The co-occurrence of 2 similar species depends on their ability to occupy different ecological niches. Here, we compared the consistency of different aspects of foraging behavior in 2 co- occurring harvester ant species (Messor ebeninus and Messor arenarius), under ﬁeld conditions. The 2 species are active concomitantly and display a similar diet, but M. arenarius features smaller colonies, larger workers on average, and a broader range of foraging strategies than M. ebeninus. We characterized the ﬂora in the 2 species’ natural habitat, and detected a nesting preference by M. arenarius for more open, vegetation-free microhabitats than those preferred by M. ebeninus. Next, we tested the food preference of foraging colonies by presenting 3 non-native seed types. Messor arenarius was more selective in its food choice. Colonies were then offered 1 type of seeds over 3 days in different spatial arrangements from the nest entrance (e.g., a seed plate close to the nest entrance, a seed plate blocked by an obstacle, or 3 plates placed at increasing distances from the nest entrance). While both species were consistent in their foraging behavior, expressed as seed collection, under different treatments over time, M. ebeninus was more consistent than M. arenarius. These differences between the species may be explained by their different colony size, worker size, and range of foraging strategies, among other factors. We suggest that the differ- ences in foraging, such as in food preference and behavioral consistency while foraging, could contribute to the co-occurrence of these 2 species in a similar habitat. Key words: behavioral consistency, coexistence mechanisms, foraging, harvester ants, plant–ant interactions. The coexistence of closely related species is intriguing, because large other Gerbillus allenbyi in the later part of the night (Kotler et al. overlaps in foraging niches enhance the risk of competitive exclusion 1993; Ziv et al. 1993). Spatial niche partitioning presents another and local extinction (Connell 1961; MacArthur and Levins 1967; mechanism of species coexistence. For example, in desert rodents, Amarasekare 2003). Co-occurring species must therefore not exceed large granivorous rodents with strong hind legs prefer open habitats a certain level of niche similarity in order to allow coexistence with sparse vegetation, while smaller rodents walking equally on all (Abrams 1983). Niche differentiation can take different forms, of 4 legs occur more under bushes (Kotler and Brown 1988). which temporal partitioning is a common one (Kronfeld-Schor and Coexisting species may differ too in their preferred diet, re- Dayan 2003). For instance, 2 gerbil species foraging in desert sand flected, for example, in different teeth length (Dayan et al. 1989, dunes for the same seeds are not active simultaneously: one species 1990). They can also differ in their diet breadth, being opportunistic Gerbillus pyramidum is active in the early night hours while the or selective in their prey choice (Bonesi and Macdonald 2004). V C The Author (2017). Published by Oxford University Press. 653 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 654 Current Zoology, 2018, Vol. 64, No. 5 Finally, some coexisting species differ in their trade-off balance co-occurring seed harvester ant species: Messor arenarius and point between exploration and exploitation: some are better at de- Messor ebeninus. Regarding microhabitat preference, another study tecting food, while others are better at exploiting it (Vance 1984; showed significant differences in microhabitat attributes of nesting Ziv et al. 1993; Avgar et al. 2008; Mehlhorn et al. 2015). sites between 2 different Messor ant species. Among other attributes, Ants are central-place foragers that retrieve food to their nests they differ in the presence of particular plant species (Solida et al. for consumption, to feed kin, or for storage. Two common questions 2011b). Generally, harvester ants and plants exist in a state of mu- of central-place foraging are those of how an organism that pos- tualism (Ho ¨ lldobler and Wilson 1990), and vegetation is about 5 sesses a nest/burrow should most effectively choose among food times denser close to harvester ant colonies than at adjacent, ant- patches and types, and how it should handle items of various sizes free, sites (Rissing 1986). Specifically, distinct separate preferences (Holder-Bailey and Polis 1987; Wetterer 1989). Ant species often for particular vegetation would contribute to the 2 species’ ability to coexist in the same habitat, and all of the above coexistence mechan- coexist. We expected that, due to its more arid climate distribution isms exist in ants. Partitioning in space is mostly related to the main- in general, M. arenarius would be found further away from tenance of territories, which depends on available food and the vegetation. presence of competing colonies (Solida et al. 2010, 2011a; Furthermore, we expected a difference in seed preference (diet Czechowski et al. 2013; Houadria et al. 2015). Co-occurring ants breadth) and in the consistency of foraging behavior that could also also demonstrate temporal-partitioning, with distinct seasonal and contribute to the 2 species’ coexistence. Although both species are daily peaks of foraging, enhancing coexistence (Andersen 1983; polymorphic, M. arenarius, featuring larger body size on average, Cerda ´ et al. 1998; Albrecht and Gotelli 2001). The exploration– but smaller colony size, and foraging either individually or in small exploitation trade-off (also known as the discovery-dominance groups, was expected to be more selective of specific seeds but more trade-off) is common in ant communities, based on the number of opportunistic in its preferred food patches. Messor ebeninus,a foragers: species with either more or fewer foragers specialize in ex- group forager, was expected to be more opportunistic than M. are- ploitation and exploration, respectively (Davidson 1998; Pierce- narius in collecting seeds but more selective in food patches. Duvet et al. 2011). Selecting specific high-quality patches would be more important for Models of optimal diet choice predict that animals should be M. ebeninus, which forages in large groups. Selecting high-quality more selective of specific food types in rich habitats but more select- seeds would be more important for the mostly individual foraging ive of specific patches in poorer habitats (MacArthur and Pianka M. arenarius, because of its lower tendency to recruit and because 1966; Kotler and Mitchell 1995). Other models predict that animals depletion of the patch might be more challenging for this species. should start by exploiting patches as specialists, but should then shift to a more opportunistic diet, and should do so faster, the longer they stay in a single patch. Patch residency time is expected to correl- Materials and Methods ate with the time required to reach the patch (Heller 1980; Brown We first characterized the habitat in which the 2 Messor species co- 1988; Barrette et al. 2010). Opportunistic and selective foragers are occur and examined whether they display distinct nesting prefer- characterized by different consistency levels in their diet choice. ences for vegetation cover. We then examined the seed preference of Such differences in consistency levels of foraging-related behaviors these 2 species, from among 3 non-local seed types. Finally, we are important for understanding how species survive, reproduce, examined inter-colony differences and intra-colony consistency in and coexist in their natural environment. Furthermore, behavioral foraging behavior under 3 different settings for 3 days, and tested consistency of an entire colony has been shown for different behav- for associations between colony behavior in each of the 3 different iors (e.g., Pinter-Wollman et al. 2012; Scharf et al. 2012). Such con- settings. sistency—the behavioral variation explained by inter-individual (or colony) differences (Bell et al. 2009)—is important due to several reasons, including its link to heritability levels (Boake 1989) and in Studied ants being a first step prior to the determination of personality (Bell et al. We used 2 co-occurring Messor species (subfamily: Myrmicinae; 2009). tribe: Pheidolini), M. arenarius and M. ebeninus, as our experimen- Three key traits of ants often affect foraging performance: (1) tal animals. Messor arenarius is heavier and larger than M. ebeninus worker body size is positively related to the maximal distance trav- (an average of 42 mg and 3.13 mm vs. 7 mg and 1.92 mm; body eled (termed “the size–distance relationship”; McIver and Loomis mass and head width, respectively; Segev et al. 2014), but both are 1993; Wright et al. 2000), probably because travel costs for larger polymorphic. Messor arenarius is distributed mainly in deserts of workers are lower. Larger workers also collect larger food items the Middle East and North Africa, while M. ebeninus occurs in (Davidson 1977a; Retana and Cerda ´ 1994; Kaspari 1996); (2) col- Europe, West Asia, and North Africa (Collingwood 1985; Kugler ony size is positively correlated with worker recruitment ability and 1988; Vonshak and Ionescu-Hirsh 2009). Messor arenarius is nu- territorial domination (Beckers et al. 1989; Gordon and Kulig merically dominant over other seed-harvester species, including M. 1996), and affects the foraging strategy applied by the colony, from ebeninus (according to findings from bait-trapping; Segev and Ziv individual to mass recruitment (Beckers et al. 1989; Dornhaus and 2012). Finally, M. ebeninus colonies comprise 100,000 individ- Powell 2010, but see Bengston and Dornhaus 2013); and (3) the for- uals, while M. arenarius colonies only comprise up to 5,000 individ- aging strategy can determine the location of each species on the ex- uals (Steinberger et al. 1991). Both species forage on plant seeds, ploration–exploitation trade-off scale. Generally, group-foraging other plant material, and occasionally also on dead invertebrates, species are more efficient in exploiting food patches, while individ- but the average weight per worker carried back to the nest by M. ual foragers are better at detecting new patches (Davidson 1977b; arenarius is greater than that carried by M. ebeninus (Steinberger Avgar et al. 2008). et al. 1992; Plowes et al. 2013; Segev et al. 2014). The 2 species col- We studied here the microhabitat preference, diet preference lect seeds of similar sizes and co-occur in the same habitats in Israel and breadth, and foraging behavior consistency of 2 congeneric (Steinberger et al. 1991; Segev 2010; this study). Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Saar et al. Coexistence of harvester ants 655 Furthermore, the 2 species differ in their common foraging strat- egy. Messor ebeninus is mostly a trunk-trail or group forager (Kunin 1994; Avgar et al. 2008), although group foragers are also able to forage individually (Bernstein 1975). Messor arenarius is more fre- quently an individual forager but can also be a group forager, with considerable differences among M. arenarius populations (mostly in- dividual forager: Warburg 1996, 2000; Avgar et al. 2008; mostly group forager: Wilby and Shachak 2000; mixed: Steinberger et al. 1991, 1992; Segev and Ziv 2012). Some harvester ants show a flex- ible foraging strategy based on seed density and distribution, which may explain this mixed evidence (Pol et al. 2015). Study site Tel Baruch coastal sand dunes (32.1283 N, 34.7867 E; 20 m above sea level) are adjacent to the Mediterranean coast in north-west Tel Aviv (250 m). The area is about 1.5 0.5 km (length width), and receives 550 mm mean annual rainfall, of which 80% occurs between November and February. Mean temperatures in August and January are 25.4 C and 12.4 C, respectively (BioGIS 2016). The dunes are roughly divided into stabilized (southern part) and semi-stabilized areas (northern part). The area is surrounded by city neighborhoods, and is frequently disturbed by human activity, similar to a city park, although the flora is primarily wild and the area is not irrigated. Figure 1. One of the 4 grids created at the study site, presenting the stations Plant cover and sampling established (diamonds) as base for plant sampling and plant cover. Messor We characterized the flora of Tel Baruch by sampling the plants and arenarius (triangles) and M. ebeninus (squares) co-occur and overlap in their habitat. determining plant cover (Abramsky et al. 1985). Characterizing the habitat is important as a background for field studies in general, and for the study of seed-harvesting ants in particular, as they rely on (Steinberger et al. 1992). During both experiments, all colonies were vegetation for foraging. Four grids were established, each marked circumscribed by a tracking trail, to trace and exclude foraging by with 40 stations in 4 rows, at 5 m intervals between stations and other animals, such as crows and beetles (see the Supplementary rows (Figure 1). Plant cover and sampling were conducted in winter Material for a detailed explanation on the construction of the tracking (February–March) and spring (May) of 2 consecutive years, 2014– trail). Seeds (2 g) were weighed in the laboratory before and after the 2015. Grids were divided between the stabilized and semi-stabilized experiment, in order to calculate foraging efficiency (mass collected sand dunes. For each grid, 12 stations were randomly selected. Plant within a given time period). Air and ground temperatures and relative cover was determined using the line-intercept method (Canfield humidity were measured at the beginning and end of each work day, 1941) and was conducted as follows: from each of the 12 chosen sta- using Sh-101 Digital Thermo-Hygrometer, by ISOLAB (see tions, we deployed a 10 m measuring tape in a random direction. Supplementary Table S1 in the Supplementary Material). No special Plant species and length cover (cm) of both perennial and annual permits were required for any of the experiments. plants under the measuring tape were documented. Plant sampling was conducted as follows: the first, second, and third perennial plant Experiment 1: seed preference closest to the focal stations were documented (plant species, length, We examined the preference of the 2 ant species for 3 seed types, width, and distance from the station). The nearest plant neighbor relatively similar in size, provided in 2 different spatial arrangements (Clark and Evans 1954) to the first closest perennial plant was also (treatments), by documenting the amount collected of each seed documented, resulting in 4 perennial individual plants sampled per type, with all 3 being offered simultaneously. We used non-native station. Finally, we documented the nearest ant colony to the station seeds: millet, sesame, and rice (see Supplementary Material, and the nearest perennial plant to the ant colony. Supplementary Table S2, for their nutritional value, and Supplementary Figure S1 for a photo showing both species foraging Field experiments on millet seeds). Non-native seeds enable standardization of the nu- All experiments were performed between March and June of 2014– tritional value of each seed type and ensure year-round experimental 2015. The seed preference test for M. ebeninus, as the only exception, access to them (Davidson 1978; Avgar et al. 2008). Twelve and 15 was performed in November 2015. Although there is some evidence colonies of M. arenarius and M. ebeninus, respectively, were tested. of seasonal effects on natural seed preferences, depending on their nat- Five-to-eight colonies received one treatment per day, in a random- ural occurrence (Crist and MacMahon 1992), we did not expect a sea- ized order of treatments, over 2 weeks (each colony was tested twice sonal difference to exist in non-natural seed preference, as such seeds with a 24-h interval). The tests were conducted for 2 h for M. are- do not occur in the ants’ natural habitat. The 2 field experiments were narius and 40 min for M. ebeninus. The experiment was shorter for performed during noon hours, when typical high activity can be M. ebeninus, because of its faster depletion of the food patch. observed for the 2 species. Nevertheless, we relied on a previous re- Individual foragers, or weak group foragers, like M. arenarius, typ- port that shows the 2 species are active simultaneously, under similar ically take longer than strict group foragers to search out and collect temperatures, and show the same seasonal activity changes seeds (Davidson 1977b). We presented the ants with the 3 choices of Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 656 Current Zoology, 2018, Vol. 64, No. 5 Figure 2. The spatial arrangements of the seed plates in the 2 ﬁeld experiments. Seed preference: (A) clustered patches, (B) scattered patches. Consistency of for- aging behavior: (C) 30 cm, (D) obstacle, and (E) distances (30, 60, and 90 cm). Nest entrance is visible in C–E (upper part of the photo). An additional empty plate presents the nest ID number. seeds (millet, sesame, and rice) in 9-cm Petri dishes, similar to previ- “obstacle”: a plate with millet seeds was placed on the tracking trail, ous studies on harvester ants (Davidson 1977b; Kunin 1994; Avgar 30 cm from the entrance to the nest. Next, a 16 8 cm white plastic et al. 2008). We employed the 2 following treatments, one treatment obstacle was placed between nest entrance and plate, 15 cm from per day: (1) “Clustered patches”: 3 plates were placed horizontally, the entrance. The purpose was to increase the energetic cost of on the tracking trail, 30 cm from the entrance to the nest and 3 cm searching by increasing the distance the workers had to cross (Figure between plates (Figure 2A). (2) “Scattered patches”: 3 plates were 2D); and (3) “distances”: 3 plates with millet seeds were each placed placed horizontally, on the tracking trail, 30 cm from the entrance on the tracking trail, 30, 60, and 90 cm from the entrance to the nest to the nest and 30 cm between plates (Figure 2B). All treatments (Figure 2E). For comparison with the previous 2 treatments, we ap- took place on one tracking trail that was cleared and renewed proached this treatment in terms of number of plates on site and between treatments. thus divided it into 3 sub-treatments. In total, we applied 5 treat- ments in this particular experiment. All treatments took place on one tracking trail that was cleared and renewed between treatments. Experiment 2: consistency of foraging behavior The aim here was to determine whether colonies of the 2 ant species exhibit consistency in foraging behavior, expressed as the amount of Statistical analyses collected seeds, over time and in different foraging contexts (treat- We analyzed plant cover and plant sampling separately. ments). We used millet seeds for this experiment, as they had been found to be most preferred by M. arenarius, while M. ebeninus had Plant cover shown no preference (see the “Results” section). Twenty-eight and We used a repeated-measures ANOVA to analyze plant cover: per- 29 colonies of M. arenarius and M. ebeninus, respectively, were ennial and annual species (length in centimeter, up to 1,000 cm) tested for 2 months. Four-to-eight colonies were tested under 3 dif- were used as response variables (measured simultaneously using the ferent treatments per day for 2 consecutive days (days 1 and 2), fol- measuring tape), with year and season as explanatory variables. lowed by 1 day of rest and then another day of testing (day 3). All Perennial and annual covers were square-root transformed due to treatments were conducted for 50 min for M. arenarius and 20 min their deviation from normal distribution. for M. ebeninus, with an interval of 20 min between treatments. As said, the experiment was shorter for M. ebeninus because of its faster depletion of the food patch. Treatments were given in a ran- Plant sampling dom order: (1) “30 cm”: a plate with millet seeds was placed on the We analyzed the 3 most common perennial plant species out of all tracking trail, 30 cm from the entrance to the nest (Figure 2C); (2) plant species documented, with each of the 3 comprising more than Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Saar et al. Coexistence of harvester ants 657 the explanatory variable and the preference indices of the 2 treat- ments (clustered vs. scattered patches) as response variables. (3) Seed preference consistency: Are colonies within each species con- sistent in their preference between treatments? We used a Pearson correlation to test for a link between the preference indices of the 2 treatments. A separate correlation analysis was conducted for each species. If colonies are consistent in their degree of selectivity, we would expect a positive correlation in their preference index across the 2 treatments. Experiment 2: consistency of foraging behavior We analyzed behavioral consistency of all treatments between days. For this purpose, we used intra-class correlations (hereafter ICC): (1) to test for correlations between the quantity of collected seeds (log -transformed) per treatment and separately for each species, across all days (1, 2, and 3), in order to test for general consistency level; and (2) consistency between the first and last days (1 and 3), in order to test whether consistency declines faster in one species than the other. High ICC values indicate high behavioral consist- ency. All data were analyzed using Systat v. 13 and Statistica v. 7. Results Plant cover and sampling analysis Plant cover and sampling were conducted in 2 consecutive years (2014–2015), during the seasons with highest vegetation (winter and spring) each year. Sixteen perennial species were identified (first, nearest neighbor to first, second and third closest to focal sta- Figure 3. (A) Perennial and annual plant cover (of 1,000 cm) at the study site in spring and winter of 2014 and 2015 (mean6 1 SE). (B) The distance (cm) of tions; N ¼ 758). A total of 13 annual plants were identified to spe- M. ebeninus and M. arenarius colonies to the nearest perennial plant cies level, 3 to genus level, and 1 to family level. Eighteen percent of (mean6 1 SE). annual plants were unidentified and classified as “non-perennial plants”. The 3 most common perennial species were Sporobolus 10% of the total vegetation. We used 2 v tests to compare the pungens (28.3% of the total perennial species), Centaurea procur- abundance of the 3 plant species between seasons and years. rens (20.3%), and Echium angustifolium (12.3%). See Supplementary Table S3 in the Supplementary Material for a list of typical perennial species identified. Ant colony-perennial plant distance Colonies belonging to 5 ant species were identified by direct ob- We compared the distance of the closest perennial plant to each ant servations in all seasons and grids: M. arenarius (33.8% of total ant colony using 3-way ANOVA, with ant species, season, and year as colonies), Cataglyphis niger (33.1%), M. ebeninus (25.6%), the explanatory variables and distance as the response variable. In Cataglyphis livida, and Camponotus fellah (the latter 2 comprising this analysis all null values were removed (if a colony was not found less than 8%; total N¼ 160 colonies). up to a radius of 5 m from the sampled station). Distance to the per- Plant cover: The 3-way interaction plant type year season ennial plant closest to the ant colony was log -transformed. had a significant effect on plant cover (F ¼ 8.85, P ¼ 0.003). 1,187 Perennial cover was higher and lower in spring and winter, respect- Experiment 1: seed preference ively, in both years. The annual cover showed a different pattern, We asked 3 questions: (1) Seed preference: Do the 2 studied species with similar levels overall, except for spring 2014, which was much reveal a preference for specific seeds and does this preference differ lower (Figure 3A). The 2-way interactions were also both significant between the species? We performed a repeated-measures ANOVA (plant type year: F ¼ 10.83, P ¼ 0.001; plant type season: 1,187 (seed types were presented to colonies simultaneously, for choice) F ¼ 57.54, P< 0.001). Lastly, plant type and year were signifi- 1,187 for each treatment separately (clustered and scattered patches), and cant, as main effects (F ¼ 32.99, P< 0.001; F ¼ 17.21, 1,187 1,187 used species as an explanatory variable and the proportions of col- P< 0.001, respectively), but season was not (F ¼ 0.23, 1,187 lected seeds as response variables. Proportions of seeds collected P ¼ 0.63). Based on the Israeli meteorological site (http://www.ims. were arcsine-transformed. (2) Difference between spatial treatments: gov.il), precipitation in the rainy season of 2015 was higher than Is there an effect of treatment (clustered vs. scattered patches) on average (106%), whereas in 2014 it was lower than average (62%), this preference? We calculated a preference index (Shannon– which may explain the lower annual plant cover in spring 2014 Wiener’s index) of the amount collected of each seed type. Low val- (Figure 3A). ues indicate a strong preference for specific seeds (selectivity) while Plant sampling: There was no difference among the 3 most abun- high values indicate a weak preference (opportunism); this prefer- dant perennial plant species between 2014 and 2015 (v ¼ 0.32, ence index was used also in the seed preference consistency analysis df ¼ 2, P ¼ 0.85). However, there was a marginally non-significant (see below). We used repeated-measures ANOVA, with species as difference between seasons: in winter, the abundance of S. pungens Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 658 Current Zoology, 2018, Vol. 64, No. 5 arenarius being more selective (Figure 4B). The 2-way interaction (treatment species) was not significant and was removed (F ¼ 0.01, P ¼ 0.92). 1,24 Seed preference consistency: Using the preference indices, M. ebeninus was found to be consistent between treatments (r ¼ 0.627, P ¼ 0.017) while M. arenarius was not (r¼0.481, P¼ 0.134). See Supplementary Figure S3 in the Supplementary Material for a correl- ation graph, comparing both species. In conclusion, M. arenarius was more selective in seed preference than M. ebeninus and preferred millet seeds. However, M. ebeninus was more consistent between treatments than M. arenarius. Experiment 2: consistency of foraging behavior Regarding the foraging pattern by seeds collected in each treatment, colonies of M. ebeninus were consistent over a longer time period than M. arenarius, with the former being significantly consistent in more treatments according to the ICC. Specifically, comparing days 1–3 (a 4-day interval), M. arenarius was never consistent, while M. ebeninus showed consistency in 2 of the 5 treatments. Comparing all days (1–2–3 days), M. ebeninus was consistent in all 5 treatments but M. arenarius in only 3 of the 5 treatments (Table 1). This sug- gests that M. ebeninus collected similar amounts of seeds between days and across treatments, and was thus more consistent in its for- aging behavior than M. arenarius. Discussion In order for co-occurring species to coexist, they need to differ in Figure 4. (A) The proportions of seeds collected by M. ebeninus and M. are- narius when offered millet, sesame, and rice (treatment 1; clustered patches). some axes of their niche (Kotler and Brown 1988). We examined (B) Seed opportunism of both ant species. Lower and higher values indicate several aspects of foraging behavior and vegetation preference of 2 higher selectivity and higher opportunism, respectively (mean6 1 SE). congeneric and co-occurring harvester ant species. First, when tested for consistency in patch exploitation under different foraging con- was proportionally higher than in spring (v ¼ 5.45, df ¼ 2, texts, M. ebeninus was consistent for longer and under more treat- P ¼ 0.066; Supplementary Table S4 in the Supplementary Material). ments than M. arenarius. Furthermore, M. ebeninus showed Ant colony-perennial plant distance: Distance of the ant colony consistency between treatments in seed preference: colonies that to the nearest perennial plant differed according to the nearest were selective in one situation were also selective in others, and vice Messor ant colony (plants were found closer to M. ebeninus than to versa for non-selective colonies. However, M. arenarius was more M. arenarius: F ¼ 4.10, P ¼ 0.047; Figure 3B), while both year 1,67 selective than M. ebeninus in its preference for a specific seed type. and season were not significant (F ¼ 0.23, P ¼ 0.63; F ¼ 0.08, 1,67 1,67 In short, M. arenarius was selective in regard to the food type chosen P ¼ 0.77, respectively). The 3-way interaction and all 2-way inter- and M. ebeninus was selective in regard to the patch in which they actions were not significant (P> 0.07 for all) and were removed. chose to forage. Finally, M. ebeninus colonies were located closer to vegetation than those of M. arenarius. We found some segregation in space in these species, which is a Experiment 1: seed preference common mechanism of species coexistence. Colonies of M. ebeninus Seed preference: For treatment 1 (clustered patches), seed preference position themselves closer to perennial plants than M. arenarius, al- differed between the species, indicated by the significant spe- though their foraging territories also overlap (Figure 1). This segre- cies seed interaction (F ¼ 7.09, P ¼ 0.002; Figure 4A). While gation, although at a fine scale, is perhaps due to M. arenarius 2,50 M. arenarius strongly preferred millet, M. ebeninus collected similar originating from desert habitats with sparse vegetation, compared proportions of the 3 seed types. Seed type as a main effect was also with the more Mediterranean distribution of M. ebeninus. In a com- significant, with a general preference for millet (F ¼ 4.29, parative example, a larger desert gerbil species prefers open habitats 2,50 P ¼ 0.019), but the 2 species did not differ in the amount of collected while a smaller species is found in bushier ones, perhaps due to dif- seeds (F ¼ 1.68, P ¼ 0.21). For treatment 2 (scattered patches), ferent levels of predation risk or to different effects of seed distribu- 1,25 the results were similar, with a significant species seed interaction tion by wind on the 2 gerbil species (Brown et al. 1988; Ben-Natan (F ¼ 17.08, P< 0.001), significant seed type as a main effect et al. 2004). While preference of the larger ant species for the open 2,50 (F ¼ 17.51, P< 0.001) and a non-significant difference between habitat and of the smaller one for the bushier habitat seems to be 2,50 the 2 species as a main effect (F ¼ 0.53, P¼ 0.47); see similar to that of the desert gerbils, the mechanism behind this re- 1,25 Supplementary Figure S2 in the Supplementary Material. mains to be tested in the Messor species. Note that the between- Difference between spatial treatments: The 2 treatments were species difference in the mean distance of colonies to perennial compared using the calculated preference index. There was no dif- plants, although significant, is about 20 cm. The importance of such ference between the 2 treatments (treatment: F ¼ 0.89, P ¼ 0.35) a short distance for the colonies in their natural habitat remains to 1,24 but only between species (F ¼ 19.96, P< 0.001), with M. be explored. 1,24 Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 Saar et al. Coexistence of harvester ants 659 Table 1. Consistency of seed collection, under 5 treatments, was measured using intra-class correlation (ICC) through days 1–2–3 and between days 1 and 3, for M. ebeninus (A) and M. arenarius (B) Treatments/days 1–2–3 1–3 ICC 95% CI P ICC 95% CI P (A) M. ebeninus 30 cm 0.594 0.367–0.779 <0.001 0.606 0.276–0.808 0.001 Obstacle 0.307 0.066–0.561 0.005 0.286 0.107–0.601 0.074 30 distance 0.566 0.342–0.754 <0.001 0.425 0.053–0.694 0.014 60 distance 0.478 0.241–0.694 <0.001 0.210 0.186–0.547 0.147 90 distance 0.319 0.078–0.572 0.004 0.238 0.157–0.567 0.116 (B) M. arenarius 30 cm 0.460 0.211–0.689 <0.001 0.184 0.211–0.528 0.178 Obstacle 0.429 0.178–0.666 <0.001 0.199 0.197–0.539 0.160 30 distance 0.282 0.039–0.546 0.011 0.197 0.199–0.538 0.162 60 distance 0.016 0.208–0.259 0.536 0.060 0.336–0.438 0.385 90 distance 0.141 0.299–0.119 0.873 0.024 0.424–0.384 0.544 Note: Signiﬁcant results appear in bold. Temperature affects foraging performance and preferences of There are several other possible explanations for the higher ants (Byron et al. 1980; Traniello et al. 1984). Different thermal per- patch exploitation consistency of M. ebeninus. First, higher consist- formance curves of 2 co-occurring species may enhance resource ency could be linked to colony size, with the larger number of for- partitioning and improve the likelihood of their coexistence (Persson agers increasing colony consistency through specializing on specific 1986). The studied Messor species forage mainly simultaneously, food patches. Large colony size often enhances worker specializa- under similar temperatures (Steinberger et al. 1992). Therefore, tion and probably increases inter-colony differences (Holbrook et al. mechanisms underlying competition between these 2 studied species 2011). A larger colony could also mean more intra-colony inter- unrelated to temperature should be further studied. actions, leading to more stable colony behavior and larger inter- Another putative coexistence mechanism is reflected in the op- colony differences. Second, M. arenarius is more diverse in its forag- portunism–selectivity axis, which differs between the 2 Messor spe- ing strategies than M. ebeninus, perhaps contributing to its lower cies in relation to diet and patch. Messor arenarius was more diet consistency in patch exploitation. selective than M. ebeninus. The former species may have preferred Animals are expected to be less diet-selective when inter-patch the millet seeds because they contain a better trade-off between distances increase, because the distance to or the likelihood of de- carbohydrates and proteins than rice (81% and 14% in millet and tecting the most preferred food type diminishes (Levey et al. 1984; 91% and 8% in rice, respectively; Supplementary Table S3). Stephens and Krebs 1986, ch. 2; Dumont et al. 2002). Our present Differences in diet breadth are a suggested mechanism of species co- findings, however, do not support this expectation, because the existence also in other multi-species systems, such as woodrats and inter-patch distance had no effect on seed selectivity of both Messor mink (Dial 1988; Bonesi and Macdonald 2004). That said, it re- species. Moreover, in a similar seed preference test for M. ebeninus, mains to be determined whether similar differences between the 2 this species showed no preference for a specific seed type, even when ant species exist concerning the natural seeds available in their a density factor was considered (rare vs. common; Kunin 1994). shared habitat. This is not to say that harvester ant selectivity is entirely unaffected Messor arenarius, the larger species, which forages more indi- by foraging distance: harvester ants sometimes become more select- vidually than M. ebeninus, was selective in its seed preference but ive with foraging distance [see Detrain et al. (2000) and references opportunistic in its patch choice (i.e., less consistent between days). therein for increased selectivity or no change]. However, although Although there is some evidence that travel costs are relatively low foraging distances may play a role in the foraging patterns of har- in general, for harvester ants (Baroni-Urbani and Nielsen 1990; vester ants, we have shown here that the species-specific differences Plowes et al. 2013), it is plausible that the energetic cost of travel for in foraging strategies can be detected even in short foraging bouts. the larger ant species is lower. This result corresponds to studies Finally, it has been suggested for harvester ants that travel distance showing that larger workers travel longer distances from the nest and energetic cost are not the main consideration of foraging work- than smaller ones (e.g., McIver and Loomis 1993). Messor arenarius ers, but rather the temporal cost (Fewell 1988; Weier and Feener is more selective perhaps also because selecting specific seeds has a 1995). higher temporal cost for the group forager than for the more indi- In summary, different mechanisms have been suggested to ex- vidually foraging ant. Messor ebeninus was more consistent in its plain how 2 similar harvester ant species coexist, such as diet parti- patch exploitation, probably due to its stronger group-oriented for- tioning in respect to seed type and size, or different foraging aging strategy that, combined with its large colony size, enabled the strategies (Davidson 1977a; Cerda ´ and Retana 1994; Solida et al. recruitment of many workers to thoroughly exploit and detect a 2011a). In our case, we suggest that differences in colony size, patch. Because patches differ more strongly in their value for worker size, and the broader range of foraging strategies have led to M. ebeninus, patch exploitation was more consistent for this species. different microhabitat preferences and especially to different levels Generally, larger species discover food patches faster than smaller of selectivity regarding seed types and patches. In other words, coex- ones but are less efficient while foraging (Brown 1989), which is istence may be supported by a difference in the level of behavioral probably also the case here. consistency of the 2 species. The findings from such studies of Downloaded from https://academic.oup.com/cz/article-abstract/64/5/653/4139747 by Ed 'DeepDyve' Gillespie user on 18 October 2018 660 Current Zoology, 2018, Vol. 64, No. 5 Brown JS, Kotler BP, Smith RJ, Wirtz WO, 1988. The effects of owl predation behavioral consistency can contribute to improving our understand- on the foraging behavior of heteromyid rodents. 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