Worker response to thermal constraints in the ant Formica obscuripes (Hymenoptera: Formicidae)

J. therm. Biol. Vol. 15, No. 2, pp. 133-140, 1990

0306-4.565/90 $3.00 + 0.00 Pergamon Press plc

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WORKER RESPONSE TO THERMAL CONSTRAINTS IN THE ANT FORMICA OBSCURIPES (HYMENOPTERA: FORMICIDAE) KEVIN M. O'NEILL l and WILLIAMP. KEMP2 'Department of Entomology and 2USDA/Agricultural Research Service, Rangcland Insect Laboratory, Montana State University, Bozeman, MT 59717, U.S.A. (Received 8 October 1988; accepted in revised form 5 June 1989)

Al~trict--l. In southwestern Montana, the ant Formica obscuripes Forel occupies open habitats where temperatures on soil and nest surfaces of 50-60°C are common in summer. Workers succumb rapidly if they remain on surfaces with temperatures in this range (determined experimentally). 2. Variation in the thermal and radiative environment is strongly correlated with variation in worker behaviour. To avoid stressful microhabitats, the workers abandon the surfaces of nests and unshaded foraging areas near midday on clear days. However, they do remain active on plants harbouring honeydew-secreting Homoptera and on shaded sections of foraging trails that constitute over 95% of the trail system between nests. Although bottlenecks do occur on the few unshaded portions of the trails, movement of workers transporting prey, nesting material, and honeydew along trails continues throughout the day.

Key Word Index--Formica obscuripes, Formicidae, foraging trails, thermal stress, solar radiation.

INTRODUCTION

Even at relatively high latitudes, small animals that conduct their activities on fully insolated soil surfaces can experience high and stressful environmental temperatures, since they are often active within a boundary layer and less able to take advantage of convective heat loss (May, 1985; Cossins and Bowler, 1987). Thermal stresses, mediated by environmental temperatures and solar radiation, have been quantified for insects in a variety of environments (e.g. May, 1985; Willmer, 1982, 1983). A number of studies have demonstrated that environmental temperatures experienced by worker ants often result in body temperatures that exceed some critical thermal maximum (Delye, 1967; Marsh, 1985b; Francke et al., 1985). Such thermal stresses limit worker activity to certain times of day (Schumacher and Whitford, 1974; Whitford et al., 1980; Marsh. 1985b; Porter and Tschinkel, 1987) and specific microhabitats (Kay and Whitford, 1978; Marsh, 1985a, b; Schumacher and Whitford, 1974), thus restricting worker movement and foraging activity. Thermal effects upon metabolic rate (Beraldo and Mendes, 1982; Traniello et al., 1984), the rate of locomotion (Holt, 1955; Marsh, 1985a; Rissing, 1982; Skinner, 1980), and foraging efficiency (Traniello et al., 1984; Lopez, 1987) have also been documented for ants. Most of the field studies cited above examined ants in southern Africa and the southern United States. In this paper, we report the results of a study in which we attempted to quantify the constraints that high environmental temperatures place upon the behaviour of workers of the ant Formica obscuripes Forel on nests and trails, and in foraging areas at a site in southwestern Montana, U.S.A. We first demonstrate that the diurnal range of environmental

temperatures in the habitat frequented by F. obscuripes includes temperatures stressful to workers exposed over short time intervals. Second, we show that thermal avoidance responses of the individual workers occur in the same temperature range within which severe thermal stress is evident. Finally, we present data in support of Weber's (1935) hypothesis, that vegetation cover over trails of the species provides a modified microclimate that allows workers to continue activity outside of the nest during times when other parts of their home range are at temperatures that exceed the critical thermal maximum for worker activity. F. obscuripes is widespread in the northcentral and western United States where it occupies open habitats and constructs nests covered with a mound of plant detritus. This diurnal species forages primarily for honeydew from Homoptera, arthropod prey, and nest materials that are brought back to the nest by workers traveling along a system of trunk trails (Weber, 1935; Wheeler and Wheeler, 1963; O'Neill, 1988). Workers of this species vary in length from 3.25 to 7.5 mm (Wheeler and Wheeler, 1963). MATERIALS AND METHODS

The thermal biology of F. obscuripes was studied over a period of 65.5h on 15 days in August and September, 1986 along an abandoned railway bed near Bozeman, Gallatin County, Mont. (latitude: 45: 40' N). The site included over 40 nests of F. obscuripes and an ant trail system connecting the nests to foraging areas and to other nests (O'Neill, 1988). Vegetation at the site consisted primarily of grasses and various weeds, particularly Canada thistle [Cirsium arvense (L.) Seop.]. The Canada thistle 133

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KE~I~ M. O'NEII.L and WILLIAMP. KEMP

occurred in large patches and hosted several species of Membracidae (Homoptera) that were tended by the ants for their honeydew. Temperatures on the surface of nests and trails were measured using iron-constantan and copperconstantan thermocouples. Ambient air temperature was measured at a height of l0 cm with a thermistor. All of the temperature probes were shaded from direct insolation. Solar radiation was measured with a pyranometer placed in an open area in the middle of the study site and is reported as Langleys/ rain ( = l cal cm -2 min -~ = 39.68 W m-Z). The ironconstantan thermocouple was monitored using a Cole-Parmer thermocouple thermometer. The other devices were connected to an Omnidata Polycorder which permitted simultaneous readings of all sensors. We conducted a simple experiment to determine if there was a negative effect upon workers forced to remain on the surface of the soil in fully insolated areas. While critical thermal maxima are available for a number of ants (Delye, 1967; Marsh, 1985b), values vary widely among species. Furthermore, we wished to expose workers to the exact conditions they experienced in the field, so that these results could be directly compared to those obtained on the correlation between temperature and behaviour. Workers were captured, held with forceps by the tarsi of one of the hind legs and placed on the ground in an area of bare, homogeneous, and fully insolated soil. Captured workers were able to stand in a normal manner (i.e. with their thoraces 2-3 mm above the surface) and struggle. The ants could not climb off the surface of the ground, since the ends of the forceps were covered with soil. They were observed for 5 min and judged to be stressed if they became immobile or apparently crippled in their movements. After 5 min, all were released. Those that did not run away, apparently unharmed, were placed in the shade to determine if they would recover. In order to examine the correlation of behaviour with microclimatic variables, ant behaviour was observed and the number of active workers counted in three locales: (I) on the surface of nests (we counted the number of ants within a l0 × 10cm frame placed on the top of the nest), (2) bare ground away from the trails where workers were scavenging and/or hunting for arthropods (we counted the number of ants present in a 1 x l m square marked on the ground), and (3) on trails (we counted the number of ants passing census points in l min). Trails from three different groups of nests were observed in this study. Two manipulations were undertaken to influence the microclimate experienced by the workers. First the vegetation was removed from a 20 cm length of part of a major trail near one of the nests. The trail was approx. 20 cm wide at this point, but vegetation was removed only across 10cm of this. Throughout the study, we kept this section of trail free of debris and covering vegetation. Second, we used a 50 x 65 cm section of plywood covered with aluminum foil placed to one side of this bare section of trail, to increase the temperatures experimentally and solar radiation load experienced by ants. By modifying the angle of the reflector with respect to the ground, we could control soil surface temperature (within limits)

Table I. Resultsof critical temperature experimentson workers of Formica obscuripes Cumulative number ants impaired or immobileat: Numberants Surface ..... not affected temp. (C) N 60 s 5 min at 5 min 31 35 2 0 0 2 36-40 2 0 0 2 41 45 4 0 0 4 46-50 4 0 0 4 51-55 12 7 8 4 56-60 8 8 8 0 2 x 2 ~(2 contingency table analysis(60 s category vs not affected category, with two temperature treatments: <51 and >~51°C: ~'~~ 23.2, P < 0.001). and monitor ant activity during alternating periods with and without the reflector in place. RESULTS

Critical temperatures Fifteen of 20 workers forced to remain on surfaces with temperatures >50°C succumbed within 60 s (Table l). Nine of the 15 showed thermal stress effects (i.e. sluggishness or jerky patterns of movement) within 30 s and two died 35 s after placement on the surface (i.e. they curled up and ceased all movement). None of the workers subsequently recovered after being placed in the shade. Twelve workers exposed to temperatures ranging from 31 to 50°C suffered no apparent ill effects in 5 min of exposure and all 12 ran off after being released, indicating that there were no obvious handling effects. Worker responses to variation in temperature: behavioural observations

environmental

Workers travelled along trails connecting foraging areas, plants occupied by Homoptera, and nests (O'Neill, 1989). Although there was ample exposed ground in the area, these trails were almost always located beneath cover. Of the approx. 325 m of trails identified, only 7 sections > l0 cm in length (totalling l l . 3 m or about 3.5% of the trail system) were uncovered by either matted vegetation (mostly grass and fallen reeds), patches of thistle, one of the few trees in the area, or miscellaneous debris, including discarded rails from the abandoned railway, that were raised off of the ground. Distinct paths, 3-4 cm wide and I cm deep and clear of debris and plants, were present beneath matted vegetation in some areas. The presence of the exposed sections of trail allowed us to examine the response of workers to increases in environmental temperatures experienced as they moved from shade into the fully insolated gaps, where the surface temperature varied widely across the day (e.g. from 15 to 64°C on 27 August and from l0 to 55°C on 4 September). We quantified two responses of workers entering exposed portions of trails. First, the running speed of 330 workers traversing open areas was highly significantly correlated with temperature (Fig. l). Second, as the temperature approached 50°C, workers coming upon gaps in the trail began to display an avoidance response; they halted at the edge of the gap or reversed course and returned to shade after moving several cm into

Worker response to thermal constraints in the ant Formica obscuripes the open area. The response was correlated with variation in surface temperature (Fig. 2), the form of the relationship suggesting that a discrete threshold for the avoidance response exists at a surface temperature of about 50~C. The response was independent of time of day, as the experiment utilizing a reflector demonstrated. During this experiment, workers readily traversed the open area when the reflector was not in place and the surface temperature of the trail remained between 31 and 43' C (N = 9 samples; Fig. 3). However, when the reflector was in place and the surface temperature ranged between 50 and 6 0 C in different samples (N = 8), the proportion of ants that crossed the exposed gap in the trail decreased dramatically. Ants avoiding the gap at high temperatures were apparently not reacting to the presence of a conspicuous and unfamiliar object alongside the trail. In each of three control samples with the reflector present and the surface temperature maintained at the relatively low level of 44-46 C , all 20 ants approaching the gap crossed without hesitation.

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Fig. 2. The proportion of workers of Formica obscuripes that completely crossed 20 cm long unshaded gap in a trail. Data collected over a 7 day period. Each sample considered 20 workers that approached the gap. Points represent data from 1 to 4 samples. Total sample size = 64. Line passes through the mean proportion for each ~C for which data was available.

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Worker responses to variation in environmental temperature: diurnal changes in worker activity The data on temperatures stressful to individual workers and the avoidance responses apparently related to these temperatures led to the hypothesis that spatial and temporal variation in microclimate would be reflected in concommitant diurnal variation in worker activity patterns. This was examined in seven locales: four sections of three separate foraging trails, in one non-trail area where workers foraged, and on the surfaces of two nests. Activity on foraging trails. As a result of the avoidance response of individuals, exposed sections of trail acted as bottlenecks during clear days and affected traffic between areas frequented by workers. The number of ants passing census points on trails containing gaps decreased markedly in the middle of the day both at the gap and elsewhere along the same I0

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trail and was highly significantly correlated with surface temperature. The data for the 20 cm long gap near nest No. 6 is presented in Fig. 4 and Table 2. In addition, when two longer gaps (i.e.i.2 and 2.8 m) in the trail system were censused on 28 August, the number of ants passing census points dropped to zero in 25 of 26 censuses when the surface temperature was > 50°C. In contrast, the number of ants passing was > 0 on all 52 censuses in which the surface temperature was < 5 0 ° C (Chi-square contingency analysis, X~=77.6, P <0.001); it was > 1 0 in 46 of the censuses. Since, only one of the nests in the area had more than two trails radiating from it, such

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KEVINM. O'NEILL and WILLIAMP. KEMP Table 2. Correlations between trail surface temperature and Formica obscuripes worker activity in three locations Correlation o f surface temperature with: Number of ants passing Location

Covered trail near nest No. 41 (4 September) (no gaps in trail) Covered trail near nest No. 9 (4 September) (gaps in this trail several metres away) Unshaded trail near nest No. 6 (4 September) Unshaded trail near nest No. 6 (28 August)

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bottlenecks probably had significant effects upon worker movement patterns. In contrast to the surface of exposed trails, the soil surface temperature on covered sections of trails varied little across the day [Fig. 4(B)]. The temperature on the exposed surface of the gap created near nest No. 6, at times when it was 45~C or higher, was always higher than the temperature on the shaded surface of the covered portion of trail just 20 cm north (mean temperature difference = 17.1~C; SE = 0.64; N = 22). On 4 September the number of ants passing on a section of trail between nests Nos 41 and 42 that did not have unshaded gaps remained relatively constant throughout the day [Fig. 4(A)] and was not correlated with surface temperature (Table 2). Of 23 trail sections running between nests, only four contained gaps that were unshaded. Some of these trails also passed through patches of plant on which Homoptera were tended. Ants remained on plants with Homoptera throughout the day, probably because shaded refuges were available and air temperature at such heights never

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exceeded 37°C on I 1 days of monitoring between 10 August and 4 September. Ants were also observed to prey upon other insects within vegetation or or near the trails. Thus, movements through some parts of the home range, as well as certain foraging activities, were not halted in the middle of the day when there were high temperatures on exposed surfaces. The census data indicate that unshaded gaps in trails disrupt the movement of workers during the middle of the day, but do not provide information on the absolute numbers of ants present along a given length of trail. In the middle of the day, when even the covered trails are warmer, the ants will have a greater running speed (Fig. l). Therefore, at higher temperatures a greater proportion of the ants present on the trail will pass the census point in ! rain than at lower temperatures (Skinner, 1980). However, by correcting for variation in running speed at different temperatures, we can estimate the linear "density" (D) in ants per metre of trail as: D = (A/V), where A = ants passing per minute and V = running speed in metres per minute. Thus, on 4 September on the trail near nest No. 41, the number of ants passing in I min at both the 910 and 1350h census was 13. However, since the velocity of the ants (taken from the regression in Fig. l) at 910 and 1315 were 1.6 and 3.0 m/min, respectively, estimates of D for these two times are 8.1 and 4.3ants/m, respectively. On covered sections of each of the two trails censused on 4 September, there was a significant correlation between the temperature of the shaded surface and the number of ants/metre (Table 2). Therefore, the actual number of ants present in the middle of the day is lower, even though there were no bottlenecks on this trail. On clear days following rains, when the soil was still wet, worker activity continued into the middle of the day when the level of solar radiation was high, but surface temperatures, moderated by the wet soil, remained within a lower range. For example, a heavy rain occurred on 21 August. On 22 August, although a clear day, worker movement across unshaded gaps in trails continued unabated through the mid-day when activity was usually halted on open surfaces. The surface temperature at ! 300 h on this day was only 32°C. Thus, even at relatively high solar radiation loads, workers can remain active in open areas when the temperature near the surface remains low. Activity in non-trail foraging areas. The decrease in the number of ants on trails even where there were no gaps may have been partially due a decrease in the

Worker response to thermal constraints in the ant Formica obscuripes number of ants foraging in open areas in the middle of the day. The activity of ants in open areas was censused on 3 days in a 1 x 1 m 2 quadrat of bare ground in the middle of the abandoned railway bed where ants foraged for both live and immobile invertebrates. The number of ants present at different times of day in this quadrat varied significantly as a function of incident solar radiation (Fig. 5). Solar radiation, rather than surface temperature, was used in the analysis because heterogeneity of the rocky surface in this area made estimation of a typical soil temperature difficult. Activity on the surface o f nests. While the mounds of F. obscuripes generally occur in open areas (Weber, 1935), variation in the proximity and relative height of vegetation and the height of the mound itself results in variation in the degree of exposure to solar radiation. The mean height of the mound of plant material was 10cm (O'Neill, 1989). Some mounds were also built upon raised portions of soil. Variation in nest exposure can be illustrated with the data for two nests censused for worker activity on 4 September. The top of nest No. 6, which was bordered on the south and west by vegetation less than 0 . 5 m high, was in full sun on 64% of 28 censuses carried out every 20 min between 0830 and 1730 h. However, nest No. 11 was in full sun only 39% of the time, since it was surrounded on all but the east side by plants up to I m in height. Within and between nest variation in the level of incident solar radiation, with its corresponding influence on nest surface temperature, was correlated with differences in the number of workers active on the surface of the nests (Fig. 6). During census periods, the surface temperature on the top of nests ranged as high as 72:C on nest No. 6 on 27 August and 61°C on nest No. 11 on 4 September. After an initial rise early in the day, the number of workers active on the exposed surface of nests decreased as surface temperature increased, with no ants present when temperatures surpassed approx. 50:C. Although the maximum temperatures attained differed little between the nests, the schedule of temperature change was different because of the nearby vegetation. On

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Fig. 6. (A) The number of workers of F. obscuripes present in a 10 x 10 cm square on the top of two nests and (B) the surface temperature on the nests within the square as a function of time of day on 4 September 1986. The correlation between temperature and the number of ants present for nest No. 6 was r = -0.83 (N =28; P < 0.01). It could not be calculated for nest No. 11, since an accurate count could not be obtained when the number of workers surpassed 50. 35

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nest No. 6, which had fewer surrounding plants to provide shade, the temperature increased and worker activity decreased gradually (Fig. 6). In contrast, on nest No. I I, where the surface of the nest was shaded until about 1045 h, the temperature increased and worker activity decreased abruptly (Fig. 6). Later in the day, worker activity on nest No. I1 increased earlier than on No. 6 because of shade encroaching upon the nest. Such patterns were apparent on all nests at the study site. During the 3 days when nest No. 6 was census•d, there was a strong relationship

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between incident solar radiation and the number of workers active, with activity dropping to zero at a level of about 1.0 Langleys/min on each day (Fig. 7). Note that the relationship differs from that in non-trail foraging areas (Fig. 5), particularly with regard to the maximum level of solar radiation at which ants were present. Ants in the open area were probably able to tolerate higher radiation loads because of small pockets of shade that provided temporary thermal refugia. Worker activity patterns were less predictable with respect to changes in ambient air temperature which peaked later than solar radiation on the three days on which the latter was measured (Fig. 8). Although worker activity ceased on the top of nests when surface temperatures reached 5ffC. activity continued on the periphery of those nests surrounded by vegetation sufficient to provide partial shade. For example, on 4 September, some workers remained active on the periphery of nests No. 6, and No. II throughout the day, even though the surface temperature on the exposed top of the nest surpassed 6ffC. For seven nests examined in early afternoon on 7 and 11 September, mean temperature recorded on the fully insolated and occupied surface of the nests ( m e a n = 53.7, SE=0.81) was significantly greater than the mean of temperatures recorded in the shade on the side of the nest where workers were still active (mean = 33.3 , SE = 1.38; t.., = 12.78, P < 0.001). Thus, those workers active on trails were able to enter and leave most nests without crossing fully insolated areas. DISCUSSION

Workers of F. obscuripes at our site experienced wide diurnal fluctuations in temperature at the soil surface. Variation in the thermal and radiative environment was strongly correlated with changes in the activity of workers observable in both individual responses (e.g. avoidance of open areas at high temperatures and changes in running speed) and in censuses of the number of workers active on trail, on nests, and in foraging areas. The change in running speed may be primarily mediated via temperaturedependent changes in metabolic rate (Beraldo and Mendes, 1982; Traniello et al., 1984). It may also represent behavioural response by workers attempting to cross the exposed area as quickly as possible. Regardless, increased running speed allowed workers to reduce the duration of their exposure to solar radiation and high surface temperatures. The correspondence between the surface temperatures at which ants rapidly succumbed in our experiments and those on nest and trail surfaces they avoided (i.e. those > 50°C) indicates that workers act to avoid thermal stress in the middle of the day. Our data suggest an apparent discrete critical threshold temperature, above which irreversible damage occurs. However, even at moderate temperatures (e.g. 45-50°C) water balance is likely to be adversely affected if the ant is exposed for longer than the 5 rain of our experiments (Sigal and Arlian, 1982). If the critical temperature experiments had been extended beyond 5 rain, non-linear relationships b e t w ~ n temperature and time to paralysis, apparent in other

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Fig. 8. Solar radiation (squares) and ambient air temperature in the shade at a height of 10cm (circles) as functions of time of day on 4 September, 1986. Both variables were measured within 3 m of nest No. 6. insects (Marsh, 1985a; O'Neill and O'Neill, 1988), may have been exposed. Therefore, although there was a threshold temperature, above which activity was impossible, census data from trails, nests, and foraging areas also demonstrated a graded relationship with activity below this threshold. This may be a function of thermal and hydric stresses, the availability of temporary thermal refuges, and diurnal fluctuation in forage availability (Whitford and Ettershank, 1975). Diurnal patterns of worker activity and distribution in Formica appear to be partially under the control of endogenous circadian rhythms entrained by temperature and photoperiod (North, 1987). However, behavioural responses of individuals and the results of the experiment with the reflector indicate that the thermal environment also controls activity on a more proximate level, thus allowing workers rapidly to adjust to environmental heterogeneity. Surface temperatures appear to be the most consistent predictor of ant activity available from our study. Although surface temperatures are slightly higher than the air temperatures experienced by an ant standing 2-3 mm above the ground in the middle of the day, an insect in full sunlight is likely to have a body temperature that exceeds air temperature (Wilmer and Unwin, 1981). Thus, surface temperatures measured in the location where workers were active are likely to provide a sufficient estimate of body temperature for animals as small as an ant (Rissing, 1982). In contrast, ambient temperatures were not an accurate correlate of the activity of most workers, because its rise each day lagged behind the increase in surface temperature. Since we measured solar radiation at only one location at our site, it produced a value that corresponded to the radiative environment that workers were subjected to only when they were on uniform and fully insolated surfaces. Thus, on the top surface of nests, the solar radiation values were highly correlated with the number of workers present. However, at other locations, such as the surface of trails following a rain, surface temperature was a better indicator of potential activity. Porter and Tsehinkel (1987) found that soil temperatures at a depth of 2 cm were the besl

Worker response to thermal constraints in the ant Formica obscuripes predictor of foraging rates for S. invicta, a species that forages in subterranean tunnels. Weber 0935) suggested that the trails of F. obscuripes are constructed under cover in order to offset "the desiccating effect of the sun's rays", allowing activity to continue through the middle of the day. Our observations confirm Weber's on the location and structure of trails and provide quantitative evidence that the microclimate on trails is usually less stressful than in open areas. The shielding of grass cover can result in a substantial reduction in the quantity of solar radiation reaching the ground, the actual amount depending upon the density of plant cover (Angstrom, 1925; Geiger, 1965). Our data also indicate that activity on the covered trails can continue into the hottest periods of the day. This may enhance colony foraging success by prolonging the daily period of activity. A similar function has been suggested for below ground foraging tunnels of the ant Solenopsis invicta (Markin et al., 1975; Porter and Tschinkel, 1987). Since the influence of temperature upon foraging behaviour and efficiency is likely to be a complex function of thermal effects upon survival, water balance (Cooper, 1983; SIobodchikoff, 1983), and metabolic rate (Traniello et al., 1984), as well as the availability of prey (Marsh, 1985a) and honeydew, our data address only a subset of the potential thermal effects upon foraging success. It appears that F. obscuripes benefits from environmental heterogeneity and lengthens its period of activity on hot days by constructing trails beneath vegetation. However, the question arises as to whether the placement of trails under cover has evolved as an adaptation to aid in thermoregulation or is simply an effect of the type of habitat frequented by the species. Our observations generally support the former hypothesis. The trails followed cover closely and crossed open ground only intermittently. This was particularly evident where the trails followed the raised rails of the old railway bed. For much of the length of the trail system, the rails provided the only extensive shade within a meter of the trails. Trails left the cover of the rails only to cross into the shade of plants or to enter nests. The ants on these trails tracked the position of the shade which changed across the day with the position of the sun in some places. Trails crossed the railway bed only at a single point, the only place where dense vegetation covered the railroad tracks. Observations and experiments on the ontogeny of trail system in an area with a mosaic of cover and open ground would provide valuable tests of the above hypotheses. Alternative hypotheses, that the overlying vegetation on trails protects workers from predators (e.g. birds) or that trails patterns are solely determined by resource distribution, cannot be tested at this time. Acknowledgements--Ronald Lang, Montana State University, determined the ant species. We thank Michael lvie, Robert Nowierski, Noah Poritz and Randall Ryti for their comments on the manuscript. This work was supported by the Montana Agricultural Experiment Station (grant MONB-! 55) and the USDA Agricultural Research Service. This is contribution number J-2019 of the Montana Agricultural Experiment Station.

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