The Males of Melipona and Other Stingless Bees, and Their Mothers1
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Apidologie 36 (2005) 169–185 © INRA/DIB-AGIB/ EDP Sciences, 2005 169 DOI: 10.1051/apido:2005014 Review article The males of Melipona and other stingless bees, and their mothers1 Hayo H.W. VELTHUISa*, Dirk KOEDAMb, Vera L. IMPERATRIZ-FONSECAb a Klemit 1, 5325 KG Wellseind, The Netherlands b Laboratório de Abelhas, Depto. de Ecologia, Instituto de Biociências, USP, Rua do Matão, Trav. 14, No. 321, CEP 05508-900, São Paulo, Brazil Received 4 November 2004 – Revised 7 January 2005 – Accepted 17 January 2005 Published online 1 June 2005 Abstract – Female behaviour in social Hymenoptera and the queen-worker conflict with respect to male production have been the focus of many studies. Although male production is an investment that is in conflict with investment in colony size, males play a vital role in colony reproduction. This paper reviews the production patterns of male stingless bees, their activities once they have reached adulthood and their origin (i.e., are they sons of workers or of queens). The existence of a broad spectrum of species-specific patterns of male production, sex ratios, and male parentage offers ample opportunities to discuss the influence of ecology on the dynamics of stingless bee colony life. The paper also argues that selfishness causes the queen and the workers to compete and each to adopt certain strategies in their effort to produce male progeny. It is this competition, expressed in various forms during the characteristic and socially complex process of cell provisioning and oviposition, that could help explain the variable outcomes of male parentage at the species level as we currently know them. stingless bee male / sex ratio / life history / male aggregation / queen-worker conflict / provisioning and oviposition process 1. INTRODUCTION monopolize male production. This characteris- tic differs greatly between Melipona species. Stingless bees form an ancient (Michener This genus, therefore, offers ample opportuni- and Grimaldi, 1988) and rather diversified ties for studies on the factors that have had an (Michener, 1974, 2000) group of mass-provi- impact on the evolutionary rules governing the sioning eusocial bees. They vary considerably dynamics of colony life. This interaction in several of the characters for which sociobio- between our concepts of primary evolutionary logical theory would predict a basic uniformity. rules and the ecology of bees will be reviewed Trivers and Hare (1976) made clear that work- in this paper. ers of hymenopteran colonies, headed by a sin- Colonies of stingless bees are made up of gle monandrous queen, have reproductive males and females, and the latter are divided interests that are different from their mother. into workers and queens. Differences between This discord has its expression in the origin of males and females start with the fertilization of the males, some of which are sons of the queen the egg: the unfertilized egg becomes a male, whereas others are sons of some of the workers. while the fertilized egg is female. Sex determi- The workers of such colonies find their genes nation, therefore, is genetic and is related to better represented in sons and nephews than in haplodiploidy. In contrast, the main decisive brothers and should, accordingly, attempt to factor in the development of a fertilized egg * Corresponding author: [email protected] 1 Manuscript editor: Gudrun Koeniger Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2005014 170 H.H.W. Velthuis et al. into a queen or a worker is the quality/quantity colony characteristics. However, major differ- of food in the brood cell. ences exist in the way in which males are pro- Queens can be reared in different ways. duced. Most genera of the tribe Meliponini construct occasionally a larger brood cell that contains more food than the common brood cells. This 2. THE PATTERNS OF MALE quantitative factor modifies the differentiation PRODUCTION of the female larva in the cell: she will become a queen. The smaller and more common cells In general, male production in a social insect harbour workers and males. Thus, like in the colony is influenced by outside factors related honeybees, queens of these genera emerge to climatic periodicity, and factors inside the from specific queen cells. Different mecha- colony such as colony strength and demo- nisms are seen in the remaining genera. In Frie- graphic composition. Under temperate condi- seomelitta, for example, large queen cocoons tions, climate has a preponderant impact. The occur, but are the result of larvae perforating seasonal factors force colonies to produce their the wall of an adjacent cell. These larvae then sexuals during a brief period, thereby synchro- gain a second portion of food, enabling the nizing the colonies of a population. In contrast, modification of their development into a queen bees in tropical regions may be largely inde- (Terada, 1974; Faustino et al., 2002). All brood pendent of such climatic influences, although cells in the genus Melipona are approximately the alternation of dry and wet seasons may the same size. In this genus it is the minute var- cause males to be more frequent in one period iation in the quantity and, perhaps, also in the of the year than in the other. Synchronous pro- quality of the food that contributes to the devel- duction at the population level, therefore, may opmental differentiation between workers and become less pronounced and the role of within- queens. A two-locus genetic mechanism may colony factors more evident. also prevent 75% of the Melipona females from Male production is an investment that is in becoming queens (Kerr, 1950; Velthuis and conflict with investment in colony size: instead Sommeijer, 1991). Because the differences in of a worker a male emerges that does not par- the food for worker or queen development are ticipate in regular colony activities like cell so small, young Melipona queens emerge quite building, cell provisioning, colony defense, regularly even though hardly any are actually and foraging. He does, however, represent the needed. These superfluous queens are then colony in the reproductive arena. Investments killed by the workers. in reproduction may occur once the existence This peculiar and seemingly overproduction and future of the colony is assured. of queens and their fascinating mechanism for How would male production be regulated at caste differentiation have stimulated many the colony level? For a perennial colony with studies on Melipona (Kerr, 1950; Velthuis a long life expectancy, which characterizes and Sommeijer, 1991; Koedam et al., 1995; Melipona species, there may be two ways: (1) Wenseleers and Ratnieks, 2004; Wenseleers constantly as a proportion of the cells produced, et al., 2004). As a result and because a in a ratio that increases both with colony size number of Melipona species have been domes- and with the rate of cell production or (2) as an ticated, the genus Melipona is better known outburst of limited duration once the proper compared to most of the other stingless bee colony size and conditions have been reached. genera. In the first instance, male production is a con- Males are the prime subject of this study. We stant but light impediment. In the second case, will discuss the patterns of their production, male production may lead to distinct fluctua- their activities once they reach adulthood, and tions in the worker force, which forces the col- their origin (i.e., are they the sons of workers ony to recover after a male producing period. or of queens?). Alhough this paper concen- Long-term ecological factors, such as the prob- trates on the genus Melipona, when appropriate ability of the presence of suitable but unoccu- other genera will be mentioned. Melipona is a pied nesting sites in the habitat, may also be neotropical genus comprising about 40 species, involved. Such habitat characteristics deter- which, to a large extent, are uniform in their mine the incidence of swarming. If swarming Males of stingless bees and their mothers 171 is frequent, we might expect colony growth rate 2.1. Temporal patterns of male to be important and thus male production to be production absent or limited in smaller colonies. One pos- sible example of this is M. mandacaia, a species It has been documented at colony level of a that lives in the caatingas of the state of Bahia, number of species, that most of the males are Brazil. These areas are exposed to extremely produced in periods with a restricted duration. long periods of drought, during which bee col- We have termed this the Male-Producing Peri- ods or MPP (this term is preferred over the onies may undergo considerable size reduction. almost equivalent term Male Emerging Period Populations, therefore, are characterized by or MEP proposed by Chinh et al., 2003). In high colony-mortality rates. Once a rainy recent studies, this phenomenon has been doc- period has caused the vegetation to bloom, the umented to occur in M. asilvai, M. bicolor, M. colonies increase rapidly in size and then favosa, and M. subnitida as well as in Plebeia swarm to occupy the nesting sites that became remota, Scaptotrigona postica, Schwarziana vacant (Castro, pers. com.). We might expect quadripunctata and Trigona (Lepidotrigona) male production in such a species to be concen- ventralis (Bego, 1982; Koedam et al., 1999; trated in time at both the population level and Velthuis et al., 2002; Sommeijer et al., 2003; the colony level, because the impact of the Alves, 2004; Alves et al., 2004; Chinh, 2004; environment is so great that the within-colony Alves, unpubl.). It is, therefore, a wide-spread factors have little influence. In contrast, there event. MPPs may be the result of a synchro- might not be a vacant nest cavity for long peri- nous, albeit differential, production of repro- ods of time for species living in areas where the ductive eggs by a number of workers, some- environment is more stable.