Spatial and temporal variations in the activity patterns ...

4 (3) : 269-278 (1997)

Spatial and temporal variations in the activity patterns of Mediterranean ant communities1 Sebastià CROS, Xim CERDÁ2, Javier RETANA3, Unidad de Ecología y CREAF, Facultad de Ciencias, Universidad Autónoma de Barcelona, E-08193 Bellaterra (Barcelona), Spain, e-mail: [email protected] Abstract: We investigated the temporal and spatial separation of the activity rhythms of ants in three Mediterranean habitats. The different abilities of ant species to tolerate thermal stress influenced the time of day and year during which they were active. Activity of ants followed environmental fluctuations both seasonally and daily. Two groups of ant species could be distinguished in the communities studied: i) heat-tolerant species that were diurnal and changed little in daily activity rhythms throughout the year; ii) heat-intolerant species that shifted activity rhythms from diurnal to crepuscular-nocturnal at higher temperatures, and had peak activity at temperatures lower than 30°C. The different environmental conditions of each site affected the activity of different ant species and, therefore, community organization. In the forest areas, canopy cover created a heterogeneous environment of sunny and shaded areas throughout the day. Heat-intolerant species benefited from this spatial heterogeneity by lengthening their period of activity on hot days in areas covered by vegetation. This decreased the abundance of heat-tolerant species. Instead, in dry and open environments such as grasslands, the lack of trees caused the daily range of temperature to be sufficient to meet the requirements both of heat-adapted and cold-adapted species. This results in an increased diversity and a reduction in the dominance of heat-intolerant species. Keywords: ant, activity rhythm, temporal partitioning, environmental factors, temperature. Résumé: Nous avons étudié les divisions spatiales et temporelles des périodes actives de fourmis dans trois habitats méditerrannéens. Selon les espèces, la tolérance au changement thermique influence la période de la journée et de l’année où les fourmis sont actives. L’activité des foumis varie selon les changements environnementaux tant saisonniers que quotidiens. Les fourmis des communautés à l’étude forment deux groupes : i) les espèces tolérant la chaleur qui sont diurnes et dont les périodes actives changent peu en cours d’année. ii) les espèces ne tolérant pas la chaleur dont la période active passe de diurne à crépusculaire-nocturne lorsque la température augmente ; la période active la plus intense pour les fourmis de ce groupe se situe à des températures sous les 30 °C. Les différentes conditions environnementales de chaque site ont eu une incidence sur l’activité de différentes espèces de fourmis et, par conséquent, sur l’organisation au sein de la communauté. Dans les régions forestières, tout au long de la journée, le couvert forestier crée un environnement hétérogène constitué de secteurs ensoleillés et ombragés. Les espèces ne tolérant pas la chaleur profitaient de cette hétérogénéité spatiale puisqu’elles tiraient partie des secteurs sous couvert végétal pour prolonger leur période active. Cela a contribué à diminuer le nombre d’espèces tolérant la chaleur. Par ailleurs, dans les environnements secs et dégagés comme les prairies, la variation quotidienne de la température était suffisante pour satisfaire à la fois les espèces adaptées au chaud et celles adaptées au froid et ce, en raison du manque d’arbres. Cela a eu pour effet d’accroître la diversité et de réduire la dominance des espèces ne tolérant pas la chaleur. Mots-clés: fourmi, période active, division temporelle, facteurs environnementaux, température.

Introduction Organization of ant communities is affected by several factors, including interspecific competition, predation, physical factors and random change (Fellers, 1989). Food can be partitioned among species by microhabitat of the foraged area, prey size or type of food eaten (Briese & Macauley, 1981; Torres, 1984; Fellers, 1987). When these aspects of foraging are similar, species may reduce or avoid interference interactions by temporal separation (Marsh, 1988; Fellers, 1989). Daily and seasonal patterns can be affected by biotic factors, such as food availability (Bernstein, 1979; Briese & Macauley, 1980; Marsh, 1985; Steinberger, Leschner & Shmida, 1992), interspecific competition (Gallé, 1986; Fellers, 1987; Savolainen & Vepsalainen, 1988; 1989; Andersen, 1992) or presence of brood in the nests (Bernstein, 1979). Nevertheless, temporal shifts in 1Rec. 1996-07-12; acc. 1997-01-20. 2Additional

address: Unidad de Ecología Evolutiva, Estación Biológica de Doñana, CSIC, Apdo. 1056, E-41080 Sevilla, Spain. 3Author for correspondence.

activity patterns are best interpreted as responses to abiotic factors of the physical environment, mainly temperature (Andersen, 1992; Gordon, 1983; Marsh, 1985; 1988; Porter & Tschinkel, 1987), but also moisture (Whitford & Ettershank, 1975; Greenaway, 1981; Steinberger, Leschner & Shmida, 1992), radiation (Sheata & Kaschef, 1971; Retana et al., 1988) and wind (Briese & Macauley, 1980; Marsh, 1988). Among these, temperature is considered to be the primary control of colony activity and metabolism (Porter & Tschinkel, 1993). Temperature has a strong and direct influence on foraging activity, regardless of the temporal scale used, due to its direct effect on oxygen consumption, water loss and transport costs of the foraging ants (Mackay & Sassaman, 1984; Nielsen, 1986; Lighton & Bartholomew, 1988; Lighton & Feener, 1989; Lighton, Weier & Feener, 1993). Thermal conditions are of special importance because the activity of small ectothermic ants will be restricted to those periods when surface conditions permit physiologically tolerable body temperatures (Marsh, 1988).

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Temperature stress also influences non-desert ants (Sanders, 1972; Cokendolpher & Francke, 1985; Porter & Tschinkel, 1987; Cokendolpher & Phillips, 1990), but it is of particular relevance in arid areas (Marsh, 1988; CloudsleyThompson, 1989; Heatwole & Harrington, 1989; De Bie & Hewitt, 1990), where microclimatic factors at the surface are subject to very large fluctuations. In these areas, spatial and temporal heterogeneity in environmental conditions can greatly affect the foraging patterns of animals. The spectrum of environmental factors encountered by each species will depend, in part, on when and where it is active. On a temporal basis, the daily and seasonal patterns of temperature variation are such that adjustment of diel or annual activity patterns can greatly influence the thermal levels to which animals are exposed (Heatwole & Harrington, 1989). On a spatial basis, temperature conditions of many habitats are far from homogeneous, especially in forests and woodlands, where insolation is patchy and highly variable. Differences in canopy cover give rise to different microclimates and create heterogeneous environments, and such variations are probably important in explaining differences in foraging activity among and within habitats (Porter & Tschinkel, 1987). Some species benefit from this environmental heterogeneity and the attenuation of environmental conditions in certain microhabitats. They lengthen their periods of activity to times of the day in which temperatures reach critical values in more open sites (Gallé, 1977; Capinera & Roltsch, 1981; O'Neill & Kemp, 1990; Lopez, Serrano & Acosta, 1992). This temporal and spatial heterogeneity may affect competitive relationships when the different species are favoured by different sorts of environmental conditions that fluctuate over time and space (Chesson & Rosenzweig, 1991). The present study was carried out in three Mediterranean habitats situated close to one another, but clearly distinguished by their different degrees of canopy cover. We have studied the activity of the entire community of each area in order to accurately assess the extent of temporal separation on a daily and seasonal basis and to determine its relationship to physical factors, mainly temperature. The main objectives have been to analyze: i) how differential abilities of ant species to tolerate temperature may influence the time of day and year at which they are active, and ii) how some of the different environmental conditions of each site affect

activity patterns of the different ant species and, therefore, community organization.

Methods This study was carried out in Canet de Mar (Barcelona, northeastern Spain) (41° 25' N, 2° 7' E) at 50 m above sea level, 750 m away from the coastline. The climate is of Mediterranean type. Mean temperatures are usually mild in winter and highest in the summer months. Rainfall is concentrated in the winter (November through April), and July and August are the driest months. Three different habitats separated by 150 m were studied: i) a savanna-like grassland, located on a south-southeast slope with canopy cover (scattered Pinus pinea pines) being less than 3%, and the main understory plant species being Hyparrhenia hirta and, to a lesser extent, Foeniculum vulgare and Brachypodium retusum; ii) an open holm oak forest located on a northwestwest slope, with a mixed overstory of holm oaks (Quercus ilex), pines (P. pinea) and carobs (Ceratonia siliqua), covering 39% of ground surface; the understory vegetation covered 23% and consisted of Q. ilex, Rubus ulmifolius and Cistus albidus; iii) a Pinus pinea forest, located on a east-southeast slope, with a canopy cover of approximately 62%, and understory vegetation of scattered Rhamnus alaternus and R. ulmifolius representing less than 10%. A total of 13, 15 and 15 ant species were recorded in the grassland, the holm oak forest and the pine forest, respectively. From those, the ten most abundant species were considered in this study and are listed in Table I. Foraging activity patterns of ant species were recorded one to three days per month throughout the activity season (from March to November). The presence of ants at baits every hour and every day were used as a way to measure daily and seasonal activity rhythms of each species in each area. Although baits represent an exceptionally rich food source which may, somehow, modify the normal activity of ants (Whitford, Deprée & Johnson, 1980), daily activity rhythms measured at the nest entry of various ant species of the grassland (Cerdá et al., 1988; 1989; Cerdá & Retana, 1994; Retana et al., 1988) mostly overlapped with those obtained at baits. Therefore, we generalized the use of data from baits to establish daily rhythms of all ant species. In

TABLE I. Characteristics of the activity rhythms of the main ant species studied. Species have been ordered according to their pattern of daily activity on the ground. Daily activity rhythms: (D) diurnal, (DC) diurnal in spring and continuous or with a midday drop in summer, (C) continuous throughout the day, (CN) continuous in spring and nocturnal in summer, (N) nocturnal, (-) only rarely found at plants. For each species, significance of differences of mean daily activity overlap between spring and summer was determined with the Wilcoxon matched-pair test, and indicated as: **p < 0.01; *p < 0.05; ns, not significant Species Cataglyphis cursor Camponotus foreli Aphaenogaster senilis Messor bouvieri Messor capitatus Camponotus cruentatus Tapinoma nigerrimum Pheidole pallidula Tetramorium semilaeve Camponotus sylvaticus 270

Daily activity rhythm Ground Vegetation D D D D D D DC DC C CN C CN C CN N C

Daily activity overlap (mean ± SE) Spring Summer ** 0.43 ± 0.06 0.15 ± 0.05 * 0.49 ± 0.06 0.37 ± 0.05 0.43 ± 0.04 ns 0.33 ± 0.05 0.44 ± 0.07 ns 0.44 ± 0.06 0.48 ± 0.07 ns 0.59 ± 0.10 0.52 ± 0.05 ns 0.56 ± 0.07 0.56 ± 0.04 ns 0.61 ± 0.10 0.48 ± 0.07 ns 0.58 ± 0.10 0.49 ± 0.06 ns 0.56 ± 0.11 * 0.25 ± 0.08 0.41 ± 0.10

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Month of maximum foraging activity July August June September October July June September June August

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Seasonal activity overlap (mean ± SE) 0.67 ± 0.05 0.69 ± 0.04 0.65 ± 0.04 0.64 ± 0.04 0.60 ± 0.05 0.64 ± 0.05 0.57 ± 0.04 0.60 ± 0.05 0.67 ± 0.03 0.63 ± 0.05

ÉCOSCIENCE, VOL. 4 (3), 1997

each area, five series of different food baits (cheese, ham, bacon, sausage, biscuit and honey) were placed on white index cards (10 cm × 10 cm) resting directly on the ground, and were replenished as necessary. These baits could not be transported to the nest by workers. They were put out for a total of 21 sampling days: 12 sampling days of 24 hours each from March to November in 1985 in the grassland, and 9 sampling days of 14 hours each from April to November in 1990 in the three study areas. Each hour, the number of ants of each species feeding at each bait was recorded. The overall number of workers counted each hour at all baits was used as a measurement of hourly activity of this species. Seasonal activity of each species was estimated from the overall number of workers counted at baits every sampling day throughout the year. Diversity at baits in each habitat was calculated using the Shannon index, H = -∑(Pi • ln P i), where P i is the proportion of baits occupied by species i. Pairwise species overlap of daily and seasonal activity was calculated as a proportional similarity index (Schoener, 1968): PS = 1-0.5(∑|pix-piy|), where pix and piy are the respective percentages of total daily (or seasonal) activity in the period i of species x and species y, respectively. Multiple comparisons of activity patterns between different seasons, different habitats or different species were analyzed using χ 2 tests. The grouping of ant species based on their activity rhythms was carried out with the CLUSTER program of the R package (Legendre & Vaudor, 1991). Two separated UPGMA (unweighted-pair groups method) analyses were performed with the spring and summer matrices of pairwise overlap values. Activity rhythms of ants at overstory and understory vegetation were determined in the three habitats throughout the activity season. Several trees (four pines in the pine forest; three pines, six holm oaks and one carob tree in the holm oak forest; and three pines in the grassland) were monitored by counting the number of ants rising or descending across a marked point at the stem (1.6 m height) during three minutes every two hours. In the understory, several individuals of the most important shrubs and entomophilous plants were marked on each sampling day. Every two hours, the number of ants of each species that were either licking nectar of flowers or collecting honeydew of aphids were counted. Together with the hourly measurements of activity at baits and vegetation, the following environmental factors were recorded: ground surface temperatures in the sun and in the shade, and temperatures at the understory vegetation

(1 m height) and tree branches (1.6 m height), with glassheaded thermocouples and a Univolt DT-830 multimeter; relative humidity, with a psychrometer; and light intensity, with a Kyoritsu illuminometer. The percentage of temperature attenuation was calculated as: T.A. = (Ts-Tsh)/Ts • 100, where Ts and Tsh were, respectively, the maximum hourly sun temperature registered in each area and the corresponding shade temperature at the same hour. The percentage of ground surface exposed to the sun was also estimated every hour in the three habitats: forty randomly distributed points were monitored in each habitat by determining whether they were in the sun or in the shade. The percent of points that were in the shade each hour in each habitat was used as a measure of hourly sun exposure. The relationship between ground surface temperature and external activity of each species was established by dividing the whole range of sun temperatures registered in the field in 2°C-classes. Considering together the data from all hours of all sampling days, the mean activity value of each species in each temperature class was calculated. To do this, only data from the grassland were considered: due to tree overstory cover, both the pine forest and the holm oak forest had, at the same time, very different ground temperatures depending on whether the areas were in the shade or in the sun; on the contrary, in the grassland the temperature in the sun could be considered a single temperature value for ants over the whole study area. The maximal activity temperature of each species was the temperature at which the mean activity value was greatest. From these data, the thermal environment of each species was subdivided into three areas: i) breadth area (sensu Huey & Stevenson, 1979; Huey & Kingsolver, 1993): this included the range of temperatures where activity was greater than 50% of the maximum activity value; ii) tolerance area: this included the range of temperatures where activity was less than 50% of the maximum activity, but not null; iii) inadequate area: this was the range of temperatures where the particular ant species was not active.

Results TEMPORAL VARIATIONS SEASONAL SHIFTS OF DAILY ACTIVITY RHYTHMS Figure 1 shows spring and summer activity rhythms of the main ant species present in the grassland (these species accounted for 98.8 and 95.6% of ants sampled at baits in 1985 and 1990, respectively). Daily activity patterns of each

TABLE II. Pairwise proportional similarity indexes of daily activity overlap in a) spring (upper part of the table), and b) summer (lower part of the table) among the different species studied. For abbreviations of column species, note that they are in the same order as row species Species Cataglyphis cursor Camponotus foreli Aphaenogaster senilis Messor bouvieri Messor capitatus Camponotus cruentatus Tapinoma nigerrimum Pheidole pallidula Tetramorium semilaeve Camponotus sylvaticus

Ccur 0.46 0.40 0.04 0.08 0.15 0.09 0.08 0.04 0.01

Cfor 0.67 0.63 0.47 0.34 0.40 0.37 0.27 0.23 0.06

Asen 0.52 0.49 0.33 0.29 0.45 0.33 0.26 0.22 0.10

Mbou 0.53 0.60 0.53 0.62 0.57 0.60 0.52 0.50 0.29

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Mcap 0.55 0.58 0.43 0.81 0.76 0.91 0.86 0.85 0.62

Cruc 0.51 0.69 0.52 0.46 0.42 0.78 0.74 0.69 0.51

Tnig 0.44 0.52 0.46 0.46 0.47 0.67 0.89 0.87 0.64

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Ppal 0.27 0.33 0.34 0.25 0.29 0.58 0.75 0.90 0.72

Tsem 0.34 0.43 0.45 0.29 0.30 0.58 0.75 0.73

Csyl 0.02 0.12 0.12 0.04 0.08 0.22 0.50 0.59 0.55

0.76 271

CROS, CERDA´ & RETANA: ACTIVITY RHYTHMS OF MEDITERRANEAN ANTS

100 80 60 40 20 0

C. cursor

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% activity

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6 10 14 18 22 2 6 A. senilis

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6 10 14 18 22 2 6 T. nigerrimum

6

T. semilaeve

6

C. sylvaticus

6 10 14 18 22 2 6 6 10 14 18 22 2 Time of the day

6

FIGURE 1. Daily activity rhythms on representative days for the main ant species in the grassland. Data have been standarized by defining the maximum hourly activity value in each season as 100% of activity. Spring: broken line; summer: solid line.

species in spring and summer were compared with a chisquare contingency test and found to be significantly different (p < 0.0001), excepting those of Camponotus sylvaticus and Cataglyphis cursor (p = 0.073 and p = 0.056, respectively). Interspecific pairwise proportional similarity indexes (PSI) of daily activity overlap were calculated in both spring and summer (Table II). Mean PSI values of C. cursor and Camponotus foreli were greater in spring than in summer, that of C. sylvaticus was greater in summer than in spring, while the other species did not show significant differences 272

between periods (Table I). Mean values of PSI for all species considered together in spring (mean ± SD: 0.449 ± 0.195) and summer (0.461 ± 0.275) were not significantly different (Wilcoxon matched-pair test, p > 0.9). The cluster classification of ant species based on the matrix of pairwise overlap values in spring and summer distinguished three distinct groups of species: i) species with diurnal activity throughout the year (C. cursor, C. foreli, Aphaenogaster senilis); ii) species placed within the diurnal species in spring and within the twilight-nocturnal species in summer (Messor bouvieri, Messor capitatus, Camponotus cruentatus); iii) species with a more or less intense twilight-nocturnal activity in both spring and summer (Tapinoma nigerrimum, Pheidole pallidula, Tetramorium semilaeve, C. sylvaticus). RESPONSE OF THE DIFFERENT ANT SPECIES TO ENVIRONMENTAL

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FACTORS

Since there was a good correlation between temperature and light (Pearson's r coefficient, r = 0.83, p = 0.001), and temperature and relative humidity (r = -0.55, p = 0.001), most species of the area followed similar patterns with these three environmental factors. C. sylvaticus was the only ant species in the area that showed daily shifts more dependent on light than on temperature: it did not start its nocturnal foraging until sunset, when light values ranged from 0 to 5000 lux (always less than 20% of maximum midday values), and stopped foraging after sunrise (when light values ranged from 0 to 6000 lux); the ground temperatures at these periods were much more variable: 21-36°C at the start of activity, and 13-30°C at the end of activity. The drastic reductions in activity at midday hours in summer of many species could be attributed to changes in the maximum ground sun temperature reached during the different seasons: sun temperature was around 40°C in spring and autumn, but surpassed 50°C in summer. The different species showed great differences in the temperatures at which they started, peaked and stopped external activity (Figure 2). Minimum foraging temperatures of all species excepting C. cursor were in the range of 10-16°C. Differences in maximum foraging temperatures were greater, M. capitatus P. pallidula T. nigerrimum T. semilaeve C. sylvaticus M. bouvieri C. cruentatus A. senilis C. foreli C. cursor 10

15

20

25 30 35 40 Temperature (°C)

45

50

55

FIGURE 2. Thermal environment of the main ant species studied. Two areas were distinguished: i) breadth area (thick line), which includes the range of temperatures where activity was greater than 50% of the maximum activity registered at any temperature; and ii) tolerance area (thin line), which includes the range of temperatures where activity was less than 50% of the maximum activity, but not null. The white dots indicate the temperature of maximum activity of each species, i.e., the temperature at which activity was greatest.

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ÉCOSCIENCE, VOL. 4 (3), 1997

T. nigerrimum

ranging from 36°C (C. sylvaticus) to 54°C (C. cursor). The maximal activity temperature varied from 22°C (M. capitatus) to 48°C (C. cursor).

SPATIAL VARIATIONS ENVIRONMENTAL CONDITIONS IN THE THREE HABITATS A pattern repeated throughout the year was that the maximum daily temperatures reached in the sun and in the shade, as well as temperature attenuation, were similar in the three habitats considered. Daily fluctuations of both sun and shade temperatures were also very similar, with minor differences related to slope. Maximum values (over 50°C in summer) were reached at midday (13-15 hours), while a steep variation was found before 10 hours and after 18 hours in all three areas. The difference between the maximum sun and shade temperatures was highest (over 20°C) in the summer months (June to August) and lower than 15°C in spring and autumn. The greatest environmental difference among the three habitats was found in the percentage of ground surface exposed to the sun, which was determined by their different canopy cover: the maximum percentage of sun exposure reached almost 100% during most of the diurnal hours (9 to 16 hours) throughout the year in the grassland (with less than 3% of canopy cover), but decreased to 60-70% in the holm oak forest (39% of canopy cover), and to 27-47% in

100 80 60 40 20 0 T. semilaeve

100 80 60 40 20 0 % activity

SEASONAL ACTIVITY RHYTHMS Most species exhibited a marked increase in activity between late spring and late summer, with a peak in midsummer (Figure 3). The exceptions to this pattern were: i) T. nigerrimum, T. semilaeve and A. senilis, which exhibited peak activity in June (and the former species in November) followed by decreased activity in summer, and ii) the two Messor species and P. pallidula, which differed from the other species by being active primarily in the autumn. The seasonal activity patterns of the three most abundant species (P. pallidula, A. senilis and T. nigerrimum) were compared with a χ2 contingency test and found to be significantly different (p < 0.0001). Seasonal PSI was calculated for all pairs of species (Table III). Specific mean PSI values ranged from 0.57 to 0.69 (Table I). The mean value of seasonal PSI for all species considered together (mean ± SD: 0.634 ± 0.131) was significantly greater than both spring and summer mean daily PSI values (Wilcoxon matched-pair test, p < 0.001 and p < 0.01, respectively).

C. foreli

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A. senilis

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P. pallidula

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C.cursor

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C. sylvaticus

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M. bouvieri

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C. cruentatus

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MAM J J A S O N

M. capitatus

MAM J J A S O N

Month FIGURE 3. Seasonal activity rhythms of the main ant species present in the grassland. Data have been standardized by defining the maximum monthly activity value of each species as 100% of activity.

the pine forest (62% of canopy cover), the maximum values only being maintained from 14 to 16 hours. DIFFERENCES OF DAILY AND SEASONAL ACTIVITY RHYTHMS IN THE THREE HABITATS

Daily changes in ant community composition in the three habitats are shown in Figure 4. The different response of species to temperature and the environmental conditions of each habitat determines activity rhythms of species in each case. Activity rhythms of P. pallidula were similar in the three habitats in both spring and autumn (χ 2 = 16.0 and 13.9, p = 0.81 and 0.97, respectively), but they differed significantly in summer (χ 2 = 54.8, p < 0.001). Other

TABLE III. Pairwise proportional similarity indexes of seasonal activity overlap among the different species studied. For abbreviations of column species, note that they are in the same order as row species Species Cataglyphis cursor Camponotus foreli Aphaenogaster senilis Messor bouvieri Messor capitatus Camponotus cruentatus Tapinoma nigerrimum Pheidole pallidula Tetramorium semilaeve Camponotus sylvaticus

Ccur

Cfor 0.86

Asen 0.69 0.72

Mbou 0.55 0.59 0.50

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Mcap 0.51 0.56 0.50 0.84

Cruc 0.85 0.80 0.64 0.52 0.49

Tnig 0.54 0.56 0.79 0.61 0.53 0.48

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Ppal 0.54 0.59 0.48 0.85 0.84 0.51 0.48

Tsem 0.69 0.74 0.88 0.62 0.56 0.66 0.70 0.55

Csyl 0.81 0.81 0.56 0.56 0.54 0.79 0.40 0.57 0.59

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P. pallidula A. senilis T. nigerrimum C.cursor

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T. semilaeve C. foreli C. cruentatus

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P. pygmaea C. sylvaticus L. humile

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M. bouvieri M. capitatus Unoccpied baits

FIGURE 4. Daily changes in ant community composition in the three habitats in May, July and September.

species with similar activity rhythms as P. pallidula, such as T. nigerrimum and T. semilaeve, were present at baits in all three seasons in the grassland, but only in spring in the forest habitats. A. senilis was also present in the three habitats. Its daily activity rhythms were similar in the three habitats in both spring (χ2 = 14.1, p = 0.82) and summer (χ2 = 24.8, p = 0.21). In autumn, P. pallidula was the most abundant species in the two forest habitats, occupying 80-90% of baits. In the grassland, this period of the year was characterized by a quite diverse spectrum of species, and by the presence of species such as Linepithema humile, Messor bouvieri and Messor capitatus, which were very rare before this date. Diversity of ants at baits was higher in the grassland (H = 1.90 and 1.79 in the 1985 and 1990 samplings, respectively) than in the holm oak forest (H = 1.01) and the pine forest (H = 0.91). Seasonal changes in ant community composition in the three habitats are represented in Figure 5. Bait occupation of two dominant species of the grassland (A. senilis and P. 274

pallidula) did not vary markedly throughout the activity season. Instead, the dominance of P. pallidula in the two forest habitats increased from mid-summer onwards. The different species showed marked seasonal peaks in certain periods of the year: in the grassland, T. nigerrimum and T. semilaeve were abundant in spring, C. cursor in mid-summer, and the two Messor species in late summer and autumn, while in the holm oak forest, C. cruentatus was abundant in spring. CHANGES IN DAILY ACTIVITY RHYTHMS IN DIFFERENT MICROHABITATS Differences in environmental conditions in different microhabitats within each habitat led to differing patterns of response by each species. Figure 6 shows the daily variations of temperature and activity rhythms of the three congeneric Camponotus species at baits (i.e., on the ground) and at fennel plants in early September in the grassland. C. foreli did not differ greatly in activity between microhabitats, confirming its diurnal pattern in both (Figure 6b). C. sylvaticus

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FIGURE 5. Seasonal changes in ant community composition in the three habitats.

became inactive during the daytime on the ground, but at least one fifth of foragers on plants (Figure 6c), where temperatures were milder, tended aphids. C. cruentatus showed a different pattern (Figure 6d): workers ceased nocturnal activity at baits when temperatures were well below 20°C,

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FIGURE 6. Daily variations of temperature (a) and activity rhythms of three congeneric Camponotus species: (b) C. foreli, (c) C. cruentatus, and (d) C. sylvaticus, on the ground (solid line) and at fennel plants (broken line) in early September. Activity data have been standardized by defining the maximum hourly activity value as 100% of activity.

but remained at fennel plants throughout the day, when night temperatures were always around 20°C (Figure 6a). These trends were repeated for the other ant species foraging at plants (Table I): diurnal species (e.g., C. cursor or C. foreli) were also strictly diurnal at plants, while preferentially-nocturnal species (T. nigerrimum or P. pallidula) were present at plants throughout the day.

Discussion Foraging activity of ants and other small invertebrates, are particularly sensitive to climatic fluctuations (Fellers, 1989). Temperature is considered the primary physical factor

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affecting foraging rates of ants (Porter & Tschinkel, 1987), which tend to retreat from the surface during periods of the day or year when the thermal environment is inadequate for them. The Mediterranean climate has great variations at both seasonal and daily levels. Temperatures are usually mild in spring and autumn and at night, and very high in summer and at midday. Ant activity follows these environmental fluctuations which give rise to changes in seasonal and daily rhythms. In the study area, seasonal rhythms showed, on average, greater overlap than daily rhythms, although peak foraging periods of ants were more or less separate: some species exhibited seasonal activity peaks in late spring-early summer (T. nigerrimum, T. semilaeve, A. senilis), others in mid-summer (C. cursor and the three Camponotus species), and the two Messor species and P. pallidula were active primarily in the autumn. Most species showed seasonal shifts in daily activity cycles: spring and summer patterns differed for most species, with a marked trend towards increased nocturnalism in summer to avoid critical temperatures. Two groups of species could be distinguished in the ant communities studied: i) heat-tolerant species were diurnal species (e.g., A. senilis, C. foreli or C. cursor) that had small changes in daily activity rhythms throughout the year, and peak temperatures in the upper site of the thermal range; ii) heat intolerant species (e.g., T. nigerrimum, T. semilaeve or P. pallidula) had shifting activity rhythms from diurnal to crepuscular-nocturnal when temperatures became hotter, and had peak temperatures lower than 30°C. When both types of species met at food resources, species that were less heat-tolerant were dominant and usually excluded subordinate, heat-tolerant species from food resources due to their greater aggressiveness and recruitment techniques (Cerdá, Retana & Cros, 1997). Under these competitive circumstances, subordinate species might be expected to avoid the dominants by foraging at different times whenever possible, so as to reduce interference. In other communities, several authors (Brian, 1955; 1956; Morse, 1974; Fellers, 1989) have documented similar restrictions of dominant species by physical factors and wider physical tolerances for subordinate species, and have proposed an inverse relationship between aggressiveness and adaptation to physical stress. To this daily and seasonal temporal variability was added a spatial variability caused by the different canopy cover of each area. In the grassland, the lack of trees caused solar radiation to have a similar effect on the whole ground surface, creating a homogeneous environment for ants at ground level. In the forest areas, however, canopy cover created a heterogeneous environment, since there were sunny and shaded areas throughout the day. Shaded areas received lower levels of solar radiation and, consequently, reached lower temperatures than sunny areas. The result was a heterogeneous thermal environment, with some ground portions subject to high temperatures and others subject to lower ones. In these forest areas, as shown in other studies (Capinera & Roltsch, 1981; O'Neill & Kemp, 1990; López, Serrano & Acosta, 1992), less heat-tolerant ants abandoned exposed surfaces with high ground temperatures in the middle of the day, but remained in shaded areas or on the trees and shrubs. This attenuating effect of vegeta276

tion was even displayed in the grassland, where several ant species with nocturnal activity on the ground surface remained on plants, licking flowers or tending aphids throughout the day, because air temperature at such heights (1-1.5 m) never exceeded 30-35°C. Heat-intolerant, dominant species benefited from this spatial heterogeneity by lengthening their period of activity on hot days in areas covered by vegetation, leading to a decrease in the abundance of subordinate species. The influence of environmental conditions on activity rhythms determines the diversity and structure of ant communities in the different habitats. Thus, areas with greater vertical stratification of vegetation, such as the two forest habitats of the study area, are better protected against sun exposure than more open habitats, and have less fluctuating temperatures (i.e. shade temperatures) over a greater proportion of their ground surface. This greater environmental heterogeneity leads to a lower diversity of ants, because the abundance of subordinate species decreases due to the lengthening of the period of activity of dominants. This pattern has also been observed in other ant communities: Du Merle et al. (1978) have obtained greater species richness in open areas than in forest plots, where they have also found a single dominant species as opposed to the various codominant species found in the clearings; Jennings, Houseweart & Francoeur (1986) also find fewer ant species in dense forest stands than in clearcuts. Otherwise, in dry and open environments, such as the grassland in the study area, the daily range of temperature may be sufficiently wide to meet the requirements both of heat-adapted and cold-adapted species, as well as a spectrum of intermediate forms, each having a sufficient allocation of time that they can avoid interference competition with each other (Heatwole & Muir, 1989). The result is that more species can coexist in the same community, even with broad overlap in the resources used, leading to increased diversity and a reduction in the dominance of the main ant species. In such cases, temporal separation may be advantageous: the adoption of alternative activity rhythms by different sympatric species might reduce the intensity of their interaction and permit more effective partitioning of available resources. Acknowledgements We are very grateful to J. Bosch and D. Company for their help in the field work. This research was partly funded by DGICYT project PB91-0114 to X. Cerdá.

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