We document a facultative Bartonella-like Rhizobiales bacterium in the giant tropical ant, Paraponera clavata. In a lowland tropical rainforest in Costa Rica, 59 colonies were assayed for the prevalence of the Bartonella-like bacterium (BLB), 14 of which were positive. We addressed three questions: First, how does the prevalence of BLB within colonies vary with environmental conditions? Second, how does diet affect the prevalence of BLB in P. clavata? Third, how does the distribution of BLB among colonies reflect ambient differences in food resources and foraging habits? A variety of environmental variables that may be predictive of the presence of BLB were measured, and diet manipulations were conducted to test whether the prevalence of BLB responded to supplemental carbohydrate or prey. The ambient frequency of BLB is much higher in young secondary forests, but is nearly absent from older secondary forests. The prevalence of BLB inside field colonies increased over the duration of a 2-week carbohydrate supplementation; however, water and prey supplementation did not alter the prevalence of BLB. The diets of the colonies located in young secondary forest, compared to other habitats, have a diet richer in carbohydrates and lower in prey. The abundance of carbohydrate, or the relative lack of N, in a colony’s diet influences the occurrence of the BLB microbe in P. clavata. As experimental diet manipulations can affect the facultative presence of an N-cycling microbe, a consistent diet shift in diet may facilitate the emergence of tighter symbioses.
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Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu YI, Basinger U, Mott BM, Buck N, Wheeler DE (2012) Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 21:2282–2296
Belk MC, Black HL, Jorgensen CD, Hubbell SP, Foster RB (1989) Nest tree selectivity by the tropical ant, Paraponera clavata. Biotropica 21:173–177
Bennett B, Breed MD (1985) On the association between Pentaclethra macroloba (Mimosaceae) and Paraponera clavata (Hymenoptera: Formicidae) colonies. Biotropica 17:253–255
Bentley BL (1976) Plants bearing extrafloral nectaries and the associated ant community: interhabitat differences in the reduction of herbivore damage. Ecology 57:815–820
Blüthgen N, Gebauer G, Fiedler K (2003) Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community. Oecologia 137:426–435
Blüthgen N, Gottsberger G, Konrad F (2004) Sugar and amino acid composition of ant-attended nectar and honeydew sources from an Australian rainforest. Austral Ecology 29: 418-429
Breed MD, Bennett B (1985) Mass recruitment to nectar sources in Paraponera clavata: a field study. Insect Soc 32:198–208
Breed MD, Fewell JH, Moore AJ, Williams KR (1987) Graded recruitment in a ponerine ant. Behav Ecol Sociobiol 20(6):407–411
Clark DA (2002) Are tropical forests an important carbon sink? Reanalysis of the long-term plot data. Ecol Appl 12:3–7
Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson JR, Ni J (2001) Measuring net primary production in forests: concepts and field methods. Ecol Appl 11:356–370
Cook SC, Davidson DW (2006) Nutritional and functional biology of exudate-feeding ants. Entomol Exp Appl 118:1–10
Davidson DW, Cook SC, Snelling RR (2004) Liquid-feeding performances of ants (Formicidae): ecological and evolutionary implications. Oecologia 139:255–266
Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47
Dyer LA (2002) A quantification of predation rates, indirect positive effects on plants, and foraging variation of the giant tropical ant, Paraponera clavata. J Insect Sci 2:18
Dyer LA, Floyd T (1993) Determinants of predation on phytophagous insects: the importance of diet breadth. Oecologia 96:575–582
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13:223–234
Gil R, Latorre A, Moya A (2004) Bacterial endosymbionts of insects: insights from comparative genomics. Environ Microbiol 6:1109–1122
Janzen DH, Carroll CR (1983) Paraponera clavata (bala, giant tropical ant). In: Janzen DH (ed) Costa Rican natural history. University of Chicago, Chicago, pp 752–753
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
Ludwig W, Strunk O, Westram R, Strehlow R et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
McDade L, Bawa KS, Hespenheide HA, Hartshorn GS (1994) La Selva: ecology and natural history of a neotropical rain forest. University of Chicago, Chicago
Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T (2010) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 38:23–28
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Ronquist F, Huelsenbeck J (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci 106:21236–21241
Schmidt JO, Blum MS, Overal WL (1984) Hemolytic activities of stinging insect venoms. Arch Insect Biochem Physiol 1:155–160
Stoll S, Gadau J, Gross R, Feldhaar H (2007) Bacterial microbiota associated with ants of the genus Tetraponera. Biol J Linn Soc 90:399–412
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tillberg CV, Breed MD (2004) Placing an omnivore in a complex food web: dietary contributions to adult biomass of an ant. Biotropica 36:266–272
Van Borm S, Buschinger A, Boomsma JJ, Billen J (2002) Tetraponera ants have gut symbionts related to nitrogen-fixing root-nodule bacteria. Proc R Soc Lond Ser B 269:2023–2027
Wolf BO, Hatch KA (2011) Aloe nectar, birds and stable isotopes: opportunities for quantifying trophic interactions. Ibis 153:1–3
Yanoviak SP, Silveri C, Hamm CA, Solis M (2012) Stem characteristics and ant body size in a Costa Rican rain forest. J Trop Ecol 28:199–204
Young AM, Hermann HR (1980) Notes on foraging of the giant tropical ant Paraponera clavata (Hymenoptera: Formicidae: Ponerinae). J Kans Ent Soc 53: 35–55
This project was conducted under the support of the National Science Foundation (OISE-1130156 and HRD-0802628). A. Haskell and F. Burt provided some early input, and we thank P. Tellez for the assistance in the field. We particularly thank Danilo Brenes and Bernal Matarrita for their consistent support in the lab and field.
Sequences from five ants are deposited into GenBank, with the following accession numbers: KC478384, KC478385, KC478386, KC478387, and KC478388.
Communicated by: Sven Thatje
Electronic supplementary material
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Spatial distribution of colonies with and without BLB throughout La Selva Biological Station. (PDF 54 kb)
P. clavata-associated bacterium, in a transmission electron micrograph of a section of the midgut of an individual worker from a BLB+ colony. Scale bars are 2 υm and 0.5 υm, respectively, for panels A and B. (PDF 1573 kb)
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Larson, H.K., Goffredi, S.K., Parra, E.L. et al. Distribution and dietary regulation of an associated facultative Rhizobiales-related bacterium in the omnivorous giant tropical ant, Paraponera clavata . Naturwissenschaften 101, 397–406 (2014). https://doi.org/10.1007/s00114-014-1168-0