Behavioral Ecology Advance Access originally published online on February 1, 2008
Behavioral Ecology 2008 19(2):441-447; doi:10.1093/beheco/arm160
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Food resources, chemical signaling, and nest mate recognition in the ant Formica aquilonia
a Department of Biology, University of Turku, FIN-20014 Turku, Finland b School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK c School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, New South Wales, Australia d Dipartimento di Biologia Animale e Genetica, Università di Firenze, Via Romana 17, I-50125 Firenze, Italy, and e Department of Biological and Environmental Sciences, University of Helsinki, PO box 65, FIN-00014 Helsinki, Finland
Address correspondence to J. Sorvari. E-mail: jouni.sorvari{at}utu.fi.
Received 8 July 2007; revised 6 December 2007; accepted 19 December 2007.
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ABSTRACT |
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Animals such as social insects that live in colonies can recognize intruders from other colonies of the same or different species using colony-specific odors. Such colony odors usually have both a genetic and an environmental origin. When within-colony relatedness is high (i.e., one or very few reproductive queens), colonies comprise genetically distinct entities, and recognition based on genetic cues is reliable. However, when nests contain multiple queens and colonies comprise multiple nests (polydomy), the use of purely genetically determined recognition labels may become impractical. This is due to high within-colony genetic heterogeneity and low between-colony genetic heterogeneity. This may favor the use of environmentally determined recognition labels. However, because nests within polydomous colonies may differ in their microenvironment, the use of environmental labels may also be impractical unless they are actively mixed among the nests. Using a laboratory experiment, we found that both isolation per se and diet composition influenced the cuticular chemical profiles in workers of Formica aquilonia. In addition, the level of aggression increased when both the proportions of dietary ingredients and the availability of food were altered. This suggests that increased aggression was mediated by changes in the chemical profile and that environmental cues can mediate recognition between colonies. These results also suggest that the underlying recognition cues are mutable in response to extrinsic factors such as the amount and the composition of food.
Key words: aggressive behavior, colony odor, cuticular hydrocarbons, diet, social insects.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Social interactions frequently entail behaviors that benefit one of the parties, at a cost to the other party. Kin selection theory predicts that when help entails costs to the donor, it should be directed toward relatives (Hamilton 1964
). This requires a means for discriminating between relatives and nonrelatives. This raises the question how animals discriminate kin from nonkin (Keller 1997). Four principal recognition strategies have been identified (Hölldobler and Michener 1980; Holmes and Sherman 1983; Sherman and Holmes 1985). First, spatial distribution, such as location in same nesting site, can be used to identify relatives. This, however, is vulnerable to intra- and interspecific brood parasitism, common especially in birds that feed any chicks present in their nests (e.g., Rohwer and Freeman 1989; Arnold and Owens 2002). Second, animals may use phenotypic markers as discriminators, where individuals with the same character identify themselves as members of the same group (the green beard effect sensu, Dawkins 1976). Third, previous interactions followed by a learning process can allow identification of potential allies. This requires a sufficient learning capacity and generally individual recognition ability (Waldman et al. 1988). Finally, in a somewhat similar fashion, animals may discriminate between unfamiliar nonkin and unfamiliar kin as well as among familiar kin of different relatedness through phenotype matching (Sherman and Holmes 1985). In this process, a perceived overlap in recognition cues is used.
Social insects live in societies that usually maintain colony closure toward conspecific or heterospecific intruders. Colony closure is maintained by cues common to all member of the same society. Such nest mate recognition is in most social insects based on chemical cues (colony odor) (Hölldobler and Wilson 1990; Espelie et al. 1994; Lahav et al. 1999; Thomas et al. 1999; Wagner et al. 2000; Florane et al. 2004). These cues are akin, but not identical, to phenotype matching as they can be of genetic and/or environmental (food, nesting material, etc.) origin (Wilson 1971; Carlin and Hölldobler 1986; Gamboa et al. 1986; Hölldobler and Wilson 1990). The chemical compounds involved can be absorbed by all nest mates by allogrooming and trophallaxis (i.e., mouth-to-mouth exchange of liquid food) causing a gestalt odor that is similar among nest mates (Crozier and Dix 1979; Boulay et al. 2003; Soroker et al. 2003). The insect cuticle is covered with a thin layer of lipids containing fatty acids and cuticular hydrocarbons, which have repeatedly been shown to be involved in nest mate recognition, as well as other types of recognition in social insects (Hölldobler and Wilson 1990; Espelie et al. 1994; Gamboa et al. 1996; Lahav et al. 1999; Thomas et al. 1999; Wagner et al. 2000; Dani et al. 2001; Hannonen et al. 2002; Ruther et al. 2002; Boomsma et al. 2003; Florane et al. 2004; Howard and Blomquist 2005).
In many species of ants, individuals acquire an odor profile during the first hours after eclosion (Hölldobler 1977; Hölldobler and Wilson 1990; Lenoir et al. 1999), but this profile can be modified during the life span of an individual by exogenous factors (Wagner et al. 1998, 2001). The most spectacular changes in odor profiles occur in queens of socially parasitic ants and wasps when these usurp host colonies (Turillazzi et al. 2000; Lenoir et al. 2001; D'Ettorre et al. 2002; Johnson et al. 2005). Their complete odor profile changes within a few hours after entering a host colony and takes on the profile of the executed resident queens (Turillazzi et al. 2000; Johnson et al. 2002). In addition to changes associated with age or reproductive status, differences in diet can modify the surface chemistry and consequently behavior. Le Moli et al. (1992) found that differences in the diet increased aggressiveness in Formica cunicularia workers. In later experiments, modification of cuticular chemical profiles in Acromyrmex subterraneus subterraneus (Richard et al. 2004) and Linepithema humile (Liang and Silverman 2000) led to discrimination against former nest mates in both species. In addition, diet manipulation led to colony disruption in L. humile (Silverman and Liang 2001). This raises the question whether the odor profile also may change when the environment of individual colonies changes.
Nest mate recognition is well developed in most species of ants such that individuals from one nest tend to reject individuals from other nests (Wilson 1971; Sudd and Franks 1987; Crozier and Pamilo 1996). However, some species have a nesting structure with extensive networks of nests (polydomy) in conjunction with multiple queening (polygyny) (Hölldobler and Wilson 1977, 1990; Rosengren and Pamilo 1983; Bourke and Franks 1995; Keller 1995; but see Hölldobler and Lumsden 1980; Traniello and Levings 1986; Snyder and Herbers 1991). Such networks may encompass entire populations (Queller and Strassmann 1998; Tsutsui et al. 2000, 2003; Giraud et al. 2002; Elias et al. 2005) or subsets of populations (e.g., Douwes et al. 1987; Seppä 1994; Seppä and Pamilo 1995). Nest mate relatedness in these networks frequently approaches zero, and discrimination among different nest units within the same colony network usually is absent, and nests may exchange workers and brood over several years (Chapuisat and Keller 1999). The absence of discrimination may have 2 causes: 1) owing to the genetic homogeneity of such networks, recognition cues may also be homogenized if based on heritable cues (Tsutsui et al. 2000, 2003) or 2) owing to the exchange of workers and brood between nests also environmentally determined cues become homogenized. In the first case, we predict that a short-term isolation of nest units should not produce aggression between nest units of the same network. By contrast, if recognition cues are based on environmental differences, also short-term isolation under different feeding regimes should produce increased aggression between previously amicable units.
Formica aquilonia is the dominant species of ant in Eurasian boreal forests and is highly polygynous and polydomous (Collingwood 1979; Rosengren and Pamilo 1983). A large nest mound may contain 1 million workers and hundreds of queens, and, as a result of frequent budding, single networks may encompass hundreds of nests. This usually results in very low relatedness among nest mate workers (Rosengren et al. 1993; Pamilo et al. 2005). In F. aquilonia, as in the mound building Formica wood ants in general, the main food resource consists of honeydew collected from aphids on pine and spruce, as well as arthropod prey available on trees (Rosengren and Sundström 1987, 1991; Punttila et al. 2004). Sugars are used as an energy source for adult workers, whereas protein is used for egg formation and larval growth (Brian 1983; Porter 1989). After forest clear-cutting, the availability of both sugar and protein declines. It is therefore reasonable to assume that both the amount of food and the balance between sugar and protein change following, for example, forest clear-cutting. If such changes in diet occur in conjunction with a decline in interactions between nests due to the disruption of communication trails, the mixing of cues between nests may also be prevented and aggression between nest units within the same polydomous colony may arise. Indeed, in a previous study, it has been shown that forest clear-cutting led to an elevated level of aggressive behavior in F. aquilonia (Sorvari and Hakkarainen 2004). Anthropogenic changes in the environment may thus modify nest mate recognition cues, but the precise causes and correlates to these changes remain unexplored. This begs the question whether recognition cues in this species are based on environmental or genetic factors, or a mixture of both.
More specifically, we ask whether the abundance and the composition of food in terms of sugar and protein affect cuticular chemistry and aggression levels in ants. We hypothesize that environmental factors such as availability of food and different proportions of nutritionally important ingredients in the diet can affect nest mate recognition in species that normally have very low intranest relatedness and live in relatively homogenous habitats. To test this, we conducted aggression tests between workers of F. aquilonia originating from the same field colony but divided into separate laboratory colonies (subcolonies) with different feeding regimes. Furthermore, to examine the relationship between cuticular chemistry and aggression, we extracted cuticular compounds from workers reared on a different diet and analyzed these with gas chromatograph/mass spectrometer techniques. If the recognition cues are mainly genetically determined, we do not expect to find changes in the aggression levels between the experimental subcolonies. Conversely, if the recognition cues are mainly environmentally determined, and the cuticular chemistry changes accordingly, we expect aggression to emerge between the subcolonies with the greatest divergence between cuticular chemical profiles. In addition, behavioral differences owing to different nutritional status may trigger some aggression.
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METHODS |
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Study material and general procedures
Nest material (including workers and queens) from 15 field colonies of F. aquilonia were collected from 8 different forest patches in central Finland (Jyväskylä, 65°15'N, 25°45'E) and brought to the laboratory. Each field colony was divided into 5 identical laboratory subcolonies set up in 10-l plastic buckets, resulting in 15 quintets of laboratory colonies (Figure 1); each subcolony contained 1 l of nest material, 1 l of peat, 2 queens, and approximately 500 workers. These subcolonies were subject to 4 different food regimes as follows: 1) 2 subcolonies received standard diet every day (Standard 1 and Standard 2); 2) 1 subcolony received standard diet only every 2 days (Starvation); 3) 1 subcolony received extra sugar daily (Sugar); and 4) 1 subcolony received added protein daily (Protein). The diet was modified from the Bhatkar–Whitcomb diet (Bhatkar and Whitcomb 1970
), where the standard diet was prepared in accordance with the recipe (1 egg and 62.5 ml honey per 500 ml water). To alter the sugar and protein composition, we used only half an egg for the sugar-rich diet and 2 eggs in the protein-rich diet. Each food portion weighted 1.75 g. The experimental colonies were kept under constant room temperature (25 °C) and were watered daily.
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Aggression tests
To test whether feeding regime changes the level of aggression between subcolonies, we ran pairwise aggression tests between different food treatment pairs within all 15 quintets of laboratory colonies. We started the aggression tests 2 weeks after the subcolonies had been established. Tests were conducted on all experimental colonies on 3 occasions with 2-week intervals from June to July 2003 (18–19 June, 2–3 July, and 15–16 July) during the day (0900–1700). Each experiment comprised 3 tests, involving the food regimes described above, and their corresponding controls, where 2 workers from the same subcolony were tested against each other (Figure 1). We chose not to test all possible combinations of food regimes against each other, as this would have led to nonindependence of replicates. Instead, we tested the direction of aggression separately (see below).
The treatment pairs are called hereafter "Standard" (Standard 1 vs. Standard 2), "Quality" (Sugar vs. Protein), "Quantity" (Standard 1 and 2 and Starvation), and "Control" (2 workers from the same subcolony, all food regimes represented; Figure 1). To assess the aggression level between 2 target subcolonies, we placed 1 worker from each subcolony (or 2 workers from the same subcolony in the control tests) on a Petri dish (Figure 1) and recorded the following behaviors on a 0–4 scale: 0 = ignoring, 1 = avoidance, 2 = investigation, antennation, 3 = aggressive movements, attack-like movements, threatening with opened mandibles, and 4 = biting (modified after Carlin and Hölldobler 1986; Beye et al. 1997, 1998; see also Holzer et al. 2006). Based on the first 10 interactions between the 2 workers, we calculated a mean aggression score for each pair of workers. Biting exceeding 10 s was scored anew for each period of 10 s. All observations were performed blinded. We repeated this procedure 5 times for each treatment pair, each time with fresh workers. The tested workers were not returned to their nest after the test. To remove potential chemical contamination of the test arena, we cleaned the arena with a towel soaked in ethanol after each test.
In the Quantity treatment, workers came alternatingly from the Standard 1 or 2 subcolony in order to avoid different rates of worker loss between the Standard 1 and 2 subcolonies. All tests were performed between subcolonies originating from the same field colony (block design, 15 blocks). At the third aggression test event, we also studied the direction of attacks in the test pair's Quantity and Quality. Instead of using color-marked workers, we always confronted a small and a large worker, alternating the source colony for the small and large worker. In this way, we avoided the possible disturbing effect of color marking on cuticular chemistry. In many ant species, such as wood ants of the Formica rufa group, large workers tend to have nest defense tasks, whereas smaller workers care for the brood (Brian 1983; Rosengren and Sundström 1987; Hölldobler and Wilson 1990). By alternating the source colony for the larger worker, we were able to control for this effect. The relative size difference of the workers was assessed by eye.
Chemical analysis
Instantly after the third testing period, we extracted cuticular compounds from workers of all subcolonies of 6 randomly chosen quintets. We placed 5 workers from each subcolony (from 1 quintet 1 worker/subcolony) into clean glass vials and stunned them by keeping them 1 h in –18 °C. The ants were then transferred individually into 1-ml glass vials and kept in –18 °C for 24 h. We extracted workers in 300 µl pentane (Rathburn Chemicals Ltd, Walkerburn, Scotland) for 2 min to minimize contamination from postpharyngeal and abdominal glands. As all samples were treated similarly, any possible contamination was equal across the sample. The pentane was then evaporated in a ventilated closet under a nitrogen stream. We redissolved the compounds in 30 µl heptane (Sigma Aldrich Slr, Milano, Italy) and injected 2 µl of the solution into gas chromatography/mass spectrometry (GC–MS). The chemical profiles were extracted from 130 workers. One sample was excluded because of failure in GC–MS process.
We injected 2 µl of solution into a Hewlett Packard (Palo Alto, CA) 5890A gas chromatograph coupled with an HP 5971A mass selective detector. A fused silica capillary column coated with 5% diphenyl–95% dimethyl polysiloxane (Rtx-5MS, 30 m x 0.25 mm x 0.5 µm; Restek, Bellefonte, PA) was used in the gas chromatography analysis. The injector port and transfer line were set at 280 °C, and the carrier gas was helium (at 12 psi). The temperature protocol was 50 °C for 2 min, 50–120 °C at a rate of 7 °C/min (held for 2 min), and 120–310 °C at 15 °C/min (held for 8.33 min). Analyses were performed in splitless mode. The location, peak height, and surface area of cuticular compounds were determined from their mass spectra produced by electron impact ionization (70 eV).
Statistical analyses of the data
We analyzed differences in aggression scores and chemical profiles (discrimination functions, see below) with mixed model analyses of variance (ANOVAs). We used colony of origin as a random variable when multiple food treatment pairs were analyzed in the same model, whereas single food treatment pair analyses were made using colony of origin as a repeated subject. Colony of origin was nested within treatment pair, subcolony, or time depending on the test. Multiple comparisons were made only when treatment pairs or subcolonies differed in the main analysis. Bonferroni corrections were used in all multiple comparisons. All mixed model ANOVAs were performed with SAS 9.1 (SAS Institute Inc., Cary, NC). Means are always reported ± 95% confidence interval.
Quantitative variation in cuticular chemistry profiles was measured as the relative abundance of each compound in individual's chemical profile. The area under each peak was measured with Data Handling software HP Productivity Chemstation. We used discriminant analysis on the quantitative variation in chemical profiles to obtain the discrimination functions for the chemical profile divergence measures between different treatments. The distances between chemical profiles were calculated trigonometrically using the observed discriminant functions (i.e., square root of the squared distance in the first discriminant function + squared distance in the second discriminant function). Each group of subcolonies originating from same colony of origin was analyzed separately. The discrimination functions were constructed with the discriminant analysis function in SPSS 11.5 statistical software, and their correlation with aggression performance was analyzed with SAS 9.1.
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RESULTS |
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The ants expressed the entire range of aggression levels encompassed by the scale 0 (ignoring/tolerating) to 4 (biting). Interestingly, aggression scores developed at different rates in the different treatment pairs (interaction term time x treatment, mixed model ANOVA, colony of origin as a random factor: F6,832 = 3.5, P = 0.002; Figure 2). Owing to this significant interaction, the effect of food treatment within each test event and the effect of time within treatment pairs were analyzed separately.
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When analyzed across treatments within each test event (treatment effect), aggression scores differed between treatments for some test events, but not for others (mixed model ANOVA, colony of origin nested within treatment pair as a random factor: F3,56 = 9.5–19.4, P < 0.001). On the first and the third test event, ants in both the Quantity and Quality tests showed significantly elevated aggression scores compared with the Standard and Control tests, whereas no significant differences in aggression scores were found in the remaining pairwise comparisons (Figure 2, Table 1). On the second discrimination test event, the aggression scores were higher in all 3 treatment pairs compared with the Control test pairs (Figure 2), whereas there were no significant differences between the Standard, Quality, and Quantity test pairs (Table 1).
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When each treatment was considered separately across the 3 test events, the aggression scores remained high in all Quantity tests, increased constantly in the Quality tests, first increased and then remained at the same level in the Standard tests, and remained low in the Control tests (mixed model ANOVAs, colony of origin within time as a repeated subject factor—Quantity: F2,222 = 0.2, P = 0.824; Quality: F2,222 = 6.4, P = 0.002; Bonferroni-adjusted comparisons—event 1 vs. 2: P = 0.381; event 1 vs. 3: P = 0.001; event 2 vs. 3: P = 0.131; Standard: F2,222 = 15.1, P < 0.001; Bonferroni-adjusted comparisons—event 1 vs. 2: P < 0.001; event 1 vs. 3: P = 0.004; event 2 vs. 3: P = 0.085; Control: F2,222 = 2.61, P = 0.076; Figure 2). Taken together, these results indicate that aggression can develop over time regardless of differences in food regime but that the effect is faster, more consistent, and more pronounced when either starvation or different nutritional composition is involved.
Workers fed with standard diet were more often the attacker than starved workers (model-based least squares mean number of attacks for Standard 1 and 2: 2.11 ± 0.42 vs. starvation: 0.85 ± 0.42; mixed model ANOVA, colony of origin within food regime as a random factor: n = 146, F1,144 = 18.87, P < 0.0001), whereas no such pattern was found in the Quality tests (mixed model ANOVA, colony of origin within food regime as a random factor: n = 74, F1,23.3 = 1.77, P = 0.197). The relative size difference between workers did not predict the attacker (mean number of attacks within each pair: smaller ants 1.47 ± 0.33, N = 110; larger ants 1.64 ± 0.33, N = 110), and the relationship between size and treatment pairs (Quality and Quantity) on attacking behavior was similar (mixed model ANOVA, colony of origin within food regime as a random factor—size: F1,217 = 0.50, P = 0.480; treatment pairs: F1,217 = 0.83, P = 0.363; size x treatment pair: F1,216 = 0.25, P = 0.616).
We found 129 compounds with a retention time between 5 and 35 min. A discriminant analysis of different food regimes excluded 6 compounds that had no effect on the discriminant functions, whereas the remaining 123 compounds were included. The chemical profiles diverged to a different degree between treatments, being smallest between Standard subcolony pairs (mean 0.73 ± 0.33) and greatest between subcolony pairs in both the Quantity (15.48 ± 5.28) and Quality (15.18 ± 10.05) treatments (mixed model ANOVA, colony of origin as a random factor: F1,10 = 7.02, P = 0.013; Bonferroni-adjusted comparisons—Standard vs. Quantity: P = 0.025; Standard vs. Quality: P = 0.028; Quantity vs. Quality: P = 1.0). Interestingly, aggression was most pronounced between the subcolonies whose chemical profiles had diverged the most (Pearson correlations, controls included: n = 24, r = 0.644, P = 0.0007; Figure 3; controls excluded: n = 18, r = 0.541, P = 0.02).
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DISCUSSION |
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Our results show that discriminative behavior can emerge between amicable nest fragments within weeks after separation. The phenomena also occurred in a species that is characterized by absence of aggression within intercommunicating nest networks. Indeed, the elevated aggression between colony fragments when both received the Standard diet shows that isolation alone can be enough to elicit discrimination among individuals originating from the same colony. This indicates that rather than relying solely on heritable cues alone, the exchange of workers, brood, and food (see Tsutsui et al. 2000
, 2003; Chapuisat et al. 2005) can homogenize recognition cues and maintain cohesion within intercommunicating networks at least in F. aquilonia.
More compellingly, our results also show that discrimination occurs sooner and is more pronounced when the diet also differs. In addition, differences in the nutritional status of colonies appear to trigger aggression, as reflected by the higher level of aggression in ants on standard diet compared with starved ants. This suggests that environmental cues mediate recognition between colonies and that the underlying recognition cues are mutable in response to extrinsic factors such as the amount and composition of food. Previous results have shown that differences in the composition of the diet can increase aggressiveness among workers of the same origin (Le Moli et al. 1992), but these authors did not manipulate the amount of food, only the composition. Contrary to our results, in a similar laboratory test, food availability did not affect the aggressiveness between nests in the Argentine ant L. humile (Thomas et al. 2005). This may indicate that there are differences in recognition mechanisms between the 2 species or differences in traits associated with nutritional requirements in the 2 species; for example, adaptation to natural fluctuations in diet in L. humile as opposed to a very stable diet in F. aquilonia.
Food manipulation experiments have often been criticized for being artificial and radical, and the outcome may therefore not apply in natural conditions (e.g., Stuart 1987). However, the degree to which we manipulated food composition was very modest and within the normal range of diet composition (Rosengren and Sundström 1987), which resulted in distinct changes in aggression. Interestingly, we also found that workers from well-fed subcolonies were more often the attackers rather than workers from poorly fed subcolonies. In contrast, no such differences were found between subcolonies on equal amounts of different diets. This suggests that ants experiencing poor conditions are less likely to initiate aggression. In the light of these results, it would be interesting to investigate the natural cannibalistic wood ant wars (Mabelis 1984) and determine who initiates those: the hungrier ones or the better fed neighbors. Contrary to expectations, the large workers were not more likely to initiate aggression, even though large workers often have defensive tasks in colonies (Brian 1983; Rosengren and Sundström 1987; Hölldobler and Wilson 1990).
The colony-specific chemical profiles were well diverged in the Quantity and Quality treatments, whereas the divergence was significantly less pronounced in the Standard treatment. This strongly suggests that the primary cause of divergence in the profiles was the diet or the amount of food and not random changes in the profile due to isolation. It is reasonable to assume that these differences had arisen during the experiment as all comparisons were made between subcolonies that had been established from the same field colony immediately before the experiment started. Our results agree with those of Richard et al. (2004) who found that isolation alone did not change colony odor profiles in A. subterraneus subterraneus.
The magnitudes of changes in aggression that we found largely matched the magnitude of changes in the cuticular chemical profiles. Indeed, the profiles were most divergent between subcolonies that showed the greatest level of aggression. These findings are consistent with aggression being elicited by differences in the colony odor profile, which in turn are mediated by dietary differences. However, the rate at which aggression developed differed between treatments, and aggression also developed in the absence of odor profile divergence (see Figure 2). This suggests the role of other factors apart from just differences in odor profiles moderate aggression. For example, the odor profiles may entail components that were not detected in our chemical analysis. It is also possible that some of the components that we excluded from our analysis underwent changes that were uncorrelated with diet but still allowed discrimination. In addition, stimuli other than odor profile, for example, nutritional stress, may moderate behavior and elicit aggression prior to any substantial divergence in odor profile. In this particular case, changes in the odor profile that was mediated by dietary differences nevertheless seem to substantially strengthen and accelerate the emergence of aggression.
In a previous study, aggression developed between nests of the same polydomous colony after deforestation (Sorvari and Hakkarainen 2004). Our results here provide new insights on the potential mechanisms behind the emergence of aggression; when the trees disappear, both the main sugar source (aphid colonies; Rosengren and Sundström 1991; Whittaker 1991; Punttila et al. 2004) and the visual orientation cues are lost (Rosengren and Pamilo 1978). This may inhibit worker, brood, and food exchange between nests and is likely to change the dietary options available to individual nests. Once contact between individual nests is lost and food sources diverge with different proportions of protein and sugar, or starvation as a consequence, a situation similar to that in our experiment may arise. Environmental factors such as food, nesting material, and spatial distance between nests have indeed been shown to modify nest mate recognition cues in Leptothorax curvispinosus (Stuart 1987), Solenopsis invicta (Obin 1986; Obin and Vander Meer 1988), and Formica pratensis (Pirk et al. 2001). Our study adds to these previous studies by demonstrating that concordant changes in diet and recognition are mediated at least partly by changes in colony odor profile.
Our results also raise issues related to the social organization of colonies and the genetic versus environmental determination of recognition labels. Whereas recognition in general is most stringent in monogyne societies, polygyne societies have been considered to be more lax in their colony closure (Hölldobler and Michener 1980; Keller and Passera 1989). When multiple matrilines are present in a colony, the within-nest genetic heterogeneity in odor cue diversity also necessarily increases relative to the population heterogeneity. As a result, colonies become chemically less distinct, recognition becomes less precise, and colony borders may become less defined (but see Stuart and Herbers 2000; van Wilgenburg et al. 2006). Unicolonial ants, where colony networks may encompass hundreds of nests all of which behave amicably toward each other, represent an extreme case of erasure of colony borders (Wilson 1971; Hölldobler and Wilson 1977, 1990). In addition, purging of genetic variation may promote such indiscriminate altruism (Tsutsui et al. 2000, 2003, but see Giraud et al. 2002). Our results show that recognition and discrimination can resurface when environmental conditions change if recognition cues are at least to some degree environmentally determined.
In conclusion, our results show that recognition labels can involve a mutable environmental component, and that changes in the environment may disrupt cooperative colony networks, by altering the chemical labels of groups through changes in nutritional balance. When this is the case, barriers are erected and amicable interactions between groups are disrupted. Hence, natural or anthropogenic disturbances, such as forest logging, may mediate dietary changes and could eventually come to alter the social system from unicoloniality to discrete colonies. Fundamental changes to social structure are, however, contingent on the permanence of such changes, and at present, it remains open whether the changes found in this study are reversible if communication trails are reestablished and the mixing of chemical cues restored. Nonetheless, the precise nature of recognition systems may crucially affect the way in which environmental change may impact ant social systems.
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FUNDING |
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Academy of Finland (206505 to L.S., 78794 to H.H.); Biological Interactions Graduate School; EU-Improving Human Potential research network "INSECTS" (HPRN-CT-2000-00052).
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ACKNOWLEDGEMENTS |
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We thank M. Chapuisat, P. Suorsa, P. Banks, and 3 anonymous referees for their valuable comments on the manuscript; S. Eirtovaara, T. Laine, and J. Muldoon for their assistance in laboratory; and P. Lehtonen and H. Ranta for supplying Petri dishes and agar.
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