Structure and thermal biology of subterranean army ant bivouacs in tropical montane forests

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 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

    Article  Google Scholar 

  2. Anderson C, Theraulaz G, Deneubourg JL (2002) Self-assemblages in insect societies. Insect Soc 49:99–110

    Article  Google Scholar 

  3. Barth M, Moritz R, Kraus F (2015) Genetic differentiation at species level in the Neotropical army ant Labidus praedator. Insect Soc 62:299–306

    Article  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    CAS  Article  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. Dunn R (2003) Imposter in the nest. Nat Hist 112:22–26

    Google Scholar 

  13. Economo E, Guénard B (2016) AntMaps. http://antmaps.org. Accessed 20 Feb 2016

  14. Eickwort GC (1990) Associations of mites with social insects. Annu Rev Entomol 35:469–488

    Article  Google Scholar 

  15. Fowler HG (1979) Notes on Labidus praedator (Fr. Smith) in Paraguay (Hymenoptera: Formicidae: Dorylinae: Ecitonini). J Nat Hist 13:3–10

    Article  Google Scholar 

  16. 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

    Google Scholar 

  17. Franks NR (1989) Thermal regulation in army ant bivouacs. Physiol Entomol 14:397–404

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    CAS  Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. Gotwald WH (1995) Army ants: the biology of social predation. Comstock, Ithaca

    Google Scholar 

  22. Harkness R, Wehner R (1977) Cataglyphis. Endeavour 1:115–121

    Article  Google Scholar 

  23. Heinrich B (1993) The hot-blooded insects: strategies and mechanisms of thermoregulation. Springer, Berlin Heidelberg, pp 457–495

    Google Scholar 

  24. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Google Scholar 

  25. Jackson WB (1957) Microclimatic patterns in the army ant bivouac. Ecology 38:276–285

    Article  Google Scholar 

  26. Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. Jones JC, Oldroyd BP (2007) Nest thermoregulation in social insects. Adv Insect Physiol 33:153–191

    Article  Google Scholar 

  29. Kadochová Š, Frouz J (2014) Red wood ants Formica polyctena switch off active thermoregulation of the nest in autumn. Insect Soc 61:297–306

    Article  Google Scholar 

  30. 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

    Google Scholar 

  31. Kipyatkov VE, Lopatina EB (2015) Comparative study of thermal reaction norms for development in ants. Entomol Sci 18:174–192

    Article  Google Scholar 

  32. Longino JT (2010) Ants of Costa Rica. http://academic.evergreen.edu/projects/ants/AntsofCostaRica.html. Accessed 20 Feb 2016

  33. Loomis H (1959) New myrmecophilous millipeds from Barro Colorado Island, Canal Zone, and Mexico. J Kansas Entomol Soc 32:1–7

    Google Scholar 

  34. 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

    Article  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    Article  Google Scholar 

  37. Nadkarni NM, Wheelwright NT (2000) Monteverde: ecology and conservation of a tropical cloud forest. Oxford University Press, Oxford

    Google Scholar 

  38. Nalepa CA (2011) Body size and termite evolution. Evol Biol 38:243–257

    Article  Google Scholar 

  39. Oberg EW, Toro I, Pelini SL (2012) Characterization of the thermal tolerances of forest ants of New England. Insect Soc 59:167–174

    Article  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecol News 22:65–108

    Google Scholar 

  43. Parton WJ, Logan JA (1981) A model for diurnal variation in soil and air temperature. Agr Meteorol 23:205–216

    Article  Google Scholar 

  44. Penick CA, Tschinkel W (2008) Thermoregulatory brood transport in the fire ant, Solenopsis invicta. Insect Soc 55:176–182

    Article  Google Scholar 

  45. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  46. Rettenmeyer CW (1962a) Arthropods associated with neo-tropical army ants with a review of the behavior of these ants. Dissertation, University of Kansas

  47. Rettenmeyer CW (1962b) The behavior of millipeds found with Neotropical army ants. J Kansas Entomol Soc 35:377–384

    Google Scholar 

  48. Rettenmeyer CW (1963) Behavioral studies of army ants. Univ Kans Sci Bull 44:281–465

    Google Scholar 

  49. 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

    Article  Google Scholar 

  50. Schneirla TC (1933) Studies on army ant raids in Panama. J Comp Psychol 15:267

    Article  Google Scholar 

  51. 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

    Google Scholar 

  52. 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

    Article  Google Scholar 

  53. 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

    Google Scholar 

  54. 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

    Article  Google Scholar 

  55. 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

    Article  PubMed  Google Scholar 

  56. Sudd JH (1972) Review of army ants, a study in social organization. Sci Prog 60:570–573

    Google Scholar 

  57. 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

    Google Scholar 

  58. Tschinkel W (1987) Seasonal life history and nest architecture of a winter-active ant, Prenolepis imparis. Insect Soc 34:143–164

    Article  Google Scholar 

  59. Watkins JF (1976) The identification and distribution of new world army ants (Dorylinae: Formicidae). Baylor University Press, Waco

    Google Scholar 

  60. 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

    Article  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to K. M. Baudier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 4976 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Labidus praedator
  • Dorylinae
  • Homeostasis
  • Thermoregulation
  • Nest architecture
  • Microclimate
  • Soil buffering
  • Myrmecophile