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Survival Strategies of Stingless Bees (Melipona Subnitida)

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Survival Strategies of Stingless Bees (Melipona Subnitida) Survival strategies of stingless bees (Melipona subnitida) in an unpredictable environment, the Brazilian tropical dry forest Camila Maia-Silva, Michael Hrncir, Claudia Inês da Silva, Vera Lucia Imperatriz-Fonseca To cite this version: Camila Maia-Silva, Michael Hrncir, Claudia Inês da Silva, Vera Lucia Imperatriz-Fonseca. Survival strategies of stingless bees (Melipona subnitida) in an unpredictable environment, the Brazilian trop- ical dry forest. Apidologie, Springer Verlag, 2015, 46 (5), pp.631-643. 10.1007/s13592-015-0354-1. hal-01284477 HAL Id: hal-01284477 https://hal.archives-ouvertes.fr/hal-01284477 Submitted on 15 Mar 2016 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 (2015) 46:631–643 Original article * INRA, DIB and Springer-Verlag France, 2015 DOI: 10.1007/s13592-015-0354-1 Survival strategies of stingless bees (Melipona subnitida ) in an unpredictable environment, the Brazilian tropical dry forest 1,2 2 1,3 Camila MAIA-SILVA , Michael HRNCIR , Claudia Inês da SILVA , 1,2 Vera Lucia I MPERATRIZ-FONSECA 1Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Avenida Bandeirantes 3900, Ribeirão Preto, SP 14040-901, Brasil 2Departamento de Ciências Animais, Universidade Federal Rural do Semi-Árido, Avenida Francisco Mota 572, Mossoró, RN 59625-900, Brasil 3Departamento de Zootecnia, Universidade Federal do Ceará, Avenida Mister Hull 2977, Campus do Pici, Bloco 808, Fortaleza, CE 60021-970, Brasil Received 23 July 2014 – Revised 15 January 2015 – Accepted 30 January 2015 Abstract – Unpredictable environments are a challenge to highly eusocial bees because unreliable food availability, owing mainly to seasonally unpredictable precipitation rates, renders the maintenance of permanent colonies difficult. Here, we investigated the strategy of the stingless bee Melipona subnitida to cope with elevated temperatures and extended, irregular periods of drought in the Brazilian tropical dry forest. We found a high association between colony behaviour (pollen foraging and brood production) and environmental parameters (abiotic factors and availability of pollen sources), suggesting that colonies tightly adjust their activities to the respective environmental conditions. This minimises unnecessary costs related to foraging and brood rearing when forage availability is low. Additionally, M. subnitida selectively foraged at the most lucrative pollen-sources (mass- flowering trees, plants with poricidal flowers), which indicates that the colonies maximise their food intake as soon as resources are available. Caatinga / floral resources / pollen foraging / brood-cell construction 1. INTRODUCTION species; Michener 2007). Of these, temperate and subtropical species as well as species of many One of the premises for classifying a social tropical regions live in largely predictable foraging insect as highly eusocial is that its colonies are environments, a fact that facilitates the maintenance long-lived (Wilson 1971; Michener 1974). of perennial colonies. On the one hand, bees of Among the bees, there are two groups of highly temperate, subtropical, and seasonal tropical envi- eusocial species, the stingless bees (Apidae, ronments experience a predictable foraging season, Meliponini, over 500 species; Michener 2013) followed by a likewise predictable season without and the honey bees (Apidae, Apini, about 11 floral resources. When periods of food scarcity are imminent, colonies of highly eusocial bees increase Electronic supplementary material The online version of their foraging activity and amass food stores within this article (doi:10.1007/s13592-015-0354-1) contains supplementary material, which is available to authorized the nest (Lindauer 1948; Michener 1974; Kleinert- users. Giovannini 1982; Roubik 1982; Seeley 1985; Corresponding author: C. Maia-Silva, Rinderer 1988). Bees living in the non-seasonal [email protected] tropics, on the other hand, do not experience severe Manuscript Editor: James Nieh variations in food availability throughout the year 632 C. Maia-Silva et al. and, consequently, have virtually year-round access forest. Specifically, we were interested in how this to resources in the environment (Bawa 1983; bee species sustains perennial colonies in this Wilms and Wiechers 1997; Kajobe and unpredictable environment. Since M. subnitida Echazarreta 2005). Here, in contrast to seasonally is not known for seasonal absconding, colonies changing environments, the accumulation of food should show alternative behavioural responses to reserves has little relevance for sustaining long- unfavourable environmental conditions. We eval- lived colonies (Schneider and Blyther 1988; uated (1) the influence of environmental factors McNally and Schneider 1992). on external (pollen foraging) and internal activi- In strong contrast to these predictable foraging ties (brood-cell construction) and (2) the pollen environments, unpredictable environments pose a resources collected by the colonies. challenge to highly eusocial bees. Temporally un- reliable food availability, often due to unpredict- 2. MATERIAL AND METHODS able climatic conditions throughout the year, ren- ders the maintenance of permanent colonies in 2.1. Study site and bee species these environments difficult. Here, the strategy of honey bees is to abandon a location in which The study was performed from May, 2011 through environmental conditions are unfavourable and to May, 2012 in a 210,000-m2 area of native Caatinga migrate into areas of greater resource abundance vegetation at the Experimental Field Station Rafael (seasonal absconding) (Michener 1974;Schneider Fernandes of the Brazilian National University of Ag- and McNally 1992a, b; Freitas et al. 2007). In riculture (UFERSA) in Mossoró-Rio Grande do Norte stingless bees, however, absconding is rare (al- (5°03′54.45″ S, 37°24′03.64″ W; altitude, 79 m). The though not impossible). This is largely due to the region is characterised by a hot and semi-arid climate fact that mated meliponine queens are unable to with an average annual rainfall of between 500 and fly, and the colonies would have to leave their 800 mm and deciduous thorn vegetation (Velloso et al. queen behind when moving to a new nesting site 2002). We investigated four colonies of the stingless bee (Michener 1974). Consequently, stingless bees are species M. subnitida Ducke 1910 (Apidae, Meliponin), much more constrained to a given nest location housed in wooden nest-boxes that had been installed than are honey bees, and putatively developed within the study area 3 months prior to the onset of the alternative strategies to sustain permanent colo- observations. The geographic distribution of nies in unpredictable environments. M. subnitida , popularly known as Bjandaira^, is restrict- An unpredictable environment, and particular- ed to the states of northeastern Brazil (Zanella 2000; ly challenging for highly eusocial bees, is the Camargo and Pedro 2012). It naturally nests in narrow Brazilian tropical dry forest, the Caatinga. The cavities (diameter≈10 cm; length≈115 cm) preferential- climate of this ecoregion in northeastern Brazil is ly of the native tree species Commiphora leptophloeos classified as semi-arid with elevated annual tem- (Burseraceae), Poincianella bracteosa (Fabaceae, peratures and extended periods of drought (Prado Caesalpinioidae), and Myracrodruon urudeuva 2003). Here, blooming of the vast majority of (Anacardiaceae) (Cámara et al. 2004; Martins et al. flowering plants occurs during a very short, yet 2004). Worker populations vary from <100 individuals unpredictable rainy season (Zanella and Martins during the dry period to >1500 during the rainy season 2003; Machado and Lopes 2004; Maia-Silva et al. (CMS, MH, personal observation). 2012). Probably due to these extreme environ- mental conditions and the associated shortage of 2.2. Environmental factors floral resources over long, irregular periods of the year, only few meliponine species naturally occur For each month of our study, we calculated the in this biome (Zanella 2000;ZanellaandMartins following environmental variables (EV): TAV G,average 2003). temperature (°C); TMAX, maximum temperature (°C); The purpose of the present study was to inves- TMIN, minimum temperature (°C); RHAV G, average rel- tigate the survival strategies of the stingless bee ative humidity (%); RAIN, total precipitation (mm); Melipona subnitida in the Brazilian tropical dry SUN, average time of sunrise; and P-FLO, total number Adaptations of stingless bees in the Caatinga 633 of plant species available as potential pollen sources. 5-min interval in which pollen foragers returned to the Data on abiotic variables were obtained from a weather colony, followed by at least two 5-min intervals with station of the National Institute of Meteorology zero counts. For the statistical analyses, time data (hour: (INMET, weather-station number A318), at a distance minute) were transformed into decimal numbers of approximately 4 km from our study area. Since data (hour+minutes/60,
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