Interspecific Variation in Life History Traits of Elasmostethus

69 Interspeciﬁc variation in life history traits of Elasmostethus (Hemiptera: Acanthosomatidae) Shin-ichi Kudo,1 Aki Yamamoto, Tadao Ichita, Haruki Tatsuta

Abstract—Life history traits, such as clutch size, egg size (weight), developmental periods of eggs, and female body (abdomen) size, were investigated in Japanese species of the genus Elasmostethus Fieber (Hemiptera: Acanthosomatidae): E. amabilis Yamamoto, E. brevis Lindberg, E. humeralis Jakovlev, E. interstinctus (Linnaeus), E. kerzhneri Yamamoto, and E. nubilus (Dallas). With the exception of clutch size, signiﬁcant differences were observed in the traits among species. No species exhibited maternal care of eggs. These data form a solid basis for future comparative analyses in the family Acanthosomatidae, which contains both subsocial and asocial species.

Acanthosomatidae (Hemiptera) consists of within this lineage, providing a strong basis for three subfamilies, 56 genera, and about 285 future comparative analyses of life history traits. species (Tsai and Rédei 2015). The monophyly of However, in order to ensure that such analyses are Acanthosomatidae has been demonstrated by sufﬁciently robust, quantitative data needs to be morphological and molecular studies (Grazia et al. collected from as many species as possible. 2008), and maternal care of eggs and young, i.e., The genus Elasmostethus Fieber belongs to the guarding against predators with shielding posture subfamily Acanthosomatinae. Monophyly of this and aggressive responses, has been reported in genus has been suggested based on molecular several genera (Tachikawa 1991; Tsai et al. 2015). phylogenetic analysis (Tsai et al. 2015). Some Costa (2006) suggested that acanthosomatids are reproductive traits, such as clutch size and egg size, well suited for comparative studies on the corre- have been recorded in E. interstinctus (Linnaeus) lated evolution of parental care and other life his- and E. humeralis Jakovlev (Mappes et al.1996; tory traits, such as egg size and clutch size (Shine Kudo 2001). While there are some descriptions 1978; Fox and Czesak 2000) and on the associa- of breeding behaviour in other Elasmostethus tion between the evolution of life history traits and species (Carter and Hoebeke 2003; Kobayashi and environmental factors (Wilson 1975; Wong et al. Tachikawa 2004), no quantitative data have been 2013). However, with the exception of studies on published for these species to date. a few closely related species (Kaitala and Mappes Here we present life history data, i.e., clutch 1997; Kudo 2001), no comparative studies have size, egg size (weight), and the developmental been conducted using this taxon. periods of eggs, which can be associated with Recently, Tsai et al. (2015) reconstructed the mortality risks (Shine 1978). We also present data phylogeny of this family using molecular data and on female body (abdomen) size, which limits the inferred the origin of maternal care in 52 species total amount of resources allocated to reproduction and one subspecies of the three subfamilies in (Fox and Czesak 2000) in E. amabilis Yamamoto, Acanthosomatidae. Based on their ﬁndings, it is E. brevis Lindberg, E. humeralis, E. interstinctus, considered that maternal care evolved repeatedly E. kerzhneri Yamamoto, and E. nubilus (Dallas).

Received 11 May 2018. Accepted 22 August 2018. First published online 20 November 2018.

S. Kudo,1 Department of Biology, Naruto University of Education, Naruto, Tokushima 772-8502, Japan A. Yamamoto, Otaru Museum, Otaru, Hokkaido 047-0031, Japan T. Ichita, Aomori Prefecutural Plant Protection Ofﬁce, Dainitonya-machi, Aomori 030-0113, Japan H. Tatsuta, Department of Ecology and Environmental Sciences, Faculty of Agriculture, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan

1Corresponding author (e-mail: [email protected]) Subject editor: Amanda Roe doi:10.4039/tce.2018.56 A previous error in this article has been corrected, please see https://doi.org/10.4039/tce.2018.65.

Can. Entomol. 151:69–72 (2019) © 2018 Entomological Society of Canada Downloaded from https://www.cambridge.org/core. University of Athens, on 25 Sep 2021 at 04:12:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2018.56 70 Can. Entomol. Vol. 151, 2019

In June and July from 1986 to 2016, we collected measure the developmental period of eggs, egg overwintered females from different localities in clutches were kept at 20.0 ± 0.5 °C under Japan; E. kerzhneri at Mount Hakkoda, Aomori, 15:9 hour light:dark conditions. We recorded the Honshu; E. brevis at Taisetsu-ko, Kamikawa, day when the first egg hatched in each clutch, but Hokkaido; E. amabilis, at Mount Haruka-yama, the egg hatching usually synchronised within Sapporo, Hokkaido; E. nubilus at Naruto, Tokushima, clutches. Female abdomen length (Fig. 2), which Shikoku; E. interstinctus at Hitsujigaoka, Sapporo, is used as a measure of female body size, was Hokkaido; and E. humeralis at Maruyama, Sapporo, measured under a stereomicroscope using a cali- Hokkaido. Voucher specimens were deposited in the brated ocular micrometer. Otaru Museum, Otaru, Hokkaido, Japan. We compared the size of the clutches laid under Females were maintained individually in a laboratory conditions against clutch sizes plastic container (9 cm in diameter, 3 cm in observed in the field in three species, i.e., height) with host plant leaves and fruit at E. humeralis (the number of field clutches and that 20.0 ± 0.5 °C under 15:9 hour light:dark condi- of laboratory clutches = 233 and 38), E. kerzhneri tions. Females typically laid clutches of eggs on (20 and 14), and E. nubilus (62 and 28). Since no the leaf (Fig. 1) or on the fruit, but occasionally on significant difference was observed within any of the inside surface of the plastic container. After the three species (all P > 0.05 using analysis of counting the number of eggs in the first clutch, variance), we pooled the data for the laboratory five to 10 eggs were randomly selected and and field clutches for inter-specificcomparison. weighed together to the nearest 0.01 mg to calcu- JMP13 (SAS Institute 2016) was used for the sta- late average egg weight. In some species, clutch tistical analyses. size and egg weight data were also obtained from Table 1 shows a summary of life history traits in clutches without scars, which might be made by six Elasmostethus species. Although clutch size predators on host plant leaves in the field. To did not vary significantly among the species

Fig. 1. Egg clutches in Elasmostethus species. A, Elasmostethus kerzhneri; B, E. humeralis; C, E. brevis; D, E. nubilus. Scale bars = 1.0 mm. A B

C D

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Fig. 2. Elasmostethus female abdomen length Araliaceae, and E. brevis and E. amabilis on measurement. Salicaceae (Yamamoto 2003; Yamamoto et al. 2009). These host plants can provide Elasmostethus with different environmental conditions in terms of physical and chemical defence mechanisms, the risk of predation and parasitism and intraspecificand interspecific competition over food resources (Price et al. 1980). Such host-specific ecological factors may exert different selection pressures on the life history traits of Elasmostethus species, promoting divergence through trade-offs between the traits. Mappes et al. (1996) reported that E. interstinctus females adjust resource allocation among clutches, particularly for clutch size, according to female age (in laying sequence). A marked variation in clutch size was observed within each Elasmostethus species in this study (Table 1); the coefficient of variation in clutch size for each species was usually over 50%. In all of the species investigated in the present study, the females produce clutches repeatedly (Mappes et al. 1996; S.K., personal observation). Although the clutch size data presented here were typically from the first clutch produced by field-collected females, examined, significant differences were observed the breeding experience of females may differ at the in the other traits. None of the species exhibited time of collection. The large variation in clutch size maternal care, including E. amabilis, for which may include components of variation not only among the reproductive behaviour was previously females, but also among clutches laid by females. unknown (Tsai et al. 2015). When these life history traits of the species Elasmostethus species use different plants for examined in this study are compared with those of breeding, on which nymphs feed on fruit (seeds); other genera in the Acanthosomatidae, some for example, E. interstinctus and E. kerzhneri meaningful trends can be found. For example, depend on members of the Betulaceae, E. humeralis clutch sizes in Elasmostethus are smaller than on Apiaceae and Araliaceae, E. nubilus on those in Elasmucha Stål and Sastragala Amyot

Table 1. A summary of life history traits of Elasmostethus species.

Coefﬁcient of variation Egg period Abdomen Clutch size (%)* Egg size (mg) (days)≅ length (mm) E. amabilis 24.9 ± 16.1 (19) 64.4 0.239 ± 0.013 (15) 6.60 ± 0.55 (5) 5.00 ± 0.25 (23) E. brevis 17.1 ± 8.95 (37) 52.3 0.299 ± 0.032 (25) 6.40 ± 0.52 (10) 5.33 ± 0.17 (28) E. humeralis 19.8 ± 9.22 (271) 46.6 0.250 ± 0.018 (25) 6.56 ± 0.50 (45) 5.96 ± 0.34 (40) E. interstinctus 19.6 ± 14.8 (14) 75.7 0.277 ± 0.019 (14) 6.78 ± 0.44 (9) 5.53 ± 0.29 (28) E. kerzhneri 20.1 ± 10.8 (34) 53.7 0.306 ± 0.025 (14) 6.36 ± 0.50 (5) 5.39 ± 0.41 (30) E. nubilus 19.7 ± 10.8 (90) 54.6 0.194 ± 0.025 (38) 5.63 ± 0.69 (27) 4.76 ± 0.40 (41) Analysis of F = 1.50, P = 0.188 F = 84.50, P < 0.001 F = 11.59, P < 0.001 F = 60.46, P < 0.001 variance** Notes: Average values with standard deviations are shown. The number in the parenthesis is sample size. * The coefﬁcient of variation of clutch size. ≅ Eggs were kept at 20.0 ± 0.5 °C under 15:9 hour light:dark conditions. ** One-way analysis of variance for the comparison of each trait among six species.

and Serville (Kaitala and Mappes 1997; Kudo Grazia, J., Schuh, R.T., and Wheeler, W.C. 2008. 2001), both of which exhibit maternal care of eggs Phylogenetic relationships of family groups in and nymphs (Tsai et al. 2015). This may imply the Pentatomoidea based on morphology and DNA sequences (Insecta: Heteroptera). Cladistics, 24: existence of a functional relationship between 932–976. clutch size and maternal care. While there do not Kaitala, A. and Mappes, J. 1997. Parental care and seem to be marked differences in egg size between reproductive investment in shield bugs (Acanthoso- Elasmostethus and Elasmucha (in some cases, the matidae, Heteroptera). Oikos, 80:3–7. egg size of the former species is larger than that Kobayashi, T. and Tachikawa, S. 2004. Eggs and of the latter species; Kaitala and Mappes 1997; nymphs of the Japanese Pentatomoidea: morphology and ecology. Yokendo, Tokyo, Japan. [In Japanese]. Kudo 2001), the egg developmental periods Kudo, S. 2001. Intraclutch egg-size variation in in the former are consistently shorter than those acanthosomatid bugs: adaptive allocation of maternal in the latter (under the same temperature used investment? Oikos, 92:208–214. in the present study; Kaitala and Mappes 1997). Mappes, J., Kaitala, A., and Rinne, V. 1996. Temporal These findings may be inconsistent with the variation in reproductive allocation in a shield bug assumptions of the safe harbour hypothesis (Shine Elasmostethus interstinctus. Journal of Zoology, 240:29–35. 1978), which proposes that species with maternal Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., care have larger eggs than asocial species, and Thompson, J.N., and Weis, A.E. 1980. Interactions that larger eggs have longer egg development among three trophic levels: influence of plants on periods. interactions between insect herbivores and natural Unfortunately, the number of species examined enemies. Annual Review of Ecology and Systema- – in this study was not sufficient for explicitly test- tics, 11:41 65. SAS Institute. 2016. JMP13 basic analysis. SAS ing hypotheses on the evolution of life history Institute, Cary, North Carolina, United States of traits (Wilson 1975; Shine 1978; Fox and Czesak America. 2000; Wong et al. 2013). Such analyses would Shine, R. 1978. Propagule size and parental care: the require the collection of data on the life histories “safe harbor” hypothesis. Journal of Theoretical of other Elasmostethus species, as well as those of Biology, 75: 417–424. other genera in the Acanthosomatidae. Tachikawa, S. 1991. Studies on subsocialities of Heteroptera in Japan. Tokyo Agricultural University Press, Tokyo, Japan. [In Japanese, with English Acknowledgements summary]. Tsai, J.-F., Kudo, S., and Yoshizawa, K. 2015. Maternal The authors thank I. Yao, T. Kanbe, Y. Sakamaki, care in Acanthosomatinae (Insecta: Heteroptera: and C. Koshio for their assistance in the field. The Acanthosomatidae) – correlated evolution with authors also thank Hokkaido Research Center, morphological change. BMC Evolutionary Biology, – Forestry and Forest Products Research Institute for 15:258,113. https://doi.org/10.1186/s12862- 015-0537-4. permission to collect insects. This study was partly Tsai, J.-F. and Rédei, D. 2015. Redefinition of supported by a grant-in-aid of Japan Society Acanthosoma and taxonomic corrections to its included for the Promotion of Science, JSPS KAKENHI species (Hemiptera: Heteroptera: Acanthosomatidae). (JP16K07518). Zootaxa, 3950:1–60. Wilson, E.O. 1975. Sociobiology: the new synthesis. Belknap Press of Harvard University Press, Cambridge, References Massachusetts, United States of America. Carter, M.E. and Hoebeke, E.R. 2003. Biology and Wong, J.W., Meunier, J., and Kölliker, M. 2013. The seasonal history of Elasmostethus atricornis (Van evolution of parental care in insects: the roles of Duzee) (Hemiptera: Acanthosomatidae), with ecology, life history and the social environment. descriptions of the immature stages and notes on Ecological Entomology, 38: 123–137. pendergrast organs. Proceedings of the Entomologi- Yamamoto, A. 2003. A revision of Japanese Elasmostethus cal Society of Washington, 105: 525–534. Fieber (Heteroptera: Acanthosomatidae). Tijdschrift Costa, J.T. 2006. The other insect societies. Belknap voor entomologie, 146:49–66. Press of Harvard University Press, Cambridge, Yamamoto, A., Hayashi, M., and Kudo, S. 2009. Host Massachusetts, United States of America. plants of Japanese acanthosomatid bugs (Heteroptera: Fox, C.W. and Czesak, M.E. 2000. Evolutionary Acanthosomatidae). Japanese Journal of Entomology ecology of progeny size in arthropods. Annual (New Series), 12:31–38. [In Japanese, with English Review of Entomology, 45: 341–369. abstract].