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Home , Acrididae, Acridoidea, Caelifera, Ensifera, Mole cricket, Neotridactylus

Turkish Journal of Zoology Turk J Zool (2016) 40: 720-728 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1510-19

Mandibular morphology and dietary preferences in two pygmy crickets of the genus (: Tridactylidae)

Kateřina KUŘAVOVÁ*, Petr KOČÁREK Research Group, Department of Biology and Ecology, Faculty of Science, University of Ostrava, Slezská Ostrava, Czech Republic

Received: 07.10.2015 Accepted/Published Online: 10.03.2016 Final Version: 24.10.2016

Abstract: Pygmy mole crickets (Tridactylidae) are an interesting but little-known group of Orthoptera; their food biology and dietary preferences have not been adequately studied. Our study focused on the diet composition and associated functional morphology of the mandibles in two European : Xya pfaendleri Harz, 1970 and X. variegata (Latreille, 1809). Based on postmortem gut content analyses, the studied species feed mainly on detritus (decaying organic particles), representing 91% and 97% of the diet in X. pfaendleri and X. variegata, respectively. The mandibular structures are associated with the processing of such food.The incisor area is equipped with three robust and sharp teeth, and the molar area consists of a small molar ridge forming a trituration area with parallel molar slats. The size of the molar ridge is determined by sex and the side (left/right) of the mandibles: females have larger molar ridges than males and left molar ridges are larger than the right. Food preferences as well as measured parameters of the mandibles were similar in both studied species due to the similar pattern of their biology. The narrow food niche indicates a low diversity of consumed food and uniformity of food intake.

Key words: Detritophagy, detritovory, food biology, mouthparts, exoskeleton

1. Introduction The food biology and dietary preferences of pygmy mole Although the food strategies of many Orthoptera species are crickets (: Tridactylidae) are poorly understood relatively well known, the food strategy in certain species has due to their small body size (up to 5 mm) and hidden only been estimated based on the structure of the mouthparts, way of life. Pygmy mole crickets build horizontal galleries habitat preferences, or feeding behavior observed in only a beneath the surface of wet damp substrates, usually on few individuals. Species of the suborder Caelifera are mostly the banks of ponds or rivers, and they are considered to herbivorous (Acridomorpha) and only rarely detrito-/ be -feeders or omnivorous (Blackith, 1987; bryophagous (Tetrigoidea). Species of Tridactylidae (pygmy Deyrup and Eisner, 1996). mole crickets) are probably omnivorous, although detailed Our study focused on determining whether the pygmy analyses of their food preferences have not been performed. mole crickets Xya pfaendleri Harz, 1970 and X. variegata The consumption of a specific diet is associated with the (Latreille, 1809) are dietary specialists or omnivorous shape and structure of the mandibles; four types of mandibles detritus feeders. This study was based on analyses of (graminivorous, forbivorous, herbivorous, and bryovorous postmortem gut contents and the mandibular structures types) have been identified in orthopterans (Isely, 1944; associated with food processing. The aims of the study were Kaufmann, 1965; Uvarov, 1977; Aguirre et al., 1987; Smith and to describe and compare the structure of the mandibles in Capinera, 2005). A correlation between mouthpart structure the two pygmy mole crickets, evaluate food preferences of and the specific diet of orthopterans has been reported for only pygmy mole crickets, and assess interspecific differences in a few species, i.e. Locusta migratoria (L., 1758); these highly similar and related species. gregaria (Forskål, 1775); desultorius Rehn, 1907; pallidipennis (Burmeister, 1838); obscura 2. Materials and methods (Thomas, 1872); and tenuicornis (Sahlberg, 1891) 2.1. Study organisms (Gangwere, 1960, 1961, 1965; Patterson, 1983, 1984; Kang et The pygmy mole crickets Xya pfaendleri and Xya variegata al., 1999; Kuřavová et al., 2014). (Orthoptera: Tridactylidae) are small (4–6 mm total body * Correspondence: [email protected] 720 KUŘAVOVÁ and KOČÁREK / Turk J Zool length), shiny, dark or black and cryptic-colored insects. (length of the mandible, determined as the distance They are characterized by stout and enlarged femurs of the between the mandibular junction and the peak of the first hind legs that are adapted for leaping. They can jump as incisor; surface of the molar ridge; number of slats) were far as 1 m (Burrows and Picker, 2010; Burrows and Sutton, measured using the software SEM JEOL/EO version 1.0. 2012). Pygmy mole crickets are riparian and thermo- The alimentary tract contents of each specimen were hygrophilous, and they have a Ponto-Mediterranean permanently mounted in Hoyer’s solution (Anderson, distribution (Zechner et al., 1999; Berg et al., 2000; 1954) on a glass microscope slide. The slides were Kočárek et al., 2005; Baur et al., 2006; Münsch et al., 2013). observed using a light microscope (Olympus CX41RF, They live in shallow burrows, which they build in sandy Hamburg, Germany) at 400× magnification and were then soil alongside bodies of water, including streams, ponds, or photographed using a camera (Canon EOS 1100D, Tokyo, sand quarries with permanent or temporal water (Blackith Japan) mounted on the microscope. The entire alimentary and Blackith, 1979; Münsch et al., 2013). tract preparation from each specimen was photographed. 2.2. Collection and treatment of samples These photographs were evaluated using BaDra 2.0 Specimens of Xya pfaendleri and X. variegata were image analysis software (BaDra, 2011). The software was collected from two localities in the southeastern part of the used to determine the proportions of food components Czech Republic. Specimens of X. pfaendleri were collected (proportion of detritus + plant cellular matter + other on 12 August 2013 in a littoral zone (sand substrate) of particles = 1): 2 a small pond (~25 m ) in the area surrounding Lanžhot Proportions of diet = ∑ pi (%) (1) (48°40′34″N, 16°55′25″E) at approximately 200 m a.s.l. where pi is the proportion in the alimentary tract content, Specimens of X. variegata were collected on 4 June 2013 and i is the type of diet component as either detritus at a sand quarry in Mušlov near Mikulov (48°47′30″N, (unidentified decaying organic particles), plant cellular 16°41′11″E). This locality has an area of 20 m2 and an matter (lower plants, algae), or other particles (fragments elevation of 250 m a.s.l. The specimens were collected of cuticles, mineral particles). by sweeping and were immediately stored in 70% The proportions of the components of the diet were alcohol for later analysis of the alimentary tract contents evaluated and were used to calculate the food niche and morphology of the mandibles. A total of 24 adult breadth based on the Gini–Simpson index (Gini, 1912, in specimens (6 males and 6 females of X. pfaendleri, 6 males Di Russo et al., 2014): 2 and 6 females of X. variegata) were used for the analysis. Gini–Simpson index = 1 – ∑pi (2) In the laboratory, both mandibles of each specimen where pi is proportion of the ith component in the were dissected, examined, and documented by scanning alimentary tract content. electron microscopy (SEM; JEOL JSM-6610LV, Tokyo, 2.3. Statistical analysis Japan) (SEI, 12 kV, WD 41 mm, SS30, 130–1500× The measured parameters of the mandibles (distance magnification). The mandibles were sputter-coated with between the mandibular junction and the first incisor, gold prior to SEM (Automatic Sputter Coater: JEOL JFC- surface of the molar ridges, and number of molar slats) are 1300, Tokyo, Japan). The parameters of both mandibles presented as the means ± SD (Table 1). According to the

Table 1. Parameters measured on the left and right mandibles of Xya pfaendleri and Xya variegata. LM - length of the mandible (distance between the mandibular junction and the peak of the first incisor); SMR - surface of the molar ridge; NS - number of slats.

Left mandible Right mandible Species LM [µm] SMR [µm2] NS LM[µm] SMR [µm2] NS X. pfaendleri Male 506.9 ± 34.9 8767 ± 703 12.5 ± 0.8 520.3 ± 7.5 8186 ± 495 12.5 ± 0.8 Female 676.0 ± 25.9 16204 ± 678 12.8 ± 0.8 612.9 ± 1.0 11720 ± 319 12.2 ± 0.5 X. variegata Male 570.9 ± 0.7 14180 ± 346 13.0 ± 0.3 530.1 ± 0.6 13453 ± 402 13.0 ± 0.3 Female 714.7 ± 29.3 21804 ± 1153 13.8 ± 0.6 653.2 ± 13.9 17730 ± 438 12.8 ± 0.6

A total of 24 specimens of X. pfaendleri and X. variegata were measured. The values (means ± SD) are in micrometers.

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Shapiro–Wilk normality test, all data were not normally 3. Results distributed. The effects of the side of the mandible, sex, 3.1. Mandible structures of pygmy mole crickets and species on the measured parameters of the mandibles The mandibles of pygmy mole crickets of the genus Xya of X. pfaendleri and X. variegata were evaluated using have an asymmetrical shape (Figure 1). The left mandibles general linear models (gamma distribution function). are longer than the right mandibles (the average difference Analysis of variance (ANOVA) was used to determine the was approximately 1% in X. pfaendleri and 8% in X. effects of the left/right mandible, sex, and species on the variegata), although the difference was significant only for measured parameters of the mandibles of X. pfaendleri and X. variegata (Table 2). The lengths of the left mandibles X. variegata. are greater than the lengths of the right mandibles, with The alimentary data were evaluated using general linear models (Gaussian distribution function). The effects the exception of males of X. pfaendleri and X. variegata. of sex, species, and the interaction of sex versus species on Both the right and left mandibles are bigger in females the proportion of food components in the alimentary tracts than in males (Table 2; Figure 2). The general shapes of the were tested using multifactorial ANOVA (general linear mandibles are similar in both species: the left mandibles model with a Gaussian distribution function). The effects are elongated and narrower and the right mandibles are of sex, species, and the interaction of sex versus species shorter and wider. Each of the mandibles consists of on the food niche breadth were tested using multifactorial two functional parts: the incisor area and the molar area ANOVA (general linear model with a Gaussian distribution (Figure 1). The incisor area is equipped with three robust function). All analyses were performed using the R Ver. and sharp teeth. The molar area consists of a small molar 2 statistical program (R Development Core Team, 2003). ridge, which is strongly concave on both mandibles. The The significance level was α = 0.05 throughout. size of the molar ridge is affected by sex and the side (left/

Figure 1. Dorsal and ventral views of the left and right mandibles of Xya pfaendleri and X. variegata. The microstructures of the mandibles were documented by scanning electron microscopy (SEM; JEOL JSM-6610LV): SEI, 12 kV, WD 50 mm, SS30, 65× magnification.

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Table 2. ANOVA results for the mandibular parameters in X. pfaendleri and X. variegata as affected by independent variables, including mandible side, sex, and studied species. LM - length of the mandible, distance between the molar junction and the peak of the first incisor; SMR - surface of the molar ridge; NS - number of slats on the molar ridge.

Independent LM SMR NS variable F-value P-value F-value P-value F-value P-value

Left/right side X. pfaendleri 2.6 0.11 23.4 <0.001* 0.75 0.39 X. variegata 28.1 <0.001* 24.3 <0.001* 2.82 0.10 Sex X. pfaendleri 73.4 <0.001* 109.6 <0.001* 0.75 0.39 X. variegata 191.7 <0.001* 149.3 <0.001* 1.25 0.11 Between species Left mandible 1.9 0.17 10.3 <0.01* 4.1 0.05 Right mandible 1.1 0.29 40.7 <0.001* 3.2 0.08

A total of 24 specimens of pygmy mole crickets were analyzed. *P < 0.05.

Figure 2. Comparison of the measured parameters of the mandibles in females (gray boxes) and males (white boxes) of Xya pfaendleri and X. variegata (Tridactylidae). a, d: length of the mandible (distance between the mandibular junction and the peak of the first incisor); b, e: surface of the molar ridge; c, f: number of molar slats. The box plots show the median (50th percentile) and 25th and 75th quartiles; error bars show the 10th and 90th percentiles. Filled symbols indicate outliers.

723 KUŘAVOVÁ and KOČÁREK / Turk J Zool right) of the mandibles: females have larger molar ridges 3.2. Dietary preferences than males, and the left molar ridges are larger than the The digestive tracts of the two species of pygmy mole right (Table 2). The molar ridge forms a trituration area crickets from the genus Xya contained mainly detritus, with parallel molar slats. The molar slats contain several defined as unidentified decomposed organic matter, which parallel teeth. These teeth are short and regularly aligned. accounted for 91% and 97% of the consumed diet in X. There was an average of 12 molar slats per molar ridge, and pfaendleri and X. variegata, respectively (Figure 4). Algae the number of molar slats was not significantly different formed a minor component and body parts of invertebrates between the sides of the mandibles or between females (fragments of cuticles, and setae) were rare, accounting for and males (Table 2). Differences in measured parameters 9% and 3% of the total diet in the alimentary tract in X. between the studied species of pygmy mole crickets were pfaendleri and X. variegata, respectively. Angiosperms, significant only with respect to the parameter surface of fungal spores, and were not found. The ratios of the molar ridge, with X. variegata having a larger molar detritus/plant cellular matter/other particles were 29:1:3 ridge than X. pfaendleri (Table 3; Figure 3). and 19:1:0 in females and 47:1:1 and 1:0:0 in males of X.

Table 3. ANOVA results for the composition of detritus, plant cellular matter, and other particles in Xya pfaendleri and X. variegata as affected by independent variables, including sex and species.

Independent Detritus Cellular matter Other particles Gini–Simpson index variable F-value P-value F-value P-value F-value P-value F-value P-value

Sex 5.52 0.03* 2.74 0.11 2.47 0.13 6.06 0.02* Species 2.74 0.11 0.05 0.82 2.47 0.13 0.12 0.12 Sex × species 0.73 0.40 2.06 0.16 2.47 0.13 0.40 0.53

A total of 24 specimens of pygmy mole crickets were analyzed. An asterisk indicates significant differences (P < 0.05) between types of diet.

Figure 3. Differences in the surfaces of the (a) left and the (b) right mandibles in Xya pfaendleri and X. variegata. The box plots show the median (50th percentile) and 25th and 75th quartiles; error bars show the 10th and 90th percentiles.

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Figure 4. The proportion of detritus in the diet of females (F) and males (M) in (a) Xya pfaendleri and (b) X. variegata as determined based on the postmortem gut content analyses. The box plots show the median (50th percentile) and 25th and 75th quartiles; error bars show the 10th and 90th percentiles. Open circles indicate outliers. pfaendleri and X. variegata, respectively. The proportion of than in males and was similar between species (Table 3; detritus in the diet differed in males and females, although Figure 5). The maximum average index was 0.1, where the proportions of cellular matter and other particles values less than 0.5 indicate a low variability of diet and were similar (Table 3; Figure 4). The diet niche breadth consumption of only a single food resource. according to the Gini–Simpson index was wider in females

Figure 5. The food niche breadths in males (M) and females (F) of (a)Xya pfaendleri and (b) X. variegata (Orthoptera: Tridactylidae). The food niche breadth was cumulatively evaluated based on the Gini-Simpson index. The box plots show the median (50th percentile) and the 25th and 75th quartiles; error bars show the 10th and 90th percentiles.

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4. Discussion the molar area acts as a grinder to fragment food into small We evaluated the dietary preferences and morphological pieces. The mandibular areas of groundhoppers have similar structure of the mandibles of two pygmy mole crickets from functions (Kuřavová et al., 2014). the genus Xya (Orthoptera: Tridactylidae). The dominant The measured parameters (the distance between the component of the diet was detritus, which we defined as mandible junction and the peak of the incisor, the surface of noncellular decomposing organic matter. Differences in the molar ridge, and the number of slats) were significantly the morphological structures of the mandibles of the two different between sexes, between sides of the mandibles, species were minimal to nonexistent. The mandibles are and between studied species. Females of Caelifera typically asymmetrical in both species; the left and right mandibles have a larger body size than males (Zechner et al., 1999; differ in size and partly in shape. Uniformity in the diet Kočárek et al., 2005; Bidau et al., 2013); therefore, the is associated with the functional morphology of the lengths of the mandibles and the molar ridges’ surface are mandibles as well as similar patterns of the biology and considerably larger in females than in males. The number habitat preferences of the studied pygmy mole crickets. of molar slats does not differ between sexes (on average 12.8 Asymmetry of body structures is a rare characteristic ± 0.3), and these structures are uniform among individuals of that have evolved independently many times of both species and between species. Some tropical species (Palmer, 2009). In Orthoptera, the fixed asymmetry is of groundhoppers (Discotettiginae, , and associated with mouthparts, side of forewing, and shape ) show different numbers of slats on the molar of genitalia (Huber et al., 2007; Palmer, 2009). Pygmy ridge (from 9 to 19 slats), although differences between mole crickets have asymmetrical mandibles, with the sexes have not been reported (Kuřavová et al., unpublished left mandible being larger than the right, which is based data). In summary, the measured parameters were not on the use of the mandibles during food intake. Other significant between the studied pygmy mole crickets; X. studied Caelifera ( and groundhoppers) also pfaendleri and X. variegata have almost the same features show asymmetry in mandible size, with the left mandible regarding the morphological structures of the mandibles, always overlapping the right (Snodgrass, 1935; Isely, 1944; likely due to similar dietary and behavioral patterns. Uvarov, 1977; Bernays et al., 1991; Chapman, 1995; Köhler The aspects of food strategies, such as food et al., 2000 for grasshoppers, and Kuřavová et al., 2014 for selection, food preferences, feeding patterns, and diet groundhoppers). The mandibular asymmetry is important specialization, have been studied by many authors in a for the correct mutual contact of mandibles during variety of grasshoppers (e.g., Williams, 1954; Mulkern, biting to assure that the cusps intermesh with each other 1967; Otte and Joern, 1976; Bernays and Chapman, (O’Brien, 1984). 1977; Uvarov, 1977; Joern, 1979, 1983, 1985; Bernays Adaptation to food intake has led to behavioral and and Bright, 1993). The food biology of groundhoppers, morphological specialization of mouthparts (Snodgrass, as detrito-/bryophagous insects, has been studied only 1935). Grasshoppers (Caelifera: Acridomorpha) are often in a few species (for references, see Kuřavová et al., 2014; phytophagous (Fry et al., 1978), and the adaptations of Kuřavová and Kočárek, 2015). The dietary preferences their mandibular structures are associated with different of pygmy mole crickets (Tridactylidae) have not been types of food and different species of ecological groups of studied in detail. Only Deyrup and Eisner (1996) recorded plants, grasses, forbs, flowers, and seeds (Bernays, 1998; filamentous algae in the gut of the pygmy mole Isely, 1944; Patterson, 1984). Blackith (1987) suggested archboldi Deyrup & Eisner, 1996. Blackith that many species of the basal orthopteran families, such as (1987) also suggested that pygmy mole crickets are algal the Tridactylidae and , are mainly algae feeders feeders. Our analysis of the alimentary tract contents (lower-plant feeders), and the mouthparts are adapted to of pygmy mole crickets showed that the species of the this food source. We found that the mandible structures of genus Xya are mainly detritophagous, and cellular matter, the pygmy mole crickets are reduced in comparison with such as algae, is consumed only incidentally together related groundhoppers of the Tetrigidae (Kuřavová et al., with detritus. Detritus is present in large amounts in the 2014). The incisor area of the groundhoppers consists of four pygmy habitat and is easily accessible inside incisors, and the molar area bears the central teeth and a their underground corridors. We confirmed that the molar ridge with parallel molar slats (Kuřavová et al., 2014). pygmy mole crickets do not search for specific matter Pygmy mole crickets have only three incisors and a molar (e.g., , mosses, or plants) as diet but utilize the ridge with only a few molar slats. The basic features (shape of diet present in their burrows and their surroundings. the incisor teeth and teeth on the molar ridge) are similar to The determined dietary uniformity could reflect their those of Tetrigidae due to their evolutionary, morphological, habitat preferences, especially their subterranean lifestyle. and functional association. The incisors of both the left and Pygmy mole crickets are forced to stay in subterranean right mandibles overlap and work as a pair of scissors, and corridors to protect themselves from predators, such as

726 KUŘAVOVÁ and KOČÁREK / Turk J Zool hymenopteran spp. (, Sphecidae, hypothesis predicts greater overall mandibular variability and Larrinae) that dig beneath the surface of the ground in forms having the broadest trophic niches. Comparisons to capture pygmy mole crickets (Kurczewski, 1966). have shown that groundhoppers of the family Tetrigidae The studied species of pygmy mole crickets had similar (Kuřavová et al., 2014; Kuřavová and Kočárek, 2015) and diet breadths. The species showed food niche breadth pygmy mole crickets of the family Tridactylidae have values of up to 0.4, which corresponds with a narrow similar patterns of mandibular variation and dietary food spectrum. For comparison, the groundhopper Tetrix preferences. The Tetrigidae have more complex mandible tenuicornis (Tetrigidae) showed a maximum food niche structures and more heterogeneous food intake than the breadth value of 0.6 (Kuřavová and Kočárek, 2015). Males Tridactylidae. This association of the morphology and of X. pfaendleri and X. variegata exhibited a significantly dietary preference in each group supports Patterson’s higher uniformity of diet than females, likely because niche variation hypothesis. females require a more nutritionally balanced diet for egg production. X. pfaendleri and X. variegata have almost the Acknowledgments same dietary preferences, and the food biology of both is This study was supported by Institutional Research Support related to their habitat preferences. The studied species grants from the University of Ostrava (SGS24/PřF/2014, have similar demands on habitat quality and occupy the SGS22/PřF/2015), Project CZ.1.05/2.1.00/03.0100 (IET), same areas, sometimes in a syntopic manner (Holuša and which was financed by the Structural Funds of the Kočárek, 1999; Gavlas et al., 2007). European Union, and by Project LO1208 of the National Patterson (1983) compared the structure of Feasibility Program I of the Czech Republic. mandibles with their niche variation. The niche variation

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