Trees Duroia Hirsuta Ants in 'Devil's Gardens' Is Increased Herbivory On
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Downloaded from rspb.royalsocietypublishing.org on January 9, 2012 The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in 'devil's gardens' is increased herbivory on Duroia hirsuta trees Megan E Frederickson and Deborah M Gordon Proc. R. Soc. B 2007 274, 1117-1123 doi: 10.1098/rspb.2006.0415 References This article cites 40 articles http://rspb.royalsocietypublishing.org/content/274/1613/1117.full.html#ref-list-1 Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on January 9, 2012 Proc. R. Soc. B (2007) 274, 1117–1123 doi:10.1098/rspb.2006.0415 Published online 13 February 2007 The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in ‘devil’s gardens’ is increased herbivory on Duroia hirsuta trees Megan E. Frederickson* and Deborah M. Gordon Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020, USA ‘Devil’s gardens’ are nearly pure stands of the myrmecophyte, Duroia hirsuta, that occur in Amazonian rainforests. Devil’s gardens are created by Myrmelachista schumanni ants, which nest in D. hirsuta trees and kill other plants using formic acid as an herbicide. Here, we show that this ant–plant mutualism has an associated cost; by making devil’s gardens, M. schumanni increases herbivory on D. hirsuta. We measured standing leaf herbivory on D. hirsuta trees and found that they sustain higher herbivory inside than outside devil’s gardens. We also measured the rate of herbivory on nursery-grown D. hirsuta saplings planted inside and outside devil’s gardens in ant-exclusion and control treatments. We found that when we excluded ants, herbivory on D. hirsuta was higher inside than outside devil’s gardens. These results suggest that devil’s gardens are a concentrated resource for herbivores. Myrmelachista schumanni workers defend D. hirsuta against herbivores, but do not fully counterbalance the high herbivore pressure in devil’s gardens. We suggest that high herbivory may limit the spread of devil’s gardens, possibly explaining why devil’s gardens do not overrun Amazonian rainforests. Keywords: ant–plant interactions; density dependence; diminishing returns; Janzen–Connell hypothesis; pure stands; resource concentration hypothesis 1. INTRODUCTION isolated D. hirsuta tree. The ants kill plants around the What limits the growth of populations engaged in mutual- D. hirsuta tree and over time other D. hirsuta trees establish in ism? Some factor must keep the growth of mutualistic the vegetation-free zone created by the ants. The ant colony populations under control else they would grow to be expands to occupy these new D. hirsuta trees and clears the infinitely large (Heithaus et al.1980; May 1981; Boucher vegetation around them. Devil’s gardens grow in this et al. 1982). Current models of mutualism emphasize that manner, sometimes reaching sizes of 600 trees or more. mutualisms can be stabilized by diminishing returns to the The density of D. hirsuta trees is 40 times higher inside than mutualism as populations grow (Holland et al. 2002; outside devil’s gardens, and a single devil’s garden can cover Bronstein et al.2003). These models propose that the more than a thousand square meters (M. E. Frederickson costs and benefits of mutualism are density dependent, as 2004, unpublished work). Nonetheless, each devil’s garden has been demonstrated by a few empirical studies (Breton & is tended by one polygynous colony of M. schumanni Addicott 1992; Morales 2000; Bronstein 2001). (M. E. Frederickson & D. M. Gordon 2007, unpublished Recently, we examined the cost due to herbivory in manuscript). Since M. schumanni colonies have multiple the mutualism between the ant species, Myrmelachista queens, they are potentially immortal and can live for schumanni Emery (Formicinae), and the plant species, hundreds of years (Frederickson et al.2005). These results Duroia hirsuta (Poeppig and Endl.) K. Schum (Rubiaceae). raise the question: what limits the spread of devil’s gardens? In the rainforests of the western Amazon, M. schumanni ants Here, we investigate whether herbivory could create nest in the swollen, hollow stems (domatia) on D. hirsuta. costs to the mutualism between M. schumanni and M. schumanni creates large, nearly monospecific stands of D. hirsuta, and thus potentially limit the growth of devil’s D. hirsuta by killing other plants using formic acid, thereby gardens. In addition to killing encroaching vegetation promoting the growth and establishment of D. hirsuta trees around their host plants, M. schumanni workers also (Frederickson et al.2005). These stands are called protect their host plants against herbivores, significantly supaychacras or ‘devil’s gardens’ because an Amazonian reducing leaf herbivory in an ant-exclusion experiment legend tells that the stands are cultivated by an evil forest (Frederickson 2005). In this way, M. schumanni behaves spirit. Here, we define a ‘devil’s garden’ as three or more similarly to many other ant species that act as mutualists M. schumanni-occupied trees clustered together in an area by reducing herbivory on plants in return for food or that is largely devoid of other plants. shelter (Bronstein 1998; Heil & McKey 2003). However, The mutualism between M. schumanni and D. hirsuta D. hirsuta trees occupied by M. schumanni often sustain begins when a M. schumanni queen colonizes a single high herbivore damage, despite the protection against herbivores provided by M. schumanni workers. Outside devil’s gardens, D. hirsuta trees are sometimes * Author and address for correspondence: Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA occupied by young M. schumanni colonies that spread over 02138, USA ([email protected]). just one or two D. hirsuta trees. Alternatively, outside Received 17 December 2006 1117 This journal is q 2007 The Royal Society Accepted 18 January 2007 Downloaded from rspb.royalsocietypublishing.org on January 9, 2012 1118 M. E. Frederickson & D. M. Gordon Herbivory cost of mutualism in devil’s gardens devil’s gardens, D. hirsuta trees can be occupied by another Myrmelachista cultivates nearly pure stands of myrmeco- ant species, Azteca depilis, or they can be unoccupied. Like phytes (ant-plants) throughout the western Amazon. It is not M. schumanni, A. depilis protects D. hirsuta against clear whether the ants are all M. schumanni or several species herbivores, but unlike M. schumanni, A. depilis does not of Myrmelachista. In different regions of the western Amazon, kill encroaching vegetation to make devil’s gardens Myrmelachista cultivates different species of ant-plants. In the (Frederickson 2005). As a result, one colony of A. depilis Sira Mountains of Peru, Myrmelachista makes nearly pure ants usually occupies only one D. hirsuta tree, while one stands of Tococa guianensis (Melastomataceae; Morawetz et al. colony of M. schumanni ants can occupy from one to 1992). At Jatun Sacha Biological Station in Ecuador, several hundred D. hirsuta trees. Myrmelachista makes stands consisting of a mixture of Previous work showed that herbivory is higher on T. guianensis and Clidemia heterophylla (Melastomataceae; M. schumanni-occupied D. hirsuta than on A. depilis- Renner & Ricklefs 1998).InMadredeDios,Peru, occupied D. hirsuta (Frederickson 2005). However, this Myrmelachista makes nearly pure stands of C. nodosa (M. E. study measured herbivory on M. schumanni-occupied Frederickson 1999, personal observation). It is not known D. hirsuta trees only in devil’s gardens and thus could not how Myrmelachista recognizes its host plants (Frederickson separate the effect of having M. schumanni from the effect of et al. 2005), nor why Myrmelachista cultivates only one or two growing in a devil’s garden. Hence, two factors could explain species of myrmecophytes when many species of myrmeco- the results of this study. Either A. depilis protects D. hirsuta phytes co-occur locally. against herbivores better than M. schumanni, or herbivores At MSBS, annual rainfall averages 2400–2800 mm, and are more abundant inside than outside devil’s gardens. Here, daily maximum and minimum temperatures average 31 and we test the latter hypothesis. 238C, respectively (Sombroek 2001; M. E. Frederickson Owing to the activities of M. schumanni, devil’s gardens 2003, personal observation). The climate of the region is are patches of very low plant diversity within an otherwise often considered aseasonal, because no month of the year hyper-diverse Amazonian rainforest. Devil’s gardens receives less than 100 mm of rain (Sombroek 2001; Vieira provide a rare opportunity to compare naturally occurring et al. 2004). However, rainfall is greater from November to pure and mixed stands of plants in the Amazonian April than from May to October in most, but not all years rainforest. Herbivore abundances are often higher in (Madigosky & Vatnick 2000; Frederickson 2006). In tropical pure stands than in mixed stands; the evidence for this forests with strongly seasonal climates, herbivore abundances comes mostly from agricultural settings (Root 1973; are usually lowest in the dry season (Wolda 1978; Coley & Andow 1991). In tropical forests, a few studies have Barone 1996). However, because the seasonality of climate at shown that herbivore pressure changes with conspecific MSBS is so weak, there may be little seasonal change in plant density (Denslow 1980; Clark & Clark 1985; herbivore abundances at this site. Blundell & Peart 1998; Sullivan 2003). A positive correlation between herbivore (or pathogen) pressure (b) Standing leaf herbivory and conspecific plant density is thought to explain the We investigated the hypothesis that herbivory is higher in pure spacing of tropical trees and even the extraordinary than in mixed stands of D. hirsuta. We measured standing diversity of tropical forests (Janzen 1970; Connell 1971; leaf herbivory on: (i) A. depilis-occupied D. hirsuta trees, Clark & Clark 1984; Peters 2003; Adler & Muller-Landau (ii) M.