Spatio-temporal Foraging Dynamics in Two CoexistingHarvester 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 grasslandarea. Baits were used to evaluate the existence of a trade-off between resourcediscovery 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 explorerandom vs non random use of time by colonies. Random vs non random utilization ofspace was instead evaluated by mapping the daily foraging area of colonies in a grid of900 plots of 1 m2 each. Results revealed that species coexistence is not preferentiallysupported by a trade-off in resource utilization with no overall effect of the examinedvariables. The foraging activity of the two species widely overlapped whilst a clearcompetition for space occurred. The observed space partitioning could represent anadvantageous 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 monopolizeresources is generally reported as evidence of competition (Fellers 1987; Savolainen and

J Insect BehavDOI 10.1007/s10905-014-9439-3

L. Solida (*) :D. D’Eustacchio :A. FanfaniDipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università degli Studi di Roma‘La Sapienza’, Viale dell’Università 32, 00185 Roma, Italye-mail: luigi.solida@uniroma1.it

L. LuiselliCentro Studi Ambientali Demetra s.r.l., Via Olona 7, 00198 Roma, Italy

D. A. Grasso : A. MoriDipartimento di Bioscienze, Università degli Studi di Parma, Viale delle Scienze 11/A, 43124 Parma,Italy

Vespäläinen 1989; Andersen 1992; Davidson 1998; Lach 2005). Differences among antspecies in the tolerance to temperature or other abiotic factors is similarly considered away 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 ecosystemfor example, dominant ant species are generally active away from dangerously hightemperatures whereas subordinate species are active near their critical thermal limits(Cerdá et al. 1998b; Bestelmeyer 2000). Territoriality is further evidence of competitionin ants (Fox et al. 1985; Davidson 1998). Colonies of territorial species partition spaceactively defending their foraging areas and included resources (Savolainen andVespäläinen 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 charac-terized by human exploitation. By means of baiting sessions we evaluated the ability ofthe two species to discover and monopolize food resources. The same procedure wasadopted to evaluate the effect of three variables, distance of a nest from a bait, airtemperature and relative humidity, on the capacity of the two ant species to discoverand monopolize baits and on the number of individuals foraging on baits. Finally, Nullmodels were used to test the existence of a competitive structure within the ant assem-blage under study in respect to two variables, time and space. More in detail, sincetheoretical expectations suggest that the outcome of an interspecific interaction at theindividual and colony-level depends on disparities in worker size or depends on numer-ical advantage stemming from asymmetries in recruitment ability or colony size(Hölldobler and Lumsden 1980; Fellers 1987; Adams 1990; Holway 1999), we assumethatM. wasmanni colonies (larger population, bigger worker size) should bemore able tomonopolize baits compared to M. minor colonies. In addition, differences in the workerdimensions 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 byworkers to collect resources may have on the workers’ ability to monopolize baits and toarrive first at a given bait. We also suppose that time and space have an important effecton the coexistence of the two ant species. In particular, the trunk trails system could havean 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 typicaldisturbed areas of the Mediterranean ecosystem consequent to human exploitation andgrazing and characterized by the presence of hot climate specialists and opportunistspecies (sensu Andersen 1995; Castracani et al. 2010). Hot climate specialists consist ofa 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). Itrepresents a typical dry grassland area, called “Coltivati”, characterized by the presence

J Insect Behav

of Dasypyrum villosum and Vulpia ligustica therophyte species organized in a typicalMediterranean phytosociological association reported as “Vulpio ligusticae-Dasypyretum villosi” (Fanelli 1998; Solida et al. 2011b). This type of disturbedecosystem is subject to ploughing practices and grazing by horses and cows of theMaremmana stock according to traditional methods. It is possible to find Dasypyrumvillosum L. phytocoenosis on irregularly cultivated or recently abandoned fields or onrubble just 1–2 years after abandonment (Fanelli 1998).

M. wasmanni and M. minor found a suitable habitat to nest in this type of disturbedenvironment (Solida et al. 2011b). The nests were overdispersed at the interspecificlevel and there were nearly equal numbers of nests of the two species (i.e. 15 nests ofM. 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 andinterspecific competition (Bestelmeyer 2000; Sanders and Gordon 2003). In the presentstudy baits were used to evaluate the effect of air temperature, relative humidity anddistance of baits from the nests on the number of foragers of both species that reachedbaits and on the ability of the two ant species to discover and monopolize baits. Baitswere further utilized to explore random vs non random use of time resource bycolonies. Random vs non random utilization of space by interspecific colonies wasinstead evaluated by mapping the daily foraging area of the colonies by means of a gridof 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 utilizedthree transects separated by a distance of 25 m each other for a total of 30 baits. Baitsconsisted of a Petri dish (diameter of 9.5 cm), filled with canary seeds (40 g), positionedon a round white card (diameter of 15 cm) in order to facilitate observation. We usedcanary seeds to exclusively attract harvester ants, among the most abundant species ofthe sampling area (Castracani et al. 2010). Preliminary tests showed that canary seedsrepresented an extremely attractive resource for the two ant species. Empty baits werere-filled with the same amount of seeds during inter-observation intervals. Observationswere conducted at seven different intervals, 15, 30, 60, 90, 120, 150 and 180 min. Theset of observations was repeated at two distinct times of the day, in the morning (from6.30 to 9.30 h) and in the afternoon (from 17.30 to 20.30 h), to cover almost all thedaily activity period of the colonies of the two ant species. Each transect was inspectedfor three consecutive days during the month of July 2009. During each observation wefirst visually inspected baits, then took a high resolution picture (Nikon D300) of thebaits, recorded the above ground air temperature and relative humidity (WeatherStation, Oregon Scientific, Model n° BA113) and measured the distance from the baitto the nest. Pictures were used to count the number of individuals of the two Messorspecies foraging on the observed bait. High resolution files in addition to differences inthe colour of the head of the foragers make it possible to avoid possible biasesconcerning species identification.

For the study of space exploitation by colonies of the two ant species we marked outthe route followed by active trunk trails inside a grid of 30×30 m. The number of nestsin 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.

J Insect Behav

The sum of plots crossed in 1 day by the colony trunk trail system corresponded to thedaily foraging area of the mentioned colony (Brown and Gordon 2000). Maps of theindividual colonies’ foraging areas were derived from observations performed duringthree 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 evaluatea possible trade-off in resource utilization among the ant species. DAI is the ratio of thenumber of baits where a species is the first to arrive (FA) to the total number of baitsvisited by that species (VB). Similarly,Monopolized index (MI) is the ratio of the numberof monopolized baits (MB) to VB. A bait is considered monopolized by a species whenforaging for more than two consecutive observation steps and if it is present alone duringthe last observation (Andersen 1992; Bestelmeyer 2000; Santini et al. 2007). Variation ofDAI and MI indexes across species were analysed by General Linear Models (GLMs)after arcsine transformation of data. Linear correlation between DAI and MI was testedby Pearson’s correlation coefficient, with numbers for both species being combined.

We also used GLMs for testing the effects of air temperature, relative humidity anddistance from the nest on (i) the number of workers of the two ant species foraging oneach bait, (ii) the number of baits where each species was first to arrive, and (iii) thenumber of baits that a species was able to monopolize. We tested for correlation amongthe considered indexes using Pearson’s correlation coefficient after having verified datanormality and homoscedasticity. However, when data were not normally distributed,we transformed them to achieve normality. For instance, percentage data were arcsinetransformed prior to apply any analyses.

Null models randomizations (Gotelli and Graves 1996) were used to evaluate theeffects of stochastic or competitive processes governing the temporal foraging dynam-ics of the ant species. Entries in the temporal analysis matrix consisted of the number ofbaits 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 timedata matrix were evaluated using a nonparametric regression model (Kendall’s Tau). Inthis case, the original dataset was randomized 1,000 times with Monte Carlo algo-rithms, and the observed tau value was compared with the average simulated tau inorder to draw a significance level for the analysis. Null models were also used toevaluate random versus non-random utilization of space by colonies of the two antspecies. As an indicator of co-occurrence non-randomness, we used the number ofcheckerboard units, with 10,000 Monte Carlo randomizations. Entries in the matrixcorrespond to: 0.0 absence of both species from the considered plot; 0.1 presence of theonly species M. wasmanni; 1.0 presence of the only species M. minor; 1.1 co-occurrence of both ant species in the same plot. Monte Carlo simulations of the originaldata matrices were performed by the EcoSim 7.7 software.

Results

The results are summarized in Table 1. DAI did not differ significantly between the twospecies (F1, 34=0.614, P=0.439), whereas MI varied significantly (F1, 34=10.798,

J Insect Behav

Table1

Num

berof

foragersof

each

antspeciesaveraged

(mean±SE)across

transects(from

1to

3),d

ay(from

1to

3)andtim

eof

theday(m

orning

andafternoon),recordedon

asinglebaitduring

thedifferentsamplingsteps

M.w

asmanni

Step

1Step

2Step3

Step

4Step

5Step

6Step

7

Bait1

4.25

±4.25

7.33

±6.31

13.72±8.93

30.55±12.78

37.05±14.69

44.22±15.82

34.00±15.08

Bait2

6.94

±4.29

27.39±10.19

45.00±14.19

59.72±17.17

76.50±15.33

78.94±15.58

56.44±15.85

Bait3

7.12

±4.19

15.00±8.90

31.50±13.07

37.72±14.52

52.05±17.20

55.61±16.41

34.83±13.48

Bait4

0.87

±0.54

23.11±9.88

45.17±15.16

61.72±19.77

68.33±18.84

65.00±19.20

58.44±17.92

Bait5

13.75±7.83

26.17±11.38

42.83±14.98

63.67±16.96

71.72±16.30

73.05±16.17

68.28±17.45

Bait6

21.19±9.04

24.33±9.85

40.78±12.56

45.78±13.27

45.67±12.32

48.89±13.13

24.00±8.58

Bait7

16.81±8.89

23.22±11.86

40.05±16.73

40.50±16.17

39.78±13.54

57.28±17.45

29.94±12.11

Bait8

17.06±11.30

19.89±13.64

33.67±17.02

38.89±15.35

44.11±15.44

51.67±17.12

26.28±9.75

Bait9

12.00±7.34

14.22±8.56

29.11±13.57

29.33±12.15

33.33±10.76

32.89±10.67

21.67±8.44

Bait10

9.87

±6.65

17.50±10.64

26.89±14.79

24.55±13.30

22.78±12.80

28.61±14.35

9.72

±6.70

M.m

inor

Step

1Step

2Step

3Step

4Step5

Step

6Step

7

Bait1

1.19

±1.19

2.61

±2.06

7.67

±3.66

6.94

±3.42

4.33

±2.39

6.89

±3.94

5.50

±2.63

Bait2

0.00

±0.00

5.28

±5.28

11.83±8.40

16.72±9.57

14.05±8.75

18.28±10.19

8.05

±5.02

Bait3

0.06

±0.06

8.94

±5.78

41.11±16.80

46.89±17.90

43.05±15.68

39.89±14.86

13.17±5.49

Bait4

0.00

±0.00

0.39

±0.33

2.33

±1.74

0.00

±0.00

0.00

±0.00

0.00

±0.00

0.00

±0.00

Bait5

1.31

±1.31

7.39

±6.65

11.33±9.44

8.78

±8.54

10.22±10.22

8.44

±7.87

3.78

±2.89

Bait6

2.94

±2.94

4.00

±3.46

11.33±6.84

16.89±10.05

15.67±11.33

9.11

±6.27

2.44

±1.80

Bait7

8.06

±6.25

25.00±12.18

54.33±21.78

82.33±30.45

58.72±21.83

68.94±23.37

25.72±9.32

Bait8

3.56

±3.43

12.08±8.11

21.22±14.62

17.50±10.61

24.44±12.89

21.22±10.44

4.05

±3.36

Bait9

4.25

±2.59

9.94

±4.21

11.61±6.14

11.17±6.69

8.17

±5.08

8.55

±4.76

3.22

±1.75

Bait10

9.87

±4.98

22.78±7.41

37.55±10.36

45.78±10.75

40.61±9.55

37.39±10.58

23.33±7.32

J Insect Behav

P=0.0024), with DAI and MI being significantly inversely correlated (R=−0.262,P<0.00001) (Table 2). In terms of MI index, the better species in monopolizing baitswas M. wasmanni. Moreover, colonies activity on baits evidenced a marked differencebetween the two ant species, with the workers of M. wasmanni more numerous thanthose of M. minor.

The three considered variables, air temperature, relative humidity and distance fromthe nest, had no overall effect on the number of workers of the two ant species foragingon each bait (F=6.664, P<0.0001), on the number of baits where a species is the first toarrive (F=2.117; P=0.093) and on the number of baits that a species was able tomonopolize (F=2.775; P=0.076). Considering the effect of the single variables, ourdata revealed that the distance of the bait from the nest did not influence the number ofworkers of the two species foraging on each bait (Tukey Honest Post-hoc comparison:P=0.116), the number of baits where each species arrived first (P=0.337) or thenumber of monopolized baits (P=0.275). The temperature had positive significanteffect on the number of workers foraging on each bait (P=0.0001), positive significanteffect on the number of baits where a species is the first to arrive (P=0.047) and on thenumber of monopolized baits (P=0.033); relative humidity had significant positiveeffect only on the number of workers foraging on each bait. The mean number offoragers during the different sampling steps did not vary remarkably between species(t=0.860, P=0.407), but there was an increase in the number of foraging ants from thebeginning of the activity (step 1) to the end (step 7) (M. wasmanni: Kendall’s tau=0.714, P=0.024; M. minor: Kendall’s tau=0.619, P=0.05; Fig. 1).

Temporally, the checkerboard analysis revealed that there was a non-random segre-gation between species (Observed Index=3.308, Mean of Simulated Indices=2.671,Variance of Simulated Indices=0.011, P obs ≤ exp=1, P obs ≥ exp=0). Considering the two

Table 2 DAI (Discovery AbilityIndex) and MI (Monopolized In-dex) values for M. wasmanni andM. minor

M. wasmanni M. minor

DAI MI DAI MI

1.00 0.50 0.83 1.00

0.00 1.00 1.00 0.67

1.00 0.67 1.00 1.00

0.00 1.00 1.00 0.50

1.00 1.00 1.00 0.00

0.75 1.00 1.00 0.75

0.90 0.90 0.00 0.00

0.67 0.83 0.67 0.67

0.90 1.00 1.00 0.00

0.88 1.00 0.67 0.67

1.00 1.00 1.00 1.00

1.00 1.00 1.00 1.00

1.00 1.00 1.00 1.00

0.78 1.00 1.00 0.33

0.89 1.00 0.50 0.50

0.89 1.00 1.00 0.50

J Insect Behav

species combined, the effect of air temperature on the foraging behaviour of the two antspecies was not relevant (Kendall’s Tau=0.044, P=0.223).

The overlap values for space co-occurrences ranged from 0.226 in October to 0.441in July, with an intermediate value of 0.367 in May. These overlap values differedsignificantly from each other using 30,000 randomizations (Means of SimulatedIndices=0.398; Variance of Simulated Values=0.001; P<0.0001), thus showing thatthe ants partitioned space more significantly than expected in all sampling occasions.Null models revealed an overall non-random structure for space between the two antspecies (Observed Index=13.173, Mean of Simulated Indices=12.660, Variance ofSimulated Indices=0.000, P obs ≤ exp=1, P obs ≥ exp=0).

Discussion

Food and space are considered the major resources that coexisting species can partition(Schoener 1974; Pianka 1986; Kneitel and Chase 2004; Luiselli 2006, 2008; Vignoliand Luiselli 2012). The trade-off between resource discovery and resource monopoli-zation is one of the most common differences in species performance capable ofstructuring ant communities (Fellers 1987; Davidson 1998; Lach 2005). Temperaturesimilarly may represent a strong limiting factor for insects and may be of crucialimportance for ant communities (Andersen 1995; Cerdá et al. 1998a; Bestelmeyer2000; Azcárate et al. 2007; van Oudenhove et al. 2011) although dominant andsubordinate species may have similar foraging patterns in relation to temperature(Andersen 1992; LeBrun 2005).

Time in the sameway is considered a resource that can be partitioned on both daily andseasonal scales (Schoener 1974; Jacksić 1982). On a daily scale, partition is likely causedby interference competition among species whilst on a seasonal scale by differences in theactivity rhythms of consumers and resource dynamics (Albrecht and Gotelli 2001).

In the present study, M. wasmanni and M. minor did not differ in their ability todiscover food resources whilst significant differences occurred concerning the number

0

20

40

60

80

100

120

140

160

180

Mea

n nu

mbe

rofa

nts

on b

aits

1 2 3 4 5 6 7

Sampling steps

Fig. 1 Number of individuals of each ant species (white bars for M. wasmanni, grey bars for M. minor)obtained for each sampling steps averaging the number of foragers (mean ± SE) recorded on the set of visitedbaits across the different sampling days (from 1 to 3) and transects (from 1 to 3)

J Insect Behav

of baits that foragers of M. wasmanni was able to monopolize compared to those ofM. minor. Results support our expectation that colonies ofM. wasmanni are better ablethanM.minor to monopolize baits by virtue of their larger population and bigger workersize (Holway 1999; Solida et al. 2011a; Steiner et al. 2011). Although interference andexploitative competition often occurs among ants, with interference more frequentlydocumented, M. wasmanni and M. minor coexistence is not mainly supported by thistrade-off. In the studied area, probably saturated by long-lived colonies, competition forfood or nest sites could be more important than asymmetries in the adopted foragingstrategies in structuring the ant assemblage (see below; Hölldobler and Wilson 1990).

The distance between nests and baits had no effect on the number of foragers visitingbaits, no effect on the capacity of both the ant species to discover or monopolize baits.Fewell et al. (1992) noticed that as the consequence of an increased distance from the nest,fewer workers were recruited to a resource. Fellers (1987) on the contrary found nosignificant correlation, except on one occasion, between the distance covered by foragersto reach baits and the speed of food location by species. Lach (2005) similarly noticed thatthe foraging behavior of three nectar-thieving invasive ant species was not affected bydistance. The motivations expressed by Lach (2005) could similarly explain our findings:cost of foraging may not differ appreciably in the range of distances involved as also themortality risk due to predators could not represent a higher cost for longer distance.

The coexistence ofM. wasmanni and M. minor is not supported by a temporal nichepartitioning between species. In general, a temporal shift in resource utilization on a dailyscale rarely leads to resource partitioning or species coexistence (Schoener 1974, 1986;Jacksić 1982; Cerdá and Retana 1994; LeBrun 2005). Temperature and in part relativehumidity influenced in the same way the foraging activity ofM. wasmanni andM.minor.Probably, differences in the worker sizes of the two ant species are too small to guaranteea different susceptibility to environmental condition (Cerdá et al. 1998a; Solida et al.2011a).M.wasmanni andM. minorwere in fact relatively similar in terms of temperaturepreferences, and so, despite being significantly influenced by it, they are not sufficientlydifferent from each other to reveal any nonrandom structure. The coexistence betweenM. wasmanni andM. minor seems to be therefore principally supported by a spatial nichepartitioning in resource utilization. The trunk trail systems of colonies may represent themain strategy adopted by harvester ants to avoid competition (Hölldobler and Wilson1990; Acosta et al. 1995). Colonies of the two examined species could redirect trails intonon overlapping zones to reduce the frequency of worker encounters (Solida et al. 2010).When the benefits of access exclusively to a resource are low if compared with the cost offighting, space partitioning could represent an advantageous strategy to adopt to avoidcompetition (Hölldobler and Wilson 1990; Brown and Gordon 2000).

To conclude, partitioning of foraging resources seems to be involved only margin-ally in species coexistence. During most of the activity season in fact, resources do notseem to be a limiting factor for M. wasmanni and M. minor (Solida et al. 2011a). It isjust before winter hibernation, when environmental seed availability collapses, that theniche overlap between the two species must decrease to reduce the negative effects ofcompetition (Solida et al. 2011a).

Competition could especially affect in this way other important phases of the life-cycle of these two ant species. Probably, in a patchy environment characterized by anhigh colonies density and by an overdispersed nests distribution (Solida et al. 2010),competition could be especially intense during the first stage of colony foundation.

J Insect Behav

Likely, after this step colonies could be favoured by an highly productive environmentsuch those represented by the Mediterranean ecosystem.

Acknowledgments We are grateful to the ‘Segretariato Generale della Presidenza della Repubblica’, to theDirector of Castelporziano Estate for the hospitality in the guest-house and to the ‘Osservatorio CentroMultidisciplinare degli Ecosistemi Costieri Mediterranei’. We are also grateful to all the undergraduatestudents that were indispensable during the field work. We wish to thank Patricia de Angelis for reviewingthe text in English, and A. Babolat, M. Sciaratopa and ‘the Trout’ R.B. for inspiration. D.D. is grateful to Mr.Romeo C. for his statistic supervision. All research conducted complied with the current legislation in Italy.

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