Cell-Sealing Efficiency and Reproductive Workers in the Species Melipona Bicolor (Hymenoptera, Meliponini): Double Standard and Possible Rogue Conduct
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Cell-sealing efficiency and reproductive workers in the species Melipona bicolor (Hymenoptera, Meliponini): double standard and possible rogue conduct Dirk Koedam, Vera Imperatriz-Fonseca To cite this version: Dirk Koedam, Vera Imperatriz-Fonseca. Cell-sealing efficiency and reproductive workers in the species Melipona bicolor (Hymenoptera, Meliponini): double standard and possible rogue conduct. Apidolo- gie, Springer Verlag, 2012, 43 (4), pp.371-383. 10.1007/s13592-011-0111-z. hal-01003535 HAL Id: hal-01003535 https://hal.archives-ouvertes.fr/hal-01003535 Submitted on 1 Jan 2012 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2012) 43:371–383 Original article * INRA, DIB and Springer-Verlag, France, 2012 DOI: 10.1007/s13592-011-0111-z Cell-sealing efficiency and reproductive workers in the species Melipona bicolor (Hymenoptera, Meliponini): double standard and possible rogue conduct 1 2 Dirk KOEDAM , Vera L. IMPERATRIZ-FONSECA 1Instituto de Estudos Avançados, Cidade Universitária, Rua da Reitoria 374, 05508-970, São Paulo, Brazil 2Laboratório de Abelhas, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, No. 321, 05508-900, São Paulo, SP, Brazil Received 8 September 2010 – Revised 6 September 2011 – Accepted 22 September 2011 Abstract – In many hymenopteran insect societies, selfish workers are policed, as selfishness can negatively affect the average inclusive fitness of one or both castes by reducing either the degree of average relatedness to the colony's male offspring or colony efficiency. In stingless bees, the rapid capping of brood cells could aid in controlling selfishness; to this end, we studied cell-sealing efficacy in Melipona bicolor. Execution of cell sealing was found to be both rapid and almost continuous. Comparing the performance of reproductive and non-reproductive workers, the former sealed the cells more efficiently when they contained their own eggs, but less so when the queens' eggs were involved. We argue that the occurrence of disruptions in cell sealing through self-serving reproductive workers is capable of undermining sealing efficacy as a policing instrument, thus making reproductive workers potential rogue individuals. stingless bees / Melipona bicolor / cell sealing / efficiency / reproductive workers / rogue conduct 1. INTRODUCTION explain this social-repression (Trivers and Hare 1976; Hammond and Keller 2004). In insect societies, the queens produce the In the Hymenoptera, a female is symmetrically bulk of the progeny, although individual repro- related to her offspring but asymmetrically related duction by nest-helpers occasionally occurs as a to her siblings, due to the haplo-diploid determi- manifestation of self-interest. Morphological nation of sex (see Kerr 1962). Furthermore, and physiological caste differentiation has set queens have a spermatheca to store sperm, certain limits to worker reproduction (Wilson whereas workers, while lacking this organ, have 1971). In addition, policing behavior, such as retained functional ovaries, thereby having the egg eating or aggression against workers with faculty to produce offspring albeit only males developed ovaries could reduce this ongoing (Wilson 1971). Thus, both queens and workers social conflict (see Ratnieks 1988). Hypotheses can produce males. Therefore, conflict over about relatedness and efficiency are used to rearing males can be expected, though its intensity may depend on the number of queens heading the colony and on the number of males Corresponding author: D. Koedam, with which the queen has mated (Ratnieks and [email protected] Reeve 1992). For instance, in Apis (Apini), Manuscript editor: Marla Spivak workers are more related to the sons of a 372 D. Koedam and V.L. Imperatriz-Fonseca multiply-mated queen (r=0.25) than to the sons see Tóth et al. 2002). Finally, an occasional of sisters (r<0.25). In addition, they should attack on the physogastric queen in Melipona always prefer their own sons (r=0.5) over subnitida (Koedam et al. 2005) reveals that brothers or nephews. Possibly, the mutual eating reproductive workers may be overtly aggressive. of each other's eggs, also called worker policing, In stingless bees, each individual develops has led to a situation in which worker reproduc- within a single, sealed cell. This development tion seldom occurs (Ratnieks 1988). It is believed starts after several different workers deposit food that worker policing is the reason why an Apis into vertically oriented cells, whereupon the queen queen produces the bulk of the colony's males. lays an egg on top of this food mass (Sakagami In contrast to Apis, stingless bee (Meliponini) 1982). Shortly after egg deposition, the cells are colonies are normally headed by one singly-mated sealed with a wax cap. Generally, soon after food queen (Peters et al. 1999). In this case, kin- provisioning ceases, or immediately after queen selection theory predicts that males should be oviposition, workers have an opportunity to predominantly produced by the workers, through deposit male-destined eggs (see Velthuis et al. their higher degree of relatedness to their sisters' 2005). Neither queens nor non-reproductive sons (r=0.375) than to their brothers (r=0.25). workers noticeably interfere with workers depos- The overall picture, based on behavioural obser- iting these eggs (see Velthuis et al. 2005). The vations of reproductive-egg laying and on analysis real threat of intra-colonial cell usurpation, which of emerging brood and genetic finger-printing occurs in many stingless bee species, is curtailed studies, fits this prediction. Even so, male- by the rapid capping of cells with a protective maternity ratios are quite variable, even within a cover. Rapid capping is thus an important single species (Tóth et al. 2004), especially since mechanical defense against nest mates seeking in a few species, workers completely lack egg-laying opportunities. Sealed cells may also activated ovaries (Sakagami and Zucchi 1968; safeguard the brood against hetero-specific par- Terada 1974). This observation, plus the patterns asitism, though this type of parasitism seems to of worker male production in several other be uncommon (Kistner 1982). eusocial Hymenoptera, like in a wasp (Foster et Together with the presumed use of chemical al. 2002) and various ant species (Evans 1998; substances as a defense against replacement of Hammond et al. 2003; see Hammond and Keller queen-derived eggs (Koedam et al. 2007), 2004), demonstrates that factors other than genetic workers also block the cell opening with their forces are at work to reduce selfishness in helper bodies most of the time, while they are sealing individuals. the cell (Sakagami and Zucchi 1963). This The harmful effect that the behaviour of selfish “body-plugging” can be more or less continu- workers may have on colony efficiency is believed ous, since these workers do not need to interrupt to be another justification for policing (Hammond their work to procure building materials for and Keller 2004). For instance, in stingless bees, producing the cell caps, because the collars of the production of males, including that by worker recently constructed cells typically provide reproduction (see Tóth et al. 2004), may be at the sufficient wax for this purpose (Sakagami expense of a future worker-force (Koedam 1999; 1982). Hence, based on cell-anatomy alone, Santos-Filho et al. 2006). Furthermore, reproduc- the actual closing of cell openings is a contin- tive or dominant hymenopteran workers were uous procedure within a narrow time frame, as found to execute certain nest-tasks in a would be expected if it is to be an effective mediocre or inefficient way (Ross 1985;Cole control of cell usurpation. On the other hand, 1986; Hillesheim et al. 1989). Even so, repro- the participation of selfish workers in cell ductive workers of the stingless bee Melipona sealing could be prejudicial to the quality of bicolor were recorded as being much more active this task. in mass-provisioning brood cells than non- For this study, we examined both speed and reproductive workers (Cepeda 2006;butalso efficiency in cell-sealing performance by mon- Cell-sealing efficiency and reproductive workers 373 itoring individually tagged workers of the faculta- 2.2. Cell sealing and its sub-phases tively polygynous species M. bicolor. We docu- ment how reproductive workers, as compared to Cell sealing follows a typical course and has non-reproductive workers, performed this task. already been documented for various stingless-bee We then provide explanations why they might do species (Sakagami and Zucchi 1974; Zucchi 1993). so and discuss how their typical participation in Sakagami and Zucchi (1974) recognized four sub- the sealing of cells into which queens oviposited phases of cell sealing: pre-operculation, rotation, may augment worker parasitism. side-working, and post-operculation. Here, we stress that the sub-phase pre-operculation, in contrast to post-operculation, is not an element of cell sealing. It 2. METHODS