by Orin Courtenay *
The interrelationships between maned wolves, the "Lobeira"
fruit,
and leaf-cutting ants have possible implications for maned wolf
conservation.
The maned wolf, Chrysocyon brachyurus, is monotypic and endemic to central South America (Berta, 1987). Agricultural expansion and direct conflict with humans is reported to threaten the species in parts of its geographical range (Ginsberg & Macdonald, 1990). Nevertheless, observations indicate that the maned wolf is able to survive alterations to its preferred habitat (Dietz, 1984; R.Dias, pers. com.; pers. obs.), and that in the last 40 years the species' range, rather than diminishing in size, has altered in configuration (Dietz, 1985a). While reports that this vulnerable species is able to colonize potentially hostile environments are reassuring, without a reasonable understanding of the behavioural mechanisms behind such range expansions and delimitations, the efficiency of conservation strategies will be limited.
Here I summarise the results, to be reported in full elsewhere (Courtenay et al., in prep), of studies conducted in the Central Brazilian plateau, where the scrub forests and savanna, collectively called cerrado sensu lato (Eiten, 1972), is the threatened native habitat of the wolf in this part of its range. Field experiments focussed on the fruiting species Solanum lypocarpum, locally known as "Lobeira" or "fruit of the wolf", at IBGE reserve (15°56' S, 47°53' W) and the wildlife sanctuary at Fazenda Sao Miguel (SM) (15°50' S, 46°30' W) in Brazil.
Dietz (1984) was the first to report the high frequency of lobeira seeds in maned wolf faeces collected in the Serra da Canastra (19°30' S, 46°30' W), which accounted for more than half (58%) of the total scat volume. We found that an average 85% (±SD18.3) of scats collected per month at IBGE contained lobeira, and Gomes da Silva (1988) working further north still, in Chapada dos Guimarães (13°30' S, 47°45' W), concluded that the fruit comprised 38% of the wolf's diet. These locations represent the equivalent of an 800 km northwest-southeast transect across the central north-south limits of the species' range (see map below), thus, we conclude that the wolf's preference for this resource is not simply a local phenomenon.
Work on the phenology of lobeira at IBGE showed that, although fruits are produced all year round, availability to the wolf varies seasonally. In contrast, consumption by the wolf (measured by proportional faeces content) is constant throughout the year (c²11=13.1, p=0.29), showing no correlation with monthly fruit availability (r²9=0.12, p = 0.3). It has yet to be shown that the wolf seeks the fruit more actively during the less productive months, nevertheless, lobeiraµs year round predominance in the diet of an animal whose diet is otherwise dependent on food availability (Dietz, 1984) is indicative of the fruitµs substantial value to the wolf. We propose that the wolf's dependence on lobeira makes this fruit a potential indicator of suitable maned wolf habitats.
Lobeira is a fast growing woody shrub which reaches heights of 4-5m, and produces hermaphroditic blue flowers pollinated by bee species of the families Andrenidae, Anthophoridae, Apidae and Halictidae (Oliveira-Filho & Oliveira, 1988). Full-size ripening fruits, weighing 300-750 gm, emerge in December, which coincides with the first rains, and reach peak production in February/March. Thereafter, during the dry months, production tails off to a minimum.
We found that the germination success of seeds which had passed through the wolf's digestive tract (faeces derived), was significantly higher (c²2= 40.2, p<0.001) than for equivalent untreated seeds (fruit derived), when experimentally planted in local cerrado soil types. Indeed, germinating lobeira seeds were frequently seen in wolf faeces deposited along dirt roads in IBGE and SM.
In a 24 ha sample plot of undisturbed cerrado sensu stricto in the SM sanctuary, we discovered an entirely unexpected component in the wolf-lobeira relationship. Each of the 34 lobeira plants located in the plot, without exception, was situated on top of an individual ant mound belonging to one of two species of Attine leaf-cutter ants, Atta sexdens and A. laevigatus. These mounds measured up to a metre high, many of which had been cleared of all other existing vegetation by worker ants.
Observations revealed that foraging ants took both fruit and wolf faeces containing seeds into the nest, and that over a period of a week, at least 40% of the seeds marked for identification purposes, were ejected from the mound via specific exit holes, along with other refuse. The germination success of lobeira seeds was significantly greater when planted in this refuse matrix (the composite of fresh ant diggings, seeds and unidentified faecal pellets), than in cerrado soil types (c²2=56.5, p0.001). Moreover, in the ant substrate, faeces-derived and fruit-derived seeds germinated equally well.
The processes behind Lobeira dispersal and establishment in undisturbed cerrado s.s. thus seem to involve a number of mutually beneficial relationships between the ant, the wolf and the lobeira. The anomalous large size of the fruit would seem to restrict potential dispersal agents to larger frugivorous vertebrate species: consumption by the wolf is constant throughout the year, the germination success of these seeds is enhanced, and the seeds are dispersed over relatively large distances. Faeces were identified on termite and ant mounds where the topography obviously suits the wolfµs habit of depositing odorous territorial markers on high ground (Dietz, 1984). However, leaf-cutter ants also appear to facilitate seed location, either from a fruit or faeces source, and provide a suitable substrate for seed germination. Whether they further aid in plant establishment, by literally cutting down vegetative competition, has yet to be confirmed. The reciprocal benefit to the ant is, we presume, that wolf faeces and fruit are suitable fertilizers for the cultivation of their fungus gardens (Weber, 1972; 1982). For the maned wolf, apart from its nutritional reward, lobeira may prove to be of further benefit if its secondary compounds (Motidome et al., 1970) are shown to be an anthelmintic.
So how does human disturbance to the cerrado affect lobeira availability to the wolf? The SM wildlife sanctuary is only 20% of the 47,000ha commercial concern, owned by the Tocantin Cement Company, for the large scale production of fuel wood. Eucalyptus plantations are established by mechanically uprooting and burning the cerrado; the fazenda therefore comprises a mosaic of plots in various stages of development.
The abundance and distribution of lobeira was compared between the 24ha sample plot of undisturbed cerrado s.s. (mentioned above), and a 23 ha plot of disturbed cerrado s.s., outside the sanctuary, which had been cleared nine months earlier prior to future planting. Regeneration of cerrado species in this plot was limited. In the undisturbed plot, lobeiras were randomly distributed (compared with a random Poisson distribution, c²3=1.98, p=0.6), but not with respect to the ant mounds. In contrast, lobeira in the disturbed cerrado were not distributed at random (c²9=303.7, p<0.01), rather, they formed aggregations along the plot edges (dispersion index [following Krebs, 1989]=2.48). Our results were consistent with the known ecology of the plant as a fast-growing invasive species on disturbed ground (Oliveira-Filho & Oliveira, 1988): the distribution pattern in the latter area was the direct result of undamaged underground rhizomes giving rise to a number of new plants in the vicinity where old plants had once existed. Consequently, there was a greater density of lobeira in the cleared area than in the undisturbed cerrado, 6.7/ha and 0.6/ha, respectively. Vegetative regeneration was noticeably infrequent in the latter plot.
Therefore, in the immediate post-clearance phase, lobeira regeneration is relatively fast and the primary result of vegetative propagation. In the longer term we can only be reassured by the fact that lobeiras commonly occurred along the plantation access roads and on even the smallest patches of waste ground, and that maned wolves were frequently sighted in these same areas. Thus, we suspect that the wolf, and probably the typically invasive Attine ants, can continue their role in lobeira dispersal even in this degraded environment.
An optimistic conclusion is that small scale alterations to the cerrado s.l. (eg. dirt roads, patchily distributed pastures) have little effect on the wolfµs livelihood. The recent predominance of hooved livestock in cerrado regions may indeed aid in seed dispersal: casual observations indicate a preponderance of lobeira plants in cow pastures and corrals; cowboys have even been reported to produce the plant to fatten swine on the fruit (Correa, 1962). Larger scale operations may encourage net fruit production under certain circumstances, as it appears in the case of Fazenda SM where cleared cerrado plots are sometimes allowed to fallow prior to planting.
The extent of geographical sympatry of the maned wolf and the plant is not well documented. In Brazil at least, S. lypocarpum is reported to occur in the states of Minas Gerais, Goias, Matto Grosso and São Paolo (Correa, 1962; 1984; refs above), an area which includes much of the 0.5 million km² ex-forested zone, where the maned wolf has extended its range in recent years (Dietz, 1985a;b). Whether lobeira invasion following deforestation is a prerequisite for the colonization of previously unsuitable areas by the maned wolf remains to be shown.
Acknowledgements. This work was conducted with S. Gillingham, R, Dias, G. Almeida and T. Martin, during an Oxford Expedition to Brazil in 1991, which studied the ecology of the Hoary fox, Dusicyon vetulus.
Berta,A . 1987. Origin, Diversification, and Zoogeography of the South American Canidae. Fieldiana: Zoology, 39: 455-471.
Correa, M.P. (ed.) 1962. Dicionário das Plantas Uteis do Brasil.
Correa, M.P. 1984. Dicionário das plantas úteis do Brasil e exóticas cultivadas. Ministério da Agricultura, Instituto Brasileiro de Desenvolvimento Florestal, Brasília, 6v.
Courtenay, O., Gillingham, S., Dias, R., Almeida, G., & Martin, T. In prep. The Ant, the Wolf, and the Lobiera: a case of coevolution?
Dietz, J.M. 1984. Ecology and Social Organization of the Maned Wolf (Chrysocyon brachyurus). Smithsonian Contributions to Zoology 392. inc 1-51.
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Krebs, C.J. 1989. Ecological Methodology. Harper & Row, New York.
Motidome, M., Leekning, M.E. & Gottlieb, O.R. 1970. A Quimica de Solanaceas Brasileiras. 1 - A presenca de Solamargina e de Solasonina no Jua e na Lobeira. An. Acad. Brasil. Cienc. 42: 375-376.
Oliveira-Filho, A.T. & Oliveira, L.C.A. 1988. Biología floral de uma população de Solanum lycocarpum St.Hil. (Solanaceae) em Lavras, MG. Revta. Brasil. Bot. 11:23-32.
Weber, N.A. 1972. Gardening ants: the Attines. Memoirs of the American Philosophical Society, 92. Philadelphia pp.146.
Weber, N.A. 1982. Fungus ants. In: Social Insects (H.R. Hermann ed.), 4: 255-363. Academic Press, New York.
As a member of WildCRU, Orin Courtenay has worked on rabies ecology of carnivores in Saudi Arabia and the role of the crab-eating fox, Cerdocyon thous, in visceral leishmaniasis in Amazonian Brazil. He is presently employed at the London School of Hygiene and Tropical Medicine to continue studies on canine leishmaniasis in Brazil.
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