Microhabitat segregation among three co-existing species of grasshoppers on a rural meadow near Seoul, South Korea.
Microhabitat selection is important for small ectothermic animals including insects (Ahnesjo and Forsman 2006, Gardiner and Hassall 2009), and for herbivores with specific diets (including those that sequester unpalatable chemicals from plants for their own protection against predators; Sword et al. 2000, Sword 2002). Different species of grasshoppers have different diets (Joern 1979, Otte 1981, Chu 2002) and they move between sunlit and shaded areas to control their body temperature (Pielou 1948, Ahnesjo and Forsman 2006). Grasshoppers also choose microhabitats that provide better camouflage (Eterovick et al. 1997). Microhabitat segregation among co-existing species of grasshoppers has been studied in North America and Europe (Isely 1937, Joern 1979, 1982, Gardiner and Hassall 2009), but rarely studied in Asia (Tan et al. 2017, T. Gardiner pers. comm.). Here, we provide basic information on microhabitat segregation among three common grasshopper species in South Korea (Park and Kim 2011) and Japan (Yoshioka et al. 2010). We chose to study the three species that were the most common at our study site: Acrida cinerea (Thunberg, 1815), Atractomorpha lata (Mochulsky, 1866), and Oedaleus infernalis Saussure, 1884. From classical ecological theory (Hardin 1960) and based on previous studies on grasshoppers (Isely 1937, Joern 1979, 1982, Gardiner and Hassall 2009, Tan et al. 2017), we expected that they would differ in their ecological niches.
Materials and methods
The observation site (37[degrees]24.07'N, 126[degrees]44.62'E) was comprised of a 10,000 [m.sup.2] lush grassland adjacent to Soraepogu Ecological Park, with an abundance of plants belonging to Asteraceae, especially Artemisia princeps and Aster pilosus. A hiking path crossed the meadow and each side of the trail was covered with a 1-m wide band of Zoysia japonica. To determine microhabitat segregation among the three species, we used a modified point-sampling technique (Joern 1982). A researcher moved very slowly through the grassland (including the 1-m wide band of Zoysia japonica) and noted the location of each detected individual grasshopper and the plant species (or ground) it was sitting on (or just jumped from). Each grasshopper species has distinctive morphology making the identification of species in the field relatively easy (Storozenko and Paik 2007, Kim 2013). Observations were carried out for four days from the end of August to the beginning of September 2017 and resulted in 327 grasshopper presence records. Plants were classified into four structural types which roughly aligned with plant family: Stem-plants, usually Asteraceae, consisted of one straight stem with leaves emanating to all sides; Low-vegetation plants, usually Zoysia japonica (Poaceae), were short and formed relatively dense cover; and Tall-grass included tall (50-150 cm) Poaceae with long and thin grass leaves. Other records of grasshoppers on rarely observed plant species were put into the category Others. Observations on the ground were classified into the Ground category. Plant structural type was closely correlated with plant family, so they are not independent. We performed two analyses, one utilizing plant family as the dependent variable and the other utilizing structural type, as two alternative and correlated analyses of substrate use by grasshoppers. We used the Fisher's exact test (function fisher.test from the stat-package in R; Mangiafico 2015) to statistically test the null hypothesis of no differences among the three grasshopper species in their use of substrates. This test was most appropriate because our data were in frequency tables with a small number of records in some of the cells.
Results and discussion
The three grasshopper species differed significantly in their association with different plant families (Fig. 1A; Fisher's exact test P < 0.001). While many individuals of Oedaleus infernalis were found on the ground, most Acrida cinerea and Atractomorpha lata were observed on Poaceae (usually Zoysia japonica) and Asteraceae (usually Artemisia princeps or Aster pilosus), respectively (Table 1). The three grasshopper species also differed significantly in their association with different plant structural types (Fig. 1B; Fisher's exact test P < 0.001). Acrida cinerea was most often observed on Low-vegetation structure plants (mostly Poaceae), Atractomorpha lata was mostly found on Stem-plants (mostly Asteraceae), and Oedaleus infernalis was largely observed on the Ground.
Atractomorpha lata utilizes host plants belonging to various families including Asteraceae, Convolvulaceae, and Fabaceae (Tanaka 2008). In this study, many Atractomorpha lata individuals were observed on Asteraceae. This is consistent with previous findings that Artemisia princeps (Asteraceae) is one of the best host plants for growth and survival of Parapodisma subastirs grasshoppers (Miura and Ohsaki 2004a, b, 2006). As we did not determine the relative abundance of different plant species at the study site, we cannot directly evaluate the host plant preferences of each species. However, we can focus on microhabitat differences between the three species at the same location.
While Atractomorpha lata was found on Asteraceae as well as other plant families, Acrida cinerea was mostly observed on Poaceae (usually Zoysia japonica). Acrida spp. grasshoppers are known to prefer grass as a food resource (Haldar et al. 1995). We also hypothesize that these differences in host plant associations may be linked to specific thermal microhabitat. Zoysia japonica on the research site had recently been trimmed and so the grass was shorter than normal, which might have contributed to an increase in surface temperature due to exposure to sunlight (Gardiner and Hassall 2009). Considering Acrida cinerea's relatively large body size (especially in females), actively seeking sunlit locations may be beneficial for effectively warming up the body (Pielou 1948, Ahnesjo and Forsman 2006).
Grasshoppers from Oedipodinae are generally known to favor bare ground (Otte 1981, Craig et al. 1999, Chu 2002, Capinera et al. 2004). Therefore, it is not surprising that individuals of Oedaleus infernalis in our study were often observed on the bare soil exposed to sun. This preference might have provided thermal benefits, especially to females, which are relatively heavy (4-5 times heavier than Atractomorpha lata and male Acrida cinerea). Warming up their heavy bodies is easier in hot locations on the ground. The body color of each grasshopper species seems to be well adapted to its own microhabitat. Oedaleus infernalis usually has a light brown body with dark brown stripes (Kim 2013), providing camouflage on typical ground coloration in the natural habitat. Conversely, the color of Acrida cinerea and Atractomorpha lata is usually green (Tanaka 2008, Pellissier et al. 2011), making it hard to recognize the individual grasshoppers against green plant parts. Additional camouflage is provided by the resting posture of Atractomorpha lata. With their hind legs tightly pressed against their body and pointy tips of head and wings visibly protruding, the individual grasshopper resembles a narrow green leaf. Acrida cinerea also have pointy head tips contributing to their camouflage while sitting on plant stems or grass leaves.
In summary, we documented microhabitat segregation among three common Asian grasshopper species and we hypothesized that food and microclimatic preferences, as well as phylogenetic history, might have contributed to the observed differences. These differences coincide with the differences between species in adaptations to camouflage their bodies in their respective microhabitats. Future experiments should determine if active preferences for specific habitats are responsible for the observed segregation, and if interspecific competition affects the segregation.
We are thankful to field helpers Eunjeong Yang and Yeojoo Yoon. We thank Tim Gardiner and Tan Ming Kai for helpful comments. The study was funded by NRF grants 2016R1D1A1B03934340 and 2013R1A2A2A01006394, the DGIST Start-up Fund Program of the Ministry of Science, and the BK 21 program awarded to the School of Biological Sciences, Seoul National University. YJ and MB designed and conducted the field work, analyzed data and wrote the paper with SIL and PGJ. All authors contributed to the final version of the manuscript.
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
Capinera JL, Scott RD, Walker TJ (2004) Field Guide to Grasshoppers, Crickets, and Katydids of the United States. Cornell University Press, 280 pp.
Chu JB (2002) Diet for an endangered insect: what does the zayante band-winged grasshopper eat? MSc Thesis, San Jose State University, 79 pp.
Craig DP, Bock CE, Bennett BC, Bock JH (1999) Habitat relationships among grasshoppers (Orthoptera: Acrididae) at the western limit of the Great Plains in Colorado. The American Midland Naturalist 142: 314-327. https://doi.org/10.1674/0003-0031(1999)142[0314:HRAGOA]2.0.CO;2
Eterovick PC, Figueira JEC, Vasconcellos-Neto J (1997) Cryptic coloration and choice of escape microhabitats by grasshoppers (Orthoptera: Acrididae). Biological Journal of the Linnean Society 61: 485-499. https://doi.org/10.1111/j.1095-8312.1997.tb01803.x
Gardiner T, Hassall M (2009) Does microclimate affect grasshopper populations after cutting of hay in improved grassland? Journal of Insect Conservation 13: 97-102. https://doi.org/10.1007/s10841-007-9129-y
Haldar P, Bhandar KP, Nath S (1995) Observations on food preferences of an Indian grasshopper Acrida exaltata (Walker) (Orthoptera: Acrididae: Acridinae). Journal of Orthoptera Research 4: 57-59. https://doi.org/10.2307/3503458
Hardin G (1960) The competitive exclusion principle. Science 131: 1292-1297. https://doi.org/10.1126/science.131.3409.1292
Isely FB (1937) Seasonal succession, soil relations, numbers, and regional distribution of north-eastern Texas acridians. Ecological Monographs 7: 317-344. https://doi.org/10.2307/1943054
Joern A (1979) Feeding patterns in grasshoppers (Orthoptera: Acrididae): factors influencing diet specialization. Oecologia 38: 325-347. https://doi.org/10.1007/BF00345192
Joern A (1982) Vegetation structure and microhabitat selection in grasshoppers (Orthoptera, Acrididae). The Southwestern Naturalist 2: 197-209. https://doi.org/10.2307/3671144
Kim TW (2013) Orthoptera of Korea. GEO Book, Seoul, 381 pp.
Mangiafico SS (2015) An R Companion for the Handbook of Biological Statistics, version 1.3.2. http://rcompanion.org/documents/RCompanionBioStatistics.pdf
Miura K, Ohsaki N (2004a) Relationship between physical leaf characteristics and growth and survival of polyphagous grasshopper nymphs, Parapodisma subastris (Orthoptera: Catantopidae). Population Ecology 46: 179-184. https://doi.org/10.1007/s10144-004-0177-9
Miura K, Ohsaki N (2004b) Diet mixing and its effect on polyphagous grasshopper nymphs. Ecological Research 19: 269-274. https://doi.org/10.1111/j.1440-1703.2004.00635.x
Miura K, Ohsaki N (2006) Examination of the food processes on mixed inferior host plants in a polyphagous grasshopper. Population Ecology 48: 239-243. https://doi.org/10.1007/s10144-006-0267-y
Otte D (1981) The North American Grasshoppers: Acrididae: Oedipodinae (Vol. 2). Harvard University Press, 376 pp.
Park SJ, Kim BJ (2011) Comparative insect faunas between Ganghwado and six other islands of west coastal in Incheon, Korea. Entomological Research 41: 285-285. https://doi.org/10.1111/j.1748-5967.2011.00397.x
Pellissier L, Wassef J, Bilat J, Brazzola G, Buri P, Colliard C, Perrin N (2011) Adaptive colour polymorphism of Acrida ungarica H. (Orthoptera: Acrididae) in a spatially heterogeneous environment. Acta Oecologica 37: 93-98. https://doi.org/10.1016/j.actao.2010.12.003
Pielou DP (1948) Observations on the behaviour of gregarious hoppers of the red locust, Nomadacris septemfasciata Serville. Physiological Entomology 23: 19-27. https://doi.org/10.1111/j.1365-3032.1948.tb00598.x
Storozenko SJ, Paik JC (2007) Orthoptera of Korea. Dalnauka, Vladivostok, 232 pp.
Sword GA (2002) A role for phenotypic plasticity in the evolution of aposematism. Proceedings of the Royal Society of London B: Biological Sciences 269: 1639-1644. https://doi.org/10.1098/rspb.2002.2060
Sword GA, Simpson SJ, El Hadi OTM, Wilps H (2000) Density-dependent aposematism in the desert locust. Proceedings of the Royal Society of London B: Biological Sciences 267: 63-68. https://doi.org/10.1098/rspb.2000.0967
Tan MK, Storozhenko SY, Hwang WS, Meier R (2017) 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.
Tanaka Y (2008) Effects of temperature on body color change in the grasshopper Atractomorpha lata (Orthoptera: Pyrgomorphidae) with reference to sex differences in color morph frequencies. Entomological Science 11: 49-54. https://doi.org/10.1111/j.1479-8298.2007.00256.x
Yoshioka A, Kadoya T, Suda SI, Washitani I (2010) Impacts of weeping lovegrass (Eragrostis curvula) invasion on native grasshoppers: responses of habitat generalist and specialist species. Biological Invasions 12: 531-539. https://doi.org/10.1007/s10530-009-9456-x
YONGJUN JUNG (1), MINJUNG BAEK (1), SANG-IM LEE (2), PIOTR G. JABLONSKI (1,3)
(1) Laboratory of Behavioral Ecology and Evolution, School of Biological Sciences, Seoul National University, Seoul 08826, South Korea.
(2) Daegu-Gyeongbuk Institute of Science and Technology School of Undergraduate Studies, Daegu 42988, South Korea.
(3) Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland.
Corresponding authors: Sang-im Lee (firstname.lastname@example.org); Piotr G. Jablonski (email@example.com)
Academic editor: A. Avanesyan | Received 24 July 2018 | Accepted 25 October 2018 | Published 5 December 2018
Table 1. Number of individuals of the three grasshopper species observed on ground and plants. The category "Others" includes Fabaceae, Lamiaceae, Onagraceae, Polemoniaceae and Cannabaceae. Substrate Grasshopper Total A. cinerea A. lata O. infernalis Ground 6 4 53 63 Asteraceae 18 116 7 141 Poaceae 51 22 28 101 Others Fabaceae 0 8 2 10 Lamiaceae 1 4 0 5 Onagraceae 0 3 1 4 Polemoniaceae 1 0 1 2 Cannabaceae 0 1 0 1 Total 77 158 92 327
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|Title Annotation:||Short Communication|
|Author:||Jung, Yongjun; Baek, Minjung; Lee, Sang-im; Jablonski, Piotr G.|
|Publication:||Journal of Orthoptera Research|
|Date:||Jul 1, 2018|
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