ALTHOUGH ant-plant mutualisms have been described in many ecosystems, the magnitude of the direct benefits from such relationships are hard to quantify. In Bako National Park, Sarawak, Malaysia, stunted ‘kerangas’ forests occur on nutrient-poor sandstone hills1-3. As trees are widely spaced and have a sparse leaf area, a significant amount of light reaches the tree trunks and enables a diverse community of epiphytes to thrive there4. One of these epiphytes, Dischidia major (Vahl) Merr. (Asclepiadaceae), has evolved unusual methods for enhancing carbon and nitrogen acquisition. We show here that a mutualistic relationship exists between ants of the genus Philidris and their host, D. major. Using stable isotope analysis, we calculate that 39% of the carbon in occupied host plant leaves is derived from ant-related respiration, and that 29% of the host nitrogen is derived from debris deposited into the leaf cavities by ants. © 1995 Nature Publishing Groups. All Rights Reserved

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Treseder, Kathleen K

Davidson, Diane W

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UC IrvineUC Irvine Previously Published WorksTitleAbsorption of ant-provided carbon dioxide and nitrogen by a tropical epiphytePermalinkhttps://escholarship.org/uc/item/2rp5h54xJournalNature, 375(6527)ISSN0028-0836AuthorsTreseder, Kathleen KDavidson, Diane WEhleringer, James RPublication Date1995-05-01DOI10.1038/375137a0Copyright InformationThis work is made available under the terms of a Creative Commons Attribution License, availalbe at https://creativecommons.org/licenses/by/4.0/ Peer reviewedeScholarship.org Powered by the California Digital LibraryUniversity of CaliforniaAbsorption of ant-provided carbon dioxide and nitrogen by a tropical epiphyte Kathleen K. Treseder*, Diane W. Davidson & James R. Ehlerlnger Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA ALTHOUGH ant-plant mutualisms have been described in many ecosystems, the magnitude of the direct benefits from such relation­ships are hard to quantify. In Bako National Park, Sarawak, Malaysia, stunted 'kerangas' forests occur on nutrient-poor sand­stone hills 1-3• As trees are widely spaced and have a sparse leafarea, a significant amount of light reaches the tree trunks and enables a diverse community of epiphytes to thrive there4• One of these epiphytes, Dischidia major (Yahl) Merr. (Asclepiadaceae), has evolved unusual methods for enhancing carbon and nitrogen acquisition. We show here that a mutualistic relationship exists between ants of the genus Philidris and their host, D. major. Using stable isotope analysis, we calculate that 39% of the carbon in occupied host plant leaves is derived from ant-related respiration, and that 29% of the host nitrogen is derived from debris deposited into the leaf cavities by ants. In addition to small coin-shaped leaves, D. major has evolved sac-like 'ant leaves' (Fig. I), in which ants of the genus Philidris5 (Dolichoderinae) frequently raise young and deposit debris (faeces, dead ants and scavenged insect parts)4·6 . Adventitious roots from D. m11jor grow through the cavity opening and prolif­erate wherever debris has accumulated4 • It has been proposed • Present address: Department or Biological Sciences. Stanford University, Stanford, California 94305, USA. NATURE · VOL 375 · 11 MAY 1995 LETTERS TO NATURE that the Dischidi11-Philidris relationship is mutualistic and that D. major uses ant debris as a nitrogen source4 ; also, the stomataon the internal surfaces of leaf cavities7 9 may absorb ant­respired carbon dioxide and thereby reduce transpirational waterloss8•9 , but neither of these suggestions is supported by experi­mental evidence.We tested these hypotheses by measuring stable isotope ratios (8 13C, 8 15N) of ants, hosts and substrates, and by capitalizing on differences in the isotope composition of possible nutrient sources. This approach enabled us to quantify the benefit to hosts from their symbiotic ants. The 8 13C value of Dischidia depends on both the 8 13C of thesource CO2 �813Cc0,) and discrimination during carbon fixation (.1 ), thus 8 1 Cp1an, = 0 13Cco, - .1. D. major has obligate crassula­cean acid metabolism (CAM)' 0·'1, and we found that uninhab-FIG. 1 Two ant-occupied leaves of Dischidia major: one is cut away to show adventitious roots and ant debris. The modified ant leaves are rolled up to form an enclosed abaxial surface and a cavity accessible through a small basal opening near the petiole4·6• Scale bar, 1 cm. 137 LETTERS TO NATURE ited plants had a mean 8 13Cp,an, value of -16.0%0, typical of CAM plants 12 • Given an atmospheric 8 13Cco, value of -7.9%0 (ref. 13), ,1 is calculated as 8.1%0. Ant respiration and decomposing debris are additional pos­sible sources of CO2 in ant-occupied leaves and could alter 8 13 Ceo,. The carbon isotope ratio of animals (and their respiration) is essentially the same as that of their food 14' 15 . Philidris antsfeed on the exudates of Homoptera4 that ingest the phloem of C3 rainforest trees. Subsequently, the ants have low 813C values averaging -25.9%0 (Fig. 2). o 13Cco, used for photosynthesis by D. major could vary from -7.9%0, ifno ant-derived CO2 is takenup, to -25.9%0, if ant-derived CO2 accounts for all fixed CO2 ,The corresponding 8 13Cpian, values would be expected to varyfrom -16%0 to -34%0.If D. major incorporates 1 3C-deficient carbon dioxide respired by the ants or their debris, colonized leaves should have lower 8 13C values than do uncolonized leaves. In addi­tion, as colonies deposit debris inside a leaf only after they have raised brood there for some time4, ant leaves with debris should have had a longer time to accumulate ant-respired CO2 • Overall, completely vacant leaves should have the highest 8 13C values (about -16.0%0), followed by ant-occupied leaves that are debris-free, and finally, by debris-filled leaves. The three groups followed the expected pattern (Fig. 2). Therefore individuals of D. major take up significant amounts of carbon from Philidris. To estimate the fraction of plant carbon derived from ant­related respiration (per cent CO2 from ants), we used the two­member mixing model: 8 13C + ii- 8 13C 01 CO f t = plant CO2.aim X JQO0/10 2 rom an s 13 13 10 8 · Cant - o · Cco,.a,mwhere 8 13Cco,.atm and o 13Can , are the isotope compositions of the atmosphere and ants, respectively. We calculated the fraction of plant carbon derived from ant-related respiration as 39% (±8%, n = 5) for ant-occupied, debris-filled leaves; 27% (±4%, -8 Atmosptierlc CO -12-16 2 -20 0 00 .J. T -24 0 .J. Ants and ant debris -28Unoccupied Occupied Occupied leaves leaves leaves with no with debris debris FIG. 2 Mean carbon isotope values ±1 s.e. for Dischidia major ant leaves and the potential CO2 sources for these leaves (atmospheric CO2 (-7.9%0), ants (-25.9%0±0.3, n = 6), or ant debris (-25.9%0±0.9, n = 3); shaded bars). Values differed significantly for the three groups of ant leaves (H15 ,5 ,61 = 9.510, P< 0.009). 813C values of ant-related debris, a possible source of carbon dioxide, did not differ significantly from those of the ants (U13.6J = 12, P=0.731). METHODS. Material was collected along the Lintang trail in Bako National Park, Sarawak, Malaysia in August 1993. With an isotope ratio mass spectrometer (Delta S, Finnigan MAT at SIRFER, University of Utah, Salt Lake City), isotope ratios of ants, leaves and ant debris were measured on 2-3 mg samples. Isotope compositions are reported in 813C values as 813C=[(13C/2Csamp1e)/(13C;12Cstandard)-1] X 1,000%0, where 13C/12Csample and 13C;12Cstandard are the isotope ratios of thesample and standard, respectively25. 138 n = 6) for ant-occupied leaves without debris; and 4% ( ±4%, n = 6) for vacant leaves.For ant-related CO2 to contribute so significantly to the car­bon balance of the plant, the CO2 concentration inside ant­occupied leaves should be raised above atmospheric values. By having interior stomata fed by an increased CO2 concentration, the plant probably significantly increases its water-use efficiency (photosynthetic carbon gain to transpirational water loss). The capture of ant-respired CO2 may increase carbon gain (enhanc­ing growth) and also reduce transpiration by curbing stomata! activity. Moreover, the interior stomata transpire into a partially enclosed cavity, where relative humidity should be higher than the surrounding atmosphere, resulting in further reduction in transpiration. Although D. major grows in a tropical climate, water loss is a concern because the epiphytes have no access to soil water. D. major also exploits ant-deposited debris as a nitrogensource, and we used nitrogen isotope analysis to quantify the extent of this (the other likely nitrogen source, rainwater, has o 15N values different from ant-provided debris). Dischidia num­mularia, which does not possess ant leaves but grows on the same host trees as D. major, has access to the same nitrogen sources, with the exception of the ant-provided debris. We found that the mean 8 15Npiant value of D. nummularia was -3.5%0; in contrast, debris deposited in the ant leaves of D. major was significantly more enriched in 15N ( Urs.21 = 0, P < 0.05; Fig. 3).This is expected, given that ant debris is composed mostly of scavenged insect parts4, and animal 8 15N values tend to be 3%o greater than those of their food sources 16• D. major leaves weresignificantly enriched in 15N compared to those of D. nummularia (Ur11.21 = 2, P<0.05; Fig. 3), suggesting that D. major absorbs nitrogen from ant-deposited debris. On average, D. major received about 29% of its nitrogen from ant debris (Fig. 3). Ant­related nitrogen could provide a large benefit to D. major, as nitrogen deficiency may be the major factor limiting epiphytic growth in the light-rich kerangas forests17 • 2 T 0 .I. 0 z -2 0 I() 00 0 -4 --6 Ant debris Oischidia Dischidia major nummularia FIG. 3 Mean nitrogen isotope values (±1 s.e.) for ant debris (n = 5) and random leaves of Dischidia major (n = 17) and D. nummularia (n = 2). Experimental procedure is described in Fig. 2 legend. Standard error bars are not visible when the standard error is smaller than the plot symbol. For D. major, we calculated the per cent nitrogen content from ant debris as 815N -815N % N from ant debris= 15 O.ma/or 15 D.nummularia X 100%8 Nant debris - /j No.nummularia where 815No.maJo, and 815No.nummularia are the nitrogen isotope ratios of leaves of the two respective species. On average, D. major received 29% of its nitrogen from ant debris. (This estimate is conservative, as both D. major and D. nummularia often grow roots into ant carton (a mache used for nest building) located on the host tree trunks, and the epiphyte may exploit this source as well17 .) NATURE · VOL 375 · 11 MAY 1995 Our observations strongly support Janzen's4 and Huxley's8•9 hypotheses of mutualism between D. major and Philidris. In exchange for shelter, ants provide significant amounts of two limiting resources: carbon dioxide and nitrogen. Both features could either expand the realized niche of D. major, enabling it to colonize hotter, drier habitats, or could provide D. major with a competitive edge over other epiphytes in this nutrient-poor ecosystem. Finally, epiphytes in other tropical regions (including those of Central and South America, Papua New Guinea, the Philip­pines and Australia) have various structures occupied by ants4•8 •9• 17 23. In a facultative myrmecophytic relationship involv­ing an ant-occupied orchid from the neotropics, Fisher et al.24 have used stable carbon isotopes to quantify the extent to which ants may forage on their own host plant. We may eventually be able to combine the two approaches and examine reciprocal benefits between plants and ants. □Received 12 August 1994; accepted 28 March 1995. 1. Anderson, J. A. R. Gdns Bull. Singapore 20, 131-228 (1963). 2. BrGnig, E. F. w. 0. UNESCO Symp. Ecol. Res. Humid Trop. Vegn. Kuching 1913, 289-313 (1965). 3. Ashton, P. S. Malayan Nature J. 24, 151-162 (1971). 4. Janzen, D. H. Biotropica I, 237-259 (1974). LETTERS TO NATURE 5. Shattuck, S. o. Sociobiology 21, 1-181 (1992). 6. Kerr, A. F. G. Br. Sclent. Proc. R. Dub/. Soc.13, 293-309 (1912). 7. Griffith. W. Trans. Linn. Soc. Lond. 20, 387-390 (1846). 8. Huxley, C. R. Biol. Rev. II, 321-340 (1980). 9. Huxley, C. R. in Insects and the Plant Surface (eds Juniper. B. & Southwood, R.) 255-282 (Arnold, London, 1986). 10. Winter, K., Wallace, 8. J., S tocker, G. C. & Roksandic, z. Oecologia 17, 129-141 (1983). 11. Treseder, K. K. thesis, Univ. Utah (1994). 12 Farquhar, G. D, Ehlerlnger, J. R. & Hubick, K. T. A. Rev. Pl. Phys/of. molec. Biol. 40, 503-537 (1989). 13. Keeling. C. D., Mook, w. G. & Tans. P. P. Nature 277, 121-123 (1979). 14. DeNiro, M. J. & Epstein, S. Geo/. Soc. Am. Abstr. Prog. 8, 834-835 (1976). 15. DeNlro, M. J. & Epstein, s. Geochim. cosmochim. Acta 42, 495-506 (1978). 16. Schoeninger, M. J. & DeNiro, M. J. Geochim. cosmochim. Acta 48, 625-639 (1984). 17. Davidson, D. W. & Epstein, W.W. in Vascular Plants as Epiphytes (ed. Lunge, U.) 200-233 (Springer, Heidelberg, 1989). 18. Rico-Gray, V., Barber, J. T., Thien, L. B., Ellgaard, E. G. & Toney, J. J. Am. J. Bot. 71, 603-608 ( 1989). 19. Benzing, D. H. Bull. Torrey Bot. 97, 109-115 (1970). 20. Madison, M. Se/byana I, 107-115 (1979). 21. Gay, H. Biol. J. Linn. Soc. Lond. lO, 221-233 (1993). 22. Huxley, C. R. New Phyto/. 80, 231-268 (1978). 23. Rickson, F. R. Am. J. Bot. ff, 87-90 (1979). 24. Fisher, B. L, Sternberg, l. S. l. & Price. D. Oeco/ol{ia 83, 263-266 (1990). 25. Ehleringer, J. R. & Osmond, C. B. in Plant Physiological Ecology (eds Pearcy, R. W., Ehleringer, J. R., Mooney, H. A. & Rundel, P. W.) 281-300 (Chapman & Hall, London, 1991). ACKNOWLEDGEMENTS. We thank D. R. Sandquist for advice, discussions and critical reading of the manuscript; B E. Howlett for help in the field; E. Medina and T. G. Whitham for comments on the manuscript; and C. S. Cook. A. l Leffler and C. F. Kitty for technical assistance. ThiS work was supported by grants from the Explorer's Club, Sigma Xi, NSF, and the HHMI Undergraduate Research Program (University o( Utah). 139 

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Absorption of ant-provided carbon dioxide and nitrogen by a tropical epiphyte

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