Abstract
Chemical compounds play a major role in the recognition processes in social insects, and one class of compounds namely hydrocarbons cover the adult body, but also the surface of their eggs. The ability to discriminate between friends from foes minimizes the exploitation of resources. We investigated for the first time whether females of Mischocyttarus cerberus, which is often attacked by other wasp species, can discriminate their own eggs over the eggs of foes. By using a non-destructive technique, we experimentally collected eggs from post-worker emergent nests, and we offered their eggs to other nests to test the policing behavior in M. cerberus. Overall, our results show that the females of M. cerberus can discriminate eggs according to their origin, and most of the removed eggs were policed within the first hour of the experiment, revealing that females have accurate discrimination skills. The discrimination skill allows females to detect eggs. We discuss that chemical cues present over the surface of eggs may be important for them to be accepted or removed, and these cues may be important to avoid parasitism. In this case, eggs represent alternative tools of communication, once they carry chemical compounds linked to their nest. Additionally, dominant females (= queens) are the most likely individuals to remove the eggs. Altogether, our results reinforce that the nestmate recognition ability is not restricted to recognizing adult relatives, but it is also extended to recognizing brood in Mischocyttarus societies.
Significance statement
Nestmate recognition is responsible to maintain social integrity in social insect colonies, as individuals can recognize friends from foes. We investigated whether nestmate recognition works on brood recognition in the primitively eusocial wasp Mischocyttarus cerberus. The nest of this species is deprived of an envelope and often can be attacked by parasitoids or other wasp species. By transplanting eggs from one colony to another using paper cells, we studied whether females would destroy introduced eggs more often. As a result, we found that M. cerberus females are capable to recognize introduced and their own eggs and remove introduced eggs more often. Hydrocarbons covering the egg surface are the likely chemical cues that allow such recognition to occur. These results suggest that nestmate recognition is not limited to perceiving adult nestmates, but also brood in this wasp species.
Similar content being viewed by others
Data availability
The data that supports the findings of this study are available in the supplementary material of this manuscript.
References
Bagneres AG, Killian A, Clement JL, Lange C (1991) Interspecific recognition among termites of the genus Reticulitermes: evidence for a role for the cuticular hydrocarbons. J Chem Ecol 17:2397–2420. https://doi.org/10.1007/BF00994590
Bonckaert W, Drijfhout FP, d’Ettorre P, Billen J, Wenseleers T (2012) Hydrocarbon signatures of egg maternity, caste membership and reproductive status in the common wasp. J Chem Ecol 38:42–51. https://doi.org/10.1007/s10886-011-0055-9
Bos N, d’Ettorre P (2012) Recognition of social identity in ants. Front Psychol 3:83. https://doi.org/10.3389/fpsyg.2012.00083
Bos N, Guerrieri FJ, d’Ettorre P (2010) Significance of chemical recognition cues is context dependent in ants. Anim Behav 80:839–844. https://doi.org/10.1016/j.anbehav.2010.08.001
Cappa F, Cini A, Signorotti L, Cervo R (2020) Rethinking recognition: social context in adult life rather than early experience shapes recognition in a social wasp. Philos Trans R Soc Lond B Biol Sci 375:20190468. https://doi.org/10.1098/rstb.2019.0468
Carlson DA, Bernier UR, Sutton BD (1998) Nov. Elution patterns from capillary GC for methyl branched alkanes. J Chem Ecol 24:1845–1865. https://doi.org/10.1023/a:1022311701355
Cervo R, Dani FR, Cotoneschi C, Scala C, Lotti I, Strassmann JE, Queller DC, Turillazzi S (2008) Why are larvae of the social parasite wasp Polistes sulcifer not removed from the host nest? Behav Ecol Sociobiol 62:1319–1331. https://doi.org/10.1007/s00265-008-0560-1
Cini A, Gioli L, Cervo R (2009) A quantitative threshold for nest-mate recognition in a paper social wasp. Biol Lett 5:459–461. https://doi.org/10.1098/rsbl.2009.0140
Clouse RM (1995) Nest usurpation and intercolonial cannibalism in Mischocyttarus mexicanus (Hymenoptera: Vespidae). J Kansas Entomol Soc 68:67–73
Cotoneschi C, Dani FR, Cervo R, Scala C, Strassmann JE, Queller DC, Turillazzi S (2009) Polistes dominulus (Hymenoptera, Vespidae) larvae show different cuticular patterns according to their sex: workers seem not use this chemical information. Chem Senses 34:195–202. https://doi.org/10.1093/chemse/bjn079
Cotoneschi C, Dani FR, Cervo R, Sledge MF, Turillazzi S (2007) Polistes dominulus (Hymenoptera: Vespidae) larvae possess their own chemical signatures. J Insect Physiol 53:954–963. https://doi.org/10.1016/j.jinsphys.2006.12.016
da Silva RC, Assis DS, de Souza AR, Nascimento FS, Giannotti E (2020a) Notes on brood morphology and the development of the Neotropical eusocial wasp Mischocyttarus cerberus (Hymenoptera, Vespidae, Polistinae). Sociobiology 67:301–307. https://doi.org/10.13102/sociobiology.v67i2.4562
da Silva RC, Prato A, Oi CA, Turatti ICC, Do Nascimento FS (2020b) Dominance hierarchy, ovarian activity and cuticular hydrocarbons in the primitively eusocial wasp Mischocyttarus cerberus (Vespidae, Polistinae, Mischocyttarini). J Chem Ecol 46:835–844. https://doi.org/10.1007/s10886-020-01206-1
da Silva RC, Silva AP, Assis DS, Nascimento FS (2019) The first record of the parasitoid wasp Pachysomoides, associated with Mischocyttarus cerberus nests and some insights about the parasitoid wasps behavior. R Bras Zoo 20:1–7. https://doi.org/10.34019/2596-3325.2019.v20.24794
da Silva RC, da Silva AP, Assis DS, Nascimento FS (2019) Occurrence and nesting behavior of social wasps in an anthropized environment. Sociobiology 66:381–388. https://doi.org/10.13102/sociobiology.v66i2.4303
Dapporto L, Dani FR, Turillazzi S (2007) Social dominance molds cuticular and egg chemical blends in a paper wasp. Curr Biol 17:R504–R505. https://doi.org/10.1016/j.cub.2007.05.002
De Souza AR, Silva NJ, Prezoto F (2012) A rare but successful reproductive tactic in a social wasp (Hymenoptera: Vespidae): Use of heterospecific nests. Rev Chil De Hist Nat 85:351–355
d’Ettorre P, Lenoir A (2010) Nestmate recognition. Ant Ecol 194–209
Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. PNAS 101:2945–2950. https://doi.org/10.1073/pnas.0308447101
Ferreira HM, da Silva RC, do Nascimento FS, Wenseleers T, Oi CA (2022) Reproduction and fertility signalling under joint juvenile hormone control in primitively eusocial Mischocyttarus wasps. Chemoecology 32:105–116. https://doi.org/10.1007/s00049-022-00370-y
Fletcher DJ, Michener CD (1987) Kin recognition in animals. John Wiley & Sons
Foster KR, Ratnieks FL (2001) Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc Biol Sci b 268(1463):169–174. https://doi.org/10.1098/rspb.2000.1346
Free JB, Winder ME (1983) Brood recognition by honeybee (Apis mellifera) workers. Anim Behav 31:539–545. https://doi.org/10.1016/S0003-3472(83)80077-3
Gamboa GJ (2004) Kin recognition in eusocial wasps. Annales Zoologici Fennici. Finnish Zoological and Botanical Publishing Board, pp 789–808
Gamboa GJ, Reeve HK, Ferguson ID, Wacker TL (1986a) Nestmate recognition in social wasps: the origin and acquisition of recognition odours. Anim Behav 34:685–695. https://doi.org/10.1016/S0003-3472(86)80053-7
Gamboa GJ, Reeve HK, Pfennig DW (1986b) The evolution and ontogeny of nestmate recognition in social wasps. Annu Rev Entomol 31:431–454
Giannotti E (1999) Social organization of the eusocial wasp Mischocyttarus cerberus styx (Hymenoptera: Vespidae). Sociobiology 33:325–338
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. https://doi.org/10.1146/annurev.ento.50.071803.130359
Jones SM, van Zweden JS, Grüter C, Menezes C, Alves DA, Nunes-Silva P, Czaczkes T, Imperatriz-Fonseca VL, Ratnieks FL (2012) The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula. Behav Ecol Sociobiol 66:1–12. https://doi.org/10.1007/s00265-011-1246-7
Klahn JE, Gamboa GJ (1983) Social wasps: discrimination between kin and nonkin brood. Science 22:482–484. https://doi.org/10.1126/science.221.4609.482
Kudô K, Oliveira LA, Mateus S, Zucchi R, Nascimento FS (2017) Nestmate larval discrimination by workers in the swarm-founding wasp Polybia paulista. Ethol Ecol Evol 29:170–180. https://doi.org/10.1080/03949370.2015.1129363
Larsen J, Fouks B, Bos N, d’Ettorre P, Nehring V (2014) Variation in nestmate recognition ability among polymorphic leaf-cutting ant workers. J Insect Physiol 70:59–66. https://doi.org/10.1016/j.jinsphys.2014.09.002
LeBoeuf AC, Waridel P, Brent CS, Gonçalves AN, Menin L, Ortiz D, Riba-Grognuz O, Koto A, Soares ZG, Privman E, Miska EA, Benton R, Keller L (2016) Oral transfer of chemical cues, growth proteins and hormones in social insects. eLife 5:e20375. https://doi.org/10.7554/eLife.20375
Lenoir A, Hefetz A, Simon T, Soroker V (2001) Comparative dynamics of gestalt odour formation in two ant species Camponotusn b fellah and Aphaenogaster senilis (Hymenoptera: Formicidae). Physiol Entomol 26:275–283. https://doi.org/10.1046/j.0307-6962.2001.00244.x
Liebig J, Monnin T, Turillazzi S (2005) Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc R Soc b: Biol Sci 272:1339–1344. https://doi.org/10.1098/rspb.2005.3073
Lorenzi MC, Filippone F (2000) Opportunistic discrimination of alien eggs by social wasps (Polistes biglumis, Hymenoptera Vespidae): a defense against social parasitism? Behav Ecol Sociobiol 48:402–440. https://doi.org/10.1007/s002650000251
Miller SE, Bluher SE, Bell E, Cini A, da Silva RC, de Souza AR, Gandia KM, Jandt J, Loope K, Prato A, Pruitt JN, Rankin D, Rankin E, Southon RJ, Uy FMK, Weiner S, Wright CM, Downing H, Gadagkar R, Cristina Lorenzi M, Rusina L, Sumner S, Tibbetts EA, Toth A, Sheehan MJ (2018) WASPnest: a worldwide assessment of social Polistine nesting behavior. Ecology 99:2405. https://doi.org/10.1002/ecy.2448
Montagna TS, Neves ÉF, Antonialli-Junior WF (2012) First report of interspecific facultative social parasitism in the paper wasp genus Mischocyttarus Saussure (Hymenoptera, Vespidae). Rev Bras Entomol 56:263–265. https://doi.org/10.1590/S0085-56262012005000025
Mora-Kepfer F (2014) Context-dependent acceptance of non-nestmates in a primitively eusocial insect. Behav Ecol Sociobiol 68:363–371. https://doi.org/10.1007/s00265-013-1650-2
Murakami AS, Shima SN, Desuó IC (2009) More than one inseminated female in colonies of the independent-founding wasp Mischocyttarus cassununga von Ihering (Hymenoptera, Vespidae). Rev Bras Entomol 53:653–662. https://doi.org/10.1590/S0085-56262009000400017
Nascimento DL, Nascimento FS (2012) Acceptance threshold hypothesis is supported by chemical similarity of cuticular hydrocarbons in a stingless bee, Melipona asilvai. J Chem Ecol 38:1432–1440. https://doi.org/10.1007/s10886-012-0194-7
Noda SCM, Silva ERD, Giannotti E (2001) Dominance hierarchy in different stages of development in colonies of the primitively eusocial wasp Mischocyttarus cerberus styx (Hymenoptera, Vespidae). Sociobiology 38:603–614
Noll FB, da Silva M, Soleman RA, Lopes RB, Grandinete YC, Almeida EA, Wenzel JW, Carpenter JM (2020) Marimbondos: systematics, biogeography, and evolution of social behavior of neotropical swarm-founding wasps (Hymenoptera: Vespidae: Epiponini). Cladistics. https://doi.org/10.1111/cla.12446
Nunes TM, Mateus S, Turatti IC, Morgan ED, Zucchi R (2011) Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals. Anim Behav 81:463–467. https://doi.org/10.1016/j.anbehav.2010.11.020
Nunes TM, Nascimento FS, Turatti IC, Lopes NP, Zucchi R (2008) Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim Behav 75:1165–1171. https://doi.org/10.1016/j.anbehav.2007.08.028
O’Donnell S (2020) Mischocyttarus. In: Starr C (eds) Encyclopedia of Social Insects. Springer, Cham. https://doi.org/10.1007/978-3-319-90306-4_78-1
Oi CA, Brown RL, da Silva RC, Wenseleers T (2020) Reproduction and signals regulating worker policing under identical hormonal control in social wasps. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-76084-4
Oi CA, Van Oystaeyen A, Oliveira RC, Millar JG, Verstrepen KJ, van Zweden JS, Wenseleers T (2015) Dual effect of wasp queen pheromone in regulating insect sociality. Curr Biol 25:1638–1640. https://doi.org/10.1016/j.cub.2015.04.040
Orlova M, Starkey J, Amsalem E (2020) A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee. J Exp Biol 223:jeb217547. https://doi.org/10.1242/jeb.217547
Panek LM, Gamboa GJ (2000) Queens of the paper wasp Polistes fuscatus (Hymenoptera: Vespidae) discriminate among larvae on the basis of relatedness. Ethology 106:159–170. https://doi.org/10.1046/j.1439-0310.2000.00502.x
Pinto NPO, Gobbi N, Noll FB, Penna MAH, Nazareth SL (2004) Coexistência interespecífica em Mischocyttarus Saussure (Hymenoptera: Vespidae, Mischocyttarini) durante a fase inicial de desenvolvimento de um ninho. Ver Etol 6:95–100
Prezoto F, Nascimento FS (1999) Nota sobre a ocorrência de usurpação de um ninho de Mischocyttarus cassununga por Polistes versicolor (Hymenoptera, Vespidae). Rev Etol 1:69–71
Saigo T, Tsuchida K (2004) Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc Royal Soc B 271:S509–S512. https://doi.org/10.1098/rsbl.2004.0238
Schultner E, Pulliainen U (2020) Brood recognition and discrimination in ants. Insectes Soc 67:11–34. https://doi.org/10.1007/s00040-019-00747-3
Singmann H, Bolker B, Westfall J, Aust F, Ben-Shachar MS (2015) Package ‘afex’. URL http://afex.singmann.science/, https://github.com/singmann/afex
Somavilla A, Schoeninger K, Carvalho AF, Menezes RS, Del Lama MA, Costa MA, Oliveira ML (2015) Record of Parasitoids in nests of social wasps (Hymenoptera: Vespidae: Polistinae). Sociobiology 62:92–98. https://doi.org/10.13102/sociobiology.v62i1.92-98
Starkey J, Brown A, Amsalem E (2019) The road to sociality: brood regulation of worker reproduction in the simple eusocial bee Bombus impatiens. Anim Behav 154:57–65. https://doi.org/10.1016/j.anbehav.2019.06.004
Strassmann JE, Seppä P, Queller DC (2000) Absence of within-colony kin discrimination: foundresses of the social wasp, Polistes carolina, do not prefer their own larvae. Naturwissenschaften 87:266–269. https://doi.org/10.1007/s001140050718
Tannure-Nascimento IC, Nascimento FS, Dantas JO, Zucchi R (2009) Decision rules for egg recognition are related to functional roles and chemical cues in the queenless ant Dinoponera quadriceps. Naturwissenschaften 96:857–861. https://doi.org/10.1007/s00114-009-0535-8
Team RC, Team MRC, Suggests MASS, Matrix S (2013) Package “Stats.”. RA Lang. Environment Stat. Comput. Vienna, Austria: R Foundation for Statistical Computing.Turillazzi S, Fanelli D, Theodora P, Lambardi D, Ortolani I, Hashim R, Baracchi D (2008) Determinants of immature brood and nest recognition in a stenogastrine wasp (Hymenoptera Vespidae). Ethol Ecol Evol 20:17–33. https://doi.org/10.1080/08927014.2008.9522540
Turillazzi S, Fanelli D, Theodora P, Lambardi D, Ortolani I, Hashim R, Baracchi D (2008) Determinants of immature brood and nest recognition in a stenogastrine wasp (Hymenoptera Vespidae). Ethol Ecol Evol 20:17–33. https://doi.org/10.1080/03949370.2021.2024270
van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. Insect Hydrocarbons: Biol, Biochem Chem Ecol 11:222–243
Vauchot B, Provost E, Bagneres AG, Riviere G, Roux M, Clement JL (1997) Differential adsorption of allospecific hydrocarbons by the cuticles of two termite species, Reticulitermes santonensis and R. lucifugus grassei, living in a mixed colony: Passive transfer by contact. J Insect Physiol 44:59–66. https://doi.org/10.1016/S0022-1910(97)00104-2
Wenseleers T, Princen S, Oliveira RC, Oi CA (2020). Conflicts of Interest within Colonies. https://doi.org/10.1007/978-3-319-90306-4_28-1
Wenseleers T, Oi CA, Caliari Oliveira R (2021) Worker Policing. In: Starr CK (ed) Encyclopedia of Social Insects. Springer, Cham. https://doi.org/10.1007/978-3-030-28102-1_137
Wenseleers T, Tofilski A, Ratnieks FL (2005) Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav Ecol Sociobiol 58:80–86. https://doi.org/10.1007/s00265-004-0892-4
Wenseleers T, Helanterä H, Hart A, Ratnieks FL (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047. https://doi.org/10.1111/j.1420-9101.2004.00751.x
Wright CM, McEwen BL, Fisher DN, Lichtenstein JL, Antoun A, Tibbetts EA, Pruitt JN (2019) Egg discrimination is mediated by individual differences in queen olfactory responsiveness and boldness. Behav Ecol 30:1306–1313. https://doi.org/10.1093/beheco/arz078
Yusuf AA, Pirk CW, Crewe RM, Njagi PG, Gordon I, Torto B (2010) Nestmate recognition and the role of cuticular hydrocarbons in the African termite raiding ant Pachycondyla analis. J Chem Ecol 36:441–448. https://doi.org/10.1007/s10886-010-9774-6
Funding
This study was financially supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and grant 2018/22461–3 São Paulo Research Foundation (FAPESP) to RCS. Funding was provided from Bilateral grant FWO-FAPESP to CAO, FSN, and TW (process numbers: 2018/10996–0 and 2021/05598-8 FAPESP and FWO: GOF8319N, FWO: GOF6622N), Research Foundation Flanders to CAO (postdoctoral fellowship FWO-12V6318N and research grant FWO-1513219N), and Conselho Nacional de Desenvolvimento Científico e Tecnológico to FSN (307702/2018–9).
Author information
Authors and Affiliations
Contributions
Conceptualization: RCS and CAO. Methodology: RCS. Formal analysis and investigation: RCS and CAO. Writing original draft: RCS and CAO. Writing review and editing: all authors. Funding acquisition: all authors.
Corresponding author
Ethics declarations
Competing interest
The authors declare no competing interests.
Additional information
Communicated by D. Naug.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Cintia Akemi Oi and Fabio Santos Nascimento shared senior authorship.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
da Silva, R.C., Wenseleers, T., Oi, C.A. et al. Tiny but socially valuable: eggs as sources of communication in the social wasp Mischocyttarus cerberus. Behav Ecol Sociobiol 77, 44 (2023). https://doi.org/10.1007/s00265-023-03319-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-023-03319-5