Comparative temperature tolerance in stingless bee species from tropical highlands and lowlands of Mexico and implications for their conservation (Hymenoptera: Apidae: Meliponini) José Macías-Macías, José Quezada-Euán, Francisca Contreras-Escareño, José Tapia-Gonzalez, Humberto Moo-Valle, Ricardo Ayala To cite this version: José Macías-Macías, José Quezada-Euán, Francisca Contreras-Escareño, José Tapia-Gonzalez, Hum- berto Moo-Valle, et al.. Comparative temperature tolerance in stingless bee species from tropical highlands and lowlands of Mexico and implications for their conservation (Hymenoptera: Apidae: Meliponini). Apidologie, Springer Verlag, 2011, 42 (6), pp.679-689. 10.1007/s13592-011-0074-0. hal-01003611 HAL Id: hal-01003611 https://hal.archives-ouvertes.fr/hal-01003611 Submitted on 1 Jan 2011 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 (2011) 42:679–689 Original article * INRA, DIB-AGIB and Springer Science+Business Media B.V., 2011 DOI: 10.1007/s13592-011-0074-0 Comparative temperature tolerance in stingless bee species from tropical highlands and lowlands of Mexico and implications for their conservation (Hymenoptera: Apidae: Meliponini) 1 2 José Octavio MACÍAS-MACÍAS , José Javier G. QUEZADA-EUÁN , 1 3 Francisca CONTRERAS-ESCAREÑO , José Maria TAPIA-GONZALEZ , 2 4 Humberto MOO-VALLE , Ricardo AYALA 1Laboratorio de Abejas, Departamento de Producción Agrícola, Centro Universitario de la Costa Sur, Universidad de Guadalajara, Independencia Nacional 151, Autlán de Navarro, Jalisco, Mexico 2Departamento de Apicultura, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Apartado postal 4-116, CP 97100, Mérida, Yucatán, Mexico 3Departamento de Producción Animal, Centro Universitario del Sur, Universidad de Guadalajara, Zapotlán el Grande, Jalisco, Mexico 4Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 21, San Patricio, Jalisco 48980, Mexico Received 18 August 2010 – Revised 1 February 2011 – Accepted 2 February 2011 Abstract – The objective of this study was to evaluate the temperature sensitivity of three stingless bee species, one from the tropical highland transition Neartic-Neotropical region (Melipona colimana) and two from the tropical lowland regions (Melipona beecheii and Scaptotrigona hellwegeri) of Mexico. The changes in thoracic temperature, behavior, and mortality rate of workers and pupae of the three species submitted to control high and low temperatures were assessed. Workers of highland M. colimana regurgitated water and fanned their wings when submitted to high temperatures, a behavior reported here for the first time in a stingless bee. M. colimana consumed syrup and increased its thoracic temperature in response to cold environment. Workers and pupae of M. colimana experienced lower mortality rates than M. beecheii and S. hellwegeri. The results of this study showed the tolerance of M. colimana to a wider temperature range, possibly as a response to extreme conditions in its native environment. The implications of thermal susceptibility differences for the conservation of highland and lowland stingless bees are discussed. Melipona / Scaptotrigona / Apidae / temperature tolerance / behavior / temperate forest / Mexico 1. INTRODUCTION also provide a physiological framework that may help to predict the effect of climatic change Critical temperatures are defined as the limits on different taxa (Huey and Stevenson 1979; of an organism’s performance and may reflect Frazier et al. 2006). In spite of the importance adaptation of ectotherms to their climate of temperature tolerance data in insects, studies (Deutsch et al. 2008). Thermal tolerance curves on temperature tolerance in bees other than the honeybees are lacking. In stingless bees, there is Corresponding author: J.O. Macías-Macías, a lack of information on thermal performance of [email protected] different species, which is urgently needed in Manuscript editor: Stan Schneider order to evaluate the effects of habitat deterio- 680 J.O. Macías-Macías et al. ration and climatic change on these key polli- response of workers and immature stages of nators of the tropical and subtropical areas of species from highland and lowland tropics. the world. In eusocial bees (Apini and Melipo- Thus, stingless bee species, inhabiting contrast- nini), colonies are perennial and the production ing climates, represent potential models on of individuals is continuous over long periods which to evaluate the individual physiology of time. Such features are linked to the ability of and behavior of temperature control that may colonies to control nest temperatures within lead to adaptation to these environments. Toler- ranges that are optimal for the development of ance to extreme cold and heat in brood and the immature brood (Tautz et al. 2003; Jones et adult workers of highland Melipona colimana al. 2005; Mc Mullan and Brown 2005). The and lowland Melipona beecheii and Scaptotri- adult workers of eusocial bees exhibit an array gona hellwegeri was studied in order to com- of physiological and behavioral responses to pare the behavioral and physiological responses extreme variations in the environment to main- to temperature fluctuation resulting from adap- tain internal nest temperatures (Heinrich 1993; tation to their contrasting environments. The Jones and Oldroyd 2007). The mechanisms that study of these species may help to determine the social insects have evolved to regulate nest ability to maintain nest homeostasis that may temperature fall into two categories: active and exist in stingless bees given the diverse range of passive. Passive mechanisms include nest site habitats and nesting sites across the tropics. selection, nest structures, and simple behaviors such as brood translocation. On the other hand, active mechanisms involve behaviors where 2. MATERIALS AND METHODS individuals modify nest temperature by physical activity like wing fanning or evaporative cool- 2.1 Study site and species description ing (Jones et al. 2005; Jones and Oldroyd 2007). In stingless bees, the role of maintaining The study was conducted at the Centro Universi- nest homeostasis is not clear (Zucchi and tario del Sur (CUSUR) of the Universidad de Sakagami 1972; Fletcher and Crewe 1981; Guadalajara in Ciudad Guzman, Jalisco, Mexico, Roubik 1983). For instance, species like Nan- localized at a latitude of 19°42′10″ and longitude of notrigona perilampoides collect water at high 103°27′45″ with an altitude of 1,507 m above sea environmental temperatures (Cauich et al. level (masl). Three stingless bee species, one from the 2004), but it is unknown if water is used to tropical highlands (M. colimana) and two from the actively cool down their nest by wing fanning lowland tropics (M. beecheii and S. hellwegeri), were and evaporation (Roubik 2006). Most species of used. M. colimana Ayala 1999 has a marked stingless bees are geographically restricted to geographic endemism to the highland pine-oak low tropical and subtropical regions which forests of western Mexico (south of Jalisco state). could be a result of their limited ability to warm This species has a black integument with yellow up their nests at low environmental temper- marks, orange pubescence, with a body length of atures. However, few species also dwell at 9.5 mm, and weight of 0.067 g. It has only been tropical highlands and may show tolerance to reported in tropical highlands from 1,500 to 1,900 cold by means of active mechanism, but this has masl (Ayala 1999). The temperature in the western not been evaluated (Sakagami 1982; Wille pine forest in Mexico is, on average, 23.1°C during 1983; Ortiz-Mora et al. 1995; Nogueira-Neto the summer and 18.6°C in the winter, but temper- 1997). Accordingly, all studies of temperature atures of 7°C can be common, and in this area, there control in stingless bee colonies have been are reports of temperatures lower than 10°C for up to conducted on species that inhabit Neotropical 40 days at a time (CONAGUA 2007b). The other two environments (Zucchi and Sakagami 1972; species under study, M. beecheii and S. hellwegeri, Fletcher and Crewe 1981; Roubik and Peralta are only found in low subtropical and tropical rain 1983) and have not compared the individual forests with sea level records at a maximum altitude Temperature tolerance of three stingless bees 681 of 1,100 masl, with a temperature average of 28.7°C worker bees (measured as syrup and water consump- and 900 to 1,100 mm of rain (Ayala 1999; CON- tion and wing fanning) and a second to determine the AGUA 2007a). M. beecheii is a species with a body tolerance (measured by survival rate) of workers and length between 9.7 and 10.7 mm, with a body weight brood pupae. of 0.057 g. It presents an almost total black integument with brownish-gray and black drawings 2.2 Thoracic temperature and behavior on the legs, whitish pubescence at the sides of the of adult workers at high and low mesosome, and ochre or orange on the rest of the temperatures body. S. hellwegeri has a body length of 4.7 to 5.1 mm with an orange and black integument (Ayala First, the change in the thoracic temperature of bees 1999), with a weight of 0.013 g. It was decided to use under controlled low and high temperatures was S. hellwegeri as a point of comparison with another evaluated. From each colony, 100 workers were taken tropical climate stingless bee genus, since some from the brood area and were placed in wooden boxes internal environmental control behaviors have been (12.5×7×5 cm) with two plastic feeders, one contain- previously reported in other Scaptotrigona species ing sugar syrup 2:1 (sugar/water) and another one (Scaptotrigona postica) (Engels et al.