Transitioning from Unstable to Stable Colony Growth in the Desert Leafcutter Ant Acromyrmex Versicolor
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Behav Ecol Sociobiol DOI 10.1007/s00265-013-1632-4 ORIGINAL PAPER Transitioning from unstable to stable colony growth in the desert leafcutter ant Acromyrmex versicolor Rebecca M. Clark & Jennifer H. Fewell Received: 1 August 2013 /Revised: 5 September 2013 /Accepted: 9 September 2013 # Springer-Verlag Berlin Heidelberg 2013 Abstract Like organisms, cohesive social groups such as in- Introduction sect colonies grow from a few individuals to large and complex integrated systems. Growth is driven by the interplay between Growth is a defining process for individuals at all levels of intrinsic growth rates and environmental factors, particularly biological organization, whether in cells in an organism or nutritional input. Ecologically inspired population growth individuals in a population or social group. For organisms to models assume that this relationship remains constant until grow successfully, they must respond robustly to environmen- maturity, but more recent models suggest that it should be less tal challenges while following an intrinsically based growth stable at small colony sizes. To test this empirically, we mon- trajectory (Salazar-Ciudad and Jernvall 2004). The interac- itored worker population growth and fungal development in the tions between environmental constraints such as nutrient in- desert leafcutter ant, Acromyrmex versicolor, over the first take and the intrinsic developmental program collectively 6 months of colony development. As a multitrophic, symbiotic shape an organism’s ontogenetic phenotype (Glazier 2005; system, leafcutter colonies must balance efforts to manage both Doi et al. 2010). A similar interplay between environmental fungus production and the growth of the ants consuming it. influences and growth shapes the ontogeny of insect societies, Both ants and fungus populations grew exponentially, but the as they grow from a few individuals to a size of thousands or shape of this relationship transitioned at a size threshold of 89± millions (Oster and Wilson 1978; Nonacs 1991;Kay2004; 9 workers. Above this size, colony mortality plummeted and Kay et al. 2006; Hou et al. 2010). colonies shifted from hypometric to hypermetric growth, with a Despite recognition that development constrains social distinct stabilization of the relationship between the worker phenotype, surprisingly few studies have characterized how population and fungus. Our findings suggest that developing complex social groups such as insect colonies navigate devel- colonies undergo key changes in organizational structure and opmental challenges as they move from foundation through stability as they grow, with a resulting positive transition in maturity (Wilson 1983; Porter and Tschinkel 1985, 1986; efficiency and robustness. Tschinkel 1988, 1991, 2011). Such characterization is critical for understanding how natural selection shapes growth and Keywords Development . Acromyrmex . Division of labor . phenotypic expression. Social groups, like individual organ- Colony growth . Leafcutter ant . Social allometry isms, must balance between allocation to growth and alloca- tion to physiological maintenance; the mechanisms used to achieve this balance are based on organizational properties Communicated by W. T. Wcislo specific to the system and subject to selection. Here, we study the growth dynamics of newly initiated Electronic supplementary material The online version of this article (doi:10.1007/s00265-013-1632-4) contains supplementary material, colonies of the desert leafcutter ant Acromyrmex versicolor which is available to authorized users. to understand how the fungus garden/worker ant relationship unfolds as colonies develop over the first 6 months of life. R. M. Clark (*) Department of Entomology, Texas A&M University, College Station, Leafcutter and related fungus-growing ant colonies provide a TX 77843, USA unique opportunity to track nutrient balancing and colony e-mail: [email protected] growth within an enclosed trophic system because the ants directly regulate the growth of their immediate food source, J. H. Fewell School of Life Sciences, Arizona State University, Tempe, the fungus garden (Weber 1972; Hölldobler and Wilson 1990; AZ 85280, USA Wirth et al. 2003;SealandTschinkel2008;Mehdiabadiand Behav Ecol Sociobiol Schultz 2010). Colony growth is thus dependent on a feed- Methods back system between the nutritional state of the fungus and the colony’s work allocation across tasks (Bass and Cherrett Study species 1994;BurdandHoward2005; Camargo et al. 2008). This balance may be particularly important during early growth, A. versicolor colonies are found along washes (arroyos) in low when colonies are more vulnerable to perturbation and/or desert areas throughout the southwestern USA and northern stochastic effects (i.e., they possess lower robustness; Kitano Mexico (Weber 1972; Wetterer et al. 2001; Johnson and Ward 2004). Indeed, mortality rates generally are highest in small, 2002;Ward2005). The ants function as generalist herbivores, young colonies, suggesting that this is a critical period in collecting both fresh and dry leaves and flowers from trees and colony life history (Autuori 1950; Fowler 1992;Cole2009; shrubs, including mesquite (Prosopis juliflora), ironwood Adams et al. 2012). Previous studies with this species and the (Olneya tesota), acacia (Acacia spp.), palo verde (Cercidium fungus gardener Trachymyrmex septentrionalis suggest un- spp.), creosote (Larrea tridentata), and ocotillo (Fouquieria stable or variable ant–fungus relationships during early colony splendens; R. Clark, personal observation; Gamboa 1975; development, but it is unclear how this occurs or at what point Wetterer et al. 2001). Mating swarms are triggered by summer it is resolved by successful colonies (Julian and Cahan 1999; monsoon rains with >2.5 cm of precipitation (Johnson and Seal and Tschinkel 2007;Kangetal.2011). Rissing 1993), which causes queens to fly from their natal nests Most models of societal growth have been based on ecolog- to aggregates, where they mate multiply and then shed their ical models of population growth with the assumption that wings and excavate new nests, typically at the canopy edge of societies retain similar organizational structure from small initial palo verde or mesquite trees (R. Clark, personal observation; sizes to maturity (Oster and Wilson 1978). While such models Reichardt and Wheeler 1996). In some areas, multiple queens may effectively predict growth patterns for larger colonies, they form pleometrotic foundress groups, and mature colonies are are less useful for predicting events in small colonies, where thought to remain polygynous (Rissing et al. 1986, 1989, 2000; internal organizational and demographic factors play an impor- Cahan and Julian 1999). This is supported by the observation tant role in determining growth rates (Porter and Tschinkel 1986; that all queens remain reproductively active in polygynous Jeanne and Nordheim 1996; Jeanne 1999; Gautrais et al. 2002; nests maintained in the laboratory (R. Clark, unpublished data). Tenhumberg et al. 2009). As an example, small colonies have to Many attine ants, including A. versicolor, possess semi- complete much of the same task repertoire as larger colonies, but claustral queens, which leave their newly excavated nests with a limited workforce (Wilson 1983; Karsai and Wenzel occasionally to forage for leaves as substrate for the fungus 1998; Augustin and Santos 2008). This has consequences for garden, which in turn provides food for the developing brood colony-level division of labor and colony growth efficiency, (Rissing et al. 1989; Fowler 1992; Fernández-Marín et al. both of which may increase with colony size (Gautrais et al. 2004). When workers emerge, queens gradually reduce their 2002; Jeanson et al. 2007;Watersetal.2010;Kangetal.2011). behavioral repertoire and remain inside the nest to lay eggs, In this study, we used noninvasive methods to correlate the while workers assume the tasks of collecting and preparing growth trajectories of the worker population and fungus gar- leaves for the fungus garden, raising brood, tending the fungus den biomass in leafcutter ant colonies from foundation garden, and removing waste materials from the nest (Cahan through the first 6 months of development. A. versicolor and Julian 1999). In laboratory nests, queens start the fungus colonies are relatively long-lived and can grow over the garden on the bottom of the nest chamber, allowing full course of several years to a size of around 10,000 workers visibility of workers and developing brood, but mature gar- prior to reproducing, making it possible to study growth dens are typically hung in patches on the chamber ceiling that processes without confounding effects from the onset of re- grow downward, forming “curtains” that increase in density production (Julian and Cahan 1999). We focus on the critical with the age of the garden, and gardens in field colonies also early phase of colony growth, from colony initiation through hang from the ceiling (U. Mueller, personal communication). sizes of 100+ workers. We show that, in colonies at this scale, the worker–fungus relationship undergoes a qualitative shift Growth study from negative, variable allometry (a hypometric relationship with fewer workers produced per unit of fungus present) to To establish colonies, we collected newly mated queens from hypermetry, where more workers are produced per unit of the field before they began excavating new nests. Queens fungus as colony size increases.