Journal of Insect Physiology 62 (2014) 21–25
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Strength in numbers: Large and permanent colonies have higher queen oviposition rates in the invasive Argentine ant (Linepithema humile, Mayr) Sílvia Abril ⇑, Crisanto Gómez Department of Environmental Sciences, University of Girona, Montilivi Campus s/n, 17071 Girona, Spain
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Article history: Received 5 July 2013 Received in revised form 1 January 2014 Accepted 9 January 2014 Available online 21 January 2014 Keywords: Formicidae Colony size Invasive species Oviposition rate Polydomy
a b s t r a c t Polydomy associated with unicoloniality is a common trait of invasive species. In the invasive Argentine ant, colonies are seasonally polydomous. Most follow a seasonal fission–fussion pattern: they disperse in the spring and summer and aggregate in the fall and winter. However, a small proportion of colonies do not migrate; instead, they inhabit permanent nesting sites. These colonies are large and highly polydomous. The aim of this study was to (1) search for differences in the fecundity of queens between mother colonies (large and permanent) and satellite colonies (small and temporal), (2) determine if queens in mother and satellite colonies have different diets to clarify if colony size influences social organization and queen feeding, and (3) examine if colony location relative to the invasion front results in differences in the queen’s diet. Our results indicate that queens from mother nests are more fertile than queens from satellite nests and that colony location does not affect queen oviposition rate. Ovarian dissections suggest that differences in ovarian morphology are not responsible for the higher queen oviposition rate in mother vs. satellite nests, since there were no differences in the number and length of ovarioles in queens from the two types of colonies. In contrast, the higher d15N values of queens from mother nests imply that greater carnivorous source intake accounts for the higher oviposition rates. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Ant societies can adopt different strategies of colony structuration. A given colony can occupy one nest (monodomy) or several socially-connected but spatially-separated nests (polydomy) (Debout et al., 2007; Hölldobler and Wilson, 1977). Polydomy associated with unicoloniality (the lack of territorial boundaries between neighboring nests) is a characteristic trait of invasive species (Debout et al., 2007). Polydomy is closely tied to the low level of genetic variation exhibited by invasive unicolonial ants and gives them a significant ecological advantage in terms of resource capture, which facilitates their spread in areas to which they have been introduced (Debout et al., 2007). The Argentine ant, Linepithema humile, clearly demonstrates the advantages of being unicolonial and polydomous. Native to South America, this invasive species has spread worldwide to regions with Mediterranean climates (Suarez et al., 1998; 2001). In the areas to which it has been introduced, the Argentine ant reduces populations of native ants and other arthropods, affects insectivorous vertebrates, and disrupts ant-mediated ecological mechanisms ⇑ Corresponding author. Tel.: +34 972418268; fax: +34 972418150. E-mail address: [email protected] (S. Abril). http://dx.doi.org/10.1016/j.jinsphys.2014.01.004 0022-1910/Ó 2014 Elsevier Ltd. All rights reserved.
such as seed dispersal and pollination (Blancafort and Gómez, 2005; Bond and Slingsby, 1984; Estany-Tigerström et al., 2010; Gómez and Oliveras, 2003; Human and Gordon, 1996, 1997; Holway, 1998; Suarez et al., 2001; Visser et al., 1996). Argentine ants are unicolonial (Passera, 1994), highly polygynous and polydomous (Hölldobler and Wilson, 1977). Its colonies in its introduced range are seasonally polydomous as a consequence of environmental conditions and food resource availability (Diaz et al., 2013; Heller and Gordon, 2006), meaning there is a seasonal pattern of nest fission and fusion (Benois, 1973; Diaz et al., 2013; Heller and Gordon, 2006; Newell and Barber, 1913). Heller et al. (2008) defined an Argentine ant colony as a group of nests who share food and among which ants travel. This definition suggests that its populations do not function ecologically as a single supercolony but rather as a mosaic of smaller and distinct colonies that consist of groups of interacting nests. Most of these colonies move seasonally. In the winter, nests associated with each colony form large aggregations. In the spring and summer, these aggregations split into small, dispersed nests. In the late fall, ants move back to the aggregation sites used the previous winter (Diaz et al., 2013; Heller and Gordon, 2006; Heller et al., 2006). However, a small proportion of colonies do not move their nesting sites seasonally; instead, they maintain permanent,
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year-round nesting sites (Diaz et al., 2013; Heller and Gordon, 2006). The degree of colony permanence shows a positive relationship with colony size (Diaz et al., 2013; Heller and Gordon, 2006). Hölldobler and Wilson (1990) state that large, mature colonies demonstrate clear nest preferences and Heller and Gordon (2006) indicate that changes in microclimate are the proximate cause of Argentine ant nest movements. Thus, it seems that larger Argentine ant colonies tend to occupy permanent nesting sites since such sites have suitable microclimatic conditions. Furthermore, moving these huge polydomous formations would require a great amount of expensive effort for the colony and would subsequently lead to another permanent nest site (Diaz, 2013). Larger colonies were shown to enhance division of labor and task specialization in some ant species (Holbrook et al., 2011; Thomas and Elgar, 2003). Additionally, the most elaborate caste and communication systems occur in species with large and perennial colonies (Hölldobler and Wilson, 1990). In consequence, these large, permanent Argentine ant colonies may be expected to show different social organization from smaller, temporal colonies. Moreover, the social structure of the Argentine ant is greatly affected by ecological constraints. More specifically, nest density, colony size, and queen number and size are affected by the invasion history of introduced populations (Abril et al., 2013; Diaz et al., 2013; Ingram, 2002). For instance, colonies at the invasion front invest more energy in creating more and larger queens (Abril et al., 2013). Whether this investment is a colony-level strategy to ensure the successful establishment of new colonies (Abril et al., 2013) or a consequence of the reduction of nitrogen-rich protein resources in the areas situated behind the invasion front (Tillberg et al., 2007) is still unknown. As Argentine ant workers are completely sterile (Markin, 1970), queens are the only caste capable of reproduction and, consequently, they are responsible for colony growth and reproduction. Therefore, identifying the factors that regulate queen reproduction will bring us closer to understanding the mechanisms underlying the superior competitive ability of introduced populations of this invasive species. Stable isotopes in ecology have been used to record dietary patterns in animals (West et al., 2006). The basic principle of this technique is that the isotopic composition of organisms reflects some aspects of their diet, such as the main sources of energy (De Niro and Epstein, 1981). In the case of ants Blüthgen and Fiedler (2002) and Davidson et al. (2003) showed that the N-isotope signatures of ants exhibiting high fidelity to nectar or honeydew differ from the N-isotope values from omnivorous or predacious ants. In 2007, Fiedler et al. (2007) made a comparison of the stable N-isotope signatures of several ant genera from central Europe and concluded that there was a relationship between the d15N values and the diet nitrogen sources. Therefore, high d15N values indicate a predominant predacious nitrogen source obtained via predation and scavenging, while low d15N values indicate a plant-derived nitrogen source obtained via trophobiosis and nectarivory (Fiedler et al., 2007). In this context, we addressed the following questions. First, we asked if the d15N values of queens from the Argentine ant differed depending on colony location relative to the invasion front and colony permanence. It might be that colonies far from the invasion front are feeding their queens a lower-predacious diet as a consequence of reduced resource availability in their forager-saturated habitat. If so, it could explain why at the invasion front there are more and bigger queens than behind it. Furthermore, larger colonies were shown to create more complex foraging groups that spend more time foraging, allowing more foragers to visit each food source and forage over longer distances than small colonies (Beckers et al., 1989; Beekman et al., 2004; Thomas and Framenau, 2005). Thus, large, permanent Argentine ant colonies may supply
their queens with a more carnivorous diet because their higher forager numbers allow them to more efficiently capture food. To test these hypotheses, we conducted isotopic analyses on queens from temporal colonies at and behind the invasion front and on queens from permanent colonies. Second, we asked whether queens from permanent and temporal colonies differed in their fecundity as a consequence of differences in colony permanence and thus structure. To address this question, we measured the oviposition rates of queens from temporal colonies (at and behind the invasion front) and permanent colonies. We dissected the ovaries of all the queens to better assess and obtain complementary data on their reproductive potential. 2. Material and methods 2.1. Study area Samples were taken from two different L. humile-invaded areas of cork oak secondary forests in the NE Iberian Peninsula. One of the areas is located at the southern edge of the Gavarres massif, near Santa Cristina d’Aro (41° 480 51.7100 N; 3° 010 50.5700 E), and the other is located in the Cadiretes massif, near a developed zone called Pedralta (41° 470 31.5300 N; 2° 580 52.7900 E). Prior to this study, invasion fronts in each area had been identified using bait sampling. Baits were placed every four meters along random transects of 100 m in length, setting a total of twelve transects. The furthest baits visited by the species defined the invasion limit. After identifying the invasion front, we defined the contact zone and the invaded zone. The contact zone was defined as the area in which L. humile and native ants were still in contact. The invaded zone was the area in which the invasion was severe: L. humile nests were highly abundant and the native ant community was almost completely displaced. The contact and invaded zones of the two study areas were ±1 km apart and had similar environmental characteristics. 2.2. Collection of samples Queens were sampled weekly during May 2012 from three types of colonies identified in a previous study (Diaz et al., 2013): (1) Large, permanent colonies (mean nest size 0.94 ± 0.29 m2; Diaz et al. (2013)) called from now on ‘‘mother colonies’’. The mother colonies were present both in the contact and invaded zones, but they were more abundant in the latter. For this reason, all the mother colonies sampled in this study were situated in the invaded zones of the two study sites; (2) Temporal colonies (i.e. remain active at the same nest site for less than 6 months) located at the invasion front, much smaller than mother colonies (mean nest size 0.04 ± 0.01 m2; Diaz et al. (2013)), called from now on ‘‘contact zone satellite colonies’’ and; (3) Temporal colonies located far from the invaded zone and also smaller than the mother colonies (mean nest size 0.04 ± 0.01 m2; Diaz et al. (2013)), called from now on ‘‘invaded zone satellite colonies’’. All the queens analyzed were collected from a total of four mother nests and ten satellite colonies from the contact zone and ten more from the invaded zone. 2.3. Measurement of oviposition rates The oviposition rates of queens from mother colonies (n = 52), contact zone satellite colonies (n = 52), and invaded zone satellite colonies (n = 45) were measured. Field-collected queens and some of their workers (3–5) were immediately isolated and kept for 24 h in test tube nests. The test tube nests consisted of a transparent plastic tube (70 mm in length 10 mm in diameter) and a plastic
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lid. The inner side of the plastic lid was covered by a layer of dry plaster of Paris, which was connected by a wick of cotton wool to a small chamber filled with water. As a result, the inside of the tube remained permanently humid over the course of our observations. The test tube nests were kept at 28 °C, which was the mean soil temperature of the sampled nests obtained using HOBO Ò H8 Pro Series data loggers. After 24 h had passed, the number of eggs laid by each queen was counted using a binocular microscope.
irrespective of the zone (contact or invaded) (GLMM t = 4.45; P < 0.0001) (Fig. 1). Pairwise comparisons indicated that there was no difference in the oviposition rates of queens from satellite colonies in contact vs. invaded zones (P = 0.761); however, they did differ between queens from mother vs. satellite colonies (P < 0.001 in both comparisons).
2.4. Isotopic analyses
The d15N of queens differed between mother colonies and both types of satellite colonies; the mean d15N was significantly higher in the former (GLMM t = 2.849; P < 0.001; pairwise comparisons: mother vs. contact satellite P < 0.05; mother vs. invaded satellite P < 0.01; contact satellite vs. invaded satellite P = 0.321) (Fig. 2).
The d15N signatures of queens from mother colonies and satellite colonies from the invaded and contact zones were compared under the prediction that queens fed with a more carnivorous diet will have higher isotopic signatures in relation to queens fed with a more plant-derived diet (Menke et al., 2010). For this reason, thirty queens for which oviposition rates had been obtained were randomly selected for use in isotopic analyses (n = 10 for each colony type). In preparation, all queens were dried at 70 °C for 24 h, ground to a fine powder, and weighed in capsules. Their abdomens were not included to prevent contamination by food residuals (Tillberg et al., 2006). Each queen was processed individually. Isotopic analyses were conducted in the Stable Isotopic Analyses Lab at the Autonomous University of Barcelona using an elemental analyser – isotope ratio mass spectrometry (EA-IRMS) technique. A Thermo Flash EA 1112 C-N-S analyser and a Thermo Delta V Advantage mass spectrometer were used. d15N values (‰) are expressed relative to atmospheric nitrogen. The reference material used was IAEA600. 2.5. Ovarian dissections To determine if queen ovarian structure differed among the three colony types, we dissected the gasters of queens who had been used in the isotopic analyses. We examined the following ovarian characteristics: (1) the presence or absence of corpora lutea (yellowish remains of nutritive cells left at the base of the ovarioles following oviposition), (2) the number of ovarioles per ovary, and (3) the length of the ovarioles. 2.6. Data analyses We used the R 2.5.1 statistical package (R Development Core Team, 2001) for all analyses. To determine if queen oviposition rate and ovariole number differed among the three colony types, we conducted generalized linear mixed models (GLMM) using a Poisson error distribution and the log-link function (MASS package). To compare queen d15N values and ovariole length among the different colony types, we conducted GLMMs using a Gaussian error distribution and the identity link function (nlme package). In all models, the nest from which a queen was sampled was used as a random factor and the colony type (mother colony, contact zone satellite colony, or invaded zone satellite colony) was the fixed factor. Using t-tests with pooled standard deviation and the Holm procedure, pairwise comparisons were used to compare different levels of the fixed factor when global significant differences were detected.
3.2. Isotopic analyses
3.3. Ovarian dissections There were no detectable differences in queen ovarian structure among the three types of colonies. All the queens had similar ovariole numbers and lengths (ovariole number: t: 1.65, P = 0.108; ovariole length: t = 1.011, P = 0.320). Furthermore, all the queens dissected had corpora lutea, which meant that they were fertile and actively laying eggs. 4. Discussion Queens from mother colonies, which are large and permanent, were more fertile than queens from satellite colonies, which are small and temporal, irrespective of the colony’s location relative to the invasion front. A recent study showed that the oviposition rates of queens from colonies situated in the contact zone did not differ from those of queens from colonies in the invaded zone within the same study area as in this study (Abril et al., 2013). In Abril et al. (2013), queens were kept in artificial nests on an artificial diet for several weeks before oviposition rates were measured. Thus, their study did not take into consideration the possibility that queens at and behind the invasion front received different diets as a result of resource depletion related to the invasion history. For this reason the measurements of the oviposition rate of queens in the present study were done while isolating the queens during 24 h immediately after their collection in the field to take into account possible differences in their diet caused by the invasion history that could affect their fecundity. However, the results of the present study
3. Results 3.1. Oviposition rates The mean oviposition rate of queens from mother colonies was significantly higher than that of queens from satellite colonies,
Fig. 1. Mean number of eggs laid in 24 h by queens from three types of colonies. MC = mother colony; SCC = satellite colony located in the contact zone; SCI = satellite colony located in the invaded zone.
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Fig. 2. Mean d15N values (‰) of queens from three types of colonies. MC = mother colony; SCC = satellite colony located in the contact zone; SCI = satellite colony located in the invaded zone.
did not differ from the results obtained by Abril et al. (2013), suggesting that the position of a satellite Argentine ant colony relative to the invasion front does not affect queen oviposition rates. The results of the ovarian dissections indicate that the higher oviposition rates observed in queens from mother colonies are not a consequence of more productive ovarian morphology. Both ovariole number and length were similar in queens from mother and satellite colonies. In insects, the ovarioles are the ovarian structures responsible for oogenesis. It is expected that a larger number of ovarioles would create a larger number of eggs. Thus, ovariole number may be a proxy for reproductive potential in female insects (Makert et al., 2006; Wheeler 1910). Furthermore, ovariole length is also related to ant queen fecundity (Edwards 1975; Glancey and Banks 1988). A relationship between ovary size and productivity has been detected in queens of the ant species Solenopsis invicta and Monomorium pharaonis (Linnaeus, 1758) that have come in contact with a juvenile hormone analog. Queens treated with this chemical ended up with ovarioles that were reduced in size and that had no developing oocytes (Edwards 1975; Glancey and Banks 1988). Therefore, it seems that ovariole length plays an important role in egg development. The ovarian structures of queens from mother and satellite colonies in our study were similar. This suggests that the differences in their mean queen oviposition rates are not a consequence of intrinsic differences resulting from a more productive ovarian morphology. The isotopic analyses show that queens from mother colonies have higher d15N values than queens from satellite colonies. Controlled laboratory experiments demonstrated that Argentine ant colonies fed on an animal-based diet had higher d15N values than colonies fed a plant-based diet (Menke et al., 2010). Furthermore, Tillberg et al., 2007 found that the primary source of nitrogen in Argentine ant colonies is protein obtained via predation and scavenging rather than from plant-based nitrogen from nectar or hemipteran honeydew. Moreover, Abril et al. (2007) observed that under field conditions foraging workers of the Argentine ant focused their attention on insect protein during the queen’s oviposition periods and during the larvae development phase. This again indicates that the main source of nitrogen in this species is obtained from predacious nitrogen sources. If we take into account all these findings, the higher d15N values of mother colony queens suggests that they consume more nitrogen obtained via predation and scavenging than satellite colony queens. Queens and larvae are the main consumers of insect protein in Argentine ant colonies (Markin, 1970). In queens, higher protein
consumption is most likely linked to egg production, since eggs are largely proteinaceous. Although stable isotope results obtained from a single time period or life stage should be interpreted with caution in ecology (Menke et al., 2010), the d15N values of queens from mother nests nonetheless suggest that the queens’ higher oviposition rates are probably a consequence of a higher carnivorous diet relative to the queens from satellite nests. In contrast, the similar d15N values of queens from contact zone satellite colonies (located at the invasion front) relative to the d15N values from invaded zone satellite colonies (behind the invasion front) strongly suggest that differences in queen size and number between contact and invaded zones (Abril et al., 2013) are not the consequence of a possible depletion of nitrogen-rich protein sources behind the invasion front (Tillberg et al., 2007). Moreover, given that the mother colonies sampled in this study were all situated in the invaded zone and that mother colony queens had higher d15N values than both types of satellite colony queens, it is clear that differences in the availability of insect protein resources in the habitat surrounding the colonies do not explain the isotopic differences observed. If resource availability was playing a role, queens from satellite nests in the invaded zone would be expected to have d15N values similar to those of queens from mother colonies, which is not the case. Instead, the larger size of these mother colonies is probably the main factor responsible for the higher oviposition rates, since colony size seems to be related to worker efficiency at the group level (Beckers et al., 1989; Beekman et al., 2004; Ruel et al., 2012; Thomas and Framenau 2005). In fact, Newell and Barber (1913) came to the same conclusion one hundred years ago based on their observations of Argentine ant queens in artificial formicaries. Specifically, they stated that ‘‘it appears probable that queens deposit eggs much more rapidly in large colonies,’’ although they did not verify this assumption in their study. Large colonies of insect societies were shown to change their foraging and recruitment system to one involving mass communication, enhancing the capacity to retrieve food items to the colony (Beckers et al., 1989; Beekman et al., 2004; Thomas and Framenau, 2005). However, how colony size affects the per capita productivity of insect societies is still poorly understood: it may decrease (Michener, 1964), increase (Jeanne and Nordheim, 1996) or have no effects (Bouwma et al., 2006). In addition, the effect of larger group sizes in some ant species can also result in a higher production of sexuals (Cole and Wiernasz, 2000; Ruel et al., 2012; Sorvari and Hakkarainen, 2007). Such results support the idea that the greater number of workers in large, permanent Argentine ant colonies may induce changes in colony social organization, leading to a social system that is more efficient at retrieving and processing food items into the colony, than that of smaller, temporal colonies. As a consequence, these large colonies may greatly enhance their brood production, at least during the season when queen egg-laying is maximal, and guarantee the growth and survival of the colony. Therefore, given their size and reproductive productivity, mother nests probably act as a source of new colony propagules. Although further research is necessary on the exact relationship between colony size and productivity in the Argentine ant, the results obtained in this study imply that these permanent, mature colonies are one of the mechanisms underlying the success of this invasive species in its introduced range. They also suggest a new research direction that could improve the current state of knowledge on the Argentine ant’s ability to invade new areas. Acknowledgments We would like to thank F. Amor for his helpful advices in ovarian dissections, J. Pearce for revision of the English language, the
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Stable Isotopic Analyses Lab from the Autonomous University of Barcelona for the isotopic analyses of queens and two anonymous reviewers for their helpful comments on previous versions of this manuscript. This work was supported by the Ministry of Science and Innovation of the Government of Spain, and EU ERDF funds (CGL2010-16451).
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Heller, N.E., Gordon, D.M., 2006. Seasonal spatial dynamics and causes of nest movement in colonies of the invasive Argentine ant (Linepithema humile). Ecological Entomology 31, 499–510. Heller, N.E., Sanders, N.J., Gordon, D.M., 2006. Linking temporal and spatial scales in the study of an Argentine ant invasion. Biol. Invasions 8, 501–507. Heller, N.E., Ingram, K.K., Gordon, D.M., 2008. Nest connectivity and colony structure in unicolonial Argentine ants. Insectes Soc. 55, 397–403. Holbrook, C.T., Barden, P.M., Fewell, J.H., 2011. Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav. Ecol. 22, 960–966. Hölldobler, B., Wilson, E.O., 1977. The number of queens: an important trait in ant evolution. Naturwissenschaften 64 (1), 8–15. Hölldobler, B., Wilson, E.O., 1990. The Ants. The Belknap Press of Harvard University Press, Cambridge, MA. Holway, D.A., 1998. Effect of Argentine ant invasions on ground-dwelling arthropods in northern California riparian woodlands. Oecologia 116, 252–258. Human, K.G., Gordon, D.M., 1996. Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105, 405–412. Human, K.G., Gordon, D.M., 1997. Effects of Argentine ants on invertebrate biodiversity in northern California. Conserv. Biol. 11, 1242–1248. Ingram, K.K., 2002. Plasticity in queen number and social structure in the invasive Argentine ant (Linepithema humile). Evolution 56 (10), 2008–2016. Jeanne, R.L., Nordheim, E.V., 1996. Productivity in a social wasp: per capita output increases with swarm size. Behav. Ecol. 7, 43–48. Makert, G.R., Paxton, R.J., Hartfelder, K., 2006. Ovariole number – a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav. Ecol. Sociobiol. 60, 815–825. Markin, G.P., 1970. Food distribution within laboratory colonies of the Argentine ant, Iridomyrmex humilis (Mayr). Insectes Soc. 17 (2), 127–158. Menke, S.B., Suarez, A., Tillberg, C.V., Chou, C.T., Holway, D.A., 2010. Trophic ecology of the invasive argentine ant: spatio-temporal variation in resource assimilation and isotopic enrichment. Oecologia 164, 763–771. Michener, C.D., 1964. Reproductive efficiency in relation to colony size in Hymenopterous societies. Insectes Soc. 11, 317–342. Newell, W., Barber, T.C., 1913. The Argentine Ant. USDA. Bureau of Entomology Bulletin 122, Washington. Passera, L., 1994. Characteristics of tramp species. In: Williams, D.F. (Ed.), Exotic Ants: Biology, Impact and Control of Introduced Species. Westview Press, Boulder, Colorado, pp. 23–43. Ruel, C., Cerdà, X., Boulay, R., 2012. Behaviour-mediated group size effect constrains reproductive decisions in a social insect. Anim. Behav. 84, 853–860. Sorvari, J., Hakkarainen, H., 2007. The role of food and colony size in sexual offspring production in a social insect: an experiment. Ecol. Entomol. 32, 11–14. Suarez, A.V., Bolger, D.T., Case, T.J., 1998. Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79, 2041–2056. Suarez, A.V., Holway, D.A., Case, T.J., 2001. Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc. Nat. Acad. Sci. USA 98, 1095–1100. Thomas, M.L., Elgar, M.A., 2003. Colony size affects división of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90, 88–92. Thomas, M.L., Framenau, V.W., 2005. Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae). Insectes Soc. 52, 26–30. Tillberg, C.V., McCarthy, D.P., Dolezal, A.G., Suarez, A.V., 2006. Measuring the trophic ecology of ants using stable isotopes. Insectes Soc. 53, 65–69. Tillberg, C.V., Holway, D.A., LeBrun, E.G., Suarez, A., 2007. Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proc. Nat. Acad. Sci. USA 104 (52), 20856–20861. Visser, D., Wright, M.G., Giliomee, J.H., 1996. The effect of the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), on flower visiting insects of Protea nitida Mill. (Proteaceae). Afr. Entomol. 4, 285–287. West, J.B., Bowen, G.J., Cerling, T.E., Ehleringer, J.R., 2006. Stable isotopes as one of nature’s ecological recorders. Trends Ecol. Evol. 21 (7), 408–414. Wheeler, W.M., 1910. Ants: Their Structure, Development and Behavior. Columbia University, New York.
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Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys
Strength in numbers: Large and permanent colonies have higher queen oviposition rates in the invasive Argentine ant (Linepithema humile, Mayr) Sílvia Abril ⇑, Crisanto Gómez Department of Environmental Sciences, University of Girona, Montilivi Campus s/n, 17071 Girona, Spain
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Article history: Received 5 July 2013 Received in revised form 1 January 2014 Accepted 9 January 2014 Available online 21 January 2014 Keywords: Formicidae Colony size Invasive species Oviposition rate Polydomy
a b s t r a c t Polydomy associated with unicoloniality is a common trait of invasive species. In the invasive Argentine ant, colonies are seasonally polydomous. Most follow a seasonal fission–fussion pattern: they disperse in the spring and summer and aggregate in the fall and winter. However, a small proportion of colonies do not migrate; instead, they inhabit permanent nesting sites. These colonies are large and highly polydomous. The aim of this study was to (1) search for differences in the fecundity of queens between mother colonies (large and permanent) and satellite colonies (small and temporal), (2) determine if queens in mother and satellite colonies have different diets to clarify if colony size influences social organization and queen feeding, and (3) examine if colony location relative to the invasion front results in differences in the queen’s diet. Our results indicate that queens from mother nests are more fertile than queens from satellite nests and that colony location does not affect queen oviposition rate. Ovarian dissections suggest that differences in ovarian morphology are not responsible for the higher queen oviposition rate in mother vs. satellite nests, since there were no differences in the number and length of ovarioles in queens from the two types of colonies. In contrast, the higher d15N values of queens from mother nests imply that greater carnivorous source intake accounts for the higher oviposition rates. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Ant societies can adopt different strategies of colony structuration. A given colony can occupy one nest (monodomy) or several socially-connected but spatially-separated nests (polydomy) (Debout et al., 2007; Hölldobler and Wilson, 1977). Polydomy associated with unicoloniality (the lack of territorial boundaries between neighboring nests) is a characteristic trait of invasive species (Debout et al., 2007). Polydomy is closely tied to the low level of genetic variation exhibited by invasive unicolonial ants and gives them a significant ecological advantage in terms of resource capture, which facilitates their spread in areas to which they have been introduced (Debout et al., 2007). The Argentine ant, Linepithema humile, clearly demonstrates the advantages of being unicolonial and polydomous. Native to South America, this invasive species has spread worldwide to regions with Mediterranean climates (Suarez et al., 1998; 2001). In the areas to which it has been introduced, the Argentine ant reduces populations of native ants and other arthropods, affects insectivorous vertebrates, and disrupts ant-mediated ecological mechanisms ⇑ Corresponding author. Tel.: +34 972418268; fax: +34 972418150. E-mail address: [email protected] (S. Abril). http://dx.doi.org/10.1016/j.jinsphys.2014.01.004 0022-1910/Ó 2014 Elsevier Ltd. All rights reserved.
such as seed dispersal and pollination (Blancafort and Gómez, 2005; Bond and Slingsby, 1984; Estany-Tigerström et al., 2010; Gómez and Oliveras, 2003; Human and Gordon, 1996, 1997; Holway, 1998; Suarez et al., 2001; Visser et al., 1996). Argentine ants are unicolonial (Passera, 1994), highly polygynous and polydomous (Hölldobler and Wilson, 1977). Its colonies in its introduced range are seasonally polydomous as a consequence of environmental conditions and food resource availability (Diaz et al., 2013; Heller and Gordon, 2006), meaning there is a seasonal pattern of nest fission and fusion (Benois, 1973; Diaz et al., 2013; Heller and Gordon, 2006; Newell and Barber, 1913). Heller et al. (2008) defined an Argentine ant colony as a group of nests who share food and among which ants travel. This definition suggests that its populations do not function ecologically as a single supercolony but rather as a mosaic of smaller and distinct colonies that consist of groups of interacting nests. Most of these colonies move seasonally. In the winter, nests associated with each colony form large aggregations. In the spring and summer, these aggregations split into small, dispersed nests. In the late fall, ants move back to the aggregation sites used the previous winter (Diaz et al., 2013; Heller and Gordon, 2006; Heller et al., 2006). However, a small proportion of colonies do not move their nesting sites seasonally; instead, they maintain permanent,
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year-round nesting sites (Diaz et al., 2013; Heller and Gordon, 2006). The degree of colony permanence shows a positive relationship with colony size (Diaz et al., 2013; Heller and Gordon, 2006). Hölldobler and Wilson (1990) state that large, mature colonies demonstrate clear nest preferences and Heller and Gordon (2006) indicate that changes in microclimate are the proximate cause of Argentine ant nest movements. Thus, it seems that larger Argentine ant colonies tend to occupy permanent nesting sites since such sites have suitable microclimatic conditions. Furthermore, moving these huge polydomous formations would require a great amount of expensive effort for the colony and would subsequently lead to another permanent nest site (Diaz, 2013). Larger colonies were shown to enhance division of labor and task specialization in some ant species (Holbrook et al., 2011; Thomas and Elgar, 2003). Additionally, the most elaborate caste and communication systems occur in species with large and perennial colonies (Hölldobler and Wilson, 1990). In consequence, these large, permanent Argentine ant colonies may be expected to show different social organization from smaller, temporal colonies. Moreover, the social structure of the Argentine ant is greatly affected by ecological constraints. More specifically, nest density, colony size, and queen number and size are affected by the invasion history of introduced populations (Abril et al., 2013; Diaz et al., 2013; Ingram, 2002). For instance, colonies at the invasion front invest more energy in creating more and larger queens (Abril et al., 2013). Whether this investment is a colony-level strategy to ensure the successful establishment of new colonies (Abril et al., 2013) or a consequence of the reduction of nitrogen-rich protein resources in the areas situated behind the invasion front (Tillberg et al., 2007) is still unknown. As Argentine ant workers are completely sterile (Markin, 1970), queens are the only caste capable of reproduction and, consequently, they are responsible for colony growth and reproduction. Therefore, identifying the factors that regulate queen reproduction will bring us closer to understanding the mechanisms underlying the superior competitive ability of introduced populations of this invasive species. Stable isotopes in ecology have been used to record dietary patterns in animals (West et al., 2006). The basic principle of this technique is that the isotopic composition of organisms reflects some aspects of their diet, such as the main sources of energy (De Niro and Epstein, 1981). In the case of ants Blüthgen and Fiedler (2002) and Davidson et al. (2003) showed that the N-isotope signatures of ants exhibiting high fidelity to nectar or honeydew differ from the N-isotope values from omnivorous or predacious ants. In 2007, Fiedler et al. (2007) made a comparison of the stable N-isotope signatures of several ant genera from central Europe and concluded that there was a relationship between the d15N values and the diet nitrogen sources. Therefore, high d15N values indicate a predominant predacious nitrogen source obtained via predation and scavenging, while low d15N values indicate a plant-derived nitrogen source obtained via trophobiosis and nectarivory (Fiedler et al., 2007). In this context, we addressed the following questions. First, we asked if the d15N values of queens from the Argentine ant differed depending on colony location relative to the invasion front and colony permanence. It might be that colonies far from the invasion front are feeding their queens a lower-predacious diet as a consequence of reduced resource availability in their forager-saturated habitat. If so, it could explain why at the invasion front there are more and bigger queens than behind it. Furthermore, larger colonies were shown to create more complex foraging groups that spend more time foraging, allowing more foragers to visit each food source and forage over longer distances than small colonies (Beckers et al., 1989; Beekman et al., 2004; Thomas and Framenau, 2005). Thus, large, permanent Argentine ant colonies may supply
their queens with a more carnivorous diet because their higher forager numbers allow them to more efficiently capture food. To test these hypotheses, we conducted isotopic analyses on queens from temporal colonies at and behind the invasion front and on queens from permanent colonies. Second, we asked whether queens from permanent and temporal colonies differed in their fecundity as a consequence of differences in colony permanence and thus structure. To address this question, we measured the oviposition rates of queens from temporal colonies (at and behind the invasion front) and permanent colonies. We dissected the ovaries of all the queens to better assess and obtain complementary data on their reproductive potential. 2. Material and methods 2.1. Study area Samples were taken from two different L. humile-invaded areas of cork oak secondary forests in the NE Iberian Peninsula. One of the areas is located at the southern edge of the Gavarres massif, near Santa Cristina d’Aro (41° 480 51.7100 N; 3° 010 50.5700 E), and the other is located in the Cadiretes massif, near a developed zone called Pedralta (41° 470 31.5300 N; 2° 580 52.7900 E). Prior to this study, invasion fronts in each area had been identified using bait sampling. Baits were placed every four meters along random transects of 100 m in length, setting a total of twelve transects. The furthest baits visited by the species defined the invasion limit. After identifying the invasion front, we defined the contact zone and the invaded zone. The contact zone was defined as the area in which L. humile and native ants were still in contact. The invaded zone was the area in which the invasion was severe: L. humile nests were highly abundant and the native ant community was almost completely displaced. The contact and invaded zones of the two study areas were ±1 km apart and had similar environmental characteristics. 2.2. Collection of samples Queens were sampled weekly during May 2012 from three types of colonies identified in a previous study (Diaz et al., 2013): (1) Large, permanent colonies (mean nest size 0.94 ± 0.29 m2; Diaz et al. (2013)) called from now on ‘‘mother colonies’’. The mother colonies were present both in the contact and invaded zones, but they were more abundant in the latter. For this reason, all the mother colonies sampled in this study were situated in the invaded zones of the two study sites; (2) Temporal colonies (i.e. remain active at the same nest site for less than 6 months) located at the invasion front, much smaller than mother colonies (mean nest size 0.04 ± 0.01 m2; Diaz et al. (2013)), called from now on ‘‘contact zone satellite colonies’’ and; (3) Temporal colonies located far from the invaded zone and also smaller than the mother colonies (mean nest size 0.04 ± 0.01 m2; Diaz et al. (2013)), called from now on ‘‘invaded zone satellite colonies’’. All the queens analyzed were collected from a total of four mother nests and ten satellite colonies from the contact zone and ten more from the invaded zone. 2.3. Measurement of oviposition rates The oviposition rates of queens from mother colonies (n = 52), contact zone satellite colonies (n = 52), and invaded zone satellite colonies (n = 45) were measured. Field-collected queens and some of their workers (3–5) were immediately isolated and kept for 24 h in test tube nests. The test tube nests consisted of a transparent plastic tube (70 mm in length 10 mm in diameter) and a plastic
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lid. The inner side of the plastic lid was covered by a layer of dry plaster of Paris, which was connected by a wick of cotton wool to a small chamber filled with water. As a result, the inside of the tube remained permanently humid over the course of our observations. The test tube nests were kept at 28 °C, which was the mean soil temperature of the sampled nests obtained using HOBO Ò H8 Pro Series data loggers. After 24 h had passed, the number of eggs laid by each queen was counted using a binocular microscope.
irrespective of the zone (contact or invaded) (GLMM t = 4.45; P < 0.0001) (Fig. 1). Pairwise comparisons indicated that there was no difference in the oviposition rates of queens from satellite colonies in contact vs. invaded zones (P = 0.761); however, they did differ between queens from mother vs. satellite colonies (P < 0.001 in both comparisons).
2.4. Isotopic analyses
The d15N of queens differed between mother colonies and both types of satellite colonies; the mean d15N was significantly higher in the former (GLMM t = 2.849; P < 0.001; pairwise comparisons: mother vs. contact satellite P < 0.05; mother vs. invaded satellite P < 0.01; contact satellite vs. invaded satellite P = 0.321) (Fig. 2).
The d15N signatures of queens from mother colonies and satellite colonies from the invaded and contact zones were compared under the prediction that queens fed with a more carnivorous diet will have higher isotopic signatures in relation to queens fed with a more plant-derived diet (Menke et al., 2010). For this reason, thirty queens for which oviposition rates had been obtained were randomly selected for use in isotopic analyses (n = 10 for each colony type). In preparation, all queens were dried at 70 °C for 24 h, ground to a fine powder, and weighed in capsules. Their abdomens were not included to prevent contamination by food residuals (Tillberg et al., 2006). Each queen was processed individually. Isotopic analyses were conducted in the Stable Isotopic Analyses Lab at the Autonomous University of Barcelona using an elemental analyser – isotope ratio mass spectrometry (EA-IRMS) technique. A Thermo Flash EA 1112 C-N-S analyser and a Thermo Delta V Advantage mass spectrometer were used. d15N values (‰) are expressed relative to atmospheric nitrogen. The reference material used was IAEA600. 2.5. Ovarian dissections To determine if queen ovarian structure differed among the three colony types, we dissected the gasters of queens who had been used in the isotopic analyses. We examined the following ovarian characteristics: (1) the presence or absence of corpora lutea (yellowish remains of nutritive cells left at the base of the ovarioles following oviposition), (2) the number of ovarioles per ovary, and (3) the length of the ovarioles. 2.6. Data analyses We used the R 2.5.1 statistical package (R Development Core Team, 2001) for all analyses. To determine if queen oviposition rate and ovariole number differed among the three colony types, we conducted generalized linear mixed models (GLMM) using a Poisson error distribution and the log-link function (MASS package). To compare queen d15N values and ovariole length among the different colony types, we conducted GLMMs using a Gaussian error distribution and the identity link function (nlme package). In all models, the nest from which a queen was sampled was used as a random factor and the colony type (mother colony, contact zone satellite colony, or invaded zone satellite colony) was the fixed factor. Using t-tests with pooled standard deviation and the Holm procedure, pairwise comparisons were used to compare different levels of the fixed factor when global significant differences were detected.
3.2. Isotopic analyses
3.3. Ovarian dissections There were no detectable differences in queen ovarian structure among the three types of colonies. All the queens had similar ovariole numbers and lengths (ovariole number: t: 1.65, P = 0.108; ovariole length: t = 1.011, P = 0.320). Furthermore, all the queens dissected had corpora lutea, which meant that they were fertile and actively laying eggs. 4. Discussion Queens from mother colonies, which are large and permanent, were more fertile than queens from satellite colonies, which are small and temporal, irrespective of the colony’s location relative to the invasion front. A recent study showed that the oviposition rates of queens from colonies situated in the contact zone did not differ from those of queens from colonies in the invaded zone within the same study area as in this study (Abril et al., 2013). In Abril et al. (2013), queens were kept in artificial nests on an artificial diet for several weeks before oviposition rates were measured. Thus, their study did not take into consideration the possibility that queens at and behind the invasion front received different diets as a result of resource depletion related to the invasion history. For this reason the measurements of the oviposition rate of queens in the present study were done while isolating the queens during 24 h immediately after their collection in the field to take into account possible differences in their diet caused by the invasion history that could affect their fecundity. However, the results of the present study
3. Results 3.1. Oviposition rates The mean oviposition rate of queens from mother colonies was significantly higher than that of queens from satellite colonies,
Fig. 1. Mean number of eggs laid in 24 h by queens from three types of colonies. MC = mother colony; SCC = satellite colony located in the contact zone; SCI = satellite colony located in the invaded zone.
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Fig. 2. Mean d15N values (‰) of queens from three types of colonies. MC = mother colony; SCC = satellite colony located in the contact zone; SCI = satellite colony located in the invaded zone.
did not differ from the results obtained by Abril et al. (2013), suggesting that the position of a satellite Argentine ant colony relative to the invasion front does not affect queen oviposition rates. The results of the ovarian dissections indicate that the higher oviposition rates observed in queens from mother colonies are not a consequence of more productive ovarian morphology. Both ovariole number and length were similar in queens from mother and satellite colonies. In insects, the ovarioles are the ovarian structures responsible for oogenesis. It is expected that a larger number of ovarioles would create a larger number of eggs. Thus, ovariole number may be a proxy for reproductive potential in female insects (Makert et al., 2006; Wheeler 1910). Furthermore, ovariole length is also related to ant queen fecundity (Edwards 1975; Glancey and Banks 1988). A relationship between ovary size and productivity has been detected in queens of the ant species Solenopsis invicta and Monomorium pharaonis (Linnaeus, 1758) that have come in contact with a juvenile hormone analog. Queens treated with this chemical ended up with ovarioles that were reduced in size and that had no developing oocytes (Edwards 1975; Glancey and Banks 1988). Therefore, it seems that ovariole length plays an important role in egg development. The ovarian structures of queens from mother and satellite colonies in our study were similar. This suggests that the differences in their mean queen oviposition rates are not a consequence of intrinsic differences resulting from a more productive ovarian morphology. The isotopic analyses show that queens from mother colonies have higher d15N values than queens from satellite colonies. Controlled laboratory experiments demonstrated that Argentine ant colonies fed on an animal-based diet had higher d15N values than colonies fed a plant-based diet (Menke et al., 2010). Furthermore, Tillberg et al., 2007 found that the primary source of nitrogen in Argentine ant colonies is protein obtained via predation and scavenging rather than from plant-based nitrogen from nectar or hemipteran honeydew. Moreover, Abril et al. (2007) observed that under field conditions foraging workers of the Argentine ant focused their attention on insect protein during the queen’s oviposition periods and during the larvae development phase. This again indicates that the main source of nitrogen in this species is obtained from predacious nitrogen sources. If we take into account all these findings, the higher d15N values of mother colony queens suggests that they consume more nitrogen obtained via predation and scavenging than satellite colony queens. Queens and larvae are the main consumers of insect protein in Argentine ant colonies (Markin, 1970). In queens, higher protein
consumption is most likely linked to egg production, since eggs are largely proteinaceous. Although stable isotope results obtained from a single time period or life stage should be interpreted with caution in ecology (Menke et al., 2010), the d15N values of queens from mother nests nonetheless suggest that the queens’ higher oviposition rates are probably a consequence of a higher carnivorous diet relative to the queens from satellite nests. In contrast, the similar d15N values of queens from contact zone satellite colonies (located at the invasion front) relative to the d15N values from invaded zone satellite colonies (behind the invasion front) strongly suggest that differences in queen size and number between contact and invaded zones (Abril et al., 2013) are not the consequence of a possible depletion of nitrogen-rich protein sources behind the invasion front (Tillberg et al., 2007). Moreover, given that the mother colonies sampled in this study were all situated in the invaded zone and that mother colony queens had higher d15N values than both types of satellite colony queens, it is clear that differences in the availability of insect protein resources in the habitat surrounding the colonies do not explain the isotopic differences observed. If resource availability was playing a role, queens from satellite nests in the invaded zone would be expected to have d15N values similar to those of queens from mother colonies, which is not the case. Instead, the larger size of these mother colonies is probably the main factor responsible for the higher oviposition rates, since colony size seems to be related to worker efficiency at the group level (Beckers et al., 1989; Beekman et al., 2004; Ruel et al., 2012; Thomas and Framenau 2005). In fact, Newell and Barber (1913) came to the same conclusion one hundred years ago based on their observations of Argentine ant queens in artificial formicaries. Specifically, they stated that ‘‘it appears probable that queens deposit eggs much more rapidly in large colonies,’’ although they did not verify this assumption in their study. Large colonies of insect societies were shown to change their foraging and recruitment system to one involving mass communication, enhancing the capacity to retrieve food items to the colony (Beckers et al., 1989; Beekman et al., 2004; Thomas and Framenau, 2005). However, how colony size affects the per capita productivity of insect societies is still poorly understood: it may decrease (Michener, 1964), increase (Jeanne and Nordheim, 1996) or have no effects (Bouwma et al., 2006). In addition, the effect of larger group sizes in some ant species can also result in a higher production of sexuals (Cole and Wiernasz, 2000; Ruel et al., 2012; Sorvari and Hakkarainen, 2007). Such results support the idea that the greater number of workers in large, permanent Argentine ant colonies may induce changes in colony social organization, leading to a social system that is more efficient at retrieving and processing food items into the colony, than that of smaller, temporal colonies. As a consequence, these large colonies may greatly enhance their brood production, at least during the season when queen egg-laying is maximal, and guarantee the growth and survival of the colony. Therefore, given their size and reproductive productivity, mother nests probably act as a source of new colony propagules. Although further research is necessary on the exact relationship between colony size and productivity in the Argentine ant, the results obtained in this study imply that these permanent, mature colonies are one of the mechanisms underlying the success of this invasive species in its introduced range. They also suggest a new research direction that could improve the current state of knowledge on the Argentine ant’s ability to invade new areas. Acknowledgments We would like to thank F. Amor for his helpful advices in ovarian dissections, J. Pearce for revision of the English language, the
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Stable Isotopic Analyses Lab from the Autonomous University of Barcelona for the isotopic analyses of queens and two anonymous reviewers for their helpful comments on previous versions of this manuscript. This work was supported by the Ministry of Science and Innovation of the Government of Spain, and EU ERDF funds (CGL2010-16451).
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