Rev. Biol. Trop., 31(2) : 213-216, 1983

Latitudinal gradients and diversity of the leaf-cutting (A tta and Acromyrmex ) ( : Formicidae)

Harold G. Fowler Department of Entomology & Economic Zoology, Cook College, New Jersey Agricultura! Experiment Station, Rutgers University, New Brunswick, New Jersey 08903. Present address: Department of Entomology, University of Florida, Gainesville, Florida 32611 U.S.A.

(Received for publication February 28, 1983)

Abstraet: Current biogeographic patterns of the 12 genera of the gardening tribe Attini are examined. Six of the genera are more concentrated in the southern subtropics of South America, and the true leaf-cut­ ting ants, Atta and Acromyrmex, markedIy so. No pattern of taxonomic diversity following phylogeny emerges, and the hypothesis that leaf-cutting ants evolved in the tropical rain-forest cannot be assumed to be confumed. The taxonomic diversity of attine ants on Caribbean islands was examined in terms of biogeo­ graphic theory. Island surface area and distan ce from the mainland were important in predicting numbers present, yet these two factors only explained less than 50% of the observed taxonomic diversity.

Taxa of the Neotropical Myrmicine relatively young group. Moreover, the absence tribe Attini all cultivate a garden of symbiotic of attines from the westerncoasts of Chile and fu ngi, and collectively are known as gardening­ Perú suggests their evolution after the formation ants. Attines are gene rally abundant in Neo­ of the Andes, and a drastically reduced taxo­ tropical habitats, and are among the most nomic diversity in Central America northward characteristic faunal markers of the Neotropics. also attests to their re1atively late evolution. Two genera of attines, Atta and Acromyrmex, Here, 1 examine the biogeographic patterns of depend almost exclusively upon fresh1y har­ the attines on a large scale, and discuss these vested vegetation as a fungal garden substrate, findings in terms of our current hypothesis and constitute the true leaf-cutting ants. The concerning the evolution and behavior of this remaining genera, except for Pseudo atta which unique group of ants. is an obligate social parasite, collect fallen vegetation and frass as a fu ngal substrate, although occasionally may, in the case of METHODS Trachymyrmex, harvest small amounts of vegetation. Thus, al1 attines may be viewed as Although detailed measures of species components of the decomposer food web, diversity have been proposed, most indices rely although both taxa of Atta and Acromyrmex upon a knowledge of the relative abundances of proximately affect the ecosystem as herbivores. the component taxa (Pielou, 1977). Few It is common1y assumed that the attines are quantitative studies are avaible on the com­ of a tropical derivation. For example, Weber position of leaf-cutting ant communities (1972) proposed that the Attini evolved in the (Fowler, 1983). Therefore, the measure of moist tropical lowlands of northem South taxonomic diversity employed here is the America. However, no attine fossils have ever number of described taxa per 100 latitude in been recovered, and their strictly Neotropical width. Data were taken from Kempfs (1972) distribution suggests that the attines are a catalog, and were supplemented by recent records (Fowler, 1980). Only species level taxons were included in the following discus­ * New Jersey Agricultural Experiment Publication sion. No. D-08001-20-82,supported by state funds.

213 214 REVIST A DE BIOLOGIATROPICAL

leaf-cutting ants. It is possible that the concen­ tration of taxa of Atta and Acromyrmex in the southern subtropics of South America is a reflection of posterior diversification of a parent stock from the tropics, a sub tropical origin of this group is just as possible based upon the available data. Because the attines are markedly Neotropical in distribution, we may assume that they evolved after the fragmentation of Gondwanaland, and are consequently not present in Africa. Similar patterns are present in many exomalopsine and nomadine genera 01' bees (Michener, 1979). The taxa present in the Antillean islands (Fig. 1) may give sorne elue to the dispersal ability of the various genera of attines, and, perhaps, give us ad­ ditional clues on their antiquity. Although attine ants. are abundant on the mainland of South America (193 species), only 32-33 species (- 19% ) are present on Carib­ bean islands, with Trinidad and Tobago, lying just off the coast, having the largest number of recorded species. Fitting the standard formula Fig. 1. The taxonomic richness for each of relating species to island area (MacArthur and 100 attine ants per latitudinal bando Genera are Wilson, 1967), we obtain S = CAO.2 05 , for all arranged in assumed phylogcnetic order, from islands. Exeluding Trinidad and Tobago, the Cyphomyrmex through Atta, and plots demostrate .239 the percentage of described species fr om that genus relationship is S = CAO . Goodness of fit per latitudinal bando islands refer to the percentage tests for all islands vs islands exeludingTrinidad of the described taxa that occur in the Anti111ean and Tobago (F = 2.74, P = 0.1258, R2 = 0.200; island chain. and F = 17.34, P = 0.0024, R2 = 0.658, respectively) indicate that the influence of RESULTS Trinidad and Tobago on the species-area relationship is great. In essence, Trinidad and Latitudinal ranges were represented graph­ Tobago may be best considered as continental. ically in terms of the percent of the number of To fu rther evaluate this relationship, a multiple described taxa occurring in succesive latitudinal linear regression was performed to account for belts for all recognized genera of attines (Fig. surface area, distance from the mainland, and 1). Taxa of the true leaf-cutting ants, Atta and their interaction. These results are summarized Acromyrmex, and their associated parasitic in Table 1. When considered separately, area genus Pseudoatta, are all concentrated in the has the greatest effect, followed by distan ce southern subtropics. Other genera with de­ from the mainland. However, considering all cidedly southern sub tropical distributions in­ factors simultaneously, no one factor can be isolated as being the most important (Type IV elude My cetosorites, My ce top hy lax, and My cetarotes. Tropically centered distributions SS; Table 1). are found in Cyphomyrmex, My cocepurus, My rmicocrypta, Ap teros tigma, Sericomyrmex DISCUSSION and Trachymyrmex. As these taxa are arranged in the assumed phylogeny of evolution, based Contemporary biogeographic patterns of the upon morphological and behavioral traits attine ants discussed here fail to provide a co­ (Weber, 1972), it is difficult to interpret the herent picture of the evolution of this unique contemporary distributions along phylogenetic group. The relatively depauperate fauna of the paths. Based on contemporary distributions, it Caribbean islands, although amenable to island is also difficult to ascribe a tropical origin to biogeographic analysis, suggests that these ants FOWLER: Latitudinal gradients and diversity of leaf-cutting ants 215

TABLE 1

Analysis of varwnce of the relative contribution of distance from the mainland and island surface area on th e occu"ence of species of attine ants on th e Caribbean islands. All variables entered are natural logs

Source D.F. Type I. SS Mean Square F Type IV SS

Ln (km from mainland) 2.9578** 0.2117

Ln (island surface area) 5.8072** 0.0616

Lnkm x LnHa 0.0008 0.0009

Total 3 8.í658 2.9219 12.27

Error 9 2.1439 0.2382

Corrected total 12 10.9098

** P 0.05 may have evolved late in the Tertiary Period, ing the distinctly sub-tropical distribution of which may also explain their absence from the Atta and Acromynnex. A combination of high western coasts of South America, as the Andes rates of predation and high plant allelochemic are also of Tertiary origino diversity may work hand in hand to promote a More importantly, these patterns shed sorne pronounced pattern of higher colony incidences doubt as to the tropical forest origin of the in structurally less complex habitats (Fowler, leaf-cutting ants, Atta and Acromynnex. Bio­ 1983). As tropical forests are also more struc­ geographic patterns of these ants run contrary turally complex (Fowler and Stiles, 1980), to reported patterns for lizards (pianka, 1966), polyphagism in harvesting vegetation may mammals (Simpson, 1964; Wilson, 1974), necessarily be too pronouced, and optimal time swallowtail butterflies (Slansky, 1973), and and space windows for harvesting suitable vege­ ants as a whole (Kusnezov, 1957; Fischer, tation for fungal substrate too short and varia­ 1960). However, these patterns fit remarkably ble (Fow1er and Stiles, 1980), to permit effi­ well with the patterns of specializations re­ cient resource tracking and harvest. Conversely, ported for xylomycetophagous beetles (Beaver, the trend toward resource specialization as­ 1979), which likewise depend upon fungus for sumed for tropical (Dobzansky, 1950) food. It is well documented that there exist may be too intense, and indeed work contrary latitudinal clines in the occurrences of plant to the possible low levels of allelochemic deto­ allelochemics which in crease in concentration xification allowed by the fungus garden. as one approaches the tropics, such as a1kaloids Finally, many taxa of Atta and Acromynnex (Levin, 1971). These compounds are generally are restricted to grasslands and ·harvest only highly fungicidal or fu ngistatic, and would thus grasses (Fowler, 1983). Sorne taxa also demon­ greatly limit the fu ngal growth of these ants, strate a strong congruence between present day which depend entirely upon fre shly harvested distributions and Pleistocene vegetational pat­ vegetation as a fu ngal resource, unlike the mi­ terns (Fowler and Haines, 1983). As the taxa of nor genera which utilize fallen vegetation and Acromynnex (Moellerius) are assumed to insect frass. High concentrations of allelo­ provide the evolutinary link to the inferred chemics would greatly influence fungal survival, more advanced taxa of Atta (Creighton, 1950), and thus ant survival. and as taxa of A. (Moellerius) are largely Rates and constancy of predation are also restricted to grasslands, the proportionally rarer assumed to be higher in the tropics (paine, expanses of grasslands in the tropics may well 1966), and especially by ants (Jeanne, 1979). help to explain the decreasing taxonomic diver­ High rates of predation may greatly influence sity as one approaches the tropics.A Pleistocene leaf-cutting ant colony survivorship, but pre­ link may also explain the depauperate taxo­ dation should affect all genera equally, and thus nomic diversity in Central and North America. cannot be considered the key factor in explain- These patterns may also shed sorne light on 216 REVISTA DE BIOLOGIA TROPICAL

the reversed cline of closer species packing Fowler, H. G. 1983. Distribution pattems of Para­ and implicit higher resource utilization to­ guayan leaf-cutting ants (Atta and Acro myrmex) ward the subtropics than has been predicted. (Hymenoptera: Formicidae : Attini) Stud. Neotrop. Fauna Environ. (in press).

ACKNOWLEDGEMENTS Fowler, H.G., & B.L. Haines . 1983. Diversidad de especies de hormigas cortadoras y termitas de tumulo en cuanto a la sucesión vegetal en pra­ 1 thank R.B. Roberts and M.D. Parrish for their thoughts on earlier versions of this draft. deras paraguayas. In P. Jaisson (e'd.). Social in­ sects in the tropics. Vo!. n. Univ. Paris, Paris (in press).

RESUMEN Fowler, H.G., & E.W. Stiles. 1980. Conservative resource management by leaf-cutting ants? The role of foraging trails and territorries and enviro n­ Los patrones biogeográficos actuales de los mental patchiness. Sociobiology, 5: 2541. 12 géneros de las hormigas jardineras de la tribu Attini indican que 6 de los géneros tienen con­ Jeanne, R.L. 1979. A latitudinal gradient in rates of centración taxonómica en los subtrópicos sure­ ant predation. Ecology, 60: 1211-1224. ños de Sur América. Entre estos 6 géneros se Kempf, W.W. 1972. Catálogo abreviado das formi­ encuentran las verdaderas hormigas cortadoras gas da Regiao Neotropical (Hymenoptera: Formi­ cidae). Stud. Entorno!., 15: 3-344. (zompopas en Centro América), Atta y Acro­ myrmex. No existe correlación entre la fJ.lo­ Kusnezov, N. 1957. Numbers of species of ants in genia de la tribu y la diversidad latitudinal de faunae of different latitudes. Evolution, 11: 298- sus miembros. La hipótesis de un origen tropi­ 299. cal de estas hormigas no se puede confirmar. Se examina la diversidad taxonómica de Attini Levin, D. A. 1971. Plant phenolics: an ecological en las islas del Caribe con respecto a la teoría perspective. Am' Nat., 105: 157-181. biogeográfica. El área de superficie y su distan­ MacArthur, R.B., & E.O. Wilson. 1967. The theory cia del continente fueron de mucha importan­ of Island Biogeography. Princeton Univ. Press, cia para calcular el número de especies; aunque Princeton. estos dos factores solamente explican menos Michener, C.D. 1979. Biogeography of bees. Ann. del 50% de la diversidad taxonómica en las Missouri Bot. Garden, 66: 277-347. islas del Caribe. Paine, R.T. 1966. Food web complexity and species diversity. Am. Nat., 100: 65-75.

LITERATURE CITED Pianka, E.C. 1966. Latitudinal gradients in species diversity : a review. Am. Nat., 100: 3346.

Beaver, R.A. 1979. Host specificity of temperate and Pielou, E. C. 1977. Mathematical Ecology . John tropical animals. Nature, 281: 139-141. Wi!ey & Sons, New York.

Creighton, W.S. 1950. The ants of North America. Simpson, G.G. 1964. Species diversity of North Amer­ Bull. Mus. Comp. Zoo!., 104: 1-585. ican recent mammals. Syst. Zoo!., 13: 57-63.

Dobzhansky, T. 195 O. Evolution in the tropics. Am. Slansky, F., Jr. 1973. Latitudinal gradients in the species diversity of the New World swallowtail ScL, 39: 209-221. butterflies. J. Res. Lepidop., 11: 201-217. Fischer, A.G. 1960. Latitudinal variations in organic diversity. Evolution, 14: 64-81. Weber, N.A. 1972. Gardening ants: the attines. Mem. Am. Phi!. Soc., 92: 1-146. Fowler, H.G. 1980. Nuevos registros de hormigas para el Paraguay (Hymenoptera : Formicidae). Wi!son, H. 1974. Analytical zoogeography of North Neotropica, 26: 183-186. American mammals. Evolution, 28 : 124-140.