Insectes Sociaux https://doi.org/10.1007/s00040-019-00716-w Insectes Sociaux

RESEARCH ARTICLE

Social structure of Gnamptogenys bisulca (Formicidae: ) in tropical forests

D. M. Urcuqui1 · J. Herrera‑Rangel1 · C. Poteaux2 · I. Armbrecht1

Received: 9 February 2019 / Revised: 27 May 2019 / Accepted: 29 June 2019 © International Union for the Study of Social (IUSSI) 2019

Abstract The study of the social organization of may help to understand why some species are able to persist in natural forests after fragmentation and anthropogenic disturbances. The Neotropical Gnamptogenys bisulca has shown to be a biologi- cal indicator of habitat quality in Andean montane forests and we proposed to explain this characteristic by investigating its social structure and the spatial distribution of colonies at fne scale. In eight 100 m2 plots located in four forests in the western Colombian Andes, the position of G. bisulca colonies was recorded for spatial distribution and their social composi- tion described: ergatoid females were found in most of the nests, isolated or together with normal queens. As ergatoids and queens were dissected to examine their reproductive status, it appeared that apparent polygyny represented, in fact, efective monogyny, with other potential reproductive females being unmated or inhibited. In the few cases of mixed colonies, a queen was always at the head of the colony. Local spatial distribution was random and did not ft the hypothesis of nesting by fs- sion, as generally observed in the case of the presence of ergatoids. However, the social structure was signifcantly diferent according to the site, the most preserved forest showing no or rare ergatoids (but queens) compared to the other sites. Our results indicated that the presence of ergatoids in G. bisulca may help colonies to adapt to slightly disturbed habitat contexts.

Keywords Ergatoids · Monogyny · Polygyny · Tropical montane forest

Introduction absence of wings in queens because this variation of the queen phenotype is generally linked to their dispersal tactics While the division of labor is a key factor in social hymenop- (Molet et al. 2009): mainly large winged queens are devoted terans explaining their ecological success, ants in particular, to far-away dispersion (through independent colony found- present huge social plasticity, with diferences not only in ing, ICF) while wingless or reduced-size queens disperse the number of queens per colony (polygyny), but also their with nestmate workers to found a new colony by budding size and morphology may vary among species, populations or fssion (dependent colony founding, DCF). Many recent and occasionally even among colonies within a population reviews have pointed out that wing dimorphism in the queen (Bourke and Franks 1995; Crozier and Pamilo 1996; Rosset is relatively common across all lineages of ants (Molet et al. and Chapuisat 2007; Heinze 2008; Lenoir et al. 2011). Many 2012; Peeters 2012; Peeters and Adams 2016; Johnson and authors have focused on the polymorphism of the presence/ Overson 2018). However, the morphology of reproductive females is also associated with the presence of several typi- Electronic supplementary material The online version of this cal queen traits linked to their fecundity (e.g., presence of article (https​://doi.org/10.1007/s0004​0-019-00716​-w) contains a spermatheca, high number of ocelli, complex structured supplementary material, which is available to authorized users. thorax, large gaster and developed ovaries) that are reduced or absent in non-reproductive castes. * I. Armbrecht [email protected] According to the novel model of developmental evolution in ants proposed by Molet et al. (2012), rare intermediate 1 Department of Biology, Universidad del Valle, Calle 13 morphotypes, such as intercaste individuals, have acciden- 100‑00. Ed. E20, Of. 3025, Cali, Colombia tally deviated from their normal developmental pathways 2 Laboratoire d’Ethologie Expérimentale et Comparée due to environmental or genetic perturbations. Thus, they EA 4443, Université Paris 13, Sorbonne Paris Cité, present mosaics of winged queens and worker characters. 93430 Villetaneuse, France

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The morphology of intercastes is reported to be highly varia- most abundant species in the Winkler extraction of leaf lit- ble in several species (e.g., Temnothorax nylanderi, Plateaux ter. Inside both riparian and secondary forests, the species 1970; Molet et al. 2012; Johnson and Overson 2018) while is among the most abundant, accounting for approximately the morphology of ergatoid (worker-like apterous queens, 40% of captures (Jiménez-Carmona et al. 2015). As expected Amor et al. 2011) can vary into distinct categories or not, for being a deep-forest species, it is almost absent in severely according to the species considered (review in Peeters 2012). transformed habitats, such as crops or pasturelands, even The study of ergatoid queens is particularly interesting to in ecologically restored ones (Donoso and Ramón 2009; understand the evolutionary signifcance of these alternative Abadía et al. 2010; Zabala et al. 2013; Chacón de Ulloa and phenotypes, since they present a simplifed thorax similar to Abadía 2014; Herrera-Rangel et al. 2015). that of workers—as a consequence of their absence of wing Despite its ecological importance as a forest bioindicator muscles—but are fully reproductive females (Peeters and (Herrera-Rangel et al. 2015), the natural history and social Adams 2016). They can occur together with alate queens structure of G. bisulca is poorly known. Therefore, this in the same colony, or replace them, but rarely occur with study sought to explore the social composition (number of brachypterous queens, other short-winged morphotypes that individuals, castes, morphology of reproductive females) in cannot fy (Johnson and Overson 2018). colonies of G. bisulca to understand the role of ergatoids, Among the ants, the Ectatomminae (: For- both in their contribution to reproduction and to spatial micidae) are relatively specialized hunter ants, whose natu- structuration of the population (DCF, polydomy). To test ral history and ecology has been largely unknown (Lattke for ecological infuences on the social organization in this 1995). However, several studies have pointed out the vari- species, we investigated the colony structure and distribution ability in the social organization of these ants: microgynes of G. bisulca in four diferent populations from natural mon- in Ectatomma ruidum (Lachaud et al. 1999; Lenoir et al. tane forests in Colombia difering in the degree of habitat 2011), gamergates due to the presence of a spermatheca disturbance: one site is located in a protected natural park in workers of Gnamptogenys menadensis and G. striatula while the rest of them are immersed in a matrix of unshaded (Gobin et al. 1998, 2001; Blatrix and Jaisson 2000; Lom- cofee crops. melen et al. 2006) but also the presence of both ergatoids and gamergates in some populations of G. striatula (Blatrix and Jaisson 2000; Giraud et al. 2001; Kaptein et al. 2003). Gnamptogenys bisulca Kempf and Brown is a species Materials and methods known from Mexico, Costa Rica, Ecuador and Colombia (García-Martínez et al. 2015). In this last country, it has been Study area and sampling for colony distribution recorded in most of the western states, at altitudes between 1000 and 2000 m.a.s.l., and from humid to dry tropical for- Sampling was carried out in several villages of La Celia ests (Lattke et al. 2008). The species, which was described Municipality, Risaralda Department, west-center in Colom- from leaf litter samples in Colombia (Kempf and Brown bia (Fig. 1; Online Resource 1). The studied landscape pre- 1968) nests in rotten wood, mainly in small twigs on the for- sented a broken relief with rugged slopes, and heterogeneous est foor (Jiménez-Carmona 2015). Their colonies are small, sight, containing towns, forest relicts (~ 24% overall), open of approximately 30 individuals, and the female reproduc- sun cofee (~ 65%), but also open cattle pastures, plantain, tive caste is composed of queens and sometimes ergatoids. maize and bean plantations among other crops (Zabala et al. While colonies frequently, but not always, present ergatoids 2013). The study was carried out inside forests located in (approximately 12% of nests, Jiménez-Carmona et al. 2015), four independent villages with a minimum of 4 km separa- their role has never been investigated. tion distance: La Secreta, El Brillante, El Tambo and La This variability in social organization may help to under- Polonia (Fig. 1; Online Resource 1). La Secreta forest, is stand why some species are able to persist in natural habi- located in Verdum Regional Natural Park, and is considered tats (usually forests) after severe fragmentation and anthro- the most conserved forest. The remaining forests were sur- pogenic disturbances. In this way, G. bisulca Kempf and rounded by sun cofee plantations in fragmented landscapes. Brown is an appropriate model because it has been described The areas of all forests studied for spatial distribution were as a biological indicator of forested habitat (Abadía et al. calculated using ArcGIS software (Version 10.3). All of 2010; Herrera-Rangel et al. 2015). Most information about them shared similar climatic conditions, within the natural G. bisulca has been gathered from sampling studies deal- zone of the Very Humid Premontane Forest, with 2500 mm ing with ant diversity (Zabala et al. 2013; Herrera-Rangel annual rainfall (Cultid-Medina and Escobar 2016), average et al. 2015) in diferent kinds of human management, such temperatures around 18 °C, 83.3% average relative humidity, as cattle pastures, and crops, as well as in riparian forests and altitudes ranging from 1718 to 2107 m a.s.l. (for details, and mainland forests. G. bisulca has shown to be one of the see Online Resource 1).

1 3 Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests

Fig. 1 Location and landscape context of the study sites in the forest coverage and white color indicates deforested areas devoted to Departments of Risaralda and Quindío, Colombia. The 12 red dots other land uses. Black thick lines indicate Department boundaries, locate the points where samplings took place. Green color indicates while grey lines are roads (color fgure online)

Inside each village, two sampling plots, separated by at were located with respect to their position inside the quadrat least 2 km from one another and located 80 m from the forest and the plot. edge, were haphazardly chosen. Sampling was carried out A set of 26 individuals from the diferent localities were between January and September of 2017, in fve sampling deposited as references at the Universidad del Valle Museum events as follows: La Secreta (plot 1 January 10–12; plot 8 of Entomology, under the Colombian Environmental Min- on September 16), La Polonia (plot 2 February 7–11 and istry permission # 0120, August 24, 2015 (compactor 5F plot 7 June 6–7), El Tambo (plots 3 and 4 March 22–28), box 19). All specimens were examined for species identifca- El Brillante (plots 5 and 6 June 3–6) (Online Resource 1). tion following Lattke et al. (2008). Each of the eight plots consisted of 10 m × 10 m areas, which were, in turn, equally divided in 1 m × 1 m quadrats using Colony composition, external morphology rope forming a grid (n = 100). Visual search and manual and ovary development collection were conducted within each of the quadrats, care- fully searching both in leaf litter and inside any fallen twigs All individuals and brood composition (number of immature or small tree trunks. In addition, when a colony was found individuals and their stages) were examined to determine near to a quadrat border, an additional search of 2 m radius the social organization of the nests. Most of the collected around that nest was made. All colonies found inside a plot individuals were examined for their external morphology,

1 3 D. M. Urcuqui et al. specifcally at the mesosoma (particularly the mesonotum), system. Density per plot was calculated in terms of the and head using Nikon stereoscopes models SMZ 645, and number of colonies per hectare. Spatial distribution of the SMZ 745, with augmentation binocular lenses up to 8.0 × colonies was determined using the nearest neighbor method (4.0 × 2.0). The external morphological structures, sclerites from Clark and Evans (1954) with Donelly’s correction to and sutures, were named according to Serna and Mackay avoid edge efect (Sinclair 1985) with 5% threshold error (2010) and after specialist revision (R. J. Guerrero). Photos considered statistically signifcant. This method is based on from the head and diferent parts of the thorax were taken the relation between the observed and expected distances with a Nikon Ds-Ri1U3 camera, Nikon SMZ_1500 stereo- of a colony and its closest neighbor. The interpretation is as scope and Nikon ECLIPSE Ni-U90 microscope. The scale follows: aggregated, random or uniform when values tend and editing of the photographs was carried out using the to zero, one, or close to 2.15, respectively. Donelly’s correc- programs Adobe Photoshop and Corel Draw. Since the dark tions serve to correct imprecisions generated by edge efects. brown color of these ants makes it difcult to distinguish Social structure was described in terms of the percentage certain structures at the mesosoma or the number of ocelli of each caste in a colony, previously confrming the presence in head, some de-colorations were made using potassium of brood in each colony (i.e., eggs, larvae and pupae or any hydroxide (KOH), using a 40% dilution, which was heated in of them). Additionally, a grid was drawn to locate all nests a water bath for 10–20 min, and rinsed afterwards. Ergatoids inside and around the plots. The nests were colored diferen- and queens were identifed and separated from workers by tially according to the type of reproductive females (without examining their head (presence and number of ocelli) as well reproductive, monogynous or polygynous queenright colo- as their mesosoma. nies and monogynous or polygynous colonies with ergatoid, As most individuals were immediately stored in 96% Online Resource 2). This spatial distribution could also pro- ethanol after collection in the feld, they were not suitable vide insights about population structure such as polydomy. for the dissection of the female reproductive organs, except Few colonies with high mortality of brood and workers were in plot 8 where they were kept alive. To obtain more infor- discarded from the analyses. Therefore, for each variable, mation about the reproductive status of the queens and erga- the sample size is given along with the mean and standard toids and for logistical reasons, we randomly sampled (not error. Comparisons of social structure among all plots in the using the quadrat system) colonies from three additional four villages were tested by χ2 with permutations using the sites. Sampling was carried out between September 2017 R program (R Development Core Team 2018). and June 2018 (Fig. 1; Online Resource 1): (1) a forest at Correlations between the number of workers (the Chorritos (19 nests); (2) two close places at El Tambo forest response variable) and, respectively, the number of ergatoids (18 nests); and (3) Filandia forest (Department of Quindío). and the number of queens were carried out using the cor.test These individuals were also used for further external mor- function of the stats library of the R program. A general lin- phological observations. eal model (GLM) analysis was used to compare the response Individuals were frst put to sleep and then killed by variable “number of workers” according to four categories placing them in a freezer at − 18 °C for 5 min, after which (“treatments”): (1) monogynous queenright colonies, (2) their gaster and petiole were withdrawn with a fne needle. polygynous queenright colonies, (3) monogynous colonies Dissection of the abdomen was made in a 0.65% sodium with ergatoids and (4) polygynous colonies with ergatoids. chloride saline solution and observed through a Nikon Mixed colonies (those with both queens and ergatoids) did E200 optical microscope, at the Laboratory of the Biology not enter the analysis because the sample size was too small Graduate Program (Universidad del Valle, Cali, Colombia). (see results). For this comparison, GLM with Negative Bino- The presence of a spermatheca was checked for evidence mial distribution was carried out, and a Fisher multiple com- of insemination. The number of ovarioles per ovary, num- parison was further conducted to determine which groups ber of the developed oocytes, and ‘presence or absence’ of were responsible for the diferences. The same procedure yellow bodies in the ovaries (as an indicator of previous was repeated for the response variable “number of individual oviposition, proposed by Peeters 1987), were also recorded. brood”, except for the Fisher comparison, with R. In some cases, due to the loss or crushing of material dur- Finally, to determine whether workers belonging to ing dissection, “n” number will not always be the same for monogynous colonies headed by either a queen or an erga- all measured variables or because some variables were not toid difered in size, Weber’s length (WL) (Weber 1938) available for all reproductive individuals. was used as an indicator for size comparison. For this, the WL of fve workers from each of 15 monogynous queen- Data analyses right colonies and 15 monogynous colonies with ergatoid (75 + 75 = 150 workers in total) was measured with the ocu- Maps were drawn by locating each colony in the plot as if lar micrometer of the stereoscope. The average length values it was a cardinal plane, using the distance in a coordinate for each colony (i.e., the sampling unit is the colony, not the

1 3 Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests individual) were used to compare the two groups of leading and 0.74 (Table 1). Average colony density was 2250/ha, reproductives (n = 15) through a t test using PAST (Pale- ranging from 800/ha (plot 1) to 3000/ha (plot 7) (Table 1). ontological statistics Version 3.20) (Hammer et al. 2001), checking previously for normality of data distribution (Sha- Morphology of female adults piro–Wilk test) and variance homogeneity (Levine’s test). Whenever the assumptions were not met, a Mann–Whitney A total of 6331 individuals from 250 nests were exam- test was performed. ined for their mesosoma and head (presence and number of ocelli). Externally, G. bisulca presents a non-prominent mesonotum in profle, without tubercles; the area between the promesonotal suture and metanotal sulcus is small, gen- Results erally of uniform width; the petiole is one segmented with a semi-quadrat subpetiolar process (with a posterior angle); Spatial distribution of colonies the gaster presents a constriction and a well-developed sting (Fig. 2a). Over all sites and samplings, a total of 274 colonies (Online Three morphological castes of females were found: Resource 1) were found, all of them located in fallen twigs workers, ergatoids and queens (Fig. 2). Weber’s length and branches in a wide range of decomposition states, rang- (WL) was not statistically different between workers ing from twigs still having diferentiable vascular tissue originated from both groups of reproductives, queens to hollow ones, although most of them were still in hard and ergatoids (WL 1.268 mm ± 0.029; n = 15 colonies wood. No other substrate was found to be colonized by G. and WL 1.284 mm ± 0.026; n = 15 colonies, respectively; bisulca. Several colonies had individuals (n = 20 in total) t = 1.5; p = 0.13) but signifcant diferences were observed with attached mites, and three other colonies were sharing among WL in the castes. Queens’ WL was statistically their nesting branch with Cyphomyrmex sp. (one nest) and longer than E1-Ergatoids’ WL (WL = 1.488 mm ± 0.041; with Heteroponera monticola (two nests). n = 11 individuals and WL = 1.347 mm ± 0.03; n = 9 indi- Over the 233 colonies collected in the plot areas, 180 viduals, respectively (Mann–Whitney U = 0.50; Z = 3.714; were located within the plot and 53 outside or around it p < 0.001), and than workers’ WL (WL = 1.488 mm; n = 11 (Table 1; Online Resource 2). Considering only the colonies vs. WL 1.268 mm n = 15; t = 15.923 p < 0.000001). Addi- inside plots, the distribution was always random at each of tionally, E1-Ergatoid’s WL was signifcantly longer than the eight plots (Table 1): the Clark and Evans index (R) workers’ WL of both origins: workers from monogynous varied between 0.71 and 1.11; and C varied between − 1.19 colonies with queens (WL = 1.347 mm vs. WL 1.268 mm,

Table 1 Distribution and demographic description of the colonies collected in each plot (P1–P8) Village La Secreta La Polonia El Tambo El Brillante P1 P8 P2 P7 P3 P4 P5 P6

Nest distribution Number of nests 8 24 29 30 22 29 23 15 Nest density/ha 800 2400 2900 3000 2200 2900 2300 1500 Clark and Evans index (R) 0.71 1.11 1.02 0.95 0.80 1.10 1.04 1.01 C − 0.94 0.73 0.17 − 0.33 − 1.19 0.74 0.29 0.04 Nest demography Number of nests located in map* 8 28 43 17 24 48 23 17 Nest with no reproductives 2 6 9 4 5 9 2 4 Monogynous Q 4 12 11 1 2 8 12 4 Polygynous Q (number queens) 1 (2) 10 (2–10) 5 (2–7) 1 (2) 2 (2) 1 (2) 4 (2–4) 4 (2–8) Monogynous E 0 0 11 3 3 12 4 3 Polygynous E (number ergatoids) 0 0 6 (2–4) 8 (2–6) 12 (2–6) 16 (2–4) 0 1 (2) Mixed (Q and E) 1 (5–1) 0 1 (1–1) 0 0 2 (1–1, 1–2) 1 (2–1) 1 (1–1)

Distribution: R: Clark and Evans’ index, C: standardization values. Nest demography: numbers inside parentheses mean minimum–maximum values. Conventions: Q for queen and E for ergatoid; mixed: nests presenting both queens and ergatoids (in parenthesis, frst the number of queens and then number of ergatoids) *These numbers do not correspond to all nests in the study, but just to those nests which provided information on social structure

1 3 D. M. Urcuqui et al.

Fig. 2 External morphology of typical Gnamptogenys bisulca females. a Worker in lateral view. b Frontal view of queen head. c Frontal view of an ergatoid with one ocellus. d Frontal view of an ergatoid with two ocelli. e Frontal view of an ergatoid with three ocelli. Scale bar 0.1 mm (color fgure online)

respectively; Mann–Whitney Z = 4.01; p < 0.0001), queens, promesonotal suture curved anterodorsally in dif- and workers from monogynous colonies with erga- ferent degrees according to individual variations; mesosoma toids (WL = 1.347 mm vs. WL 1.284 mm, respectively; appears intermediate between that of workers and queens Mann–Whitney Z = 3.89; p < 0.0001). with four variations (Online Resource 3): type E1 is the most Workers None of the 5939 workers checked, presented frequent, with 146 individuals (= 72% of the total) from 80 ocelli. Their metanotum was fused with the propodeum. All diferent nests presenting this morphology. The three other individuals, except two (≈ 0.03%), presented the same exter- types are less frequent, with 17% for E2 (35 individuals nal mesosomal morphology (Online Resource 3). from 26 diferent nests), 9% for E3 (18 individuals from Queens 190 queens from 106 colonies were externally 16 diferent nests) and only 2% for E4 (three individuals observed. All queens had three ocelli (Fig. 2b) and wing from two nests), respectively. De-colorations of these indi- scars (Online Resource 3). Promesonotal suture was curved viduals made further morphological measurements of these anterodorsally in diferent degrees according to individual individuals unavailable. There was no apparent relation variations; metanotum was always separated from the propo- between the number of ocelli and the particular variations deum by a fovea. All queen individuals presented the same of the mesosoma. morphology (Online Resource 3), except one individual (= 0.5% of cases). Development of the reproductive organs Ergatoids 202 ergatoids from 124 colonies were observed externally. Their head presented one (56.9% of individu- The reproductive organs in the female castes were composed als), two (10.8%) or three ocelli 32.6% (Fig. 2c–e). As in of two polytrophic ovarioles, each one emptying in a lateral

1 3 Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests common oviduct; the ovarioles were close to each other and empty and yellow bodies were absent (except for fve indi- the frst nervous ganglion concealed the oviducts externally. viduals or 9.4%). Those females with underdeveloped ovari- The development and number of the ovariole chambers var- oles represent mainly dealated unmated gynes or inhibited ied among ants according to the castes (Fig. 3). queens and were mainly found in polygynous nests, although Workers 62 workers from 32 nests were dissected to two were from monogynous ones (Fig. 3d, e). observe their ovary development. A spermatheca was always Ergatoids From the additional samples collected in Filan- absent. Workers presented two short ovarioles, which were dia and in El Tambo, 20 colonies (n = 37 ergatoids dissected usually not developed (Fig. 3a), but some variations in the in total) provided information about ergatoid reproductive number and activity of the ovariole chambers were observed: status (no ergatoids were found in Los Chorritos). Ten nests one or two oocytes developed in only one or both ovarioles were monogynous, with an ergatoid as the only reproductive, (Fig. 3b). Dissected workers came from both queenright and all of them, except two, had developed ovarioles: the (monogynous and polygynous) and queenless colonies; it number of oocytes was, on average, 5.21 (ranging from 2 to means that ovarioles of workers from queenless colonies 10 oocytes), the spermatheca was always full of sperm and were not more developed than those of workers from queen- most of the individuals presented yellow bodies (Fig. 3f). right nests. Yellow bodies were absent. Eight nests were polygynous and all of them always had Queens 85 queens from 35 colonies were dissected (19 only one reproductive ergatoid, all other ergatoids being from plot 8 at La Secreta, and 16 from Los Chorritos). The non-reproductive, except for one nest. Two nests were found queens always presented two ovarioles. The spermatheca, a with the two kinds of reproductives simultaneously: a queen rough sack, was always present and overlapped the common (in both, one queen) and some ergatoids (two and four). In oviduct below the frst nervous cord ganglion; it appeared these cases, the real reproductive female was the queen. translucent when empty (gynes; Fig. 3h) and yellowish when We found no correspondence between the external mor- full (queens; Fig. 3i). phological characters (both number of ocelli and shape of In 36.9% of queens, the two ovarioles were usually long thorax, Online Resource 3: E1, E2, E3) and ovarian develop- and well developed, each containing at least 12 chambers ment (Fig. 3f, g) in ergatoids. From the 37 dissected erga- with oocytes and nurse cells in diferent degrees of develop- toids, 24 were of E1 type (the half presenting highly devel- ment; the spermatheca was always full of sperm and most oped ovarioles), 5 were E2 (one and four with developed and of the individuals presented yellow bodies. All queens from not-developed ovarioles, respectively), 6 were E3 (two and monogynous colonies presented this high ovarian develop- four, respectively); and 2 were E4 (both with underdevel- ment and only one of the queens in all polygynous colonies oped ovarioles) even though this type is the most similar to a (Fig. 3c). queen. In summary, from the 37 ergatoids dissected, 41% had The remaining 63.1% dissected individuals presented two long developed ovarioles (Fig. 3f). The remaining 59% underdeveloped ovaries, with zero to three oocytes per ovari- dissected ergatoids, mainly from polygynous nests (all but ole (mean of 1.21 oocytes), the spermatheca was generally two) presented underdeveloped ovarioles with a maximum

Fig. 3 Dissections of reproductive organs in Gnamptogenys bisulca ovarioles chambers. e Unreproductive queen’s organ without devel- workers, queens and ergatoids. a Worker without development of opment of oocytes in the ovarioles. f Ergatoid with development oocytes in the ovarioles. b Worker with one oocyte developing in an of oocytes along the chambers of the ovarioles. g Ergatoid without ovariole while the other is empty. c Queen reproductive organ with oocyte development in the ovariole’s chambers. Scale bar 0.25 mm. several oocytes developed along the ovarioles chambers. d Unre- h Empty spermatheca. Scale bar 0.04 mm. i Full spermatheca (sperm productive queen’s organ with various oocytes developed along the cells). Scale bar 0.04 mm (color fgure online)

1 3 D. M. Urcuqui et al. of three oocytes per ovariole, the spermatheca was generally corrected) showed that there was no diference between the empty and yellow bodies were absent (Fig. 3g). number of workers in monogynous vs. polygynous colo- nies with ergatoids ( x̄ = 18.60 vs. x̄ = 18.91, respectively; Social organization and demography p = 1.0). Neither was there a diference between the number of workers in mono and polygynous colonies with queens Colonies in plots were represented with colors in the plot ( x̄ = 33.96 vs. x̄ = 40.61, respectively; p = 0.11), although maps, depending on their social organization (Online the average number of workers in colonies with queens Resource 2). A range of 9–28% (in total, n = 41 over 208) of was signifcantly higher than in colonies with ergatoids the excavated nests were collected without any reproductive. ( x̄ = 35.73 vs. x̄ = 18.76, respectively, p < 0.01). In polygy- However, these colonies presented only few workers (≤ 10 nous colonies, the number of workers was signifcantly and individuals), and were either completely lacking a brood positively related to the number of queens (Spearman = 0.32, or presented few eggs and larvae, except in 13 cases that p = 0.001), but it was not related to the number of ergatoids could correspond to the loss of the queen during the collec- (Spearman = 0.09, p = 0.41). tion or a dying colony due to the death of the reproductive The number of immature individuals, i.e., eggs, lar- female. These colonies were excluded from further analyses vae and cocoons (Table 2), was not statistically differ- (Table 1). ent (Chi = 1.70, p = 0.64) when compared among nests From the inspected colonies containing reproductive with one queen ( x̄ = 36.6 ± 4.3; n = 61) or several queens females, about one quarter (n = 54 or 25.9%) contained ( x̄ = 28.1 ± 5.6; n = 35), or in monogynous colonies with monogynous queenright colonies, although, as stated above, ergatoid ( x̄ = 29.7 ± 3.5; n = 43) and polygynous ergatoid the species presented facultative polygyny (n = 28, especially ( x̄ = 26.6 ± 3.4; n = 43) colonies. in plot 8), with 2–11 queens per colony. As described above, Twelve colonies were small, with 10 of them having 1 the species also presented ergatoids both in a monogy- queen and 10 or fewer workers, which could correspond to nous (n = 36) or polygynous colonies (n = 43, with a range a foundation by a queen, with one case of a single queen. of 2–6 ergatoids per colony), but they were rarely found For monogynous colonies with ergatoids, colonies were also together with a “normal” queen (n = 6, representing 2.8% of small since 37% of these colonies contained ten or fewer nests). Indeed, a signifcantly negative relationship between workers but without any cases of ergatoids alone in a colony. the number of queens and ergatoids was found (Spear- man = − 0.83, p = < 0.001). Social organization and ecological context Taking both types of reproductive females into considera- tion, 53.8% (n = (54 + 36)/167) of colonies were monogy- The forest areas were as follows: 8 ha for El Tambo, 135 ha nous, headed by a queen or an ergatoid, respectively. The for el Brillante, 637 ha for La Polonia and more than 1531 ha rate of polygyny, including ergatoids, ranged from 0.23 in for la Secreta (Online Resource 1). Social organization in plot 5 to 0.74 in plot 3 (mean ± SE = 0.46 ± 0.18). the plots from the four villages at La Celia Risaralda was The number of adult individuals per colony varied from tested through a 6 × 5 contingency table (see “Data analy- 1 to 88 with a mean of 22.3 ± 1.1, although 71.6% of the ses”), which showed highly signifcant diferences in the nests contained less than 30 individuals. The number of proportion of the types of colony (χ2 = 63.087; p < 0.001) workers per colony was statistically diferent depending with a high Cramer contingency coefcient of 0.354. In the on the type and number of reproductives inside the colony two plots at La Secreta, the forest which belongs to Verdum (Table 2) (analysis of deviance, type II tests, Chi = 46.45, Regional Natural Park, almost all colonies presented at least p < 0.001). Fisher multiple comparisons (Bonferroni one queen as reproductive, while the other forests, which

Table 2 Colony size according to the type of reproductive females Queen Ergatoid Mixed nest Monogynous Polygynous Monogynous Polygynous

N (nests counted for workers) 97 36 43 43 4

Nworkers 33.9 ± 1.9 (2–84) 40.6 ± 3.2 (4–81) 18.6 ± 2.2 (2–56) 18.9 ± 1.6 (2–61) 41.5 ± 8.27 (18–56) N (nests counted for brood) 61 35 43 42 4

Nbrood 36.6 ± 4.3 (0–156) 28.1 ± 5.6 (0–97) 29.7 ± 3.5 (0–94) 26.6 ± 3.4 (0–71) 79.75 ± 3.97 (66–94)

N number of nests, Nworkers mean (± standard error) number of workers (minimum and maximum values in parenthesis), Nbrood mean (± SE) number of immature individuals (eggs, larvae and cocoons). Note that N changes for each response variable because not all colonies in the study could be evaluated for all variables

1 3 Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests were located in highly fragmented landscape contexts, had distribution found in this study suggests low intraspecifc high proportions of colonies with ergatoids (Table 1). competition and that resources are abundant in the leaf litter In terms of local distribution, there were no monogy- of forests (Soares and Schoereder 2001). nous queenright colonies or polygynous queenright colo- However, either interspecifc competition or coexistence nies being surrounded by colonies with ergatoids (Online may occur for certain ecological resources, especially for Resource 2), neither was there a pattern of colonies with nesting sites: three colonies were shared in the same branch workers but without reproductives surrounding colonies with two other ant species, one nest with Cyphomyrmex sp. with queens or ergatoids. and two nests with H. monticola (nests were independent but inside the same twig). This species is known to share leaf litter nesting microhabitat with at least 44 other ant species Discussion (Armbrecht et al. 2004; Souza et al. 2012) and up to 112 leaf litter forest ant species, as found by Jiménez-Carmona Nesting ecology, demography and local spatial (2015) close to the study place. distribution Castes and morphological gradation of ergatoids All G. bisulca’s colonies collected in this study were found in G. bisulca inside fallen twigs and branches, which is consistent with the records in other Andean forests (Filandia, Quindío, Colom- Three types of female were observed: queens were found bia; n = 70; Jiménez-Carmona 2015). It can, therefore, be to be signifcantly larger than ergatoids, which were them- stated that this species is a specialist for substrate nesting selves, larger than workers. However, workers did not difer (in fallen twigs and branches). Other Gnamptogenys spe- in size when they were produced in a colony headed by a cies such as G. horni and G. striatula have been reported queen or an ergatoid. to nest in the same type of structure but also under leaf lit- The four forms of ergatoids observed seemed to present ter or organic matter even 1 m from the soil (Lattke et al. intermediate morphologies from worker to queen thorax: 2008). Due to its specialization of nesting in small twigs, the simpler structure observed in type E1, which resembled the colonies of G. bisulca are relatively small, 2/3 of nests a worker all the way to type E4, which had a more complex presenting less than 30 individuals. However, this study and sculptured thorax, much similar to the queen’s thorax. reports nests with more than 80 individuals while Jiménez- Queen-specifc traits as the number of ocelli and the devel- Carmona et al. (2015) found a maximum of 30 individuals opment of reproductive organs varied among ergatoid types by examining 70 nests in a population close to this study but were not expressed coherently in intercastes: ergatoids site (Filandia, Quindío, Colombia). In species of the same E4, the more morphologically similar to queen, did not pre- , the colonies are also usually small, with a number of sent the most developed ovarioles. This feature has already individuals between 80 and 120 in G. aculeaticoxae, more been observed in intercastes of other species (e.g., in T. than 200 in G. moelleri and in the rare G. horni (Lattke nylanderi, Okada et al. 2013). To our knowledge, this is 1990; Pratt 1994; Lattke et al. 2008) and 12–193 in G. the frst study that reports diferent morphological types of menadensis (Gobin et al. 1998, 2001). The most crowded ergatoids in G. bisulca living in the same habitat. colonies belong to G. striatula nests, consisting of 150–200 The development of caste individuals inside a colony is individuals (Lattke 1990) and up to 660 individuals have mainly related to the division of labor, to increase its ef- been collected in Brazil (Blatrix and Jaisson 2000; Oliveira ciency. An immature individual develops into a reproductive et al. 2015). female (here, queen or ergatoid) or a worker depending on The spatial distribution according to the R index was ran- its nutrition (Smith et al. 2008) but also on other environ- dom in all plots while the aggregation of colonies would be mental factors such as temperature, queen pheromone level expected due to the presence of ergatoids (possibly linked and also genetic control (Anderson et al. 2008; Belgade et al. to colony fssion, see below). Nest availability and food 2011). Thus, a rich larval diet may result in high levels of the resources are among the main ecological factors afecting Juvenile Hormone being produced, which may lead larvae the spatial distribution of ants (Bernstein and Gobbel 1979; to develop into queens. In this way, wingless reproductive McGlynn 2010). As twigs constitute a restricted (because females like ergatoids are less costly to produce than nor- they are small) and unstable nesting place (since they mal queens for a colony (Heinze 1998; Molet et al. 2009; decompose quickly), colonies may need to move frequently Molet et al. 2012) and their presence would be favored when to a new place. This could be exacerbated by an increase in habitat is limited in resources. This could be the case in this the size of the colonies, if nesting resources become avail- study, where the frequency of ergatoids was higher in the able from new fallen twigs, or due to other disturbing factors forests that were immersed in agricultural matrices, which in leaf litter such as army ant raids (Kaspari 1996). The nest are more fragmented/degraded contexts. Although we did

1 3 D. M. Urcuqui et al. not prove it, it could be hypothesized that the environmental the action of pheromones, which alter the size and develop- conditions in these small forest fragments are worse for these ment of their ovaries (Fletcher and Blum 1981; Giraud et al. forest ants than in La Secreta and Los Chorritos, because 2001; Lenoir et al. 2011). Furthermore, the queens and erga- these last two sites belong to the Verdum Natural Park, a toids found in this study appeared not to have been mated, more preserved and less fragmented place. possibly corresponding to young individuals which have not yet left the colony for mating, or females whose own Social structure and reproductive strategies in G. reproduction failed and who consequently were readopted bisulca by their natal colony. Thus, only one queen in each colony contributed to the growth and composition of the colony, At least one reproductive female (queen or ergatoid) headed and the others may help with other tasks within the colony most colonies. Fewer than 20% of nests were found with (Gobin et al. 1998; Steiner et al. 2010). Another Ectatom- no reproductive individuals, but with the presence of few minae, E. ruidum, has also been reported to have functional workers with a small amount of brood. This fnding could be monogyny, with inhibited mated queens (Lenoir et al. 2011). considered a consequence of either the constant turnover of This study also found that colonies with queens contained colonies according to nesting resource dynamics, or a con- double the workers than those with reproductive ergatoids, sequence of polydomy, the fact that a colony occupies more which supports the idea of fssion by ergatoids and a set of than one nest, these interconnected satellites being more or workers, as a complementary mode for dispersal (Peeters less distant according to the species (review in Ellis et al. and Ito 2001). Indeed, ergatoids are low-cost reproductives 2017). However, the rare cases showing a mature colony because they have no developed fying muscles (Peeters size (up to 46 workers) with the presence of abundant brood and Ito 2001). Ergatoids have been reported in numerous suggest recent queenless colonies due to the death of the ant species (Heinze 1998; Peeters and Ito 2001; Johnson founding queen rather than a polydomous structure of the 2010; Peeters and Adams 2016) and queens coexist with population (e.g., Ellis et al. 2017). Although we did not test ergatoids in at least fve more ant genera, such as Monomo- especially for this hypothesis in this study, we argue that rium, Myrmecia, Octostruma, Megalomyrmex and Harpa- polydomy is less likely considering that no nests without goxenus (Heinze 1998 and references therein). Evolutionar- reproductive females were observed close to queenright ily, queens can be completely replaced by wingless female colonies or colonies with ergatoids (Online Resource 2) and reproductives depending on ecological conditions (Heinze that we did not observe any transportation of workers or 1998). While our data did not show a pattern of aggregation brood during the collection of the colonies. Further studies of ergatoid colonies around colonies with queens, we sug- regarding the polydomy in this species could be performed gest that ergatoids were possibly produced as an alternative with genetic analyses of colonies relationships based on reproductive strategy to occupy the surroundings of their polymorphic nuclear markers. natal colony by fssion, especially when habitat conditions Gnamptogenys bisulca appears to be facultatively polygy- deteriorate. Thus, we propose that this species possesses nous in all of the studied plots, with a low number of repro- both systems of founding: (1) independent colony foun- ductives per colony, with colonies containing (in the same dation with normal queens (ICF), in which queens found plot) normal queens or ergatoids. In contrast, dissection of alone, and (2) DCF in which ergatoids found, by budding, the reproductive organs supports a functional monogyny: a more secure colony due to the presence of workers from ovaries of only one queen were fully developed in polygy- their natal colony (Peeters and Ito 2001; Peeters and Molet nous colonies with several queens. We observed the same 2010). In fact, it has been argued that the loss of fight in pattern for polygynous colonies with ergatoids (only one reproductive females could be an adaptation to promote sur- showing developed ovaries), but in the few cases of mixed vival in homogenous persistent habitats, with predictable colonies, presenting the two types of females, a single resources (Johnson 2010) such as the forests in this study. queen was always the true reproductive. In contrast to other Thus, the benefts of founding success by ergatoid queens Gnamptogenys species presenting gamergates (e.g., workers may compensate for the disadvantages associated with the with spermatheca in G. menadensi and G. striatula, Gobin high mortality of the foundress queens during their aerial et al. 1998, 2001; Blatrix and Jaisson 2000; Lommelen et al. dispersal, mating and founding in deteriorated habitats or 2006), we found no evidence that G. bisulca workers partici- habitats with fewer resources (Johnson 2010). This could pated in the reproduction of colonies. Some workers had one also be the case in G. bisulca, in which cheaper ergatoids or two developed oocytes, which opened the possibility of were mainly produced in forests of degraded landscapes (El laying trophic eggs (Gobin et al. 1998; Steiner et al. 2010), Brillante, El Tambo and La Polonia). The fact that only one but they never presented a spermatheca. case of ergatoid was found associated with queens in the Functional monogyny could result from the inhibition most conserved landscape at La Secreta supports the idea of additional females by the reproductive queen, through that social structure could act as a driver for the ecological

1 3 Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests success of G. bisulca in Andean montane forests. The plas- Chacón de Ulloa P, Abadía JC (2014) Dos décadas de estudio de la ticity to switch from queen to ergatoid morphology could diversidad de hormigas en Colombia. Rev Acad Colomb Cien Exac Fís y Nat 38:250–260 be a strategy to deal with the challenges of habitat quality Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure due here to anthropogenic forest fragmentation and degrada- of spatial relationships in populations. Ecol Soc Am 35:445–453 tion (edge efects, population bottlenecks, changing resource Crozier RH, Pamilo P (1996) Evolution of social colonies sex dynamics among other triggers). allocation and kin selection. Oxford University Press, Oxford Cultid-Medina CA, Escobar F (2016) Assessing the ecological To conclude, this study showed a high variation in the response of dung beetles in an agricultural landscape using social structure of G. bisulca colonies within and among number of individuals and biomass in diversity measures. Envi- forest contexts and landscapes. The presence of two types ron Entomol 45:310–319 of reproductive females (queens and ergatoids), the faculta- Donoso DA, Ramón G (2009) Composition of a high diversity leaf litter ant community (Hymenoptera: Formicidae) from an Ecua- tive polygyny but functional monogyny observed in colonies dorian pre-montane rainforest. Ann Société Entomol de France (with queens or ergatoids as reproductives), the diferences 45:487–499 in ergatoid frequencies according to the site and the low ter- Ellis S, Procter D, Buckham-Bonnett P, Robinson E (2017) Inferring ritoriality of the colonies constituted features that provided polydomy: a review of functional, spatial and genetic methods for identifying colony boundaries. Insectes Soc 64:19–37 fexibility in this species, a high advantage for the adaptation Fletcher DJ, Blum MS (1981) Pheromonal control of dealation and to the dynamic environment where it lives. oogenesis in virgin queen fre ants. Science 212:73–75 García-Martínez MA, Quiroz-Robledo LN, Valenzuela-González JE Acknowledgements Giovany Copete, Alexander Velez y Juan Sebas- (2015) Nuevos registros de hormigas (Hymenoptera: Formici- tian Ramírez helped in feld work. Roberto José Guerrero reviewed for dae) para México y los estados de Oaxaca y Veracruz. Dugesi- morphological structures. Wilmar Torres (Graduate Biology Program ana 22:107–109 ofce, Universidad del Valle, Cali, Colombia) helped in statistical Giraud T, Blatrix R, Poteaux C, Solignac M, Jaisson P (2001) High analyses, GEAHNA ’s research group for facilities, equipment and genetic relatedness among nestmate queens in the polygynous laboratory. Photos were taken by Juan Felipe Ortega, Francisco Lopez ponerine ant Gnamptogenys striatula in Brazil. Beha Ecol Machado and Diana Marcela Urcuqui at the Images Laboratory from Sociobiol 49:128–134 the Biology Graduate Program Department of Biology, Universidad Gobin B, Peeters C, Billen J (1998) Colony reproduction and arbo- del Valle. Helen Burnham checked for proper English. This study real life in the Ponerine ant Gnamptogenys menadensis (Hyme- was fnanced by Universidad del Valle, Research Vicerrectory ofce, noptera: Formicidae). Neth J Zool 48:53–63 through the Project “Estructura del paisaje como modelador del fujo Gobin B, Billen J, Peeters C (2001) Dominance interactions regulate génico de dos especies de hormigas cazadoras en la zona cafetera de mating in Gnamptogenys menadensis. Ethology 107:495–508 los andes”, code CI 71075 and by the bilateral Project Colciencias/Ecos Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological Nord/Universidad del Valle/Université Paris 13 entitled “Estrategias de statistics software package for education and data analysis. Pal- reproducción y estructuras de poblaciones en diferentes especies de aeontologia Electronica 4(1):9 insectos sociales en Colombia” Contract FP44842-672-2015. Heinze J (1998) Intercastes, intermorphs and ergatoid queens: who is who in ant reproduction? Insectes Soc 45:113–124 Heinze J (2008) Social plasticity: ecology, genetics, and the structure of ant societies. In: Korb J, Heinze J (eds) Ecology of social evolution. 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