Abstract
Some burrower bugs (Heteroptera: Cydnidae) show complex patterns of maternal care, including defense against predators and the provisioning of food to nymphs. Recently, the subsocial cydnid bugs have attracted the interest of researchers as model systems to study the behavioral ecology of parental investment. However, there have been few attempts to quantify the fitness benefits of maternal behavior other than provisioning. Here, we examined the maternal behavior of Adomerus triguttulus and its adaptive significance in terms of offspring survival in the field. A. triguttulus young depend on fallen nutlets of myrmecophorous mints, Lamium spp. Under field conditions, females attend offspring, from eggs to second instar nymphs, in nests on the ground under the litter. When disturbed, the females showed aggressive responses against the source of disturbance. The females often carried spherical clutches of eggs away from the nest when heavily disturbed. Female-removal experiments in the field demonstrated a defensive function of the female behavior; predators, such as ants, attacked egg clutches without females and the clutches often disappeared during the experiment. Egg clutches without females sometimes also suffered from fungal infection. Selective factors on maternal defensive behavior in A. triguttulus are discussed in terms of habitat properties possibly emerging from insect–plant associations.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Agrawal AF, Brodie ED III, Brown J (2001) Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292:1710–1712
Agrawal AF, Combs N, Brodie ED III (2005) Insights into the costs of complex maternal care behavior in the burrower bug (Sehirus cinctus). Behav Ecol Sociobiol 57:566–574
Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge
Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu Rev Entomol 43:347–367
Costa J (2006) The other insect societies. Belknap Press of Harvard University Press, Cambridge, MA
Eberhard WG (1975) The ecology and behavior of a subsocial pentatomid bug and two scelionid wasps: strategy and counterstrategy in a host and its parasites. Smithson Contrib Zool 205:1–39
Filippi L, Hironaka M, Nomakuchi S, Tojo S (2000) Provisioned Parastrachia japonensis (Hemiptera: Cydnidae) nymphs gain access to food and protection from predators. Anim Behav 60:757–763
Filippi L, Hironaka M, Nomakuchi S (2001) A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource. Popul Ecol 43:41–50
Filippi L, Hironaka M, Nomakuchi S (2002) Risk-sensitive decisions during nesting may increase maternal provisioning capacity in the subsocial shield bug Parastrachia japonensis. Ecol Entomol 27:152–162
Filippi-Tsukamoto L, Nomakuchi S, Kuki K, Tojo S (1995) Adaptiveness of parental care in Parastrachia japonensis (Hemiptera: Cydnidae). Ann Entomol Soc Am 88:374–383
Hardin MR, Tallamy DW (1992) Effects of predators and host phenology on the maternal and reproductive behaviors of Gargaphia lace bugs (Hemiptera: Tingidae). J Insect Behav 5:177–192
Hironaka M, Nomakuchi S, Iwakuma S, Filippi L (2005) Trophic egg production in a subsocial shield bug, Parastrachia japonensis Scott (Heteroptera: Parastrachiidae), and its functional value. Ethology 11:1089–1102
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Massachusetts
Kight SL (1997) Factors influencing maternal behaviour in a burrower bug, Sehirus cinctus (Heteroptera: Cydnidae). Anim Behav 53:105–112
Kight SL (1998) Precocene II modifies maternal responsiveness in the burrower bug, Sehirus cinctus (Heteroptera). Physiol Entomol 23:38–42
Kight SL, Cseke JJ (1998) The effects of ambient temperature on the duration of maternal care in a burrower bug (Heteroptera: Cydnidae). J Kans Entomol Soc 71:185–187
Kölliker M, Vancassel M (2007) Maternal attendance and the maintenance of family groups in common earwigs (Forficula auricularia): a field experiment. Ecol Entomol 32:24–27
Kölliker M, Chuckalovcak JP, Brodie ED III (2005) Offspring chemical cues affect maternal food provisioning in burrower bugs, Sehirus cinctus. Anim Behav 69:959–966
Kölliker M, Chuckalovcak JP, Haynes KF, Brodie ED III (2006) Maternal food provisioning in relation to condition-dependent offspring odours in burrower bugs (Sehirus cinctus). Proc R Soc Lond B 273:1523–1528
Kudo S (1990) Brooding behavior in Elasmucha putoni (Heteroptera: Acanthosomatidae), and a possible nymphal alarm substance triggering guarding responses. Appl Entomol Zool 25:431–437
Kudo S (1996) Ineffective maternal care of a subsocial bug against a nymphal parasitoid: a possible consequence of specialization to predators. Ethology 102:227–235
Kudo S (2000) The guarding posture of females in the subsocial bug Elasmucha dorsalis (Heteroptera: Acanthosomatidae). Eur J Entomol 97:137–139
Kudo S (2002) Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae). Behav Ecol 13:742–749
Kudo S, Hasegawa E (2004) Diversified reproductive strategies in Gonioctena (Chrysomelinae) leaf beetles. In: Jolivet PH, Santiago-Blay JA, Schmitt M (eds) New developments in the biology of Chrysomelidae. SPB Academic Publishing bv, The Hague, Netherlands, pp 727–738
Kudo S, Nakahira T (2004) Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug. Oikos 107:28–35
Kudo S, Nakahira T (2005) Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions. Oikos 111:459–464
Kudo S, Sato M, Ohara M (1989) Prolonged maternal care in Elasmucha dorsalis (Heteroptera, Acanthosomatidae). J Ethol 7:75–81
Kudo S, Maeto K, Ozaki K (1992) Maternal care in the red-headed web-spinning sawfly, Cephalcia isshikii (Hymenoptera: Pamphiliidae). J Insect Behav 5:783–795
Kudo S, Ishibashi E, Makino S (1995) Reproductive and subsocial behaviour in the ovoviviparous leaf beetle Gonioctena sibirica (Weise) (Coleoptera: Chrysomelidae). Ecol Entomol 20:367–373
Kudo S, Nakahira T, Saito Y (2006) Morphology of trophic eggs and ovarian dynamics in the subsocial bug Adomerus triguttulus (Heteroptera: Cydnidae). Can J Zool 84:723–728
Lamb RJ (1976) Parental behavior in the Dermaptera with special reference to Forficula auricularia (Dermaptera: Forficulidae). Can Entomol 108:609–619
Mappes J, Mappes T, Lappalainen T (1997) Unequal maternal investment in offspring quality in relation to predation risk. Evol Ecol 11:237–243
Marquis RJ (1996) Plant morphology and recruitment of the third trophic level: subtle and little-recognized defenses? Oikos 75:330–334
Melber A, Schmidt GH (1975) Sozialverhalten zweier Elasmucha-Arten (Heteroptera: Insecta). Z Tierpsychol 39:403–414
Melber A, Schmidt GH (1977) Sozialphänomene bei Heteropteren. Zoologica 127:19–53
Melber A, Hölscher L, Schmidt GH (1980) Further studies on the social behaviour and its ecological significance in Elasmucha grisea L. (Hem.-Het.: Acanthosomatidae). Zool Anz 205:27–38
Nafus DM, Schreiner IH (1988) Parental care in a tropical nymphalid butterfly Hypolimnas anomala. Anim Behav 36:1425–1431
Nakahira T (1992) Reproductive history and parental behaviour in the cydnid bug Adomerus triguttulus. M.Sc. Thesis. Hokkaido University, Sapporo (in Japanese)
Nakahira T (1994) Production of trophic eggs in the subsocial burrower bug Admerus (sic) triguttulus. Naturwissenschaften 81:413–414
Nomakuchi S, Filippi L, Tojo S (1998) Selective foraging behavior in nest-provisioning females of Parastrachia japonensis (Hemiptera: Cydnidae): cues for preferred food. J Insect Behav 11:605–619
Ohara M, Higashi S (1987) Interference by ground beetles with the dispersal by ants of seeds of Trillium species (Liliaceae). J Ecol 75:1091–1098
Oi DH, Pereira RM (1993) Ant behavior and microbial pathogens (Hymenoptera: Formicidae). Fla Entomol 76:63–74
Price PW, Burton CE, Gross P, McPherson BA, Thompson JN, Weise AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65
Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJ
Smith RL (1997) Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 116–149
Strohm E, Linsenmair KE (2001) Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol 26:198–203
Suzuki S (2001) Suppression of fungal development on carcasses by burying beetle Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol Sci 4:403–405
Tachikawa S (1991) Studies on subsocialities of heteroptera in Japan. Tokyo Agricultural University Press, Tokyo
Tallamy DW (2001) Evolution of exclusive paternal care in arthropods. Annu Rev Entomol 46:139–165
Tallamy DW, Denno RF (1981) Maternal care in Gargaphia solani (Hemiptera; Tingidae). Anim Behav 29:771–778
Tallamy DW, Schaefer CW (1997) Maternal care in the Hemiptera: ancestry, alternatives, and current adaptive value. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 94–115
Tallamy DW, Wood TK (1986) Convergence patterns in subsocial insects. Annu Rev Entomol 31:369–390
Tsukamoto L, Tojo S (1992) A report of progressive provisioning in a stink bug, Parastrachia japonensis (Hemiptera: Cydnidae). J Ethol 10:21–29
Windsor DM (1987) Natural history of a subsocial tortoise beetle, Acromis sparsa Boheman (Chrysomelidae, Cassidinae) in Panama. Psyche 94:127–150
Wood TK (1976) Alarm behavior of brooding female Umbonia crassicornis (Homoptera: Membracidae). Ann Entomol Soc Am 69:340–344
Acknowledgments
This study was supported in part by Grant-in-Aid for Scientific Research (C: 13640628) from the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nakahira, T., Kudo, Si. Maternal Care in the Burrower Bug Adomerus triguttulus: Defensive Behavior. J Insect Behav 21, 306–316 (2008). https://doi.org/10.1007/s10905-008-9129-0
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-008-9129-0

