Maternal care in Gargaphia decoris (Heteroptera, Tingidae), with comments on this behavior within the genus and family

Marcus Guidoti Douglas W. Tallamy Alberto Luiz Marsaro JúniorAbout the authors

Abstract

Maternal care in Gargaphia decoris is described for the first time. A video is presented as supplementary material. The knowledge on such trait within Tingidae is summarized. The behavior within the family is discussed, and the potential as a source of phylogenetic characters for further analyses is stressed.

Gargaphia; Neotropical; Parental care; Solanum concinnum


Maternal care in Tingidae was first reported for Gargaphia tiliae (Walsh, 1864) ( Weiss, 1919Weiss, H.B., 1919. Notes on Gargaphia tiliae Walsh, the linden lace-bug. Proc. Biol. Soc. Wash. 32, 165-168.) and since then just a few additional species have been observed with this rare behavior. Besides G. tiliae, there are records of maternal care for six other species distributed in three other genera, two from the New World and one from Africa. Within Gargaphia Stål, G. solani Heidemann, 1914, G. iridescens Champion, 1897 and G. decoris Drake, 1931 also present this trait ( Fink, 1915Fink, D.E., 1915. The eggplant lace-bug. Bull. U.S. Dep. Agric. 239, 1-7., Torre-Bueno, 1942Torre-Bueno, J.R., 1942. Maternal solicitude in Gargaphia iridescens champion. Bull. Brooklyn Entomol. Soc. 37, 131. and Olckers, 2000Olckers, T., 2000. Biology, host specificity and risk assessment of Gargaphia decoris, the first agent to be released in South Africa for the biological control of the invasive tree Solanum mauritianum. BioControl 45, 373-388.). Other taxa exhibiting maternal care are Corythucha bulbosa Osborn and Drake, 1916 ( Sheeley and Yonke, 1977Sheeley, R.D., Yonke, T.R., 1977. Biological notes on seven species of Missouri Tingids (Hemiptera: Tingidae). J. Kansas Entomol. Soc. 50, 342-356.), C. hewitti Drake, 1919 ( Faeth, 1989Faeth, S.H., 1989. Maternal care in lace bug, Corythucha hewitti (Hemiptera: Tingi- dae). Psyche (Stuttg) 96, 101-110.) and Leptobyrsa decora Drake, 1922 ( Melksham, 1984Melksham, J.A., 1984. Colonial oviposition and maternal care in two strains of Lep- tobyrsa decora Drake (Hemiptera: Tingidae). J. Aust. Entomol. Soc. 23, 205-210) in the New World and Compseuta picta Schouteden, 1923 ( Tallamy and Iglay, 2004Tallamy, D.W., Iglay, R.B., 2004. Maternal care in Compseuta picta, an African lace bug (Heteroptera: Tingidae). J. Insect Behav. 17, 247-249.) in Africa. A complete list of references treating this subject in Tingidae is provided ( Table 1). There are several differences in how maternal care is expressed among these taxa. Egg-dumping, egg-guarding, colonial oviposition, and aggressive defense against predators have all been reported in various combinations within Tingidae.

Table 1.
List of references on maternal care behavior in Tingidae.

Leptobyrsa decora is a Neotropical species, which presents colonial oviposition and egg-guarding. Females remain with immatures until the fourth instar ( Melksham, 1984Melksham, J.A., 1984. Colonial oviposition and maternal care in two strains of Lep- tobyrsa decora Drake (Hemiptera: Tingidae). J. Aust. Entomol. Soc. 23, 205-210). Loeb and Bell (2006)Loeb, M.L.G., Bell, L.K., 2006. Distribution of care-giving effort in a communally breeding lace bug: fair guarding without coercion. J. Insect Behav. 19, 19-30. suggested that cooperation between females with the task of egg-guarding is controlled by chemical cues and not physical cohercion among partners. Melksham (1984)Melksham, J.A., 1984. Colonial oviposition and maternal care in two strains of Lep- tobyrsa decora Drake (Hemiptera: Tingidae). J. Aust. Entomol. Soc. 23, 205-210 showed differences in the number of egg batches and adult guards between two different populations of this lace bug. This may be correlated with unequal predation pressure. Still, according to Melksham (1984)Melksham, J.A., 1984. Colonial oviposition and maternal care in two strains of Lep- tobyrsa decora Drake (Hemiptera: Tingidae). J. Aust. Entomol. Soc. 23, 205-210, wing-fanning was observed in this species but the context of this behavior was not defined. Within the genus Corythucha, maternal care has been observed in two species ( Sheeley and Yonke, 1977Sheeley, R.D., Yonke, T.R., 1977. Biological notes on seven species of Missouri Tingids (Hemiptera: Tingidae). J. Kansas Entomol. Soc. 50, 342-356. and Faeth, 1989Faeth, S.H., 1989. Maternal care in lace bug, Corythucha hewitti (Hemiptera: Tingi- dae). Psyche (Stuttg) 96, 101-110.), but this behavior apparently is absent in several others ( Tallamy and Denno, 1981bTallamy, D.W., Denno, R.F., 1981b. Alternative life history patterns in risky environ- ments: an example from lacebugs. In: Denno, R.F., Dingle, H. (Eds.), Insect Life History Patterns: Habitat and Geographic Variation. Springer-Verlag New York Inc., pp. 129-147.). Faeth (1989)Faeth, S.H., 1989. Maternal care in lace bug, Corythucha hewitti (Hemiptera: Tingi- dae). Psyche (Stuttg) 96, 101-110. observed egg-guarding in C. hewitti, but not aggressive brood protection. Females seem to communicate with their young through chemicals dispersed from abdominal movements. This communication may regulate nymphal aggregation, offering protection from the dilution effect of predation or it may be a mechanism to guide nymphal movements ( Faeth, 1989Faeth, S.H., 1989. Maternal care in lace bug, Corythucha hewitti (Hemiptera: Tingi- dae). Psyche (Stuttg) 96, 101-110.). In addition to egg-guarding, wing-fanning was observed in Corythucha bulbosa against a spider ( Sheeley and Yonke, 1977Sheeley, R.D., Yonke, T.R., 1977. Biological notes on seven species of Missouri Tingids (Hemiptera: Tingidae). J. Kansas Entomol. Soc. 50, 342-356.). Compseuta picta, the first tingid outside the New World in which maternal care has been recognized, presented egg-guarding and wing-fanning every time an inanimate aggressor approached its eggs or nymphs ( Tallamy and Iglay, 2004Tallamy, D.W., Iglay, R.B., 2004. Maternal care in Compseuta picta, an African lace bug (Heteroptera: Tingidae). J. Insect Behav. 17, 247-249.). The experiments with these females were interrupted due to time constraints, but females remained with and defended their offspring throughout the two days of observation ( Tallamy and Iglay, 2004Tallamy, D.W., Iglay, R.B., 2004. Maternal care in Compseuta picta, an African lace bug (Heteroptera: Tingidae). J. Insect Behav. 17, 247-249.).

Two alternative reproductive strategies have been observed in the Gargaphia species cited above: egg-dumping and egg-guarding. Although these strategies have been better studied in G. solani and G. tiliae, G. iridescens also exhibits these behaviors ( Torre-Bueno, 1935Torre-Bueno, J.R., 1935. Notes on Gargaphia tiliae. Bull. Brooklyn Entomol. Soc. 30, 78. and Tallamy, 2005Tallamy, D.W., 2005. Egg dumping in insects. Annu. Rev. Entomol. 50, 347-370.). Egg dumping is analogous to the avian behavior of certain taxa which regularly or occasionally lay eggs in the nests of conspecifics ( Tallamy, 2005Tallamy, D.W., 2005. Egg dumping in insects. Annu. Rev. Entomol. 50, 347-370.). Maternal Gargaphia are not the only invertebrates to exhibit conspecific egg-dumping, this behavior also has been recognized in subsocial bees and wasps (e.g., Brockmann, 1993Brockmann, H.J., 1993. Parasitizing conspecifics: comparisons between hymenoptera and birds. Trends Ecol. Evol. 8, 2-4.) and treehoppers ( Eberhard, 1986Eberhard, W.G., 1986. Possible mutualism between females of the subsocial mem- bracid Polyglypta dispar (Homoptera). Behav. Ecol. Sociobiol. 19, 447-453. and Zink, 2003Zink, A.G., 2003. Intraspecific brood parasitism as a conditional reproductive tactic in the treehopper Publilia concava. Behav. Ecol. Sociobiol. 54, 406-415.). Once physiologically committed to egg-guarding, a female protects eggs and nymphs under her care by offensively moving toward the predator while wing-fanning, sometimes even climbing on the top of the predator ( Tallamy and Denno, 1981aTallamy, D.W., Denno, R.F., 1981a. Maternal care in Gargaphia solani (Hemiptera: Tingidae). Anim. Behav. 29, 771-778.). Egg-dumpers, in contrast, abandon their eggs to the care of egg-guarders and go off to produce more eggs elsewhere. In this way egg-dumpers can produce more than twice as many eggs as egg-guarders in their lifetime ( Tallamy and Horton, 1990Tallamy, D.W., Horton, L.A., 1990. Costs and benefits of the egg-dumping alternative in Gargaphia lace bugs (Hemiptera: Tingidae). Anim. Behav. 39, 352-359. and Tallamy, 2005Tallamy, D.W., 2005. Egg dumping in insects. Annu. Rev. Entomol. 50, 347-370.). Egg-guarders suspend further egg production until their first clutch reaches adulthood and independence ( Tallamy and Denno, 1982Tallamy, D.W., Denno, R.F., 1982. Life history trade-offs in Gargaphia Solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63, 616-620.).

Rather than being victims of egg-dumpers, egg-guarders benefit from receiving dumper eggs because they are typically laid around the perimeter of the guarder's egg mass, providing a buffer against incoming predators. This buffer dilutes losses of the guarding female's eggs and nymphs (Tallamy and Horton, 1990Tallamy, D.W., Horton, L.A., 1990. Costs and benefits of the egg-dumping alternative in Gargaphia lace bugs (Hemiptera: Tingidae). Anim. Behav. 39, 352-359.). Whenever possible, females dump their eggs instead of caring for their brood, since the egg-dumping strategy yields more eggs and avoids the hazards associated with predator encounters (Monaco et al., 1998Monaco, E.L., Tallamy, D.W., Johnson, R.K., 1998. Chemical mediation of egg dump- ing in the lace bug Gargaphia solani Heidemann (Heteroptera: Tingidae). Anim. Behav. 56, 1491-1495.). When a suitable egg mass is not available for would be egg-dumpers, gravid females lay and care for their own eggs. The egg-guarding/egg-dumping alternatives are controlled by juvenile hormone (JH); high levels of JH promote egg-dumping behavior and low levels trigger egg-guarding (Tallamy et al., 2002Tallamy, D.W., Monaco, E.L., Pesek, J.D., 2002. Hormonal control of egg dumping and guarding in the lace bug, Gargaphia solani (Hemiptera: Tingidae). J. Insect Behav. 15, 467-475.). The relationship between maternal alternatives and JH in Gargaphia lacebugs is consistent with other demonstrated roles of JH in parental care, vitellogenesis, and oviposition (e.g., Martinez and Huerta, 1997Martinez, M.I., Huerta, C., 1997. Coordinated activity of the ovary, pars inter- cerebralis and corpus allatum during the prenesting and nesting cycles of Copris incertus Say (Coleoptera: Scarabaeidae: Scarabaeinae). Coleopts. Bull. 51, 351-383. and Rankin and Riddiford, 1977Rankin, M.A., Riddiford, L.M., 1977. Hormonal control of migratory flight in Oncopeltes fasciatus: the effects of the corpora cardiacum, corpora allatum and starvation on migration and reproduction. Gen. Comp. Endocrinol. 33, 309-321.). The complex behavioral interactions between egg-dumpers and egg-guarders have been extensively studied in G. solani in which trade-offs, proximate regulation, chemical mediation, egg-mass recognition and relatedness were explored ( Tallamy and Denno, 1981aTallamy, D.W., Denno, R.F., 1981a. Maternal care in Gargaphia solani (Hemiptera: Tingidae). Anim. Behav. 29, 771-778., Tallamy and Denno, 1982Tallamy, D.W., Denno, R.F., 1982. Life history trade-offs in Gargaphia Solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63, 616-620., Tallamy and Tallamy, 1993Tallamy, C.D., Tallamy, D.W., 1993. The effect of relatedness on Gargaphia egg dump- ing behavior. Anim. Behav. 45, 1239-1241., Monaco et al., 1998Monaco, E.L., Tallamy, D.W., Johnson, R.K., 1998. Chemical mediation of egg dump- ing in the lace bug Gargaphia solani Heidemann (Heteroptera: Tingidae). Anim. Behav. 56, 1491-1495., Loeb et al., 2000Loeb, M.L.G., Diener, L.M., Pfennig, D.W., 2000. Egg-dumping lace bugs preferentially oviposit with kin. Anim. Behav. 59, 379-383. and Parr et al., 2002Tallamy, D.W., Denno, R.F., 1982. Life history trade-offs in Gargaphia Solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63, 616-620.).

In July 2013, females of Gargaphia decoris presenting egg-guarding behavior were observed ( Fig. 1). We found this species in the municipality of Passo Fundo, Rio Grande do Sul, Brazil (28°13' S, 52°24' W), on the abaxial surface of leaves of Solanum concinnum (Solanaceae). Vouchers were deposited in the Museu de Ciências Naturais of Fundação Zoobotânica do Rio Grande do Sul (MCNZ), in Porto Alegre, Rio Grande do Sul. Four leaves, three containing a guard female with eggs, and one containing a female with eggs hatching to first instar nymphs, were collected for preliminary laboratory tests. Under a stereomicroscope, we disturbed the female with a needle, touching her sides and advancing toward the egg batch in front of her. These tests were filmed, and a video is available as supplementary material ( Guidoti et al., 2015Guidoti, M., Tallamy, D.W., Marsaro Jr., A.L., 2015. Gargaphia decoris (Heteroptera, Tingidae) maternal care display. figshare. Available at: http://dx.doi.org/10.6084/m9.figshare.1375660.(accessed 13 April 2015).
http://dx.doi.org/10.6084/m9.figshare.13...
). The wing-fanning behavior was observed only for the female guarding both eggs and nymphs. When disturbed on the side of the body, the female just moved a little, returning to the guard position right after the needle was withdrawn. When disturbed by frontal movements in direction of the egg batch, the female moved aggressively toward the needle. The female fanned her wings only after she charged the needle. Further studies were not possible due a cold wave that substantially reduced the populations of this lace bug. Olckers (2000)Olckers, T., 2000. Biology, host specificity and risk assessment of Gargaphia decoris, the first agent to be released in South Africa for the biological control of the invasive tree Solanum mauritianum. BioControl 45, 373-388. reported but did not describe maternal care for G. decoris; our description now provides details that suggest maternal care in G. decoris is similar to that described in other species of Gargaphia thus far. More experiments are needed to fully characterize the behavior in G. decoris.


Fig. 1. Gargaphia decoris Drake, 1931 female guarding an egg batch with first instar nymphs. Scale bar: 1 mm. Photo: Marsaro Júnior, A.L.

Gargaphia, as it is currently defined, is a New World genus comprising about 70 species, but it lacks a phylogenetic hypothesis designed specifically to test its monophyly. Recently, G. arizonica Drake and Carvalho, 1944, G. tiliae and G. solani were included in a molecular phylogenetic analysis, supporting the monophyly of the genus ( Guilbert et al., 2014Guilbert, É., Damgaard, J., D'Haese, C.A., 2014. Phylogeny of the lacebugs (Insecta: Heteroptera: Tingidae) using morphological and molecular data. Syst. Entomol. 39, 431-441.). However, an unpublished thesis suggests Gargaphia should be divided into several distinct genera ( Smith, 1996Smith, R.M., (Thesis) 1996. Phylogenetic analysis and revision of Gargaphia (sensu lato) (Heteroptera: Tingidae) with descriptions of one new genus and three new species groups. Texas A&M University.). Although the aforementioned Gargaphia species exhibit maternal care with the exception of G. arizonica ( Hardin and Tallamy, 1992Hardin, M.R., Tallamy, D.W., 1992. Effect of predators and host phenology on the maternal and reproductive behaviors of Gargaphia lace bugs (Hemiptera: Tingi- dae). J. Insect Behav. 5, 177-192.), these four species are both morphologically and behaviorally similar, and therefore we suggest that maternal care could be a defining trait of a single subsection of Gargaphia. Thus, the behavior could be included as character for future phylogenetic analyses of this group.

The fact that different expressions of maternal care have been observed in Tingidae enhances the evolutionary questions regarding this trait in the family. Even though we expect that maternal care has evolved in more Tingidae species than is currently recognized (Tallamy and Iglay, 2004Tallamy, D.W., Iglay, R.B., 2004. Maternal care in Compseuta picta, an African lace bug (Heteroptera: Tingidae). J. Insect Behav. 17, 247-249.), it has still only been observed in a few species, indicating that Tingidae systematics could benefit from additional data on the presence or absence of brood protection across the family. Not only would genus-level systematics improve from the availability of such data, but additional behavioral descriptions would enable the testing of hypotheses about the evolution of maternal care in Tingidae. Therefore, more attention should be given to this behavior in other Tingidae. We urge that such data should not be neglected and the presence or the absence of such trait should always be reported.

Acknowledgments

We thank Aline Barcellos, Carolina Adami and Filipe Michels for their comments on the first version of this manuscript. To Dennis Kopp, Eric Guilbert Joe Eger, Randall Schuh and Thomas Henry, for their encouragements in publish this data. CNPq (Brazil) for the Master's Degree fellowship supporting the first author.

References

  • Brockmann, H.J., 1993. Parasitizing conspecifics: comparisons between hymenoptera and birds. Trends Ecol. Evol. 8, 2-4.
  • Eberhard, W.G., 1986. Possible mutualism between females of the subsocial mem- bracid Polyglypta dispar (Homoptera). Behav. Ecol. Sociobiol. 19, 447-453.
  • Faeth, S.H., 1989. Maternal care in lace bug, Corythucha hewitti (Hemiptera: Tingi- dae). Psyche (Stuttg) 96, 101-110.
  • Fink, D.E., 1915. The eggplant lace-bug. Bull. U.S. Dep. Agric. 239, 1-7.
  • Guidoti, M., Tallamy, D.W., Marsaro Jr., A.L., 2015. Gargaphia decoris (Heteroptera, Tingidae) maternal care display. figshare. Available at: http://dx.doi.org/10.6084/m9.figshare.1375660.(accessed 13 April 2015).
    » http://dx.doi.org/10.6084/m9.figshare.1375660
  • Guilbert, É., Damgaard, J., D'Haese, C.A., 2014. Phylogeny of the lacebugs (Insecta: Heteroptera: Tingidae) using morphological and molecular data. Syst. Entomol. 39, 431-441.
  • Hardin, M.R., Tallamy, D.W., 1992. Effect of predators and host phenology on the maternal and reproductive behaviors of Gargaphia lace bugs (Hemiptera: Tingi- dae). J. Insect Behav. 5, 177-192.
  • Kearns, R.S., Yamamoto, R.T., 1981. Maternal behavior and alarm response in the eggplant lace bug, Gargaphia solani Heidemann (Tingidae: Heteroptera). Psyche (Stuttg) 88, 215-230.
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  • Loeb, M.L.G., Bell, L.K., 2006. Distribution of care-giving effort in a communally breeding lace bug: fair guarding without coercion. J. Insect Behav. 19, 19-30.
  • Loeb, M.L.G., Diener, L.M., Pfennig, D.W., 2000. Egg-dumping lace bugs preferentially oviposit with kin. Anim. Behav. 59, 379-383.
  • Martinez, M.I., Huerta, C., 1997. Coordinated activity of the ovary, pars inter- cerebralis and corpus allatum during the prenesting and nesting cycles of Copris incertus Say (Coleoptera: Scarabaeidae: Scarabaeinae). Coleopts. Bull. 51, 351-383.
  • Melksham, J.A., 1984. Colonial oviposition and maternal care in two strains of Lep- tobyrsa decora Drake (Hemiptera: Tingidae). J. Aust. Entomol. Soc. 23, 205-210
  • Monaco, E.L., Tallamy, D.W., Johnson, R.K., 1998. Chemical mediation of egg dump- ing in the lace bug Gargaphia solani Heidemann (Heteroptera: Tingidae). Anim. Behav. 56, 1491-1495.
  • Olckers, T., 2000. Biology, host specificity and risk assessment of Gargaphia decoris, the first agent to be released in South Africa for the biological control of the invasive tree Solanum mauritianum. BioControl 45, 373-388.
  • Parr, A., Tallamy, D.W., Monaco, E.L., Pesek, J.D., 2002. Proximate factors regulat- ing maternal options in the eggplant lace bug, Gargaphia solani (Heteroptera: Tingidae). J. Insect Behav. 15, 495-511.
  • Rankin, M.A., Riddiford, L.M., 1977. Hormonal control of migratory flight in Oncopeltes fasciatus: the effects of the corpora cardiacum, corpora allatum and starvation on migration and reproduction. Gen. Comp. Endocrinol. 33, 309-321.
  • Sheeley, R.D., Yonke, T.R., 1977. Biological notes on seven species of Missouri Tingids (Hemiptera: Tingidae). J. Kansas Entomol. Soc. 50, 342-356.
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  • Tallamy, D.W., Denno, R.F., 1982. Life history trade-offs in Gargaphia Solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63, 616-620.
  • Tallamy, D.W., Horton, L.A., 1990. Costs and benefits of the egg-dumping alternative in Gargaphia lace bugs (Hemiptera: Tingidae). Anim. Behav. 39, 352-359.
  • Tallamy, C.D., Tallamy, D.W., 1993. The effect of relatedness on Gargaphia egg dump- ing behavior. Anim. Behav. 45, 1239-1241.
  • Tallamy, D.W., Iglay, R.B., 2004. Maternal care in Compseuta picta, an African lace bug (Heteroptera: Tingidae). J. Insect Behav. 17, 247-249.
  • Tallamy, D.W., Monaco, E.L., Pesek, J.D., 2002. Hormonal control of egg dumping and guarding in the lace bug, Gargaphia solani (Hemiptera: Tingidae). J. Insect Behav. 15, 467-475.
  • Torre-Bueno, J.R., 1935. Notes on Gargaphia tiliae. Bull. Brooklyn Entomol. Soc. 30, 78.
  • Torre-Bueno, J.R., 1942. Maternal solicitude in Gargaphia iridescens champion. Bull. Brooklyn Entomol. Soc. 37, 131.
  • Weiss, H.B., 1919. Notes on Gargaphia tiliae Walsh, the linden lace-bug. Proc. Biol. Soc. Wash. 32, 165-168.
  • Zink, A.G., 2003. Intraspecific brood parasitism as a conditional reproductive tactic in the treehopper Publilia concava. Behav. Ecol. Sociobiol. 54, 406-415.

  • Appendix A. Supplementary data Supplementary material associated with this article can befound in the online version at doi:10.1016/j.rbe.2015.03.004.

Publication Dates

  • Publication in this collection
    Apr-Jun 2015

History

  • Received
    21 Aug 2014
  • Reviewed
    09 Feb 2015
  • Accepted
    09 Apr 2015
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