Research Article |
Corresponding author: Ming Kai Tan ( orthoptera.mingkai@gmail.com ) Academic editor: Corinna S. Bazelet
© 2017 Ming Kai Tan, Huiqing Yeo, Wei Song Hwang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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
|
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 bio-indicators for the freshwater swamp forest, owing to their sensitivity to microhabitat conditions.
abundance, ecology, limno-terrestrial, microhabitat association, Singapore
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.
Orthoptera (grasshoppers, crickets and katydids) are among the largest group of terrestrial insects, comprising more than 27,000 described species (
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 (
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 (e.g.
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 (
— Four sites, situated along the main stream within the NSSF were opportunistically sampled. In each site, eight 20 × 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 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 auto-correlation. 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 (
— 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) water-logged, (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 (
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 (
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 (
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 (
All statistical analyses were done in the R software version 3.3.3 (
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.
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
Effect of Microhabitat NMDS1 and NMDS2 and proximity to main stream on total abundance of pygmy grasshoppers. Marginal R2 (R2m) represents variance explained by fixed effects whereas conditional R2 (R2c) represents variance explained by both fixed and random effects.
df | logLik | AICc | delta | weight | R2m | R2c | |
~ Microhabitat NMDS1 + Microhabitat NMDS2 | 4 | −70.70 | 150.9 | 0.0 | 0.51 | 0.35 | 0.35 |
~ Microhabitat NMDS1 | 3 | −72.29 | 151.4 | 0.6 | 0.38 | 0.27 | 0.28 |
~ Microhabitat NMDS1 + Proximity to main stream | 4 | −72.24 | 154.0 | 3.1 | 0.11 | 0.27 | 0.28 |
~ Microhabitat NMDS2 + Proximity to main stream | 4 | −76.57 | 162.6 | 11.8 | 0.00 | 0.25 | 0.25 |
~ 1 | 2 | −80.08 | 164.6 | 13.7 | 0.00 | 0.00 | 0.06 |
~ Microhabitat NMDS2 | 3 | −79.25 | 165.3 | 14.5 | 0.00 | 0.10 | 0.10 |
~ Proximity to main stream | 3 | −79.55 | 166.0 | 15.1 | 0.00 | 0.03 | 0.10 |
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
Effect of specific environmental variables on total abundance of pygmy grasshoppers.
df | logLik | AICc | delta | weight | R2m | R2c | |
---|---|---|---|---|---|---|---|
~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 and grasses | 3 | −77.99 | 162.8 | 22.4 | 0.00 | 0.14 | 0.14 |
~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 |
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
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 (
As the diet of pygmy grasshoppers generally consists of algae, moss, fungi and lichen that thrive on wetter conditions (
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 (
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 NSSF. 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 (
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.
Data type: Table