(Hymenoptera Formicidae) on sand dunes in southern

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Space use, foraging success and competitive relationships in Formica cinerea (Hymenoptera Formicidae) on sand dunes in southern Finland a

B. Markó & W. Czechowski

b

a

Department of Taxonomy and Ecology, Babeş-Bolyai University, Clinicilor 5–7, 400006, Cluj-Napoca, Romania b

Museum and Institute of Zoology, Polish Academy of Sciences, Laboratory of Social and Myrmecophilous Insects, Wilcza 64, 00-679, Warsaw, Poland Available online: 14 Dec 2011

To cite this article: B. Markó & W. Czechowski (2012): Space use, foraging success and competitive relationships in Formica cinerea (Hymenoptera Formicidae) on sand dunes in southern Finland, Ethology Ecology & Evolution, 24:2, 149-164 To link to this article: http://dx.doi.org/10.1080/03949370.2011.634438

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Ethology Ecology & Evolution 24: 149–164, 2012

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Space use, foraging success and competitive relationships in Formica cinerea (Hymenoptera Formicidae) on sand dunes in southern Finland B. MARKÓ 1,3 and W. CZECHOWSKI 2 1

Department of Taxonomy and Ecology, Babe¸s-Bolyai University, Clinicilor 5–7, 400006 Cluj-Napoca, Romania 2 Museum and Institute of Zoology, Polish Academy of Sciences, Laboratory of Social and Myrmecophilous Insects, Wilcza 64, 00-679 Warsaw, Poland Received 17 January 2012, accepted 12 September 2011

The foraging strategy of a colony of social insects, e.g. ants, is made up of simple individual decisions being influenced by a series of factors like climatic conditions, properties and availability of food and competitive context. We studied the use of space, foraging success and competitive relationships in Formica cinerea around its nests in field conditions in the absence and in the presence of artificial food sources on sand dunes in Finland. Generally, the abundance of foragers was low around colonies. Sources in close proximity were mostly discovered. However, the fact that distant sources were sometimes preferred over discovered close sources during mass exploitation appeared to confer a certain sub-optimality upon the foraging strategy of the species. The use of baits allowed us to analyse the species’ competitive position as well. Generally, rivals could dominate sources far from the nest of F. cinerea, thus a facultative inhibition zone was established around the studied colonies. Although, mostly dominant in contests, F. cinerea could give up food sources to rivals if these were already gathered on the bait. The mixture of submissive and aggressive features, which characterise F. cinerea allows this species to adapt to the current competitive context and the availability of food sources. KEY WORDS:

ants, baits, collective decision-making, competition, conflicts, trunk trails, Formica cinerea.

INTRODUCTION

Ants, like social insects in general, are central-place foragers, meaning that they retrieve food to the colony, where it is distributed among nest mates and consumed (e.g. HÖLLDOBLER & WILSON 1990). A variety of food retrieval strategies are applied: from 3 Corresponding author: Bálint Markó, Department of Taxonomy and Ecology, Babe¸ s-Bolyai University, Clinicilor 5–7, 400006 Cluj-Napoca, Romania (E-mail: [email protected]).

ISSN 0394-9370 print/ISSN 1828-7131 online © 2012 Dipartimento di Biologia Evoluzionistica dell’Università, Firenze, Italia http://dx.doi.org/10.1080/03949370.2011.634438 http://www.tandfonline.com


150

B. Markó and W. Czechowski

the entirely solitary collection of food to intricate collective retrieving behaviour (e.g. HÖLLDOBLER & WILSON 1990). Usually, species with small colonies are more likely to use individual foraging or tandem recruitment, while species forming large colonies use efficient pheromone-based mass recruitment (BECKERS et al. 1989; MAILLEUX et al. 2003). Predictions founded upon the optimal foraging theory would also imply a capacity on the part of colonies to adjust the intensity of their foraging behaviour as a function of a discovered food source’s properties (e.g. quality, quantity, and distance from the nest), through communication among individuals. A key to understanding the contribution that individual actions make to emerging collective patterns is provided where self-organisation theory is applied to explain foraging patterns in ants (DETRAIN et al. 1999; CAMAZINE et al. 2001; DETRAIN & DENEUBOURG 2006; MEYER et al. 2008). While the emergence of collective patterns might be attributed to complex and sophisticated communication among individuals, several studies have now shown how simple the rules underpinning complex collective decisions may be (BONABEAU et al. 1998a, 1998b; DETRAIN et al. 1999; DE BISEAU & PASTEELS 2000; PORTHA et al. 2004; GORDON et al. 2008; MEYER et al. 2008). Higher quality or greater abundance of a food source elicits more intense trail-laying behaviour, more active recruitment, or a stronger response from nest mates (PASTEELS et al. 1987a; BONSER et al. 1998; DE BISEAU & PASTEELS 2000; PORTHA et al. 2004; MEYER et al. 2008). Where closer sources are concerned, the simple fact that individuals return from them sooner can again ensure more intense exploitation of the closer source (DETRAIN et al. 1999; MEYER et al. 2008). These all contribute to the emergence of biases in the distribution of foragers around colonies. Most studies on space use and foraging strategies in ants use ex situ laboratory experiments. These studies focus on the making of foraging choices as a function of food item properties or else internal organisation, the state of the colony (for a review see DETRAIN et al. 1999; DETRAIN & DENEUBOURG 2006). However, relatively few studies deal with the use of space by foragers and optimality issues in situ (e.g. BONSER et al. 1998; DETRAIN et al. 2000; BURD 2001; COGNI & OLIVEIRA 2004). The circumstances of field studies make it much more difficult, if not even impossible, for mechanisms to be revealed as they would be under laboratory conditions. There is, nevertheless, an important factor present that is lacking ex situ, i.e. the natural competitive and/or predatory context that goes a long way towards determining the foraging strategy applied (SANDERS & GORDON 2003; ADLER et al. 2007). The fiercest competitors of ants are other ants. For these reasons, observed foraging behaviour can be explained satisfactorily by reference to inter- and intraspecific relationships (VEPSÄLÄINEN & PISARSKI 1982; CZECHOWSKI 1985; SAVOLAINEN & VEPSÄLÄINEN 1988; SAVOLAINEN 1991; SANDERS & GORDON 2003; MARKÓ & CZECHOWSKI 2004; ADLER et al. 2007). In the presence of territorial species, a significant alteration may take place in the behaviour of the non-territorial (i.e. subordinate) species. For example they may shift their foraging strategy in space (VEPSÄLÄINEN & SAVOLAINEN 1990) and in time (REZNIKOVA 1983), or they may select smaller food items (SAVOLAINEN 1991). On the other hand, competition can even intensify their recruitment (DETRAIN et al. 1999). The in situ study of foraging strategy, from the perspective of the optimal foraging theory, in a non-territorial ant species would offer interesting insights as to the constraints acting upon foraging in ants. An ideal study subject of this profile is Formica cinerea with its strange competitive in-between status (territorial vs non-territorial), while foraging on food sources both permanent (aphid colonies) and ephemeral and confronting competitive pressure due to general food scarcity (see GALLÉ 1991; MARKÓ & CZECHOWSKI 2004; CZECHOWSKI & MARKÓ 2005).

Foraging strategy and competition in F. cinerea

151


Our study considered the following hypotheses, issues, and presented questions: 1. Colonies are expected to maximise the probability of food discovery, because of the scarcity of food in the harsh environmental conditions of the sand dunes. Foragers should cover the area around the nest. Nevertheless, the foraging effort around colonies might be strongly biased towards certain previously rewarding sites (DETRAIN et al. 2000; BEVERLY et al. 2009). 2. How does a colony allocate foraging effort between permanent food sources (e.g. aphid colonies) and other sources occurring on the sand surface? 3. Closer food sources should always be preferred over distant food sources (if they are equal in size and quality). Such a preference would optimise the net benefit/cost ratio, and/or ensure the safety of exploitation (e.g. the possibility of fast retrieval in case conflicts arise) (e.g. DETRAIN et al. 1999). 4. Are there biases in the distribution of rival ant species around the nests of F. cinerea which could reveal competitive effect of this species? Does this effect reflect in the foraging success of the rivals? 5. Finally, how could the competitive position of F. cinerea be characterised?

MATERIAL AND METHODS Species, site and colonies studied Formica (Serviformica) cinerea is an oligotope of dry grasslands and forests that occurs in sun-exposed, mostly sandy habitats, from coastal and inland dunes to light pine forests or towns (SEIFERT 2002). Both monogynous (one functional queen within a colony) and polygynous (several functional queens) colonies occur, which frequently develop into very extensive and populous polydomous systems, which are made up of several interrelated nests (SEIFERT 2002). Formica cinerea lives largely by way of predation and scavenging, while also feeding on honeydew. Its competitive hierarchical status has not been decisively determined. While some data (e.g. PISARSKI & VEPSÄLÄINEN 1989) point to its territorial status, there are researchers (e.g. GALLÉ 1991) who consider F. cinerea to be a non-territorial species. Some observations also point to an in-between status of this species (MARKÓ & CZECHOWSKI 2004). The studies were carried out in a complex of sand dunes near the village of Tvärminne on the Hanko Peninsula of southern Finland (59◦ 50 N, 23◦ 15 E) from June to August 2002. Formica cinerea mainly inhabits there more or less open sandy areas, sparsely overgrown with young Scots pines (Pinus sylvestris), with barely a cover of low herbs (Festuca ovina, Carex arenaria), and with patches of lichens and mosses (GALLÉ 1991). Our studies centred on a total of nine separate colonies distributed over approximately one hectare of dune area (i.e. colonies 1–9). Additionally, one further aggregation of colonies (hereinafter nest complex 10 [or colonies FC-1, FC-1∗ and FC-1∗∗ in CZECHOWSKI & MARKÓ 2005 and CZECHOWSKI et al. 2009]) was initially studied as a single entity. Aggression tests only later revealed that it was composed of separate colonies, which were clearly aggressive towards each other (see CZECHOWSKI & MARKÓ 2005). Consequently, the results for this nest complex could be used only with regard to Formica cinerea’s competitive relationships. The majority of colonies also had well-delimited trails (generally one) leading to aphids on pines, which were constantly tended during the study period. Foraging around colonies Baits are established means to study foraging patterns and behaviour of ants around their nests. The presence of large food sources does enhance, and thus alter, the activity of ants in the specific area in which a bait is placed (VEPSÄLÄINEN & PISARSKI 1982; SAVOLAINEN &


152


VEPSÄLÄINEN 1988; VEPSÄLÄINEN & SAVOLAINEN 1990). For this reason, the distribution of foragers was also recorded in the absence of baits (‘nudum’ observations), to obtain an appropriate view of the foraging strategy in a specific ant species (see also MARKÓ & CZECHOWSKI 2004; CZECHOWSKI & MARKÓ 2005). We located eight observation plots (each of 19 cm × 19 cm) around the nest areas of the studied colonies (Fig. 1; see also MARKÓ & CZECHOWSKI 2004; CZECHOWSKI & MARKÓ 2005). Each plot was observed for the number and species of foraging ants present, as well as the frequency and type of ant-ant aggressive encounters (fights or attempts to drive others away). The location of the first observation plot was selected randomly. Other plots were located in relation to the first. Plots were arranged systematically in two distance categories. The centres of the closer observation plots (n = 4) were at 0.5 m, while the centres of the more distant plots were 1.5 m distance from the border of the colony’s nest area. Generally, in laboratory experiments much smaller distances are applied between an ant nest and the food source, when studying foraging in ants (see e.g. DE BISEAU et al. 1997; DE BISEAU & PASTEELS 2000). Thus, we considered that the applied distances in our case could offer reliable information on the distribution of foragers around colonies in field conditions. Formica cinerea foragers are active all day long in the studied population (see MARKÓ & CZECHOWSKI 2004). However, summertime activity peaks at around 09:00–10:00, and around 16:00–18:00, as the ants tended to avoid both cooler mornings and evenings, and the heat of midday, at which time the temperature of the sand surface could exceed 45 ◦ C (see MARKÓ & CZECHOWSKI 2004 for detailed analysis). According to this observations were made during three 220-min periods a day (08:00–11:40, 12:40–16:20 and 17:20–21:00), which covered the active period of the species. Within each period, each plot was checked for one min every 20 min. This way of checking ensured that each 220-min period consisted of 11 observations. Consequently, in the case of each colony we obtained 33 observations for each plot during one observation day, with the exception of colonies 1 (n = 18), 3 and 4 (n = 22), where a sudden rain shortened the series

Fig. 1. — The arrangement of rectangular observation plots around a colony. Distances of plots are given from the border of the colony’s nest area to the centre of each plot.



153

of bait-free observations. In the case of each colony 2-day observations were carried out: 1st-day observations were made in the absence of baits (‘nudum’), whereas baits were put out in the centre of each plot on day 2. To avoid any effect due to seasonal variation in food preferences, baits included both animal protein (tuna flakes) and carbohydrate (mixed-flower honey). Bait portions of ca 3.5 cm in diameter were placed on 9.5 cm plastic plates. The portions were put out 10 min before the first observation at the beginning of each period. The baits were retrieved at the end of each period. The division of workforce among trunk trails and sand surface was studied around colonies 7 and 8. Both colonies had one well-delimited trunk-trail leading to a pine tree. Here, after the regular 2-day observations (on 11 and 12 July), ‘nudum’ observations were subject to fourfold replication (on 16, 21, 26, and 31 July), i.e. with each replicate separated by 5 days. To obtain an accurate picture of foraging activity on trails, one observation plot was also placed on the trunktrails of the said colonies during these last for ‘nudum’ observations. The centre of the trail plots was a 0.5 m away from the nest area borders of the colonies. Observations regarding activity on trunk trails were conducted parallel to observations of activity in plots. Data from these observations were used only to assess the differences in the investment of colonies in different types of food sources.

Data management The effect of distance from the colony’s nest area border on the distribution of Formica cinerea foragers was analysed by the use of generalised linear mixed model (GLMM) (Poisson distribution) for ‘nudum’ observations. All individual observations were included (see Foraging around colonies for no. of observations/colony); distance from the border was treated as fixed factor, while colonial identity and repetitions for the same plot were treated as random factors. The Kruskal-Wallis test was used in order to reveal differences in the distribution of foragers among plots located at the same distance category during ‘nudum’ observations, separately for each colony. In the case of colonies 7 and 8 only data from 1st-day ‘nudum’ observations were included. The differences in the number of F. cinerea foragers between trails and plots were also analysed by the use of GLMM (Poisson distribution) in the case of the four replicates of ‘nudum’ observations, which included trail observations at colonies 7 and 8. In order to assess the differences in foragers’ distribution between trails and non-trail areas, data from plots were pooled for each 20-min observation series, resulting in 33 observations/colony. The same number of observations was obtained in the case of each trail per observation day. Replicates were treated as random factors, the observation area (plot vs trail) was handled as fixed factor. The 4-day replicates of ‘nudum’ observations, when trail inspections were carried out, were included as interacting fixed factors, in order to assess whether the abundance of individuals varied significantly among different days. The predictability of the baits’ exploitation pattern was studied by correlating the daily mean number of F. cinerea foragers in plots around colony nest areas in the absence of baits with the daily mean for F. cinerea foragers observed at baits using Spearman rank correlation. Biases in the distribution of rival species in relation to the distance from the nest area borders of F. cinerea colonies were analysed by the use of GLMM (Poisson distribution) for ‘nudum’ and bait observations as well. All individual observations were included (see Foraging around colonies for no. of observations/colony) with the exception of data from those colonies, where only F. cinerea was detected (see Results). In the case of colonies 7 and 8 again only data from 1st-day ‘nudum’ observations were included. Data from nest complex 10 were also included (see Species, site and colonies studied). Distance from nest area border was treated as fixed factor, the number of F. cinerea foragers was handled as covariate, while colonial identity and replicates for the same plot were treated as random factors. The same type of analysis was conducted separately for the two most abundant rivals at baits, Lasius psammophilus and Myrmica schencki. Only data from those colonies were included where these species occurred (see Results).

154


We used table-wide sequential Bonferroni-correction (RICE 1989) to reveal the exact significance level when performing multiple analyses of related datasets (e.g. Kruskal-Wallis analysis, Spearman rank correlations). All statistical analyses were carried out using the R 2.9.1 statistical package (R DEVELOPMENT CORE TEAM 2010).

RESULTS


Dynamics and spatial distribution of foragers around nests in the absence of baits Formica cinerea foragers were present in low abundance around their colonies (mean = 0.54 ind./obs., SD = ± 1.18). Distance from the colony border did not affect the distribution of F. cinerea foragers as a general rule (GLMM, z = − 1.7, P = 0.09, n = 2080), although foragers were more abundant in plots close to a colony’s nest area at many colonies in the absence of baits (Fig. 2). The number of foragers also showed significant variations among close plots (Kruskal-Wallis χ 2 ≥ 11.82, P < 0.01, n = 33 observations, df = 3) in the case of almost each colony, with the exception of colonies 3 and 7. In the case of distant plots significant variations among plots (Kruskal-Wallis χ 2 ≥ 12.76, P < 0.05, n = 33 observations, df = 3) could be revealed only in half of the cases, while no such differences were detected at colonies 1, 2, 5 and 8. Thus, the probability of food discovery was, generally, spatially biased around the studied colonies, and these biases were more enhanced in the case of close plots. The distribution of foragers was also clearly affected by the type of food source – permanent (aphid colonies on trees) vs ephemeral (food items on the sand surface) –

Fig. 2. — Distribution of foragers between close and distant plots around colonies during observations in the absence of baits.



155

Fig. 3. — Distribution of F. cinerea foragers between trails and plots at colonies 7 and 8 during the four replicates of observations in the absence of baits.

they were foraging for at colonies 7 and 8 in the absence of baits, as revealed by the GLMM analysis (plot z = 3.02, P < 0.01, trail z = 4.96, P < 0.0001, n = 528). The number of foragers was generally higher on trails leading to aphid colonies, than in plots (Fig. 3). The abundance of foragers on trails showed also significant variations among replicates (trail vs replicates z ≥ 4.53, P < 0.0001, n = 528, Fig. 3), while no such differences were discovered in plots (plot vs replicates z ≤ 1.71, P = NS, n = 528, Fig. 3). Foraging success and predictability Generally, colony members discovered the majority of baits around Formica cinerea nest areas, especially those close to the nest (Fig. 4, Wilcoxon signed-rank test W = 15, P = 0.04, n = 9 colonies). The exception here was small colony 2. Recruitment mostly occurred in the case of close baits, but there were also examples of the reverse situation (at colonies 4, 6, and 9; see Fig. 4). The exploitation pattern did not prove to be predictable; significant relationships between the distribution of foragers in ‘nudum’ situation and at baits were found only at colonies 6, 7 and 9 (Spearman r ≥ 0.81, P < 0.05, n = 8 plots). However, the exploitation pattern was stable all day long in the majority of cases: Spearman’s r was significant (r ≥ 0.73, P < 0.05) among the mean numbers of foragers observed at baits in the three observation periods at all colonies, with the exception of colony 8 (only 1st vs 3rd and 2nd vs 3rd periods), and colony 3. Dealing with competitors Aside from Formica cinerea itself, the three ant species quite frequently observed around the studied F. cinerea colonies were Lasius psammophilus, Myrmica schencki


156


Fig. 4. — Number and location of baits discovered by the studied F. cinerea colonies, and numbers of baits dominated and exploited through recruitment (max. four baits/distance category).

and Temnothorax tuberum (Table 1). In addition, several other species were occasionally detected, i.e. Formica sanguinea at colony 1 (mean = 0.02 ind./obs. in ‘nudum’ vs 0.005 ind./obs. at baits), Lasius niger at colony 2 at baits (mean = 0.005 ind./obs.), Tetramorium cf. caespitum at nest complex 10 (mean = 0.004 ind./obs. in ‘nudum’ vs 1.24 ind./obs. at baits), Formica fusca at baits at colonies 9 and 4 (mean = 0.03 and 0.01 ind./obs.), and Myrmica ruginodis at baits at colony 4 (mean = 0.003 ind./obs.). The numbers of foragers of other species were generally higher in the presence of baits (Table 1). Some additional species which were previously not recorded in the absence of baits also appeared. In the absence of baits, based on the GLMM analysis neither the distance from the studied Formica cinerea colony, nor the number of F. cinerea foragers, nor their interaction (z ≤ 1.33, P = NS, n = 1640) seemed to influence the distribution of workers of other species. The introduction of baits also did not cause significant bias in the distribution of foragers of other species with regard to the distance from F. cinerea colony’s nest area border (GLMM, z = 1.644, P = NS, n = 1848); nevertheless the number of F. cinerea foragers had a significant negative effect on their abundance (z = − 2.93, P < 0.01), and this effect varied according to distance from the F. cinerea colony (z = 2.7, P < 0.01). The separate analysis of the two most abundant rival species gathered at baits yielded different results. Lasius psammophilus was not influenced by the distance (GLMM, z = − 0.055, P = NS, n = 1144), but it was clearly affected by the abundance of F. cinerea (z = 16.72, P < 0.001) and the effect varied according to distance from the

0.27 (0.24)

0.1 (0.12)

2.26 (1.23)

26.07∗

31.07∗

0.49 (0.24)

0.16 (0.14)

9

10

∗

0.29 (0.3)

21.07∗

—

—

n.a.

n.a.

n.a.

n.a.

3.36 (3.01)

n.a.

n.a.

n.a.

n.a.

1.11 (2.01)

28.19 (11.8)

6.76 (4.74)

2.86 (1.84)

10.89 (5.42)

3.87 (1.5)

11.44 (9.73)

Bait

Only ‘nudum’ observations were carried out.

9.28 (5.5)

0.42 (0.44)

16.07∗

0.37 (0.33)

31.07∗

0.38 (0.32)

0.29 (0.19)

11–12.07

8

0.17 (0.18)

7

26.07∗

0.8 (0.36)

6

21.07∗

0.53 (0.38)

5

0.19 (0.19)

0.19 (0.22)

4

0.14 (0.16)

0.34 (0.23)

3

16.07∗

0.62 (0.4)

11–12.07

1.49 (0.8)

2

Nudum

F. cinerea

1

Colony

—

—

—

—

—

—

—

0.004 (0.02)

—

—

—

—

—

0.03 (0.05)

—

—

0.003 (0.02)

0.01 (0.03)

Nudum

0.01 (0.03)

0.03 (0.08)

n.a.

n.a.

n.a.

n.a.

3.11 (4.74)

n.a.

n.a.

n.a.

n.a.

3.61 (4.62)

—

3.73 (1.58)

1.03 (1.33)

—

—

0.1 (0.23)

Bait

L. psammophilus

0.19 (0.18)

0.04 (0.09)

—

—

—

—

—

—

—

—

—

—

—

—

0.01 (0.04)

—

0.04 (0.08)

—

Nudum —

Bait

0.01 (0.04)

0.5 (0.12)

n.a.

n.a.

n.a.

n.a.

—

n.a.

n.a.

n.a.

n.a.

—

—

—

0.01 (0.03)

—

0.07 (0.09)

T. tuberum

2.1 (3.6)

3.64 (6.47)

—

—

—

—

—

—

—

—

—

—

—

—

0.005 (0.03)

—

0.003 (0.02)

—

Nudum

—

—

—

Bait

n.a.

n.a.

n.a.

n.a.

—

n.a.

n.a.

n.a.

n.a.

—

—

—

0.14 (0.17)

M. schencki

Mean number (SD) of foragers/plot and minute (n = 33 in most cases; the number of individuals was pooled over the eight plots) belonging to the most frequent species with baits absent or present around the studied F. cinerea colonies. Data on nest complex 10 are also included.

Table 1.


Foraging strategy and competition in F. cinerea 157


158


colony border (z = 31.23, P < 0.001). Myrmica schencki, in turn, was not affected either by the distance from F. cinerea colony or by the number of foragers or their interaction with distance (GLMM, z ≤ 0.25, P = NS, n = 792). Baits were, generally, dominated by Formica cinerea. This species was recorded in 67% of the observations. Lasius psammophilus also occurred frequently at baits, followed by Myrmica schencki and Temnothorax tuberum (Fig. 5). The rate of co-occurrence with F. cinerea was generally high in most species, with the exception of L. psammophilus (Fig. 5), which seemed to avoid (or be avoided by) F. cinerea. Besides Formica cinerea only a few other species succeeded in exploiting baits, these being Lasius psammophilus, Myrmica schencki and Tetramorium cf. caespitum. In all these cases the general rule was that the species which discovered the bait first and started recruitment also kept this food source. These baits were mostly far from the studied F. cinerea colonies (Fig. 6), with the exception of the small colony 2, and a close bait at colony 7 dominated by L. psammophilus. This latter bait was not found at all by F. cinerea at any time during the study period. Since F. cinerea did not find the bait, L. psammophilus was able to exploit the source undisturbed (see colony 25 in MARKÓ & CZECHOWSKI 2004). We rarely observed direct conflicts in the absence of baits. However, because of the relatively large number of Formica cinerea foragers, intraspecific conflicts were expected to arise, as indeed they did, if only rarely. One aggressive intraspecific encounter was recorded at both colonies 1 and 5 (in close plots), while there were four such encounters at colony 2 (one and three on close and distant plots respectively). Cases of interspecific aggression involving F. cinerea were also observed: four

Fig. 5. — Frequency of the occurrence of different species (regardless of their abundance) and their co-occurrences with F. cinerea at baits around the studied F. cinerea colonies.



159

Fig. 6. — Number and location of baits dominated (through recruitment) by different species, around the studied F. cinerea colonies (max. four baits/distance category).

interactions with Formica sanguinea and three with Myrmica schencki workers. These interspecific conflicts took place in distant plots, and F. cinerea dominated in all cases. Naturally, conflicts took place more frequently at baits (Table 2), the majority of these being intraspecific ones. These conflicts took place almost irrespective of the distance from the margin of the studied Formica cinerea colony’s nest area. Interspecific conflicts, in turn, occurred mainly at long distances from the F. cinerea colonies. These interspecific disputes were generally won by F. cinerea, except in the case of some of the conflicts with Lasius psammophilus and Myrmica schencki (Table 2).

DISCUSSION

The foraging strategies of social insect colonies can be considered to be evolutionary responses seeking to maximise collective efficiency in food-source exploitation (see DETRAIN et al. 2000). Ideally, an ant colony should maximise the acquisition of food sources by matching the spatial and temporal distributions of foragers to that of the availability of food sources around nests (DE BISEAU & PASTEELS 2000; DETRAIN et al. 2000; GORDON et al. 2008; BEVERLY et al. 2009), or even by fitting the structure of a colony itself to the distribution of food sources, as in multi-nest systems sometimes

160


Table 2. Number of individuals involved in different types of negative interactions with F. cinerea in the presence of baits in close vs distant plots (lost – no. of individuals losing a conflict to F. cinerea specimens; won – no. of individuals winning a conflict against F. cinerea specimens). Direct aggression Species

Close F. cinerea


F. sanguinea

Frightened off

Outcome

Lost

Distant

Close

Distant

26

23

7

2

2

2

—

1

F. fusca

Lost

6

—

2

—

L. psammophilus

Won

—

2

—

1

Lost

—

6

—

2

M. schencki

Won

—

4

5

—

Lost

3

21

—

7

Lost

—

4

2

3

T. tuberum

(CZECHOWSKI 1975; CERDÁ et al. 2002). We studied and analysed the distribution of individuals around nests and competitive relationships in a Formica cinerea population where colonies have to deal with multiple constraints: extreme climatic conditions, a shortage of food on the sand surface, efficient work force division between different types of source, and competitive pressure. The biases in the distribution of foragers around an ant colony reflect different levels of interest in the surrounding areas (PORTHA et al. 2004; BEVERLY et al. 2009), and consequently the biases affecting discovery probabilities. Contrary to expectations in Formica cinerea the number of individuals is generally not higher close to a colony, although there are considerable variations among colonies. Foragers cover the close vicinity of the colony’s nest area less evenly than the wider area around the nest. F. cinerea foragers probably leave the nest on more or less diffuse exit trails, only spreading out farther from the colonies, as observed in other ant species as well (BEVERLY et al. 2009). Not surprisingly, foraging activity on trails is much more intense than diffuse foraging on the sand surface off the trails. Aphid colonies are reliable and constant sources, thus rewarding in almost any conditions. Our results indicate that the pattern of exploitation of such ephemeral food sources as baits is not predictable. Although, as expected, close baits were discovered more easily, recruitment occurred in the case not only of close baits, but also of some distant ones. Massive exploitation of distant baits even took place in cases in which each of the close baits had been discovered, and yet despite their discovery the close baits were not exploited. Paradoxically, such sub-optimal choices can become optimal if distant baits are placed close to a trunk-trail, so that the colony is ultimately ‘spared’ the cost of any recruitment process (as with one distant bait at colonies 4 and 6 respectively). In the case of other species, such as Lasius fuliginosus, it is known that trunk-trail foragers may exploit ephemeral sources appearing along trails, while ignoring others at greater distances from the trails (QUINET et al. 1997; BONSER et al. 1998). As not all of the distant baits that were exploited were situated along trunk-trails, other factors also seem to count. The baits in question were discovered sooner, and by more foragers, which could result in a higher rate of recruitment (DE BISEAU et al. 1997).



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BONSER et al. (1998) found that foraging workers of Lasius niger and Myrmica ruginodis spend more time at distant baits. The anticipated result of this is more enhanced exploitation of closer baits, as foragers spend less time at these baits and also return to the colony sooner. Ultimately, the low proportion of exploited vs discovered baits and the relative preference for distant over close baits suggest that Formica cinerea colonies are neither good distance optimisers nor appropriate communicators when it comes to efficiency of recruitment. While changes in the exploitation pattern were expected to occur in the course of observation, e.g. shifts to more intense exploitation of close baits from distant ones, the foraging pattern stayed surprisingly stable throughout the day. Such a conservative pattern could reflect high site-constancy on the part of the foragers. High site fidelity could be an appropriate strategy especially for the species in extreme habitats, as in our case of Formica cinerea on more or less open sand dunes. Where food is scarce the discovery of a valuable source favours conservative behaviour, as opposed to haphazard searching for new food sources. So, can it still be advantageous for a colony not to concentrate fully on a single source, or a few sources, but rather to divide foragers among several, as in the case of Formica cinerea? If colonies engage in the simultaneous exploitation of more sources, individuals could stick to their choice, and information is retained on available food sources around the colony. In the event that one of the heavily exploited sources becomes depleted, the colony can shift to another. Paradoxically then, the presence of ‘conservative’ individuals can confer a degree of plasticity upon a colony, in conditions where food sources are scarce or hard to retain (PASTEELS et al. 1987a, 1987b). Food items on a sand surface are distributed unevenly in both temporal and spatial terms, and there are also great differences in quality. The noisiness of the colonial response can be adaptive and crucial, in the event of sources exploited en masse becoming depleted or less accessible (PASTEELS et al. 1987a; MEYER et al. 2008). Competition is one of the main factors influencing foraging decisions, and ultimately success (VEPSÄLÄINEN & PISARSKI 1982; CZECHOWSKI 1985; SAVOLAINEN & VEPSÄLÄINEN 1988; SAVOLAINEN 1991; SANDERS & GORDON 2003; MARKÓ & CZECHOWSKI 2004; CZECHOWSKI & MARKÓ 2005). Our results suggest that a facultative interspecific inhibition zone is only established around Formica cinerea colonies in the presence of food sources, and it is mostly generated directly as a response to changes in the abundance of F. cinerea foragers. The facultative character of this inhibition is emphasised by the differential effect of F. cinerea on two of its most abundant rivals. While its direct negative impact on the abundance of Lasius psammophilus can be attributed to the enhanced competition between these two species (see MARKÓ & CZECHOWSKI 2004), as also mirrored by the low frequency of their co-occurrences, in the case of Myrmica schencki no such direct effect was detected. However, the numerous conflicts clearly tell us about the existence of antagonistic relationship between M. schencki and F. cinerea. Probably the submissive character of M. schencki (see VEPSÄLÄINEN & SAVOLAINEN 1990) lets it coexist to a given extent at baits with the dominant F. cinerea. The existence of this intra- and interspecific inhibition zone is reflected more conspicuously referring solely to the spatial pattern of exploited food sources, as rival species and colonies can massively exploit mostly sources placed at bigger distance from F. cinerea colonies. The outcomes of observed conflicts taking place over baits clearly show how F. cinerea may even dominate when confronting such territorial species as Formica sanguinea or Formica rufa (CZECHOWSKI & MARKÓ 2005). In spite of this, the number of conflicts lost to such otherwise clearly inferior species as Myrmica schencki and Lasius psammophilus shows certain plasticity in the


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behaviour of Formica cinerea. While F. cinerea is generally dominant in one-on-one confrontations, it usually gives up more easily when outnumbered by rivals. Thus, F. cinerea could be viewed as an aggressive species. The low efficiency of its recruitment strategy, relative to the more efficient strategy of rival species, could play an important role in deciding which species takes over a specific source. The rapidity and magnitude of recruitment could be decisive, as DE BISEAU et al. (1997) showed for Myrmica sabuleti competing with Formica fusca. In our case, M. schencki and L. psammophilus succeeded in some situations, against all odds. Their success could also be attributed to a faster and more precise recruitment strategy, in patches otherwise dominated by the more aggressive, larger and numerically dominant F. cinerea (MARKÓ & CZECHOWSKI 2004). Ultimately, the mixture of plastic and conservative features of the foraging strategy of Formica cinerea is what allows this species to adapt to both the availability of food sources and the competitive context on the northern sand dunes. Seemingly sub-optimal decisions of individuals, such as exploiting distant sources, could give rise to optimal patterns at colony level given the right context, such as proximity of trunk-trails, and competition. On the other hand, there are several aspects attesting to ‘weaknesses’ in the F. cinerea strategy: the non-discovery of certain baits, for example, or the lack of recruitment to specific close baits. It would be worth studying whether the more efficient pheromone-based recruitment could even occur in this species while foraging on a sand surface that sometimes shows temperatures of 40 ◦ C (MARKÓ & CZECHOWSKI 2004). The lack of such a system would at least partially explain the conservative character of certain patterns.

ACKNOWLEDGEMENTS We are grateful for the valuable comments of Kari Vepsäläinen concerning optimisation theory. The critical remarks of anonymous reviewers on earlier versions of the manuscript contributed essentially to its improvement. We are indebted for the rigorous linguistic corrections made by James Richards and Mary Lewandowska, which improved the manuscript’s quality considerably. Bálint Markó’s stay in Finland was supported by a grant from the Romanian Ministry of Education and Research (ONBSS 2001). His work during the preparation of the manuscript was supported by 31/1342 CNCSIS and ID-552 IDEI PNII. Wojciech Czechowski’s stay in Finland took place within a program of scientific cooperation between the Polish Academy of Sciences and the Academy of Finland. Both of us are grateful for the support offered by the Tvärminne Zoological Station of the University of Helsinki in the course of fieldwork, as well as for the splendid environment for study that was offered. We are also thankful for the help and advice provided by Alex Radchenko.

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