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Foraging Plasticity of Atta Cephalotes (Hymenoptera: Formicidae) in Response to Temperature Differences Between Forest and Pasture

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Foraging Plasticity of Atta Cephalotes (Hymenoptera: Formicidae) in Response to Temperature Differences Between Forest and Pasture Foraging plasticity of Atta cephalotes (Hymenoptera: Formicidae) in response to temperature differences between forest and pasture Santiago Bustamante1 & Angela Amarillo-Suárez2 1. Universidad Tecnológica de Pereira, Carrera 27 #10-02 Barrio Alamos - Risaralda - Colombia; [email protected] 2. Pontificia Universidad Javeriana, Departamento de Ecología y Territorio Bogotá D.C. Carrera 7 No. 40 - 62; [email protected] Received 22-X-2018. Corrected 21-V-2019. Accepted 29-VII-2019. Abstract. Introduction: Changes in microclimatic conditions due to land cover transformations influence varia- tions in population life histories and the developmental patterns of organisms. These variations can have a genetic basis, an environmental basis, or both. Objective: To determine the differences between habitats in the foraging activity of Atta cephalotes in response to changes in temperature and the extent to which any such differences are due to phenotypic plasticity, genetic variability, or both. Methods: We performed foraging experiments; each colony (4 colonies sourced from pasture and 3 colonies sourced from forest) underwent eight temperature treat- ments from 10 to 45 ºC (± 1 ºC) at 5 ºC intervals, using common garden and reciprocal transplant experiments. Results: We found high plasticity in the foraging activity of Atta cephalotes in response to temperature, with the foraging activity gradually increasing from 15 to 35 ºC. Additionally, we found no significant differences in the foraging activity between the colonies sourced from the pasture and forest. Conclusions: The foraging activity of A. cephalotes was directly proportional to temperature, with ants exhibiting thermophilic behaviors and high plasticity, and there were no differences in the foraging activity between colonies sourced from both habitats. Key words: leaf-cutting ants; plasticity; temperature; microclimatic changes; tropical dry forest. Bustamante, S., & Amarillo-Suárez, A. (2019). Foraging plasticity of Atta cephalotes (Hymenoptera: Formicidae) in response to temperature differences between forest and pasture. Revista de Biología Tropical, 67(4), 963-974. Anthropogenic transformations of land- Shaw, 1997; Stockwell & Weeks, 1999) such as scapes due to agriculture and cattle ranching fish, (Heath, Heath, Bryden, Johnson, & Fox, cause ecological differences between nearby 2003), reptiles (Phillips & Shine, 2006), mam- areas as climatic changes and reduction in mals (Pigeon, Festa-Bianchet, Coltman, & Pel- diversity. These differences generate differen- letier, 2016), plants (Burger & Ellstrand, 2014; tial selection pressures that can cause adaptive Colautti & Barrett, 2013), and insects (Singer, changes in populations over very short time 2000), including Coleoptera (Szucs, Schaffner, scales, even less than a hundred years. This Price, & Schwarzländer, 2012) Phasmatodea process, known as contemporary evolution (Farkas, Mononen, Comeault, Hanski, & Nosil, (Colautti & Lau, 2015; Stockwell, Hendry, & 2013), Hymenoptera (White, 2011), and Lepi- Kinnison, 2003), has been extensively docu- doptera (White, 2011). mented in recent literature and occurs in a vari- Human activities such as agriculture and ety of organisms (Bone & Farres, 2001; Reznick cattle grazing strongly modify the structure & Ghalambor, 2001; Reznick, Shaw, Rodd, & and composition of plant communities and Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(4): 963-974, September 2019 963 the physical structure of ecosystems (Nunes is a function of the genotype expression under de Oliveira, Abílio de Carvalho, Trancoso specific environmental conditions. In a reaction Gomes, Fontes Guimarães, & Concepta Mar- norm, the x-axis represents the environmental garet, 2017), altering nutrient cycles and their gradient, and the y-axis represents the pheno- prevailing microclimatic regimes (Wilson, type (Pigliucci, 2001). If there is plasticity, the Liang, Wilson, & Akiwumi, 2018). Changes reaction norm will have a slope different than in microclimatic conditions influence varia- zero. If there is no variation in plasticity in the tions in population life histories and the devel- population, all reaction norms should be paral- opmental patterns of organisms (Kinnison, lel, whereas in the absence of genetic variation Hendry, & Stockwell, 2007; Stockwell et al., in the trait itself, there should be a single reac- 2003). These variations can have a genetic tion norm (Mousseau et al., 2000). However, if basis, an environmental basis, or both (Kin- there is variation in phenotypic plasticity, the nison et al., 2007; Stockwell et al., 2003). If population is represented by a set of reaction the variation in a trait has a genetic component norms with different slopes, which indicate and responds to a particular microclimatic pat- an interaction between genotype and environ- tern, it results in adaptive changes (Hoffmann ment. The graphical model of the genotype due & Sgró, 2011). There is evidence from many to environmental interactions is a more formal plants and animals suggesting the existence statistical interaction (Mousseau et al., 2000). of heritable variations in all types of adaptive Thus, phenotypic plasticity offers a theoretical traits (Pigliucci, 2001), including physiological framework to study the influence of genes and (Houle, 1991; Shirangi, Dufour, Williams, & the environment on the genotype (Mousseau Carroll, 2009), morphological (Arnold, 1981; et al., 2000). A trait is considered plastic if the Grant & Grant, 2006), life history (Mousseau test (e.g., an ANOVA) for the effect of an envi- & Fox, 1998), developmental and behavioral ronmental factor on that trait is statistically sig- traits (Avise, 2008; James & Partridge, 1995). nificant (Pigliucci, 2001; Richards et al., 2006). To understand trait evolution, it is neces- Leaf-cutting ants (LCAs) from the genera sary to consider the patterns of environmental Atta and Acromyrmex (Hymenoptera: Formi- heterogeneity and the ways in which natural cidae: Attini) are an ideal group for studying selection affects the phenotypic traits of organ- the adaptation of local populations to envi- isms (Mousseau, Sinervo, & Endler, 2000). ronmental variations such as microclimatic Because of environmental heterogeneity, local change. These ants evolve in dry or seasonally adaptations may arise from the differential dry habitats and disperse to a large variety of effects of natural selection on a deme due to habitats (Branstetter et al., 2017). They are differences in phenotypic traits between organ- considered central-place foragers, which allow isms. In this case, organisms are assumed to the monitoring of behaviors for long periods exhibit higher fitness under local environmen- of time under field conditions (Burd & How- tal conditions than under the conditions of other ard, 2005). These ants are very common and habitats (Kawecki & Ebert, 2004; Mousseau et widely distributed in the lowlands of Colombia al., 2000). Differences in phenotype result from (Fernández, Cartro-Huertas, & Serna, 2015). differences in genotype, changes in environ- Atta cephalotes can develop successfully in mental factors over the same genotype, or the different habitats and microclimatic conditions interaction between genotype and environment. (Montoya-Lerma, Giraldo-Echeverri, Arm- Phenotypic plasticity has been defined as brecht, Farji-Brener, & Calle, 2012). A. cepha- the property of a single genotype to express lotes is a common species in the Cauca Valley, different phenotypes across different environ- (Chacon, Osorio-García, Achury, & Bermúdez, mental conditions (Richards, Bossdorf, Muth, 2012; Montoya-Lerma et al., 2012), a region Gurevitch, & Pigliucci, 2006). This plasticity that was originally forested but has undergone can be expressed by the reaction norm, which deforestation since 1550 (CVC, 1990). This 964 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(4): 963-974, September 2019 process has been driven by the introduction of MATERIALS AND METHODS cattle grazing and sugar cane plantations. As a consequence, the landscape includes only a few This study was conducted in the area of 2 remaining forest fragments, which corresponds the Cauca River Valley, which is a 15 000 km to less than 2 % of the original forest area inter-Andean valley with a gradient ranging (Arcila Cardona, Chacon, & Valderrama, 2012) from 900 to 1 000 m.a.s.l. This area has been immersed in a matrix of pastures dedicated to highly transformed by agriculture and cattle cattle grazing (CVC, 1990). The microclimatic grazing since 1550 (Etter & van Wyngaarden, conditions of the foraging trails of A. cepha- 2000). Within the valley, there are only a few lotes differ greatly between these two habitats small forest remnants (covering less than 2 % (Bustamante, 2017). For example, the mean of the original area), with an average area of soil temperature at noon can be 5 ºC higher in 12 ha (GEMA, 1998). The average annual the pasture than in the forest, and the maximum rainfall is 1 700 mm/year with the major- soil temperature can be 11 ºC higher in the pas- ity occurring in wet seasons (March-May and ture than in the forest. Additionally, the relative September-November). There are two wet and humidity (RH) in the pasture is 15 % lower than two dry seasons in the region throughout a year that in the forest (Bustamante, 2017). Despite (Ramírez, Chacon, Armbrecht, & Calle, 2002). these strong differences in microclimatic con- The annual average temperature is 24 °C. ditions,
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