J Insect Behav DOI 10.1007/s10905-014-9439-3
Spatio-temporal Foraging Dynamics in Two Coexisting Harvester Ants (Hymenoptera: Formicidae) Luigi Solida & Luca Luiselli & Donato A. Grasso & Dario D’Eustacchio & Alessandra Mori & Alberto Fanfani
Revised: 15 January 2014 / Accepted: 21 January 2014 # Springer Science+Business Media New York 2014
Abstract Different aspects of the foraging strategies of two harvester ant species, Messor wasmanni and M. minor, were investigated in a Mediterranean dry grassland area. Baits were used to evaluate the existence of a trade-off between resource discovery and domination as well as the effect of three variables (air temperature, relative humidity and distance) on the trade-off. Baits were also utilized to explore random vs non random use of time by colonies. Random vs non random utilization of space was instead evaluated by mapping the daily foraging area of colonies in a grid of 900 plots of 1 m2 each. Results revealed that species coexistence is not preferentially supported by a trade-off in resource utilization with no overall effect of the examined variables. The foraging activity of the two species widely overlapped whilst a clear competition for space occurred. The observed space partitioning could represent an advantageous strategy for the coexistence of the two ant species. Keywords Harvester ants . discovery-dominance trade-off . temperature . territoriality . null models . coexistence
Introduction In ant communities, differences among ant species in abilities to discover or monopolize resources is generally reported as evidence of competition (Fellers 1987; Savolainen and L. Solida (*) : D. D’Eustacchio : A. Fanfani Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università degli Studi di Roma ‘La Sapienza’, Viale dell’Università 32, 00185 Roma, Italy e-mail:
[email protected] L. Luiselli Centro Studi Ambientali Demetra s.r.l., Via Olona 7, 00198 Roma, Italy D. A. Grasso : A. Mori Dipartimento di Bioscienze, Università degli Studi di Parma, Viale delle Scienze 11/A, 43124 Parma, Italy
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Vespäläinen 1989; Andersen 1992; Davidson 1998; Lach 2005). Differences among ant species in the tolerance to temperature or other abiotic factors is similarly considered a way to partition resources and to permit coexistence (Andersen 1995; Cerdá et al. 1997; Retana and Cerdá 2000; Lessard et al. 2009; Solida et al. 2011b; van Oudenhove et al. 2011; Wehner and Wehner 2011; Wiescher et al. 2011). In the Mediterranean ecosystem for example, dominant ant species are generally active away from dangerously high temperatures whereas subordinate species are active near their critical thermal limits (Cerdá et al. 1998b; Bestelmeyer 2000). Territoriality is further evidence of competition in ants (Fox et al. 1985; Davidson 1998). Colonies of territorial species partition space actively defending their foraging areas and included resources (Savolainen and Vespäläinen 1988; Hölldobler and Wilson 1990; Solida et al. 2010). In the present study we describe the foraging strategies adopted by two harvester ants, Messor wasmanni and M. minor, inhabiting a Mediterranean dry grassland area characterized by human exploitation. By means of baiting sessions we evaluated the ability of the two species to discover and monopolize food resources. The same procedure was adopted to evaluate the effect of three variables, distance of a nest from a bait, air temperature and relative humidity, on the capacity of the two ant species to discover and monopolize baits and on the number of individuals foraging on baits. Finally, Null models were used to test the existence of a competitive structure within the ant assemblage under study in respect to two variables, time and space. More in detail, since theoretical expectations suggest that the outcome of an interspecific interaction at the individual and colony-level depends on disparities in worker size or depends on numerical advantage stemming from asymmetries in recruitment ability or colony size (Hölldobler and Lumsden 1980; Fellers 1987; Adams 1990; Holway 1999), we assume that M. wasmanni colonies (larger population, bigger worker size) should be more able to monopolize baits compared to M. minor colonies. In addition, differences in the worker dimensions could cause different responses of species to temperature or relative humidity (Cerdá et al. 1998a). We also explored the potential effect that the distance travelled by workers to collect resources may have on the workers’ ability to monopolize baits and to arrive first at a given bait. We also suppose that time and space have an important effect on the coexistence of the two ant species. In particular, the trunk trails system could have an important role in space partitioning during the foraging activity of both species (Hölldobler and Wilson 1990; Acosta et al. 1995; Gordon 1995; Solida et al. 2010).
Materials and Methods Study Area Low vegetation sites as well as cultivated fields, dry and wet grasslands, are typical disturbed areas of the Mediterranean ecosystem consequent to human exploitation and grazing and characterized by the presence of hot climate specialists and opportunist species (sensu Andersen 1995; Castracani et al. 2010). Hot climate specialists consist of a functional group that includes, among others, ants belonging to the genus Messor (subfamily Myrmicinae). The study site was located inside the Presidential Estate of Castelporziano (Rome). It represents a typical dry grassland area, called “Coltivati”, characterized by the presence
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of Dasypyrum villosum and Vulpia ligustica therophyte species organized in a typical Mediterranean phytosociological association reported as “Vulpio ligusticaeDasypyretum villosi” (Fanelli 1998; Solida et al. 2011b). This type of disturbed ecosystem is subject to ploughing practices and grazing by horses and cows of the Maremmana stock according to traditional methods. It is possible to find Dasypyrum villosum L. phytocoenosis on irregularly cultivated or recently abandoned fields or on rubble just 1–2 years after abandonment (Fanelli 1998). M. wasmanni and M. minor found a suitable habitat to nest in this type of disturbed environment (Solida et al. 2011b). The nests were overdispersed at the interspecific level and there were nearly equal numbers of nests of the two species (i.e. 15 nests of M. wasmanni and 18 nests of M. minor; Solida et al. 2010). Sampling Baiting procedure are frequently used to study the response of ants to microclimate and interspecific competition (Bestelmeyer 2000; Sanders and Gordon 2003). In the present study baits were used to evaluate the effect of air temperature, relative humidity and distance of baits from the nests on the number of foragers of both species that reached baits and on the ability of the two ant species to discover and monopolize baits. Baits were further utilized to explore random vs non random use of time resource by colonies. Random vs non random utilization of space by interspecific colonies was instead evaluated by mapping the daily foraging area of the colonies by means of a grid of 30×30 m divided in 900 plots of 1 m2 each. Ten baits were placed at 5 m intervals along a linear transect of 45 m. We utilized three transects separated by a distance of 25 m each other for a total of 30 baits. Baits consisted of a Petri dish (diameter of 9.5 cm), filled with canary seeds (40 g), positioned on a round white card (diameter of 15 cm) in order to facilitate observation. We used canary seeds to exclusively attract harvester ants, among the most abundant species of the sampling area (Castracani et al. 2010). Preliminary tests showed that canary seeds represented an extremely attractive resource for the two ant species. Empty baits were re-filled with the same amount of seeds during inter-observation intervals. Observations were conducted at seven different intervals, 15, 30, 60, 90, 120, 150 and 180 min. The set of observations was repeated at two distinct times of the day, in the morning (from 6.30 to 9.30 h) and in the afternoon (from 17.30 to 20.30 h), to cover almost all the daily activity period of the colonies of the two ant species. Each transect was inspected for three consecutive days during the month of July 2009. During each observation we first visually inspected baits, then took a high resolution picture (Nikon D300) of the baits, recorded the above ground air temperature and relative humidity (Weather Station, Oregon Scientific, Model n° BA113) and measured the distance from the bait to the nest. Pictures were used to count the number of individuals of the two Messor species foraging on the observed bait. High resolution files in addition to differences in the colour of the head of the foragers make it possible to avoid possible biases concerning species identification. For the study of space exploitation by colonies of the two ant species we marked out the route followed by active trunk trails inside a grid of 30×30 m. The number of nests in this sampled area was 15 for M. wasmanni and 18 for M. minor (Solida et al. 2010). A plot was considered as part of the foraging area of a colony when crossed by its trails.
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The sum of plots crossed in 1 day by the colony trunk trail system corresponded to the daily foraging area of the mentioned colony (Brown and Gordon 2000). Maps of the individual colonies’ foraging areas were derived from observations performed during three 10-day periods, in May, August and October 2007 (Solida et al. 2010). Data Analysis We calculated the discovery ability index (DAI) and monopolized index (MI) to evaluate a possible trade-off in resource utilization among the ant species. DAI is the ratio of the number of baits where a species is the first to arrive (FA) to the total number of baits visited by that species (VB). Similarly, Monopolized index (MI) is the ratio of the number of monopolized baits (MB) to VB. A bait is considered monopolized by a species when foraging for more than two consecutive observation steps and if it is present alone during the last observation (Andersen 1992; Bestelmeyer 2000; Santini et al. 2007). Variation of DAI and MI indexes across species were analysed by General Linear Models (GLMs) after arcsine transformation of data. Linear correlation between DAI and MI was tested by Pearson’s correlation coefficient, with numbers for both species being combined. We also used GLMs for testing the effects of air temperature, relative humidity and distance from the nest on (i) the number of workers of the two ant species foraging on each bait, (ii) the number of baits where each species was first to arrive, and (iii) the number of baits that a species was able to monopolize. We tested for correlation among the considered indexes using Pearson’s correlation coefficient after having verified data normality and homoscedasticity. However, when data were not normally distributed, we transformed them to achieve normality. For instance, percentage data were arcsine transformed prior to apply any analyses. Null models randomizations (Gotelli and Graves 1996) were used to evaluate the effects of stochastic or competitive processes governing the temporal foraging dynamics of the ant species. Entries in the temporal analysis matrix consisted of the number of baits visited by each species during each observation step (from 1 to 7) for each “transect-day-time of the day” combination. The effects of air temperature on the time data matrix were evaluated using a nonparametric regression model (Kendall’s Tau). In this case, the original dataset was randomized 1,000 times with Monte Carlo algorithms, and the observed tau value was compared with the average simulated tau in order to draw a significance level for the analysis. Null models were also used to evaluate random versus non-random utilization of space by colonies of the two ant species. As an indicator of co-occurrence non-randomness, we used the number of checkerboard units, with 10,000 Monte Carlo randomizations. Entries in the matrix correspond to: 0.0 absence of both species from the considered plot; 0.1 presence of the only species M. wasmanni; 1.0 presence of the only species M. minor; 1.1 cooccurrence of both ant species in the same plot. Monte Carlo simulations of the original data matrices were performed by the EcoSim 7.7 software.
Results The results are summarized in Table 1. DAI did not differ significantly between the two species (F1, 34 =0.614, P=0.439), whereas MI varied significantly (F1, 34 =10.798,
6.94±4.29 7.12±4.19
0.87±0.54 13.75±7.83
21.19±9.04 16.81±8.89
17.06±11.30
12.00±7.34 9.87±6.65
Bait 2 Bait 3
Bait 4 Bait 5
Bait 6 Bait 7
Bait 8
Bait 9 Bait 10
1.19±1.19 0.00±0.00
0.06±0.06 0.00±0.00
1.31±1.31 2.94±2.94
8.06±6.25 3.56±3.43
4.25±2.59 9.87±4.98
Bait 1 Bait 2
Bait 3 Bait 4
Bait 5 Bait 6
Bait 7 Bait 8
Bait 9 Bait 10
Step 1
M. minor
4.25±4.25
Bait 1
Step 1
M. wasmanni
9.94±4.21 22.78±7.41
25.00±12.18 12.08±8.11
7.39±6.65 4.00±3.46
8.94±5.78 0.39±0.33
2.61±2.06 5.28±5.28
Step 2
14.22±8.56 17.50±10.64
19.89±13.64
24.33±9.85 23.22±11.86
23.11±9.88 26.17±11.38
27.39±10.19 15.00±8.90
7.33±6.31
Step 2
11.61±6.14 37.55±10.36
54.33±21.78 21.22±14.62
11.33±9.44 11.33±6.84
41.11±16.80 2.33±1.74
7.67±3.66 11.83±8.40
Step 3
29.11±13.57 26.89±14.79
33.67±17.02
40.78±12.56 40.05±16.73
45.17±15.16 42.83±14.98
45.00±14.19 31.50±13.07
13.72±8.93
Step 3
11.17±6.69 45.78±10.75
82.33±30.45 17.50±10.61
8.78±8.54 16.89±10.05
46.89±17.90 0.00±0.00
6.94±3.42 16.72±9.57
Step 4
29.33±12.15 24.55±13.30
38.89±15.35
45.78±13.27 40.50±16.17
61.72±19.77 63.67±16.96
59.72±17.17 37.72±14.52
30.55±12.78
Step 4
8.17±5.08 40.61±9.55
58.72±21.83 24.44±12.89
10.22±10.22 15.67±11.33
43.05±15.68 0.00±0.00
4.33±2.39 14.05±8.75
Step 5
33.33±10.76 22.78±12.80
44.11±15.44
45.67±12.32 39.78±13.54
68.33±18.84 71.72±16.30
76.50±15.33 52.05±17.20
37.05±14.69
Step 5
8.55±4.76 37.39±10.58
68.94±23.37 21.22±10.44
8.44±7.87 9.11±6.27
39.89±14.86 0.00±0.00
6.89±3.94 18.28±10.19
Step 6
32.89±10.67 28.61±14.35
51.67±17.12
48.89±13.13 57.28±17.45
65.00±19.20 73.05±16.17
78.94±15.58 55.61±16.41
44.22±15.82
Step 6
3.22±1.75 23.33±7.32
25.72±9.32 4.05±3.36
3.78±2.89 2.44±1.80
13.17±5.49 0.00±0.00
5.50±2.63 8.05±5.02
Step 7
21.67±8.44 9.72±6.70
26.28±9.75
24.00±8.58 29.94±12.11
58.44±17.92 68.28±17.45
56.44±15.85 34.83±13.48
34.00±15.08
Step 7
Table 1 Number of foragers of each ant species averaged (mean ± SE) across transects (from 1 to 3), day (from 1 to 3) and time of the day (morning and afternoon), recorded on a single bait during the different sampling steps
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P=0.0024), with DAI and MI being significantly inversely correlated (R=−0.262, P
