Worker morphology of the ant Gnamptogenys striatula Mayr (Formicidae, Ectatomminae) in different landscapes from the Atlantic Forest domain

Abstract

Morphological traits, such as size and shape, may reflect a combination of ecological and evolutionary responses by organisms. Ants have been used to evaluate the relationship between the environment and species coexistence and morphology. In the present study, we analyzed the morphology of workers of Gnamptogenys striatula Mayr in different landscapes from the Atlantic Domain in southeastern Brazil, focusing on the variation in the morphological attributes of these populations compared to those from a dense ombrophilous forest. Eighteen morphological traits of functional importance for interactions between workers and the environment were measured to characterize the size and shape of the workers. In general, the results show that ants of urban areas possess some morphological attributes of smaller size, with highly overlapped morphological space between the populations in forested ecosystems. Further, some of the traits related to predation were relatively smaller in modified land areas than in the populations from preserved areas of dense ombrophilous forest. These results help broaden the knowledge regarding morphological diversity in G. striatula, suggesting that the characterization of the morphology may be important to quantify the effects of land use on morphological diversity, and presumably, to facilitate the use of ants as biological indicators.

Biological indicators; Atlantic Forest; Body size; Morphometric; Weber's length

Introduction

During evolution, organisms undergo selection based on their morphological traits (Irschick et al., 2013), such as body size (Peters, 1983). These quantitative measurements are influenced by the species' evolutionary history and ecology (Wainwright, 1994; Yates and Andrew, 2011), making them a basic tool for analyzing the relationships between taxa and environment. Body size is related to fertility (Kovacs et al., 2008), survival (Schorr et al., 2009), and dispersal ability (Pearce-Duvet et al., 2011), and can be shaped by direct genetic effects, maternal effects or the social environment (Meunier and Chapuisat, 2009).

Arthropod populations are influenced by climatic factors, different soil-management strategies, and the quality and availability of resources (Andow, 1991; Lomônaco and Germanos, 2001; Silva et al., 2009). Overtime, these factors can lead to morphological and physiological changes and behavioral traits in individuals from each population (Silva et al., 2009). In beetles (Ribera et al., 2001), termites (Scharf et al., 2007), shredders (Larrañaga et al., 2009), and ants (Yates and Andrew, 2011) alterations have been described in the external morphology in response to environmental modifications.

Ants are particularly interesting for the study of the causes and consequences of variations in body size (Oster and Wilson, 1978; Pie and Tschá, 2013) due to their complex social organization, combined with the fact that the morphology of an individual ant colony is a distribution of its workers' size and shape (Weiser and Kaspari, 2006). In these insects, body size can indicate significant interactions among genetic factors, the resource availability in the habitat, the energetic cost of producing individuals of different sizes, abiotic factors such as temperature (Kaspari, 1993; Kaspari et al., 2000a, b), and possibly the environment heterogeneity (Kaspari and Weiser, 1999, 2007; Costa et al., 2010; Gibb and Parr, 2013).

Gnamptogenys striatula Mayr, 1884 is a polygynous ant species and their colonies contain either differentiated queen or gamergates (Giraud et al., 2000). This species can be classified as a medium-sized generalist predator (Silva and Brandão, 2010) and it feeds on small arthropods, among several species of insects (Lattke, 1990). The colonies of this ant consist of 150 to 200 individuals (Lattke, 1990). The ants do not monopolize large amounts of resources, and trails of pheromones are more commonly used for shifting the nest than for foraging (Blatrix et al., 2002). This species occurs throughout Central and South America (Kempf, 1972; Giraud et al., 2000) and across biomes, including disturbed areas (Souza et al., 2010; Mentone et al., 2011). Gnamptogenys striatula can form nests in trunks (Lattke, 1990) and twigs (Fernandes et al., 2012; Souza et al., 2012) at different stages of decomposition in the litterfall; however, nests can also be built under rocks and in rock crevices (Lattke, 1990), and workers can be observed foraging in the litterfall (Morini et al., 2012; Suguituru et al., 2011, 2013). More data about the biology of G. striatulahave been reported by Giraud et al. (2000) and Blatrix and Jaisson (2000).

The present study investigates populations of G. striatula from different locations in southeastern Brazil using morphological traits. Because this species has been reported in various ecosystems with distinct land uses (Lattke, 1990; Morini et al., 2007; Pacheco et al., 2009), we analyzed the morphology of workers of G. striatula compared to those from a dense ombrophilous forest, which represents a preserved environment. The main aim of this study is to characterize continuous morphological traits of G. striatula in various landscapes from the Atlantic Forest Domain.

Material and methods

Gnamptogenys striatula workers were obtained during different collection expeditions in southeastern Brazil using Winkler extractors, Berlese funnels, pitfall traps, and sardine baits. A distance of 20m between the sampling points was used for all of the collection methods to avoid pseudoreplication (Baccaro et al., 2011). Four ecosystem types with distinct phytophysiognomies were selected (Table 1). Regardless of their actual floristic composition, all of the ecosystems belonged to the Atlantic Forest Domain (Fiaschi and Pirani, 2009) (Fig. 1). The number of collection areas in each ecosystem ranged from two to four (Table 1).

Table 1.
Characterization of the Gnamptogenys striatula worker-collection areas in the Brazilian Atlantic Domain.

Types of ecosystems	Litterfall	Number of workers
Dense ombrophilous forest; > 80 years of regeneration.	Abundant litterfall	Rainforest (RF1)	Rainforest (RF2)	Rainforest (RF3)	Rainforest (RF4)
		N = 20	N = 20	N = 20	N = 20
Exotic vegetation; Pinus elliotti andEucalyptus saligna; crops abandoned > 30 years (developed understory).	Litterfall consisting of acicular (Pinus) and eucalyptus leaves.	Exotic Forest (EF1)	Exotic Forest (EF2)	Exotic Forest (EF3)	Exotic Forest (EF4)
		N = 20	N = 20	N = 20	N = 20
Underbrush from squares and urban parks	Not very abundant litterfall	Urban area (UA1)	Urban area (UA2)
		N = 20	N = 20
Commercial Eucalyptus saligna; crop (without understory; managed for 7 years)	Not very abundant litterfall; consists of eucalyptus leaves when present	Commercial crop (CC1)	Commercial crop (CC2)
		N = 5	N = 6

Figure 1.
Sampling sites in São Paulo, Brazil, showing the fragments of Atlantic Rainforest where the study was conducted.

The morphological parameters were measured using a micrometer ruler coupled to a stereoscopic microscope. Eighteen traits (Table 2) with functional significance were measured in each G. striatula worker following Silva and Brandão (2010). According to available nests, eleven to 80 workers were measured in each of the selected ecosystems.

Table 2.
Mean (and standard deviations) in the morphological traits of Gnamptogenys striatula workers from each area of the Atlantic Domain in southeastern Brazil. Measurements in mm.

Measure	Rainforest	Commercial crop	Exotic forest	Urban area
Head width (HW)	0.88 (0.04)	0.84 (0.03)	0.86 (0.04)	0.83 (0.03)
Head length (HL)	1.06 (0.05)	0.99 (0.01)	1.04 (0.05)	1.02 (0.03)
Mandible length (ML)	0.46 (0.06)	0.52 (0.00)	0.48 (0.04)	0.46 (0.02)
Mandible width (MW)	0.24 (0.03)	0.29 (0.02)	0.24 (0.02)	0.22 (0.02)
Mandible gape width (MG)	0.60 (0.03)	0.73 (0.03)	0.62 (0.06)	0.58 (0.03)
Scape length (SL)	0.93 (0.06)	0.92 (0.04)	0.90 (0.04)	0.86 (0.03)
Clypeus length (CL)	0.27 (0.03)	0.30 (0.01)	0.27 (0.03)	0.26 (0.02)
Eye length (EL)	0.17 (0.02)	0.15 (0.00)	0.17 (0.01)	0.17 (0.01)
Eye width (EW)	0.12 (0.01)	0.10 (0.00)	0.12 (0.01)	0.12 (0.01)
Distance of eye to mandible insertion (DEM)	0.39 (0.03)	0.37 (0.01)	0.38 (0.03)	0.36 (0.02)
Interocular distance (ID)	0.78 (0.05)	0.78 (0.04)	0.76 (0.04)	0.73 (0.03)
Pronotum width (PrW)	0.70 (0.05)	0.70 (0.05)	0.70 (0.05)	0.66 (0.03)
Weber’s length (WL)	1.26 (0.08)	1.29 (0.07)	1.27 (0.09)	1.21 (0.07)
Hind tíbia length (TL)	0.81 (0.06)	0.78 (0.04)	0.80 (0.05)	0.77 (0.04)
Hind femur length (FL)	1.12 (0.08)	1.10 (0.10)	1.09 (0.06)	1.05 (0.05)
Petiole width (PeW)	0.47 (0.03)	0.47 (0.04)	0.48 (0.03)	0.45 (0.02)
Petiole length (PeL)	0.35 (0.03)	0.37 (0.01)	0.36 (0.03)	0.33 (0.02)
Petiole height (PeH)	0.55 (0.14)	0.50 (0.02)	0.49(0.07)	0.44 (0.03)

We analyzed trait variability according to the different levels of variation using both single-trait (linear mixed models) and multi-trait analyses (principal component analyses). We used linear mixed effects models, which are appropriate to represent hierarchical data structures. Models were used for each morphological trait using the forest type as a fixed effect and a random-intercept site effect. Variances were estimated by maximizing the log-likelihood using Restricted Maximum Likelihood (REML). The residual of the regression for each trait on a measure of body size (Weber's length) was used in the analysis because ant traits were significantly and positively correlated to body size. We used principal component analysis based on covariance matrix of the original measures at the individual level to describe the morphological space's general structure. Further, we determined the probability of correctly attributing a given individual to a forest based on the individual's morphological traits. This matching was conducted by performing a linear discriminant analysis (LDA), which identifies the linear combination of continuous explanatory variables that best separates two or more classes of a categorical variable. LDA maximizes the ratio of the between-groups variance to the total variance and can be projected onto new observations. All the statistical analyses were performed with R. 3.0.2 (R Core Team, 2014) using the packages nlme, ade4 and MASS.

Results

The variation in morphological traits among G. striatula workers in each area of the Atlantic Domain in southeastern Brazil was quantified (Table 2). PCA on the data at the individual level showed that the first axis explains 41% of the variance, which was mainly related to petiole height (0.59), femur length (0.49) and Weber's length (0.45). Principal component 1 reflected size variance, but as the coefficients are not equal and mandible length had a negative coefficient of the eigenvectors, it retained some size allometry. The second principal component explains 22% of the variance, which was related to petiole height (0.58), mandible length (-0.31), tibia length (-0.24) and Weber's length (-0.23) (Table 3; values in bold). The PCA suggested a size gradient from ants from urban areas to exotic and rainforest individuals. The upper left part of the biplot shows individuals with lower size on both PC1 and PC2 axes; the lower right part shows individuals associated with larger size (but smaller petiole height relative to their body size); some individuals from exotic forest and from dense ombrophilous forest showing a large petiole height relative to their size were associated with high positive values along axes 1 and 2, determining a cluster of points in the morphospace (Fig. 2).

Table 3.
Loadings of principal components for the 18 morphological traits, their respective eigenvalues and the percentage of variance for which each axis accounted. The four higher loadings in each axis were highlighted in bold.

	PC1	PC2	PC3
HW	0.267	–0.164	0.107
HL	0.214	–0.203	0.190
ML	–0.021	–0.313	–0.030
MW	0.086	0.004	–0.008
MG	0.176	–0.210	–0.171
SL	0.363	0.073	0.004
CL	0.133	0.117	–0.099
EL	0.022	–0.056	0.011
EW	0.023	–0.012	0.014
DEM	0.107	–0.016	0.055
ID	0.226	–0.165	0.089
PrW	0.277	–0.117	0.066
WL	0.459	–0.232	–0.407
TL	0.271	–0.247	0.153
FL	0.498	–0.016	0.164
PeW	0.147	–0.117	0.046
PeL	0.109	–0.025	–0.094
PeH	0.593	0.590	–0.008
Cumulative % Explained Variance	42%	64%	73%

Figure 2.
Principal Component Analysis between commercial crop (CC), exotic forest (EF), dense ombrophilous forest (RF), and urban areas (UA), showing the dispersion of individuals of Gnamptogenys striatula in the trait space. The trait space was described by 18 morphological characters as explained in Material and Methods. Axis 1 = 41%, Axis 2 = 22%.

The probabilities of attributing individuals to the correct forest based on the individuals' trait values were overall moderate; in total, 58% of specimens were predicted accurately. The specimens of commercial crops were well predicted (100%), while the specimens from other sites were moderately successfully predicted (52%, 58%, and 57%) for exotic forest, dense ombrophilous forest and urban areas, respectively.

The single-trait analyses resulting from the linear mixed models suggest that some population's traits in commercial crops and urban areas were different from the traits of the dense ombrophilous forest population. Overall, we did not find differences between size (Weber's length), head length, mandible length, interocular distance, clypeus length, leg size (femur and tibia length), or petiole shape (size, width or height). Populations of urban areas showed relatively shorter scape length, pronotum width, mandible width, and eyes position (distance of the eye to the mandible insertion) compared to rain forest populations; further, commercial plantations had significant differences in relative head size (smaller head width and eyes size) (Fig. 3), but larger mandible width and mandible gape. We did not find morphological differences between G. striatula individuals in the rain forest and exotic forest area (Table 4).

Figure 3.
Morphological traits that differentiate the workers of Gnamptogenys striatula of urban areas and commercial crops compared to those of preserved forest. () urban areas; () commercial crops; () urban areas and commercial crops. (Image: S.S. Suguituru). DEM= Distance of eye to mandible insertion; EL=Eye length; HW= Head width; MW= Mandible width; PrW= Pronotum width; SL= Scape length.

Table 4.
t-values from linear mixed models testing the effect of land use on selected morphological characters of Gnamptogenys striatula workers. Analyses were performed across all ants measured in each area. All measurements, except Weber's Length, are based on residuals with Weber's Length. Atlantic Forest areas were the reference level to comparisons (Intercept values). Values shown are t-values. Significance levels: *P < 0.05, *** P < 0.001.

	Intercept values	Commercial crop	Exotic forest	Urban area
HW	1.608	–2.458*	–1.228	–2.153
HL	0.717	–2.093	–0.554	–0.713
ML	–0.714	2.011	0.913	0.091
MW	0.618	4.717***	–0.724	–2.284*
MG	–0.829	4.682***	0.968	–0.443
SL	1.762	–0.761	–1.732	–2.298*
CL	0.158	1.012	–0.233	–0.390
EL	0.052	–2.551*	–0.143	0.863
EW	0.757	–5.363***	–0.235	–0.098
DEM	1.957*	–1.944	–1.570	–2.674*
ID	1.317	–0.110	–0.101	–2.185
PrW	0.935	–0.629	–0.077	–2.504*
WL	62.167***	0.688	0.314	–1.342
TL	0.831	–1.246	–0.585	–1.198
FL	1.231	–0.847	–1.148	–1.597
PeW	–0.002	–0.272	0.933	–1.354
PeL	0.012	1.042	0.446	–1.112
PeH	0.919	–0.668	–0.929	–1.095

Discussion

Our data suggested that G. striatula workers occurring in modified habitats, particularly commercial crops and urban areas possess some morphological attributes of smaller size than workers inhabiting rainforests. However, G. striatula workers in anthropized areas of the Atlantic Forest in northeastern Brazil possessed similar head width to that of the workers in the rainforest from the present study (see Blatrix and Jaisson, 2001).

In most cases, morphological variation in insects is related to phenotypic plasticity (Via and Lande, 1985; Lomônaco and Germanos, 2001). Phenotypic plasticity is the organism's ability to change its phenotype in distinct environments (Scheiner, 1993), and it can be considered an important adaptive tool for survival in unstable and heterogeneous environments (Parsons, 1990), including those that vary due to human interference (Silva et al., 2009).

According to taxonomic studies, G. striatula workers show strong morphological variation in size, sculpturing, and pilosity, and some have reported that G. striatula is a species complex despite having many shared morphological traits (Lattke, 1995; Arias-Penna, 2008). Our results suggest a large overlap of the multivariate morphological space among the populations of G. striatula from the different areas, and that the classification error based on 18 morphological traits can be relatively high. The morphometric analysis of eighteen morphological traits suggests two clusters of individuals, one found in all four habitat types and the second one of individuals found only in the rainforest. Furthermore, we found that the individuals from urban areas were significantly different from those from the other regions, based on both the single and multivariate analyses, suggesting at least a strong effect on morphology in strongly disturbed areas (or a third species in this complex as an alternative hypothesis). It is well known that urban areas have reduced ant habitat and less-appropriate climate, temperature, and primary productivity (Murphy, 1997; Rickman and Connor, 2003). In contrast, in forest environments, there is a great concentration and circulation of energy in the litterfall (Golley et al., 1978). In this forest stratum, there is a diverse fauna that actively participates in nutrient cycling and the degradation of organic matter (Seastedt, 1984), which affects the invertebrate communities that serve as food for ants (Jacquemin et al., 2012).

In anthropized areas of southeastern Brazil, resources are not very diversified and are sometimes scarce due to the lack of litterfall, as in the case of urban areas (McIntyre et al., 2001; Yamaguchi, 2004, 2005) and commercial eucalyptus plantations (Lima, 1993). Resource quality or availability can affect the diet of worker ants (Fowler et al., 1991), which care for the brood and can manipulate offspring number or resource allocation (Chapuisat and Keller, 1999; Meunier et al., 2008), and worker morphology depends on the nutritional conditions during juvenile development (Kaptein et al., 2005). Furthermore, the environment and nutritional status are responsible for the differentiation of alternative caste phenotypes in social insects (Scharf et al., 2007).

In ants, the head width is an important morphological trait that is used as a proxy for size (Kaspari, 1993, 1996; Weiser and Kaspari, 2006) and is related to behavior during prey searches (Kaspari, 1993). Thus, other traits such as head length, pronotum width, interocular distance, mandible gape, and mandible width (Fowler et al., 1991; Kaspari, 1993; Kaspari and Weiser, 1999; Weiser and Kaspari, 2006) are relevant, and all of these traits were found to be significantly different (smaller or larger) in the workers from the anthropized environments described in the present study.

Leg length in ants is a strong predictor of how fast individuals within a species are able to move during maximal performance (Hurlbert et al., 2008) and is a determinant of foraging behavior (Pearce-Duvet et al., 2011). In tropical forests, where the litterfall is deep and diverse, there is high rugosity (Farji-Brener et al., 2004), and ants with shorter legs are favored (Farji-Brener et al., 2004; Kaspari and Weiser, 2007), whereas longer legs are favored in environments with less ground cover (Wiescher et al., 2012), such as urban parks and commercial crops. Yates and Andrew (2011) found that the relationship between the thorax and mid-femur length differed significantly among land-use types, with assemblages in crop stubble exhibiting a significantly higher femur:thorax ratio compared to ants from native remnants. In G. striatula, we did not detect any significant difference in leg length among the workers from the different collection sites. Our results suggest that leg size in G. striatuladoes not respond to habitat modification; this result was unexpected, considering that the land-use types studied have different rugosity levels.

In ants, bioindication may occur in several ways, such as changes in species richness and abundance (see the review on this topic by Ribas et al., 2012) or shifts in biological attributes, such as body size or symmetry, as observed in other insects (Kambach et al., 2013 for butterflies/moths; Souto et al., 2011 for flies). Our results showed large variability in the morphological characteristics and some significant changes in the size and shape of the selected morphological traits in a common ant species under different land-use types in the Atlantic Forest. We suggest that quantifying the population variability in ant traits related to ecosystem function under varying land uses may be interesting with regard to the use of ants as biological indicators of environmental change.

Acknowledgments

Thanks to the São Paulo Research Foundation (FAPESP) (Protocol nº. 10/50294-2), the Foundation for the Support of Teaching and Research/University of Mogi das Cruzes (FAEP/UMC), and the National Council for Technological and Scientific Development (CNPQ) (Protocol nº. 301151/2009-1 and 302363/2012-2) for their financial support. We would also like to thank two anonymous referees for their constructive comments, and Gabriela Procópio Camacho (Universidade Federal do Paraná), who has kindly confirmed the identification of Gnamptogenys striatula samples.

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Publication Dates

• Publication in this collection
  Jan-Mar 2015

History

• Received
  23 June 2014
• Accepted
  24 Oct 2014