 2012, Jach et al. 2013). As the pygmy grasshoppers were usually small and had small dispersal range, we expected that they would form close associations with their preferred microhabitats.

Materials and methods

Study area.--Four sites, situated along the main stream within the NSSF were opportunistically sampled. In each site, eight 20 x 10 m belt transects were opportunistically demarcated based on accessibility. Within each site, four belt transects were situated along the stream banks less than 1 m away from the main stream and four other belt transects were situated at least 5 m from the main stream. In total, 32 belt transects were surveyed. Each belt transect was surveyed once.

Sampling of pygmy grasshoppers.--Sampling was conducted between late August 2013 and early February 2014, during the cooler and wetter part of the year in Singapore. Surveys were conducted between 7:30 pm (after last light) and 10 pm. Nocturnal survey was found to be more appropriate for representative estimation of pygmy grasshopper abundance as they are more easily sighted at night than in the day. Two belt transects from a single site were opportunistically sampled per survey night. Each site was surveyed across the entire span of the sampling period, rather than restricted to a single month, to minimize the effect of temporal autocorrelation. Each belt transect was surveyed systematically for 20 min by two equally trained and efficient surveyors (MKT and HY) working together at the same time, from one end of the belt transect to the other. Adults and juveniles were actively searched using both headlamps and hand torches. The ground, low-lying vegetation and dead logs were searched. Pygmy grasshoppers were thoroughly sampled within the time frame and belt transect. Abundance was quantified as the total number of individuals found in each belt transect. Adult specimens were tentatively identified to morpho-species because Tetrigidae in Singapore are generally not well studied with species delimitation remaining unresolved and many species undescribed (Tan et al. 2017b). All adults were likely to be capable of flight owing to the presence of developed hind wings whereas the nymphs were flightless.

Microhabitat quantification.--At every 1 m along the belt transect, the surface and vegetation types were recorded. Surface types include: (1) dry dicot leaf litter, (2) wet dicot leaf litter, (3) dry muddy (fine and claying substrate), (4) wet muddy, (5) dry sandy (coarser and porous substrate), (6) wet sandy, (7) gravel and rocks, (8) wet dead woody structure (i.e. log and exposed roots), (9) dry woody structure (i.e. log, trunk and exposed roots), (10) waterlogged, (11) wet ceramics (e.g. broken ceramic tiles left over from past settlement) and (12) dry monocot leaf litter. We distinguished dicot leaf litter, muddy surface and sandy surface between wet and dry. For surface types 7 to 12, they were always either wet or dry and hence not distinguished between wet and dry. We summarized different plant forms as vegetation types that included: (1) herbaceous plants and grass, (2) woody plants (i.e. trees, woody shrub), (3) creepers and vines, (4) rattans (including Pandanus), (5) ferns and (6) palms. The prominence of each microhabitat (both surface and vegetation type) was quantified by counting the number of times they were recorded within the belt transect. Within each belt transect, the ambient surface temperature and ambient surface relative humidity were also recorded three times, at approximately the two ends and midpoint, and averaged.

Data analyses.--As the different types of substrate and vegetation were not mutually exclusive, they were likely to be highly intercorrelated. To summarize substrate and vegetation into major gradients of variation, non-metric multidimensional scaling (NMDS) using Bray-Curtis distance was performed using the 'metaMDS' function implemented with the community package vegan version 2.3-1 (Oksanen et al. 2015). Stress values of 0.20 and below were deemed acceptable for interpretation of patterns (Clarke 1993), and where this was exceeded, the plots were ordinated on three dimensions. NMDS axes representing the microhabitat variation were labelled Microhabitat NMDS1 and Microhabitat NMDS2. The scores for the NMDS axes were scaled and checked for collinearity. Variance inflation factor (vif) values of below 3.0 were deemed acceptable (Zuur et al. 2010).

To test if the pygmy grasshoppers were associated with specific microhabitat axes, the abundance of pygmy grasshoppers was fitted as a generalized linear mixed-effects model using Poisson error structure using the 'glmer' function. We included the scores on the two scaled NMDS axes and proximity to main stream (either close or far) as fixed effects and the site location as random effect.

We postulated that pygmy grasshoppers had habitat preferences, and thus occurred at higher abundances associated with specific microhabitat conditions. Additionally, owing to their preference for aquatic habitat, we also postulated that more pygmy grasshoppers would be found on belt transects closer to the main stream. The following models were proposed and ranked accordingly to Akaike information criterion with adjustments (AICc) using the 'MuMIn' package (Barton and Barton 2015):

1. ~ Microhabitat NMDS1

2. ~ Microhabitat NMDS2

3. ~ Microhabitat NMDS1 + Microhabitat NMDS2

4. ~ Proximity to main stream

5. ~ Microhabitat NMDS1 + Proximity to main stream

6. ~ Microhabitat NMDS2 + Proximity to main stream

7. ~ 1 (null model)

We interpreted the models with delta (difference in the AICc of a particular model and that of the best model) less than 2.0 (Burnham and Anderson 2002) in tandem. Subsequently, we also selected surface and vegetation types based on the NMDS plot that might have been important to explain the abundance. To better understand how each of these environmental variables correlated with the abundance, we proposed various models containing each of these environmental variables as fixed effect and ranked accordingly to Akaike information criterion with adjustments (AICc).

Since adults and juveniles could have different microhabitat requirements and dispersal abilities, we performed separately the same analyses using the subset of (i) adult and (ii) juvenile abundances to investigate if the same patterns persisted. The assemblage (or beta-diversity) of adults were correlated with major gradients of variation in microhabitat conditions (i.e., Microhabitat NMDS1 and NMDS2). This was done by performing canonical analysis of principal coordinates (CAP) with Euclidean distance using the 'capscale' function implemented with the community package vegan version 2.3-1 (Oksanen et al. 2015).

All statistical analyses were done in the R software version 3.3.3 (R Development Core Team 2017).

Results

A total of 94 adult and juvenile pygmy grasshoppers were collected during the sampling of 32 belt transects (19 from Site 1 (= Woodcutter Trail), 13 from Site 2 (= Nee Soon interior), 28 from Site 3 (= Nee Soon main pond) and 13 from Site 4 (= Upper Seletar). In total, 62 adults and 32 juveniles were collected. We identified the adults into six morpho-species, with one dominant morpho-species. All morpho-species were collected across the entire sampling period and there appeared to be no clear evidence of species turnover with time.

The first two scaled NMDS axes summarized the microhabitat conditions (including vegetation and surface types) and had a stress value of 0.17 (below the threshold of 2.0), indicating that they were sufficient to represent the variation in the microhabitat conditions (Fig. 1). Subsequently, we obtained the scores for the two axes to test our hypotheses. The Microhabitat NMDS1 showed that belt transects with wetter microhabitats (waterlogged, wet muddy and wet dicot leaf litter) had higher scores than those with drier microhabitats (dry sandy, dry muddy and dry dicot leaf litter). The Microhabitat NMDS2 showed that belt transects with coarser surface type (i.e. sand, tiles, rock and gravel) had a lower score than those with finer surface type (i.e. mud). Microhabitat NMDS2 also summarized the vegetation types. A PERMANOVA also showed that the microhabitat conditions were dissimilar between the belt transects nearer to the main streams and those further away (F-value = 4.81, [R.sup.2] = 0.14, p-value = 0.003) (Fig. 2).

When we correlated the total abundance of pygmy grasshoppers with the NMDS axes and proximity to main streams, the two best models with delta less than 2.0 both had NMDS1 as fixed effect (Table 1). The best model also had NMDS2 as fixed effect. The best model explained 35% of variance, about 10% more than that explained by the second best model (Table 1). Total abundance had a strong positive relationship with Microhabitat NMDS1 (97.5% CI[0.75, 2.06] in best model and 97.5% CI[0.71, 2.10] in second best model) and a weak negative relationship with Microhabitat NMDS2 (97.5% CI[-1.81, 0.09] in best model). This showed that higher abundance of pygmy grasshoppers could be found in wetter microhabitats (waterlogged, wet muddy and wet dicot leaf litter) than in drier microhabitats (dry sandy, dry muddy and dry dicot leaf litter). Proximity to main stream was not among the best models.

Since total abundance of pygmy grasshoppers had a strong positive relationship with NMDS1, we proposed further models, each model with a single environmental variable as a fixed effect: (1) dry dicot leaf litter, (2) wet dicot leaf litter, (3) wet muddy, (4) dry sandy, (5) waterlog and (6) herbaceous plants and grasses. Upon ranking them using AICc, the best models with delta < 2.0 had dry and wet dicot leaf litter as fixed effects and explained 40% and 37% of variance, respectively (Table 2). Total abundance had a strong negative relationship with dry dicot leaf litter (97.5% CI[-0.12, -0.05] as best model (Fig. 3) and a positive relationship with wet dicot leaf litter 97.5% CI[0.05, 0.11] as second best model). This showed that wetness of dicot leaf litter had a strong effect on the abundance of pygmy grasshoppers.

When we performed the analyses using adults and juveniles separately, the same patterns were observed. Higher abundance of adult and juvenile pygmy grasshoppers were found in wetter microhabitats than in drier microhabitats (Suppl. material 1: Tables 1 and 2). Juvenile abundance had a strong positive relationship with Microhabitat NMDS1 (97.5% CI[0.35, 2.63] in best model and 97.5% CI[0.39, 2.56] in second best model) and a weak negative relationship with Microhabitat NMDS2 (97.5% CI[-2.14, 0.94] in second best model). Likewise, adult abundance had a strong positive relationship with Microhabitat NMDS1 (97.5% CI[0.58, 2.15] in best model and 97.5% CI[0.59, 2.26] in second best model) and a strong negative relationship with Microhabitat NMDS2 (97.5% CI[-2.20, -0.03] in best model). Specifically, we found that wetness of dicot leaf litter had a strong effect on the abundance of both adults and juveniles (Suppl. material 1: Tables 3 and 4). Juvenile abundance had a strong relationship with dry dicot leaf litter (97.5% CI[-0.16, -0.03] and wet dicot leaf litter 97.5% CI[0.04, 0.15]). Adult abundance had a strong relationship with dry dicot leaf litter (97.5% CI[-0.14, -0.05]). Proximity to main stream was not among the best models. Lastly, we found the assemblage of pygmy grasshoppers was significantly correlated to Microhabitat NMDS1 and Microhabitat NMDS2 (proportion variance explained = 0.17, pseudo-F-value = 2.89, number of permutations = 999, p-value = 0.013) (Fig. 4). No apparent difference was detected between the six morpho-species.

Discussion

Our study in NSSF demonstrated that pygmy grasshoppers in general were not associated with the main streams in freshwater swamp forests. Instead, the pygmy grasshoppers were found to be associated with wetter microhabitats in general. This is despite the microhabitats between the belt transects nearer to and further away from the main streams being different. In Southeast Asia, many Scelimeninae can be found to occupy river banks and forage for submerged food resources (Kuravova et al. 2017a). The pygmy grasshoppers from the freshwater swamp forest in Singapore, which include Scelimeninae, however, had different microhabitat associations. This was to be expected since the freshwater swamp forest is a different habitat to that of a typical river. The highly dynamic water level within the freshwater swamp forest leads to the formation of a dense network of main streams and smaller ephemeral streamlets (O'Dempsey and Chew 2013). This also indicates that different pygmy grasshoppers from different habitats and lineages can have very different life histories.

As the diet of pygmy grasshoppers generally consists of algae, moss, fungi and lichen that thrive on wetter conditions (Paranjape et al. 1987, Hochkirch et al. 2000, Kocarek et al. 2008, Bidau 2014, Kuravova and Kocarek 2015, Kuravova et al. 2017a, 2017b), our findings also suggested that greater abundance of food sources in wetter microhabitats can account for higher abundance of pygmy grasshoppers in general. We also found that specifically, the wetness of dicot leaf litter is strongly positively correlated with the abundance of pygmy grasshoppers. We inferred that areas with wet dicot leaf litter provided suitable microhabitats for pygmy grasshoppers owing to the availability of food resources. Additionally, wet microhabitats could also provide suitable conditions for egg development (Paranjape et al. 1987). Since pygmy grasshoppers are known to lay eggs on substrate (Hartley 1962, Paranjape et al. 1987), wet leaf litter, in particular, might reduce rate of drying of the underlying substrate. From our observational studies, we could only infer these behaviors, and how precisely pygmy grasshoppers from tropical Southeast Asia utilize their microhabitats should be further investigated under laboratory conditions. This will then provide better mechanistic understanding of the biology of these pygmy grasshoppers.

On the other hand, pygmy grasshoppers did not appear to be associated with the vegetation types in the swamp forest since their food sources were often not affected by the vegetation types (Paranjape 1985, Paranjape and Bhalerao 1985). This is contrary to previous studies showing diet preference of orthopterans is often closely linked to their association with specific vegetation or host plants (Joern 1982, Schaffers et al. 2008, Badenhausser et al. 2015), although these studies do not focus on pygmy grasshoppers. Nonetheless, comparing our findings to other ecological studies of pygmy grasshoppers also revealed that association with the environment can be different among Southeast Asian species and with counterparts from other regions. For example, Tetrix undulata was shown to associate with habitats with preferred thermal properties (Ahnesjo and Forsman 2006) whereas Tetrix tenuicornis had differing preferences for microhabitats in accordance to changes in the weather conditions (Musiolek and Kocarek 2016). On the other hand, a riverine species, Tetrix ceperoi, prefers hotter, damper and bare areas, similar to species from NSSF (Groning et al. 2007). Unlike previous studies (Ahnesjo and Forsman 2006, Groning et al. 2007, Musiolek and Kocarek 2016) which focused on a single species of pygmy grasshopper, we investigated the overall abundance of all pygmy grasshoppers, while also examining possible differences between adults and juveniles. The main reason was because of the difficulty to identify closely related species and juveniles among Southeast Asian pygmy grasshoppers owing to unstable taxonomic status of many species (Blackith 1992, Kim and Kim 2004, Tan and Artchawakom 2015). Juveniles of many species were almost impossible to identify using morphology.

Interestingly, we did not find any difference in microhabitat association between the adults and juveniles. While adult and juvenile pygmy grasshoppers can have differing life history (e.g. dispersal ability, dependency on moisture), we did not find evidence for ontogenetic shift for the pygmy grasshoppers in NSSE It appears that the species of pygmy grasshoppers had very similar association for specific microhabitat conditions since the assemblage of adults also showed similar trends as that of their abundance. We speculate that NSSF may be a unique ecosystem in which small insects such as the pygmy grasshoppers occupy very unique microhabitats.

Owing to the sensitivity of orthopterans to their environment, orthopterans have been proposed as bio-indicators of forests (Fartmann et al. 2012). Nevertheless, the tropical ecology of Southeast Asian orthopterans, along with many other invertebrates, are still under studied. Here, we demonstrated for the first time that pygmy grasshoppers from Southeast Asian freshwater swamp forests are not associated to waterbodies, unlike counterparts from the temperate and subtropical regions. Instead, these pygmy grasshoppers in general prefer wetter microhabitats. Loss or changes in these microhabitats owing to climate change or anthropogenic disturbances can potentially affect the populations (Inamke et al. 2016, Sueyoshi et al. 2016). This is especially so for the freshwater swamp forest which is currently small and isolated and for the pygmy grasshoppers with limited dispersal ability. We propose that pygmy grasshoppers can indeed be potential bio-indicators of freshwater swamp forest. Extending similar studies into other ecosystems can confirm if pygmy grasshoppers can also provide the same service. We hope that our study can help to fill in knowledge gaps in the ecology of pygmy grasshoppers in Southeast Asia, thus providing information for better management of threatened habitats, such as the NSSE

Acknowledgements

The authors thank Kwek Yen Chong for advice on the statistical analyses and review of manuscript. The permission to conduct this study was granted by the National Parks Board (NParks), Singapore (research permit NP/RP10-073-2). This is based mainly on the results from MKT's National University of Singapore (NUS) Undergraduate Research Opportunities Programme in Science (UROPS) Project. This study is also part of the Nee Soon Swamp Forest Biodiversity and Hydrology Baselines Studies by the NParks in collaboration with the NUS.

References

Ahnesjo J, Forsman A (2006) Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance. Evolutionary Ecology 20: 235-257. https://doi.org/10.1007/s10682-006-6178-8

Amedegnato C, Devriese H (2008) Global diversity of true and pygmy grasshoppers (Acridomorpha, Orthoptera) in freshwater. Hydrobiologia 595: 535-543. https://doi.org/10.1007/s10750-007-9132-z

Badenhausser I, Gross N, Cordeau S, Bruneteau L, Vandier M (2015) Enhancing grasshopper (Orthoptera: Acrididae) communities in sown margin strips: the role of plant diversity and identity. Arthropod-Plant Interactions 9: 333-346. https://doi.org/10.1007/s11829-015-9376-x

Balian EV, Leveque C, Segers H (2008) Freshwater Animal Diversity Assessment. Springer. 656 pp. https://doi.org/10.1007/978-l-4020-8259-7

Barton K, Barton MK (2015) Package 'MuMIn' Version 1.

Bastow JL, Sabo JL, Finlay JC, Power ME (2002) A basal aquatic-terrestrial trophic link in rivers: algal subsidies via shore-dwelling grasshoppers. Oecologia 131: 261-268. https://doi.org/10.1007/s00442-002-0879-7

Bidau CJ (2014) Patterns in Orthoptera biodiversity. I Adaptations in ecological and evolutionary contexts. Journal of Insect Biodiversity 2: 1-39.

Blackith RE, Blackith RM (1987) Tridactylids and pygmy grasshoppers (Orthoptera) from Sulawesi, Indonesia. Overgedrukt uit het Tijdschrift voor Entomologie 130: 1-10.

Blackith RE (1992) Tetrigidae (Insecta; Orthoptera) of Southeast Asia: Annotated catalogue with partial translated keys and bibliography. Ashford Co., JAPAGA, Rockbottom, 248 pp.

Brooks TM, Mittermeier TA, Mittermeier CG, Da Fonseca GA, Rylands AB, [Constant WR Flick P, Pilgrim J, Oldfield S, Magin G, Hilton-Taylor C (2002) Habitat loss and extinction in the hotspots of biodiversity Conservation Biology 16: 909-923. https://doi.org/10.1046/).1523-1739.2002.00530.x

Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York, 488 pp.

Cigliano MM, Braun H, Eades DC, Otte D (2017) Orthoptera species file online. Version 5 (5.0). http://orthoptera.speciesfile.org

Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117-143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x

Fartmann T, Kramer B, Stelzner F, Poniatowski D (2012) Orthoptera as ecological indicators for succession in steppe grassland. Ecological Indicators 20: 337-344. https://doi.org/10.1016/j.ecolind.2012.03.002

Gorochov AV, Tan MK (2012) New crickets of the subfamilies Phaloriinae and Pteroplistinae (Orthoptera: Gryllidae) from Singapore. Zootaxa 3525: 18-34.

Groning J, Krause S, Hochkirch A (2007) Habitat preference of an endangered insect species, Cepero's groundhopper (Tetrix ceperoi). Ecological Research 22: 767-773. https://doi.org/10.1007/s11284-006-0315-2

Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JM, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecology Letters 12: 1029-1039.

Hartley JC (1962) The egg of Tetrix (Tetrigidae, Orthoptera), with a discussion on the probable significance of the anterior horn. Journal of Cell Science 3: 253-259.

Hochkirch AJ, Groning LT, Metzing C, Reichelt M (2000) Specialized diet and feeding habits as key factors for the habitat requirements of the grasshopper species Tetrix subulata (Orthoptera: Tetrigidae). Entomologia Generalis 25: 39-51. https://doi.org/10.1127/entom.gen/25/2000/39

Inamke RS, Panpatte D, Parvez N, Pathak L, Patel A, Khatri K, Jani J (2016) Insect Conservation: A Synthesis of Management Approaches. In: Chakravarthy AK, Sridhara S (Eds) Arthropod Diversity and Conservation in the Tropics and Sub-tropics. Springer, Sinagapore, 297-313. https://doi.org/10.1007/978-981-10-1518-2_18

Jach MA, Diaz JA, Skale A (2013) The Hydraenidae (Coleoptera) of the Republic of Singapore. The Raffles Bulletin of Zoology 61(1): 53-71.

Joern A (1982) Vegetation structure and microhabitat preference selection in grasshoppers (Orthoptera, Acrididae). The Southwestern Naturalist 27: 197-209. https://doi.org/10.2307/3671144

Kim TW, Kim JI (2004) A Taxonomic Study of Korean Tetrigidae (Orthoptera: Caelifera: Tetrigoidea). Entomological Research 34(4): 261-267. https://doi.org/10.1111/j.1748-5967.2004.tb00121.x

Knops JM, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J, Ritchie ME, Howe KM, Reich PB, Siemann E, Groth J (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecology Letters 2: 286-293. https://doi.org/10.1046/j.1461-0248.1999.00083.x

Kocarek P, Grucmanova S, Filipcova Z, Bradova L, Plasek V, Holusa J (2008) Bryophagy in the grasshopper Tetrix ceperoi (Orthoptera: Tetrigidae): analysis of alimentary tract contents. In: Kocarek P, Plasek V, Malachova K, Cimalova S (Eds) Environmental changes and biological assessment IV Ostrava: Scripta Facultatis Rerum.

Kuravova K, Kocarek P (2015) Seasonal variation in the diet of Tetrix tenuicornis (Orthoptera: Tetrigidae). Entomological Science 18: 489-501. https://doi.org/10.1111/ens.12145

Kuravova K, Sipos J, Wahab R, Kahar RS, Kocarek P (2017a) Feeding patterns in tropical groundhoppers (Tetrigidae): a case of phylogenetic dietary conservatism in a basal group of Caelifera. Zoological Journal of the Linnean Society, https://doi.org/10.1111/zoj.12474

Kuravova K, Grucmanova S, Filipcova Z, Plasek V, Drozd P, Kocarek P (2017b) Is feeding on mosses by groundhoppers in the genus Tetrix (Insecta: Orthoptera) opportunistic or selective?. Arthropod-Plant Interactions 11: 35-43. https://doi.org/10.1007/s11829-016-9461-9

Musiolek D, Kocarek P (2016) Weather-dependent microhabitat use by Tetrix tenuicornis (Orthoptera: Tetrigidae). The Science of Nature 103: 68. https://doi.org/10.1007/s00114-016-1393-9

Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858. https://doi.org/10.1038/35002501

Ng PKL, Lim KKP (1992) The conservation status of the Nee Soon Fresh Water Swamp Forest of Singapore. Aquatic Conservation-Marine and Freshwater Ecosystems 2: 255-266. https://doi.org/10.1002/aqc.3270020305

O'Dempsey T, Chew PT (2013) The freshwater swamp forests of Sungei Seletar Catchment: a status report. Proceedings of Nature Society, Singapore's Conference on 'Nature Conservation for a Sustainable Singapore' 16 Oct.2011: 121-166.

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: Community Ecology Package. R package version 2.0-10.

Paranjape SY (1985) Behavioural analysis of feeding and breeding in Orthopteran insects. Proceedings: Animal Sciences 94: 265-282. https://doi.org/10.1007/bf03186268

Paranjape SY, Bhalerao AM (1985) Bioecological observations on a pigmy locust, Potua sabulosa Hancock (Tetrigidae: Orthoptera). Psyche 92(2-3): 331-336. https://doi.org/10.1155/1985/30570

Paranjape SY, Bhalerao AM, Naidu NM (1987) On etho-ecological characteristics and phylogeny of Tetrigidae. In: Bacetti BM (Ed.) Evolutionary biology of Orthopteroid insects. Ellis Horwood, New York, 386-395.

Pincebourde S, Casas J (2015) Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits. Ecology 96: 986-997. https://doi.org/10.1890/14-0744.l

R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Reynolds JD, Blackith RE, Blackith RM (1988) Dietary observations on some tetrigids (Orthoptera: Caelifera) from Sulawesi (Indonesia). Journal of Tropical Ecology 4: 403-406. https://doi.org/10.1017/S0266467400003072

Schaffers AP, Raemakers IP, Sykora KV, Ter Braak CJ (2008) Arthropod assemblages are best predicted by plant species composition. Ecology 89: 782-794. https://doi.org/10.1890/07-0361.l

Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW (2010) The state and conservation of Southeast Asian biodiversity. Biodiversity and Conservation 19: 317-328. https://doi.org/10.1007/s10531-009-9607-5

Song H, Amedegnato C, Cigliano MM, Desutter-Grandcolas L, Heads SW, Huang Y, Otte D, Whiting MF (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics 31: 621-651. https://doi.org/10.1111/cla.12116

Sueyoshi M, Ishiyama N, Nakamura F (2016) [beta]-diversity decline of aquatic insects at the microhabitat scale associated with agricultural land use. Landscape and Ecological Engineering 12: 187-196. https://doi.org/10.1007/s11355-015-0283-1

Tan MK, Choi J, Shankar N (2017a) Trends in new species discovery of Orthoptera (Insecta) from Southeast Asia. Zootaxa 4238: 127-134. https://doi.org/10.11646/zootaxa.4238.1.10

Tan MK, Storozhenko S, Hwang W, Meier R (2017b) Integrative taxonomy reveals two sympatric species of the genus Eucriotettix Hebard, 1930 (Orthoptera: Tetrigidae). Zootaxa 4268: 377-394. https://doi.org/10.11646/zootaxa.4268.3.4

Tan MK, Artchawakom T (2015) A new species from the genus Gorochovitettix (Tetrigidae: Metrodorinae) from Thailand. Zootaxa 3990: 444-450. https://doi.org/10.11646/zootaxa.3990.3.9

Thom MD, Daniels J (2017) Patterns of microhabitat and larval host-plant use by an imperiled butterfly in northern Florida. Journal of Insect Conservation 1-14. https://doi.org/10.1007/s10841-016-9950-2

Tumbrinck J (2014) Taxonomic revision of the Cladonotinae (Orthoptera: Tetrigidae) from the islands of South-East Asia and from Australia, with general remarks to the classification and morphology of the Tetrigidae and descriptions of new genera and species from New Guinea and New Caledonia. Biodiversity biogeography and nature conservation in Wallacea and New Guinea 2: 345-396.

Wardhaugh CW, Edwards W, Stork NE (2013) Variation in beetle community structure across five microhabitats in Australian tropical rainforest trees. Insect Conservation and Diversity 6: 463-472. https://doi.org/10.1111/icad.12001

Wilcove DS, Giam X, Edwards DP, Fisher B, Koh LP (2013) Navjot's nightmare revisited: logging, agriculture, and biodiversity in Southeast Asia. Trends in Ecology & Evolution 28: 531-540. https://doi.org/10.1016/j.tree.2013.04.005

Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3-14. https://doi.org/10.1111/j.2041-210X.2009.00001.x

Supplementary material 1

Authors: M.K. Tan, H. Yeo, W.S. Hwang

Data type: Table

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: https://doi.org/10.3897/jor.26.14551.suppll

MING KAI TAN (1), HUIQING YEO (2), WEI SONG HWANG (3,1)

(1) Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore.

(2) Environment Health Institute, National Environment Agency, 11 Biopolis Way, Singapore 138667, Republic of Singapore.

(3) Lee Kong Chian Natural History Museum, National University of Singapore, 2 Conservatory Drive, Singapore 117377, Republic of Singapore.

Corresponding author: M. K. Tan (orthoptera.mingkai@gmail.com)

Academic editor: Corinna Bazelet | Received 26 March 2017 | Accepted 29 May 2017 | Published 28 June 2017

http://zoobank.org/1C923552-96E1-4ED7-98F0-C77E60C2BD17

Citation: Tan MK, Yeo H, Hwang WS (2017) Ground dwelling pygmy grasshoppers (Orthoptera: Tetrigidae) in Southeast Asian tropical freshwater swamp forest prefer wet microhabitats. Journal of Orthoptera Research 26(1): 73-80. https://doi.org/10.3897/jor.26.14551
Table 1. Effect of Microhabitat NMDS1 and NMDS2 and proximity to main
stream on total abundance of pygmy grasshoppers. Marginal [R.sup.2]
([R.sup.2]m) represents variance explained by fixed effects whereas
conditional [R.sup.2] ([R.sup.2]c) represents variance explained by
both fixed and random effects.

                                                 df  logLik  AICc

~ Microhabitat NMDS1 + Microhabitat NMDS2        4   -70.70  150.9
~ Microhabitat NMDS1                             3   -72.29  151.4
~ Microhabitat NMDS1 + Proximity to main stream  4   -72.24  154.0
~ Microhabitat NMDS2 + Proximity to main stream  4   -76.57  162.6
~1                                               2   -80.08  164.6
~ Microhabitat NMDS2                             3   -79.25  165.3
~ Proximity to main stream                       3   -79.55  166.0

                                                 delta  weight

~ Microhabitat NMDS1 + Microhabitat NMDS2         0.0   0.51
~ Microhabitat NMDS1                              0.6   0.38
~ Microhabitat NMDS1 + Proximity to main stream   3.1   0.11
~ Microhabitat NMDS2 + Proximity to main stream  11.8   0.00
~1                                               13.7   0.00
~ Microhabitat NMDS2                             14.5   0.00
~ Proximity to main stream                       15.1   0.00

                                                 [R.sup.2]m  [R.sup.2]c

~ Microhabitat NMDS1 + Microhabitat NMDS2        0.35        0.35
~ Microhabitat NMDS1                             0.27        0.28
~ Microhabitat NMDS1 + Proximity to main stream  0.27        0.28
~ Microhabitat NMDS2 + Proximity to main stream  0.25        0.25
~1                                               0.00        0.06
~ Microhabitat NMDS2                             0.10        0.10
~ Proximity to main stream                       0.03        0.10

Table 2. Effect of specific environmental variables on total abundance
of pygmy grasshoppers.

             df  logLik  AICc   delta  weight  [R.sup.2]m  [R.sup.2]c

~dry dicot
leaf litter  3   -66.80  140.5   0.0   0.54    0.40        0.45
~wet dicot
leaf litter  3   -66.97  140.8   0.3   0.46    0.37        0.45
~wet mud     3   -77.38  161.6  21.2   0.00    0.07        0.18
~dry sand    3   -77.54  161.9  21.5   0.00    0.06        0.16
~herbaceous
plants       3   -77.99  162.8  22.4   0.00    0.14        0.14
and grasses
~1           2   -80.08  164.6  24.1   0.00    0.00        0.06
~waterlog    3   -79.96  166.8  26.3   0.00    0.01        0.06
COPYRIGHT 2017 The Orthopterists' Society
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Research Article
Author:Tan, Ming Kai; Yeo, Huiqing; Hwang, Wei Song
Publication:Journal of Orthoptera Research
Article Type:Report
Geographic Code:9SING
Date:Jan 1, 2017
Words:6021
Previous Article:Adapting the Dragonfly Biotic Index to a katydid (Tettigoniidae) rapid assessment technique: case study of a biodiversity hotspot, the Cape Floristic...
Next Article:Erechthis katydids (Tettigoniidae: Conocephalinae) in the Caribbean: new species from The Bahamas and Hispaniola.
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters