Abstract
Active brood-warming in army ant nests (bivouacs) is well documented for surface-dwelling Eciton burchellii and E. hamatum colonies in lowland tropical forests. However, little is known about thermoregulation by the below-ground bivouacking army ants that comprise all other species in subfamily Dorylinae. Here we report the first observations of subterranean Labidus praedator bivouacs in tropical montane and premontane conditions (Monteverde, Costa Rica), and present the first evidence for active nest warming in underground bivouacs. We measured bivouac temperatures at depth increments of 10 cm through the center of a 1565 m elevation bivouac and compared these to simultaneous measurements at the same soil depths 1 m outside the bivouac. The bivouac was actively heated to over 6 °C higher than the adjacent soil. Another bivouac showed warming of up to 3.7 °C above surface ambient. We measured critical thermal maxima (CTmax) and minima (CTmin) of L. praedator workers of a range of body sizes including callows, as well as thermal tolerances of inquiline millipedes from the bivouac. CTmax varied positively with worker body size. CTmin was lower for mature than for callow workers. Symbiotic millipedes had lower CTmax and higher CTmin than ant workers. Temperatures below the thermal tolerance ranges of symbiotic millipedes and near the bottom thermal tolerance range for callow workers were recorded in the bivouac periphery and in adjacent soil, suggesting active bivouac warming protects some members of L. praedator bivouac communities from cold-limitation at high elevations in the tropics.
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References
Abril S, Oliveras J, Gómez C (2010) Effect of temperature on the development and survival of the Argentine ant, Linepithema humile. J Insect Sci 10:1–13
Anderson C, Theraulaz G, Deneubourg JL (2002) Self-assemblages in insect societies. Insect Soc 49:99–110
Barth M, Moritz R, Kraus F (2015) Genetic differentiation at species level in the Neotropical army ant Labidus praedator. Insect Soc 62:299–306
Baudier KM, Mudd AE, Erickson SC, O’Donnell S (2015) Microhabitat and body size effects on heat tolerance: implications for responses to climate change (army ants: Formicidae, Ecitoninae). J Anim Ecol 84:1322–1330
Beeren C, Maruyama M, Kronauer DJ (2016) Cryptic diversity, high host specificity and reproductive synchronization in army ant-associated Vatesus beetles. Mol Ecol 25:1–16
Berghoff S, Weissflog A, Linsenmair K, Mohamed M, Maschwitz U (2002) Nesting habits and colony composition of the hypogaeic army ant Dorylus (Dichthadia) laevigatus Fr. Smith. Insect Soc 49:380–387
Brady SG (2003) Evolution of the army ant syndrome: the origin and long-term evolutionary stasis of a complex of behavioral and reproductive adaptations. Proc Natl Acad Sci USA 100:6575–6579
Brady SG, Fisher BL, Schultz TR, Ward PS (2014) The rise of army ants and their relatives: diversification of specialized predatory doryline ants. BMC Evol Biol 14:1–14
Bulova S, Purce K, Khodak P, Sulger E, O’Donnell S (2016) Into the black and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae). Naturwissenschaften 103:1–11
Coenen-Stass D, Schaarschmidt B, Lamprecht I (1980) Temperature distribution and calorimetric determination of heat production in the nest of the wood ant, Formica polyctena (Hymenoptera, Formicidae). Ecology 61:238–244
Diamond SE, Nichols LM, McCoy N, Hirsch C, Pelini SL, Sander NJ, Ellison AM, Gotelli NJ, Dunn RR (2012) A physiological trait-based approach to predicting the responses of species to experimental climate warming. Ecology 93:2305–2312
Dunn R (2003) Imposter in the nest. Nat Hist 112:22–26
Economo E, Guénard B (2016) AntMaps. http://antmaps.org. Accessed 20 Feb 2016
Eickwort GC (1990) Associations of mites with social insects. Annu Rev Entomol 35:469–488
Fowler HG (1979) Notes on Labidus praedator (Fr. Smith) in Paraguay (Hymenoptera: Formicidae: Dorylinae: Ecitonini). J Nat Hist 13:3–10
Franks NR (1985) Reproduction, foraging efficiency and worker polymorphism in army ants. In: Hölldobler B, Lindauer M (eds) Experimental behavioural ecology. Gustav Fischer, Stuttgart, New York, pp 91–107
Franks NR (1989) Thermal regulation in army ant bivouacs. Physiol Entomol 14:397–404
Frouz J (2000) The effect of nest moisture on daily temperature regime in the nests of Formica polyctena wood ants. Insect Soc 47:229–235
Galushko D, Ermakov N, Karpovski M, Palevski A, Ishay J, Bergman D (2005) Electrical, thermoelectric and thermophysical properties of hornet cuticle. Semicond Sci Tech 20:286
Ghalambor CK, Huey RB, Martin PR, Tewksbury JJ, Wang G (2006) Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integ Comp Biol 46:5–17
Gotwald WH (1995) Army ants: the biology of social predation. Comstock, Ithaca
Harkness R, Wehner R (1977) Cataglyphis. Endeavour 1:115–121
Heinrich B (1993) The hot-blooded insects: strategies and mechanisms of thermoregulation. Springer, Berlin Heidelberg, pp 457–495
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge
Jackson WB (1957) Microclimatic patterns in the army ant bivouac. Ecology 38:276–285
Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249
Jílková V, Frouz J (2014) Contribution of ant and microbial respiration to CO2 emission from wood ant (Formica polyctena) nests. Eur J Soil Biol 60:44–48
Jones JC, Oldroyd BP (2007) Nest thermoregulation in social insects. Adv Insect Physiol 33:153–191
Kadochová Š, Frouz J (2014) Red wood ants Formica polyctena switch off active thermoregulation of the nest in autumn. Insect Soc 61:297–306
Kaspari M, O’Donnell S (2003) High rates of army ant raids in the Neotropics and implications for ant colony and community structure. Evol Ecol Res 5:933–939
Kipyatkov VE, Lopatina EB (2015) Comparative study of thermal reaction norms for development in ants. Entomol Sci 18:174–192
Longino JT (2010) Ants of Costa Rica. http://academic.evergreen.edu/projects/ants/AntsofCostaRica.html. Accessed 20 Feb 2016
Loomis H (1959) New myrmecophilous millipeds from Barro Colorado Island, Canal Zone, and Mexico. J Kansas Entomol Soc 32:1–7
Lutterschmidt I, Hutchison VH (1997) The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can J Zoolog 75:1553–1560
McGlynn TP, Dunn T, Wayman E, Romero A (2010) A thermophile in the shade: light-directed nest relocation in the Costa Rican ant Ectatomma ruidum. J Trop Ecol 26:559–562
Monteiro AF, Sujii ER, Morais HC (2008) Chemically based interactions and nutritional ecology of Labidus praedator (Formicidae: Ecitoninae) in an agroecosystem adjacent to a gallery forest. Rev Bras Zool 25:674–681
Nadkarni NM, Wheelwright NT (2000) Monteverde: ecology and conservation of a tropical cloud forest. Oxford University Press, Oxford
Nalepa CA (2011) Body size and termite evolution. Evol Biol 38:243–257
Oberg EW, Toro I, Pelini SL (2012) Characterization of the thermal tolerances of forest ants of New England. Insect Soc 59:167–174
O’Donnell S, Kaspari M, Kumar A, Lattke J, Powell S (2011) Elevational and geographic variation in army ant swarm raid rates. Insect Soc 58:293–298
O’Donnell S, Lattke J, Powell S, Kaspari M (2007) Army ants in four forests: geographic variation in raid rates and species composition. J Anim Ecol 76:580–589
Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecol News 22:65–108
Parton WJ, Logan JA (1981) A model for diurnal variation in soil and air temperature. Agr Meteorol 23:205–216
Penick CA, Tschinkel W (2008) Thermoregulatory brood transport in the fire ant, Solenopsis invicta. Insect Soc 55:176–182
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Rettenmeyer CW (1962a) Arthropods associated with neo-tropical army ants with a review of the behavior of these ants. Dissertation, University of Kansas
Rettenmeyer CW (1962b) The behavior of millipeds found with Neotropical army ants. J Kansas Entomol Soc 35:377–384
Rettenmeyer CW (1963) Behavioral studies of army ants. Univ Kans Sci Bull 44:281–465
Rettenmeyer CW, Rettenmeyer ME, Joseph J, Berghoff SM (2011) The largest animal association centered on one species: the army ant Eciton burchellii and its more than 300 associates. Insect Soc 58:281–292
Schneirla TC (1933) Studies on army ant raids in Panama. J Comp Psychol 15:267
Schneirla TC (1949) Army-ant life and behavior under dry-season conditions: the course of reproduction and colony behavior. B Am Mus Nat Hist 94:1–82
Schneirla TC, Brown RZ, Brown FC (1954) The bivouac or temporary nest as an adaptive factor in certain terrestrial species of army ants. Ecol Monogr 24:269–296
Seeley TD, Heinrich B (1981) Regulation of temperature in the nests of social insects. In: Heinrich B (ed) Insect thermoregulation. Wiley, New York, pp p159–p234
Soare TW, Tully SI, Willson SK, Kronauer DJC, O’Donnell S (2011) Choice of nest site protects army ant colonies from environmental extremes in tropical montane forest. Insect Soc 58:299–308
Soare TW, Kumar A, Naish KA, O’Donnell S (2014) Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii. Mol Ecol 23:96–109
Sudd JH (1972) Review of army ants, a study in social organization. Sci Prog 60:570–573
Sumichrast F, Norton E (1868) Notes on the habits of certain species of mexican hymenoptera presented to the American Entomological Society, No. 1. T Am Entomol Soc 2:39–46
Tschinkel W (1987) Seasonal life history and nest architecture of a winter-active ant, Prenolepis imparis. Insect Soc 34:143–164
Watkins JF (1976) The identification and distribution of new world army ants (Dorylinae: Formicidae). Baylor University Press, Waco
Weiner S, Upton C, Noble K, Woods W, Starks P (2010) Thermoregulation in the primitively eusocial paper wasp, Polistes dominulus. Insect Soc 57:157–162
Acknowledgments
We thank anonymous reviewers who provided useful feedback. Students at the Monteverde Friends School, Nicole Arcilla, Johnathan Ogle, Heather Gosse, Rumaan Malhotra, Catherine D’Amelio, and Elisabeth Sulger provided field assistance. Historic Monteverde, Martha Campbell, Lucy, Wilford and Benito Guindon permitted access to private lands. The Monteverde Conservation League permitted access to the Children’s Eternal Rainforest for work in San Gerardo. We thank John T. Longino and Susan Bulova for project feedback. Christoph von Beeren, Jon Gelhaus, and Jason Weintraub aided in myrmecophile identification and imaging. Michael O’Connor, Steven Pearson, Tom Radzio and Dane Ward assisted with thermal equipment. Research was conducted under research and collection permits issued by the Costa Rican government (MINAET). Funding provided by start-up funds and NSF grant IOS-1207079 to S. O’D, and by the Organization for Tropical Studies Tyson Research Fellowship as well as the Academy of Natural Sciences of Drexel University McLean Fellowship to K. M. B.
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Baudier, K.M., O’Donnell, S. Structure and thermal biology of subterranean army ant bivouacs in tropical montane forests. Insect. Soc. 63, 467–476 (2016). https://doi.org/10.1007/s00040-016-0490-2
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DOI: https://doi.org/10.1007/s00040-016-0490-2