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Structure and Thermal Biology of Subterranean Army Ant Bivouacs in Tropical Montane Forests

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Structure and Thermal Biology of Subterranean Army Ant Bivouacs in Tropical Montane Forests See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/303808248 Structure and thermal biology of subterranean army ant bivouacs in tropical montane forests Article in Insectes Sociaux · June 2016 DOI: 10.1007/s00040-016-0490-2 CITATIONS READS 9 148 2 authors: Kaitlin Baudier Sean Odonnell Arizona State University Drexel University 29 PUBLICATIONS 165 CITATIONS 154 PUBLICATIONS 4,244 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Army ant ecology, thermal biology and behavior View project Theoretical models of division of labor and social evolution View project All content following this page was uploaded by Kaitlin Baudier on 17 October 2016. The user has requested enhancement of the downloaded file. Insect. Soc. (2016) 63:467–476 DOI 10.1007/s00040-016-0490-2 Insectes Sociaux RESEARCH ARTICLE Structure and thermal biology of subterranean army ant bivouacs in tropical montane forests 1 1 K. M. Baudier • S. O’Donnell Received: 1 March 2016 / Revised: 21 May 2016 / Accepted: 23 May 2016 / Published online: 4 June 2016 Ó International Union for the Study of Social Insects (IUSSI) 2016 Abstract Active brood-warming in army ant nests periphery and in adjacent soil, suggesting active bivouac (bivouacs) is well documented for surface-dwelling Eciton warming protects some members of L. praedator bivouac burchellii and E. hamatum colonies in lowland tropical communities from cold-limitation at high elevations in the forests. However, little is known about thermoregulation by tropics. the below-ground bivouacking army ants that comprise all other species in subfamily Dorylinae. Here we report the Keywords Labidus praedator Á Dorylinae Á Homeostasis Á first observations of subterranean Labidus praedator Thermoregulation Á Nest architecture Á Microclimate Á bivouacs in tropical montane and premontane conditions Soil buffering Á Myrmecophile (Monteverde, Costa Rica), and present the first evidence for active nest warming in underground bivouacs. We mea- sured bivouac temperatures at depth increments of 10 cm Introduction through the center of a 1565 m elevation bivouac and compared these to simultaneous measurements at the same The typically soft-bodied, altricial brood of many social soil depths 1 m outside the bivouac. The bivouac was insects are more sensitive to thermal variation than adult actively heated to over 6 °C higher than the adjacent soil. nest mates (Nalepa 2011). Social insect nests are often Another bivouac showed warming of up to 3.7 °C above thermally homeostatic with temperature control achieved by surface ambient. We measured critical thermal maxima passive and/or active thermoregulation (Seeley and Hein- (CTmax) and minima (CTmin)ofL. praedator workers of a rich 1981; Jones and Oldroyd 2007). Passive range of body sizes including callows, as well as thermal thermoregulation involves behavioral responses to envi- tolerances of inquiline millipedes from the bivouac. CTmax ronmental thermal gradients (Jones and Oldroyd 2007). varied positively with worker body size. CTmin was lower Examples of passive thermoregulation among social insects for mature than for callow workers. Symbiotic millipedes include foraging site and nest site selection, nest construc- had lower CTmax and higher CTmin than ant workers. tion and orientation, and relocation of brood within nests Temperatures below the thermal tolerance ranges of sym- (Coenen-Stass, Schaarschmidt and Lamprecht 1980; Frouz biotic millipedes and near the bottom thermal tolerance 2000; Penick and Tschinkel 2008; McGlynn et al. 2010; range for callow workers were recorded in the bivouac Jı´lkova´ and Frouz 2014). Actively thermoregulating organisms use physiology to modify internal or ambient temperatures via metabolic heating or physical activity Electronic supplementary material The online version of this (Seeley and Heinrich 1981; Jones and Oldroyd 2007). article (doi:10.1007/s00040-016-0490-2) contains supplementary material, which is available to authorized users. Examples of active thermoregulation among social insects include worker clustering, flight muscle twitching to gen- & K. M. Baudier erate heat, and wing-fanning to promote evaporative [email protected] cooling (Heinrich 1993; Anderson, Theraulaz and Deneu- 1 Department of Biodiversity Earth and Environmental Science, bourg 2002; Weiner et al. 2010). Most ant species rely on Drexel University, Philadelphia, USA passive thermoregulation to modify nest temperatures 123 468 K. M. Baudier, S. O’Donnell because workers are wingless, preventing active ther- Brady et al. 2014). Therefore, data on bivouacking behavior moregulation via fanning or flight muscle shivering in other doryline genera can provide evidence of how (Ho¨lldobler and Wilson 1990). However, some Neotropical bivouac thermoregulation evolved in the above-ground army ants in the subfamily Dorylinae create homeostatic species. thermal conditions within their temporary nests (bivouacs) Labidus praedator is an abundant subterranean- via active thermoregulation (Jones and Oldroyd 2007). In bivouacking army ant that raids both on the surface of the two above-ground active species, Eciton burchellii and E. forest floor and underground (Rettenmeyer 1963;Kaspari hamatum, bivouacs are composed of hundreds of thousands and O’Donnell 2003; O’Donnell et al. 2007). Labidus of clustering worker bodies that surround and insulate the praedator ranges from the southern United States brood and queen. These bivouacs are actively warmed via (N30°500,W93°450)toArgentinaandSouthernBrazil collective metabolic heat, and bivouac temperature varia- (S30°20,W51°120). Labidus praedator occurs in the low- tion is lower than ambient (Schneirla, Brown and Brown lands near sea level, though this species is most abundant 1954; Jackson 1957; Coenen-Stass, Schaarschmidt and from 1000 to 1600 masl in Costa Rica (Schneirla 1949; Lamprecht 1980; Franks 1985, 1989; Anderson, Theraulaz Watkins 1976; Kaspari and O’Donnell 2003; Longino and Deneubourg 2002; Jones and Oldroyd 2007; Kadochova´ 2010; O’Donnell et al. 2011; Economo and Gue´nard 2016). and Frouz 2014). All other army ant species bivouac below Brood development in L. praedator is apparently syn- ground (Rettenmeyer 1963). Here, we present the first chronous with statary and nomadic colony phases observed measurements of subterranean bivouac thermal physiology in Neotropical lowland wet forests of Panama (N09°090, and brood developmental synchrony in the army ant Labi- W79°51) as well as in the tropical dry forest of southern dus praedator (Smith 1858). Mexico (N18°270,W96°120) (Rettenmeyer 1963;Sudd Previous studies of army ant thermoregulation have pri- 1972). Possible evidence of seasonal asynchrony in brood marily focused on above-ground E. burchellii and E. development has been reported at the southernmost extent hamatum bivouacs (Schneirla, Brown and Brown 1954; of this species’ range in Paraguay (S 25°200,W57°320) Jackson 1957; Rettenmeyer 1963). Lowland E. burchellii during extended winter statary phases with air temperatures bivouacs thermoregulated their brood at relatively reaching below 12.5 °C at night (Fowler 1979). Fowler stable elevated temperatures of 28 ± 1 °C (average 2 °C (1979) suggested temperatures within a Paraguay L. higher than ambient, maximum 6 °C higher than nocturnal praedator bivouacwerelessvariablethansurfaceair low temperatures) (Schneirla, Brown and Brown 1954; temperatures but bivouac temperatures were not elevated. Franks 1989), while lowland bivouacs of E. hamatum were However, Fowler (1979) measured temperature at a single on average 1 °C higher and less thermally variable than bivouac point and did not measure adjacent soil tempera- ambient conditions of 22–29°C (Jackson 1957). Active tures, making interpretation of the data problematic. We bivouac thermoregulation and homeostasis is thought to be asked whether tropical L. praedator colonies warm and/or tightly linked to the synchronous brood development cycles buffer temperatures within their bivouacs when exposed to that characterize the dichotomous statary (egg/pupal) and relatively low ambient temperatures in montane and pre- nomadic (larval) phases of Eciton colony activity (Sch- montane forest. neirla, Brown and Brown 1954; Jackson 1957; Franks Air temperatures are relatively low year-round in high- 1989). Whether active or passive bivouac thermoregulation elevation tropical sites, which can select for localized low- and brood synchrony occur in other species of Dorylinae is temperature adaptations (Janzen 1967; Ghalambor et al. unknown. Eciton species are not representative of Doryli- 2006). However, army ant colonies are nomadic. For nae, in part because they raid and frequently bivouac above example, colonies of the highly epigaeic army ant E. ground (Schneirla 1933; Schneirla, Brown and Brown 1954; burchellii parvispinum move nomadically across elevations Rettenmeyer 1963; Gotwald Jr 1995). In contrast, most in premontane and montane forests of Monteverde, poten- Neotropical army ant species are at least partly subter- tially experiencing a variety of mean annual temperatures at ranean, bivouacking underground and raiding partly or different elevations (Soare et al. 2014). Eciton burchellii entirely below ground (Rettenmeyer 1963; Gotwald Jr bivouacs are more likely to be located in sheltered refuges in 1995). These differences in foraging and bivouacking soil montane forest than in lowland forest, suggesting
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