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Thermal properties of the tent of early instar colonies of the eastern tent caterpillar, Malacosoma americanum (Lepidoptera: Lasiocampidae)
Journal of Thermal Biology 37 (2012) 615–624
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Thermal properties of the tent of early instar colonies of the eastern tent caterpillar, Malacosoma americanum (Lepidoptera: Lasiocampidae) Terrence D. Fitzgerald n, Steven Miller, Michael Smith Department of Biological Sciences, State University of New York at Cortland, Cortland, NY 13045, USA
a r t i c l e i n f o
abstract
Article history: Received 12 March 2012 Accepted 30 July 2012 Available online 11 August 2012
The extent to which the small tents of the early instars of Malacosoma americanum warmed when irradiated by sunlight was investigated by continuous electronic monitoring of field colonies for 137 colony-days. Tent temperatures exceeded the threshold for larval growth of 15 1C on 88–96% of the study days, exceeding in degree-minutes the ambient excess-over-threshold by a factor of approximately five. In still air, tents constructed by third instar caterpillars achieved greater temperature excesses over ambient than did a model of a tightly sealed glass house, but smaller tents and tents exposed to simulated wind did not perform as well. Tents of M. americanum warmed more rapidly and to a high temperature than silk nests of markedly different design constructed by other species. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Thermoregulation Social caterpillars Silk Basking
1. Introduction The communal silk nests of social caterpillars are multifunctional structures. They serve to shield caterpillars from predators and parasitoids, enclose moist internal microclimates conducive to molting, provide resting areas from which intermittent forays in search of food are launched, act in some species as communication centers from which nest mates are recruited to food finds, and facilitate en masse thermoregulation (Fitzgerald, 1993 and references therein; Fitzgerald, 1995; Rehnberg, 2002, 2006; Ruf and Fiedler, 2002). It is the latter function that has drawn the attention of most researchers. The nests of different species of caterpillars vary markedly in size, shape, and in the density of their walls, but all show marked temperature gains when exposed to solar radiation (Knapp and Casey, 1986; Joos et al., 1988; Casey et al., 1988; Fitzgerald and Underwood, 2000; Ruf and Fiedler, 2002; Fitzgerald et al., 2003; Rehnberg, 2002, 2006). The best studied of these structures are those of the lasiocampid caterpillars, the nests of which are referred to as tents. Lasiocampids in the genera Malacosoma and Eriogaster construct their tents by laying down new strands of silk over existing tent walls during intermittent en masse spinning bouts. The strands are stretched slightly before they are attached and their subsequent axial retraction causes sheets of newly spun silk to tighten and lift from subjacent silk surfaces (Fitzgerald and Willer, 1983; Fitzgerald et al., 1991). Successive episodes of spaced spinning bouts result in the creation of a structure that consists
n
Corresponding author. Tel.: þ1 607 756 4504; fax: þ1 607 753 2927. E-mail address: fi[email protected] (T.D. Fitzgerald).
0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2012.07.010
of multiple layers of silk separated by air-filled gaps. When exposed to solar radiation, the layered structure of the tent creates a thermally heterogeneous environment within which the caterpillars thermo regulate by moving between warmer and cooler layers (Casey et al., 1988; Ruf and Fiedler, 2002). Eastern tent caterpillars (M. americanum) are widely distributed throughout eastern North America (Stehr and Cook, 1968). They typically eclose from their eggs in mid-April and initiate the construction of a tent in the branches of the host tree shortly thereafter (Fitzgerald, 1995). Basking on or in the tent is essential to the growth of the caterpillars because ambient air temperatures in the early spring are often too low to allow the caterpillars to digest their meals. Both the forest tent caterpillar M. disstria (Hodson, 1941; Ives, 1973) and M. americanum (Knapp and Casey, 1986; Casey et al., 1988) grow little if at all when their Tb’s (body temperatures) fall below approximately 15 1C. On cold mornings, eastern tent caterpillars are commonly found clustered just under the surface of their tent on the side that faces the morning sun. Their dark bodies absorb solar radiation and the walls of the tent limit convective heat loss, resulting in significant gains in Tb over Ta (air temperature). This enables the caterpillars to process food collected during their overnight forays (Knapp and Casey, 1986; Casey et al., 1988; Joos et al., 1988; Fitzgerald, 1995). Although spot measurements of clusters of early instar eastern tent caterpillars by Knapp and Casey (1986) showed that the small caterpillars had Tb’s in excess of Ta, all previous studies of the ability of lasiocampid tents to gain heat when irradiated have focused on the large, many-layered structures of the maturing caterpillars (Casey et al., 1988; Joos et al., 1988; Ruf and Fiedler, 2002). Heat trapping by the relatively thin and airy tents inhabited by the caterpillars during their first several stadia, however,
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is likely to be even more important to the growth and survival of the caterpillars. This is the case because the caterpillars are among the earliest to emerge in the spring and during the first few weeks of their lives ambient temperatures commonly fall below freezing. During early spring, basking is essential not only to growth but to survival as well and whole populations of M. americanum have perished during their first stadium when persistent cloudy and cold weather prevented the caterpillars from processing food (Blackman, 1918; personal observation). Ruf and Fiedler (2005) also determined that the inability of the caterpillars of Eriogaster lanestris to build an initial tent or their failure to maintain an existing tent were the most important factors affecting colony survival. We report here the results of a study of the small tents of first to third instar eastern tent caterpillars undertaken to determine their effectiveness in creating a thermal environment which fosters the growth and development of the caterpillars.
2. Materials and methods 2.1. Field study site and host species Field studies were conducted at the State University of New York at Cortland on the Hoxie Gorge campus (42 degree 32 min 48 s N, 76 degree 4 min 32 s W). The study site, at an elevation of approximately 425 m, consists of an old field succession containing numerous apple (Malus pumila) and cherry trees (Prunus serotina and Prunus. virginiana), ovipositional host species for the caterpillars. 2.2. Field studies A study to determine the extent to which the inhabited tents of the eastern tent caterpillar warmed when exposed to sunlight was conducted at the study site from April 20 to May 21, 2005. Tent caterpillars began to eclose on April 13 and small tents were evident by April 20. On the latter date, thermistor sensors 3.2 mm in diameter by 18 mm long attached to Hobo Stowaway temperature data loggers (Onset Computer Co., Bourne, Massachusetts, USA.) were inserted into each of two, naturally occurring tents, approximately 1 cm below their south-facing surfaces. As the tents grew in size, the sensors were moved to maintain this approximate position. Care was taken to minimize disruption of the tent silk during this process and new silk was soon added by the caterpillars, fully embedding the sensors in the new positions. The loggers were programmed to record temperature every 15 min. The caterpillars moved in an out of the compartments of the tents fitted with the sensors so the temperatures were recorded though the whole range of tent occupancy. An additional thermistor sensor was encased in an RS1 solar radiation shield (Onset Computer Co.) and situated near the tents to record ambient temperature. Loggers were downloaded to a shuttle every 48 h and the data compiled with Boxcar Pro software (Onset Computer Corporation). In 2008, three additional tents were monitored in the same manner at this same site. In 2008, eclosion occurred on April 21 and recording began when thermistors were placed in the tents on April 25. Recording continued uninterrupted until May 20. 2.3. Laboratory studies 2.3.1. Temperature gain in occupied tents A study was conducted in the laboratory to obtain measurements of temperature gain in occupied tents and isolated caterpillars when both were exposed to an infrared lamp. Nine tents
Fig. 1. Left to right: second instar tent of M. americanum, third instar tent of M. americanum, third instar nest of E. socialis, third instar nest of E. psidii.
constructed by second–third instar colonies of tent caterpillars (Fig. 1) were collected from the field and held overnight in a refrigerator at approximately 2 1C. To conduct the study, a tent was transferred to a walk-in cooler having an average ambient temperature of 6.970.19 1C (SE). A 30-gauge copper-constantan thermocouple connected to a BAT-12 thermometer (Sensortek, Inc., Clifton, New Jersey) was inserted approximately 1 cm below the light-facing surface of the tent which was situated 50 cm from the front surface of a 250 W heat lamp (Extralife IR Lamp LR 48263) and the temperature gain of the tent recorded over 15 min. Another thermocouple wire was inserted into a recently killed third instar caterpillar and placed in the path of the infrared light at the same distance as the tent to determine the ability of a solitary, exposed caterpillar to gain heat. IR heat lamps have been previously used in this manner to irradiate tents in studies conducted by Breuer and Devkota (1990), Fitzgerald and Underwood (2000), Rehnberg (2002), and Fitzgerald et al. (2003). Temperature readings from the irradiated tent and exposed caterpillars were taken at 30 s intervals for the first minute and at 1 min intervals thereafter for a total of 15 min. The cooler’s fan created weak air movement in the chamber throughout the study period causing a slight fluttering of loose silk strands at the tent surface.
2.3.2. Temperature gain in unoccupied tents and comparison with glass house Two previous studies reported that tents devoid of the thermal mass afforded by the enclosed caterpillars warmed little when exposed to sunlight (Knapp and Casey, 1986; Ruf and Fiedler, 2002) while another reported that the temperatures of empty tents rose significantly in sunlight (Joos et al., 1988). Moreover, Joos et al. (1988) reported that tents of M. americanum functioned like miniature glass houses while Ruf and Fiedler (2002) stated that this was not the case for tents of similar design constructed by E. lanestris. To further investigate these conflicting reports, the extent to which 11 tents of first–second instars, devoid of caterpillars, and a model of a glass house gained heat when exposed to an IR light source was investigated. The tents used in this study were collected from the field and were different tents than those used in the study outlined above. They were markedly smaller and had thinner silk walls than those of the third instars. In the laboratory, caterpillars were collected while feeding off the tents to evacuate them. Stragglers were manually removed from the tents. A thermocouple was inserted through a small hole drilled into a branch supporting a tent to gain access to the interior without tearing the fragile silk of the small structure.
T.D. Fitzgerald et al. / Journal of Thermal Biology 37 (2012) 615–624
The glass house was constructed with 0.15 mm thick glass and was box-shaped with a volume of approximately 303 cm, approximating that of an average experimental tent. Four sections of cherry branches, 4 cm-long 4–5 mm diameter were enclosed in the house to provide thermal mass similar to that enclosed by the tent. A thermocouple wire was suspended in the air at the center of the house. The house was tightly sealed with transparent tape on all edges. Temperature gain was recorded at 30 s intervals for the first minute, then at 1 min intervals for a total of 15 min. The IR source was then turned off and the cool-down of the structures recorded for an additional 10 min. For statistical analysis, the maximum temperatures achieved by each of the 11 tents were compared to the mean maximum temperature obtained by the glass house with a One-Sample t-test.
2.3.3. Temperature gain of fully formed third-instar tents vs glass house in still and moving air This glass house study detailed above was repeated with the larger, fully-formed tents of third instar colonies using a procedure identical to that detailed above except that the structures were exposed to the IR lamp for 30 min before cooling down. To obtain tents for this study, laboratory colonies of newly eclosed caterpillars were situated at the centers of wooden frames and allowed to construct their tents (Fig. 2). Food was provided at the ends of bridges that extended from the frames. Before the caterpillars initiated tent construction, thermocouples were attached to the center supports of the frames, following the procedure of Casey et al. (1988), such that they would be at the approximate centers of the fully constructed tents. The caterpillars were allowed to build tents until they reached the end of their third instar when they were removed from the tents as described above. A total of five tents were prepared in this manner. A larger glass house than used in the previous experiment was used in this study to more nearly approximate the size of the larger tents. The box shaped house was constructed with glass walls 2.4 mm thick and enclosed a volume of approximately 172 cm3. Four sections of cherry branches, 6 cm long 5–7 mm diameter were enclosed to add thermal mass. This study was also replicated using the identical procedure and the same tents except that a fan was employed through the duration of each of the 30 min trials to simulate the effect of an approximate 8 km/h wind on the thermodynamics of the structures. For both of these studies, each trial consisted of running one tent along side the glass house. For statistical analysis, the maximum temperature achieved by each of the five tents was compared to the mean
maximum temperature obtained by the glass house over the five runs with a One-Sample t-test. 2.3.4. Comparison of temperature gain of tent caterpillar nests to nests of different design The silk nests of caterpillars of different species vary markedly in size, shape, and density and would be expected to be adapted to perform differently when irradiated. However, there have been no previous attempts to compare the performance of these nests. Nor has there been an agreed upon standard procedure for assessing thermal performance that would allow for comparisons across space and time. A preliminary attempt at obtaining such comparative data was made during the present study. Using the procedure outlined above for assessing the performance of tents when irradiated in the laboratory, we compared the relative performance of nests constructed by M. americanum up to the end of the third instar, and nests of comparable volume constructed by Eucheria socialis (Pieridae) and the lasiocampid Eutachyptera psidii. All nests were devoid of caterpillars and the thermocouples were placed near the centers of the structures. Nests of these species were chosen because they are fundamentally different in overt form and construction (Fig. 1). The study was replicated with seven different field collected nests of each type, all devoid of caterpillars. 2.4. Data analysis Temperature data were graphed and analyzed with SigmaPlot, ProStat and SigmaStat software. Data were analyzed by t-tests, One-Sample t-tests or by One-Way ANOVA’s. If normality or equal variance considerations precluded a parametric test, a Kruskal– Wallis One Way ANOVA followed by a Tukey test for multiple comparisons was performed.
3. Results 3.1. Field studies In 2005 and 2008 ambient temperature exceeded the threshold for growth of 15 1C on 48% and 56% of the study days, respectively (Table 1). Temperature probes in tents exceeded the growth threshold on 87% of the days in 2005 and from 88% to 96% of the days in 2008. Ambient temperature probes took Table 1 Number of days during the study periods when ambient and tent temperatures exceeded the threshold for caterpillar growth of 15 1C, time between initial sunstrike and the achievement of threshold, and time relative to ambient to reach 15 1C. Means in each year followed by a different letter are significantly different po 0.05. Year and study duration (days) 2005 (31) Ambient Tent 1 2005 Tent 2 2005 2008 (25) Ambient Tent 1 Tent 2 Tent 3
Fig. 2. Tent constructed in the laboratory on a dowel frame by a colony of M. americanum caterpillars.
617
a
Number days Z 15 1C)
Mean7 SE minutes Mean7 SE minutes after 0700 h to achieve earlier than ambient to reach 15 1Ca 15 1C
15 27
3107 34a 184 734b
– 206 735
27
166 735b
221 738
14 24 23 22
3107 42a 161 725b 185 726b 158 740b
– 209 731 194 726 239 731
Data only for days when ambient temperature reached 15 1C.
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Fig. 3. Daily records of tent (grey) and ambient temperatures for two colonies of M. americanum monitored in 2005.
Fig. 4. Daily records of tent (grey) and ambient temperatures for three colonies of M. americanum monitored in 2008.
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approximately 2 h to 2.5 h longer to reach the growth threshold than did temperature probes inserted into tents in both 2005 (ANOVA, F¼3.83, df¼2, p ¼0.0268) and 2008 (Kruskal–Wallis one way ANOVA, H¼12.06, df¼3, p ¼0.007). On those days when ambient temperatures reached 15 1C, (15 of the 31 study days in 2005 and 14 of the 25 study days in 2008) tent probes reached the growth threshold approximately 3–4 h sooner (Table 1). Although sunrise occurred at approximately 0545 h during the study periods, sunlight did not strike the tents until approximately 0700 h. Both ambient and tent temperatures typically achieved their daily maxima between 1300 h and 1400 h. Daily ambient and tent temperatures for tents monitored in 2005 and 2008 are shown in Figs. 3 and 4. On cloudless mornings, the temperatures of the irradiated tents rose precipitous (Fig. 5) with the greatest rate of change typically occurring between 0700 h and approximately 1000 h. During this period for all study days in 2005 and 2008, regardless of the extent of early morning cloud cover, the mean rate at which tents gained temperature greatly exceeded the rate of ambient temperature increase (Table 2, 2005: Kruskal–Wallace test, H¼24.7, df¼2. po 0.001; 2008: H¼9.1, df ¼3, p ¼0.03). The maximum rate of heat gain recorded during the whole of the study occurred during this 3 h interval on sunny days in mid-May in both 2005 and 2008. The maximum overall rate of change occurred on the morning of May 13, 2008. On that day the temperature of tent 1 at 1000 h was 42.9 1C greater than its temperature at 0700 h, an average rate of increase of 14.3 1C/h, exceeding at that time ambient temperature by 31.0 1C. The most precipitous rate of change recorded over any 1 h period was for tent 1 on May 14, 2005 between 0930 h and 1030 h (Fig. 5). During this period, the internal temperature of the tent increased at an average rate of 0.42 1C/min, a rate 8.4 times greater than that recorded for ambient temperature during this same period. The maximum temperature achieved by a tent during both study years occurred on May 6 and 13, 2008 when tent 1 reached 49.5 1C. Though the tents warm rapidly to high temperatures, they are poorly insulated against heat loss. Their internal temperatures are sustained above ambient only during the period of irradiation and decline rapidly to the ambient temperature as sunset approaches (Fig. 5). Table 3 and Figs. 6 and 7 compare the number of degreeminutes in excess of 15 1C registered by tent and ambient temperature probes for the whole of the 2005 and 2008 study periods. To calculate degree-minutes, the average temperature
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Table 2 Rate of warming of ambient and tent probes between 0700 h and 1000 h. Means within the same year followed by different letters are significantly different (po 0.05). Study year 2005 Ambient Tent 1 Tent 2 2008 Ambient Tent 1 Tent 2 Tent 3
Number of days monitored
Mean7SE (1C/h)
31 28 31
1.87 0.2a 5.27 0.6b 4.97 0.5b
25 25 25 25
1.77 0.3a 4.47 0.7b 3.37 0.5b 3.97 0.6b
Table 3 Degree-minutes in excess of the threshold for growth of 15 1C for ambient and tent thermal probes. Means in each year followed by different letters are significantly different (p o0.05). Year
2005 Ambient Tent 1 Tent 2 2008 Ambient Tent 1 Tent 2 Tent 3
Days Mean 7SE degreemonitored minutes in excess of 15 1C/day
Total degree-minutes in excess of 15 1C for entire study periods
31 28 31
835.7 7 321.0a 4573 7 824b 4159 7 757b
26,465 123,478 128,918
26 26 26 26
727 7 253a 2597 7 534b 3555 7 635b 3699 7 700b
18,903 67,527 92,423 96,181
between two successive readings was calculated then multiplied by the number of minutes in the interval between readings to obtain degree-minutes. Only mean temperature values in excess of 15 1C were used in these calculations. For both years, daily and total degree-minutes in excess of the threshold value were significantly greater for tent than ambient probes (Table 3, 2005: Kruskal–Wallace Test, H¼ 22.8 df¼2, po0.001, 2008: H¼21.3, df¼3, p ¼ o0.001). Daily and total values for tents exceeded ambient values by a factor of approximately 5 with the exception of tent 1-2008, which exceed ambient values by a factor of approximately 3.5. The greatest excesses of tent over ambient in degree-minutes were registered on May 10, 2005 (for tents 1 and 2, 6429 and 7329 degree min, respectively) and on May 13, 2008 (for tents 1–3, 7775, 11577 and 9536 degree min, respectively). 3.2. Laboratory studies 3.2.1. Temperature gain in occupied tents Under laboratory conditions, when irradiated by an IR lamp, third instar tents containing caterpillars warmed rapidly, achieving a maximum average temperature in excess of ambient of 21.571.5 1C. Caterpillar models also warmed above ambient but to lesser extent than the tents, achieving a maximum average temperature in excess of ambient of 9.670.74 1C (t-test, t ¼14.42, df¼8, p o0.0001, Fig. 8).
Fig. 5. Five day record of the temperature of tent 1-2005 (black line) and ambient temperature. Rectangles indicate daylight hours between local sunrise and sunset.
3.2.2. Temperature gain in unoccupied tents and comparison with glass house Eleven unoccupied tents constructed by first to second instar caterpillars heated well above ambient in laboratory tests (Fig. 9) but the maximum average temperature achieved (14.970.65 1C)
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Fig. 6. Degree-minutes per day in excess of 15 1C for two tents of M. americanum (grey) monitored in 2005 and the corresponding ambient excess. Temperature data were not collected on days indicated by (x) due to recorder malfunction.
was approximately 7 1C less than the maximum temperature achieved by the larger, occupied tents of third instar caterpillars used in the study reported above. Both the denser walls of the larger tents and their greater thermal mass, due to the presence of caterpillars, likely contributed to their achieving higher final temperatures. The average maximum temperature achieved by the 11 tents was also significantly less than that of the glass house (19.0 1C, One-Sample t-test, t ¼6.24, p o0.001, Fig. 9). The difference between the two is most likely attributable to the stronger negative effect of convective air flow on the small, thin-walled tents than on the tightly sealed glass house. The performance of four, first instar tents, from which the caterpillars had been removed, measured under field conditions, confirms the results of these laboratory tests showing that the interior of empty tents warms well above ambient (Fig. 10).
3.2.4. Comparison of temperature gain of tent caterpillar nests to nests of different design The performance of the tents of third instar M. americanum is compared to that of the nests of two other species in Fig. 12. When exposed to an IR light source in the laboratory, the nests of the tent caterpillar rose much more precipitously and achieved significantly higher maximum temperatures (26.972.3 1C) than the nests of E. socialis (15.171.2 1C) or E. psidii (10.7 71.0 1C, Kruskal–Wallace Test, H¼14.95 df ¼2 po0.001). Although the nests of E. socialis achieved higher temperatures than those of E. psidii at all measurement points, Tukey’s multiple comparison test indicated that there was no significant difference in the maximum temperatures they achieved (p 40.05).
4. Discussion 3.2.3. Temperature gain of fully formed third-instar tents vs glass house in still and moving air In contrast to the performance of the tents of first–second instar caterpillars, the maximum average temperature achieved by the empty tents of third instar caterpillars in still air (26.270.72 1C), was significantly greater than that of the glass house (22.1 1C, OneSample t-test, t¼5.65, p¼0.005, Fig. 11). However, when the structures were subjected to air moving at approximately 8 km/h both the tents and the glass house achieved lower maximum temperatures (17.370.87 1C and 18.3 1C) which were not significant different from each other (One-Sample t-test, t¼ 1.26. p¼0.27). The greater average temperature drop for the tents (34%) than for the glass house ( 17%) in moving air can be attributed to greater convective heat loss in the former.
Our study shows that the small tents of M. americanum constructed during the first several stadia of larval life effectively facilitate larval thermoregulation. On most of our study days, the tents warmed to temperatures well above the threshold for digestion by 1000 h. Daily temperature excesses of most tents measured in degree-minutes above the threshold for growth exceeded ambient excesses calculated in the same manner by a factor of approximately five, the same value previously calculated by Knapp and Casey (1986) for the basking later instars. Under permissive field conditions, tent caterpillars forage at dusk, at dawn, and in the mid-afternoon (Fitzgerald et al., 1989) packing their foreguts with leaves. In the early spring, the caterpillars are likely to be too cold to fully process food collected during either their dusk or dawn forays, and their ability to
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Fig. 7. Degree-minutes per day in excess of 15 1C for three tents of M. americanum (grey) monitored in 2008 and the corresponding ambient excess.
elevate their Tb’s after sunrise by basking on or in the tent is essential to their growth and development. Prolonged basking at elevated Tb’s also assures that the foreguts of the caterpillars are fully empty at the start of their afternoon foray, maximizing the amount of food that can be collected and subsequently processed at the milder temperatures likely to occur in the afternoon. Past studies of themoregulation in lasiocampid caterpillars have been based largely on measurements taken within the mass of caterpillars basking in or on the tent (Knapp and Casey, 1986; Ruf and Fiedler, 2002). These investigators reported that the large tents of maturing colonies, devoid of the thermal mass afforded by the aggregated caterpillars, had little ability to warm above ambient. Small tents, however, enclose host tree branches to a much greater extent on a per unit volume basis than larger tents (Fig. 1) and the dark colored branches readily absorb and emit captured heat. As tents are expanded, the thermal storage afforded by enclosed branches decreases relative to small tents
not only because of their greater volume but also because the branches are shielded from the sun by a greater number of silk layers. As Ruf and Fiedler (2002) observed, the silk layers of the tent are only semi-trasparent to short wavelengths and their study indicated that even a thin layer of tent silk blocks a significant fraction of the incoming radiation. Both Knapp and Casey (1986) and Ruf and Fiedler (2002) reported that when devoid of caterpillars, large, irradiated tents warmed to only 2–5 1C above ambient. The differing results of our study, showing that tents devoid of caterpillars had much greater temperature gains over ambient, may reflect in part the relative importance of encased, non-caterpillar thermal mass. This does not explain, however, why Knapp and Casey (1986) also reported that areas of the small tents of early instar tent caterpillars only a centimeter or so distant from the caterpillar mass had temperatures that were not significantly different from ambient. Moreover, the results of a study by Joos et al. (1988) stand in marked
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Fig. 8. Mean temperature of nine tents (black circles) and nine caterpillar models (triangles) of M. americanum irradiated with an infrared light source.
Fig. 9. Performance of 11 empty tents of first to second instar M. americanum (open circles) and a glass house in still air under laboratory conditions.
disagreement with these earlier reports. Their study showed temperature excesses (Tb–Ta) as great as 23 1C at the center of an empty, full-sized tent. Two undocumented variables may account for these discrepancies. None of the investigators reported wind velocity at the time their measurements were made nor did they note the depth within the tent at which their measurements were made. As shown in this study, even a slight breezes strips a tent of heat and the effect might be even more
marked near the surface of larger tents whose internal, noncaterpillar thermal mass may have less of a buffering effect than that of small tents. Rehnberg (2002) also document the profound negative affects of convective currents on the ability of the irradiated nests of Hyphantria cunea to retain heat. Ruf and Fiedler (2002) performed photospectronic studies showing that the tent silk of E. lanestris effectively blocked incoming light such that less than 4% of the incident radiant energy penetrated to the deepest layers of tents. They thus took issue with the observations of Joos et al. (1988) that the tents function as miniature glass-houses since the latter, in contrast to the walls of the tent, are highly transparent to short wave radiation. They also stated that glass-houses differ from tents in that glass blocks infrared radiation, trapping and preventing the escape of heat. Nonetheless, our empirical studies comparing third instar tents to a miniature glass-house showed that their performance exceeded that of a glass house in still air (Fig. 11). In still air, when the radiation source was removed, the loss of heat from the glass model occurred as precipitously as loss from the tent, indicating that any trapping effect that the glass might have on infrared radiation gave it no advantage over the tent. While the loss of heat from the tent can be largely attributable to convective currents, heat loss from the glass house can be attributable to conduction across the glass since the house was impervious to convective losses. Thus, the ability of the glass house to retain heat would be expected to vary depending on the thickness of the glass. In the absence of a radiant heat source, the body temperatures of aggregated social caterpillars may be several degrees centigrade above ambient temperature. This phenomenon was first reported by Mosebach-Pukowski (1937) in Vanessa caterpillars. Subsequently, Breuer and Devkota (1990) noted that the shelter of the pine processionary caterpillar Thaumetopoea pityocampa rose 2–3 1C when occupied by the caterpillars and cooled down when they left the structure to feed. Recently, Ruf and Fiedler (2000) made careful measurements that showed that when the caterpillars of E. lanestris aggregate in their tent, the internal temperature of the structure exceeded ambient temperature by as much as 6.7 1C, though the average temperature gain of 2–3 1C was in line with that reported by previous investigators for other species. The thermal gains appear attributable to the trapping of the metabolic heat generated by the caterpillars as they process food. As Ruf and Fiedler (2000) noted, even the small temperature gains attributable to the metabolic heat generated by aggregated caterpillars may facilitate growth but as yet there are no data from field populations of any species that bear on this possibility. The thermal performance of the nests of only a small number of species of lepidopterous caterpillars has been previously assessed. Studies have been conducted on the nests of H. cunea (Rehnberg, 2002, 2006), E. lanestris (Ruf and Fiedler, 2002), T. pityocampa (Breuer et al., 1989; Breuer and Devkota, 1990; Fitzgerald et al., 2003) and E. socialis (Fitzgerald and Underwood, 2000), all showing that the nests experience varying degrees of temperature gain when irradiated. The nests of these species, and those observed in the present study, can be sorted into three categories based on their overt structure. (1) The nests of M. americanum, E. lanestris and H. cunea are thinly spun structures consisting of definitive layers of silk which in the former two species alternate in a regular way with air-filled spaces. (2) Those of T. pityocampa, and E. psidii are dense, with a mop-like arrangement of their silk having no definitive internal structure. (3) That of E. socialis is unique in consisting of an external shell of densely woven silk enclosing a largely hollow internal space that contains branches and the resting caterpillars. The results of previous studies of caterpillars whose nests are of the first category and data from the present study (Fig. 12) show that they warm
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Fig. 10. Temperature gains of four empty tents of first instar M. americanum (filled circles) exposed outdoors to the morning sun on different days and corresponding ambient temperatures (open circles). (A) data for two tents, (B) data for one tent at the center (grey circles) and one-cm below the surface (black circles). Arrows in (B) and (C) indicate time when the tents were shaded from the sun.
quickly when exposed to sunlight and reach maximum temperatures far in excess of ambient. Indeed, the temperature of these nests may warm to an extent that renders them uninhabitable. When this occurs, the caterpillars of Malacosoma and Eriogaster evacuate the structures and may hang by their prolegs from the shaded back side, cooling their bodies by both minimizing contact with the surface of the tent and maximizing convective heat loss to the surrounding air (Joos et al., 1988; Fitzgerald, 1995; Ruf and Fiedler, 2002). Larvae of the fall webworm are not known to behave in this manner but move to cooler areas of their expansive nests to avoid intense solar radiation during the hottest part of the day (personal observations). The nests of caterpillars belonging to the second category are also capable of heating to well above ambient on hot, cloudless days under prolonged exposure to sunlight (Fitzgerald et al., 2003) but, as shown in Fig. 12, are slower to warm and do not reach temperatures as great as those of category 1 nests under identical levels of irradiation. This is the case because the
structures consist of densely packed silk which more effectively blocks solar radiation than the loosely packed silk of the nests in the first category. The single nest in the third category, that of E. socialis, is also capable of warming well above ambient after exposure to sunlight (Fitzgerald and Underwood, 2000) in its native habitat. But the extremely dense and brilliantly white outer shell of silk is an effective barrier to sunlight. The nests used in this study were collected at approximately 2600 m and 24 degree N latitude and it is likely that their structure is adapted to deal with the higher solar radiation that occurs at high altitude in this southerly habitat. Both E. socialis, E. psidii, and T. pityocampa forage only at night and their nests form secure retreats during the heat of the day because they do not warm to the extent that would require their evacuation (Fitzgerald and Underwood, 2000) list—please make the list complete or remove the reference from the text: ‘‘Fitzgerald and Underwood (2000)’’. –>; Fitzgerald et al., 2003). The palatability of the leaves of the host trees of M. americanum decline rapidly (Fitzgerald, 1995) and it may be that
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Acknowledgments The U. S. Department of Agriculture APHIS issued permits to import the nests of E. socialis (951340) and E. psidii (P526P-0900995). Thanks are extended to Alfonso Pescador-Rubio for collecting the nests of E. psidii used in this study and to Daniel Davis for his helping in collecting data. Merle Canfield and Haim Bar provided assistance with the statistical analysis of the data.
References
Fig. 11. Performance of five empty tents of third instar M. americanum (black circles) and a glass house (open circles) in still air under laboratory conditions.
Fig. 12. Performance of empty tents of third instar M. americanum (black circles), Eucheira socialis (open circles) and E. psidii (black triangles) in still air under laboratory conditions.
the caterpillar sacrifices the security afforded by a structure that never requires evacuation for the speed in growth afforded by one that heats rapidly to temperatures that facilitate digestion and maximize the rate of larval development.
Blackman, M.W., 1918. Apple tent caterpillar. J. Econ. Entomol. 11, 432–433. Breuer, M., Devkota, B., 1990. Studies on the importance of nest temperature of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae). J. Appl. Entomol. 109, 331–335. Breuer, M., Devotka, B., Douma-Petridou, E., Koutsaftikis, A., Schmidt, G.H., 1989. Studies on the exposition and temperature of nests of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae) in Greece. J. Appl. Entomol. 107, 370–375. Casey, T.M., Joos, B., Fitzgerald, T.D., Yurlina, M.E., Young, P.A., 1988. Synchronized foraging, thermoregulation, and growth of eastern tent caterpillars in relation to microclimate. Physiol. Zool. 61, 372–377. Fitzgerald, T.D., 1993. Sociality in caterpillars. In: Stamp, N.E., Casey, T.M. (Eds.), Caterpillars: Ecological and Evolutionary Constraints on Foraging. Chapman and Hall, New York, pp. 372–403. Fitzgerald, T.D., 1995. The Tent Caterpillars. Cornell University Press, Ithaca, NY. Fitzgerald, T.D., Casey, T.M., Joos, B., 1989. Daily foraging schedule of field colonies of the eastern tent caterpillar Malacosoma americanum. Oecologia 76, 574–578. Fitzgerald, T.D., Clark, K., Vanderpool, R., Phillips, C., 1991. Leaf shelter-building caterpillars harness forces generated by axial retraction of stretched and wetted silk. J. Insect Behav. 4, 21–32. Fitzgerald, T.D., Panades, I., Blas, X., 2003. Mid-winter foraging of colonies of the pine processionary caterpillar Thaumetopoea pityocampa schiff. (Thaumetopoeidae). J. Lepidop. Soc. 57, 161–167. Fitzgerald, T.D., Underwood, D.L., 2000. Winter foraging patterns and voluntary hypothermia in the social caterpillar Eucheira socialis. Ecol. Entomol. 25, 1–10. Fitzgerald, T.D., Willer, D.E., 1983. Tent building behavior of the eastern tent caterpillar Malacosoma americanum (Lepidoptera: Lasiocampidae). J. Kansas Entomol. Soc. 56, 20–31. Hodson, A.C., 1941. An ecological study of the forest tent caterpillar, Malacosoma disstria Hbn., in Northern Minnesota. U. Minn. Agric. Expt. Sta. Bull. 148, 1–55. Ives, W.G.H., 1973. Heat units and outbreaks of the forest tent caterpillar, Malacosoma disstria (Lepidoptera: Lasiocampidae). Can. Ent. 105, 529–543. Joos, B., Casey, T.M., Fitzgerald, T.D., Buttemer, W.A., 1988. Roles of the tent in behavioral thermoregulation of eastern tent caterpillars. Ecology 69, 2004–2011. Knapp, R., Casey, T.M., 1986. Thermal ecology, behavior, and growth of gypsy moth and eastern tent caterpillars. Ecology 67, 598–608. ¨ Mosebach-Pukowski, E., 1937. Uber die Raupengesellschaften von Vanessa io und ¨ kol. Tiere. 33, 358–380. Vanessa urticae. Z. Morphol. O Rehnberg, B.G., 2002. Heat retention by webs of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae): infrared warming and forced convective cooling. J. Therm. Biol. 27, 525–530. Rehnberg, B.G., 2006. Temperature profiles inside webs of the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae): influence of weather, compass orientation, and time of day. J. Therm. Biol. 31, 274–279. Ruf, C., Fiedler, K., 2000. Thermal gains through collective metabolic heat production in social caterpillars of Eriogaster lanestris. Naturwissenschaften 87, 193–196. Ruf, C., Fiedler, K., 2002. Tent-based thermoregulation in social caterpillars of Eriogaster lanestris (Lepidoptera: Lasiocampidae): behavioral mechanisms and features of the tent. J. Therm. Biol. 27, 493–501. Ruf, C., Fiedler, K., 2005. Colony survivorship of social caterpillars in the field: a case study of the small eggar moth (Lepidoptera: Lasiocampidae). J. Res. Lepidop. 38, 15–25. Stehr, F.W., Cook, E.F., 1968. A revision of the genus Malacosoma Hubner in North America (Lepidoptera: Lasiocampidae): systematics, biology, immatures, and parasites. U.S. Nat. Mus. Bull., 276.
Contents lists available at SciVerse ScienceDirect
Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio
Thermal properties of the tent of early instar colonies of the eastern tent caterpillar, Malacosoma americanum (Lepidoptera: Lasiocampidae) Terrence D. Fitzgerald n, Steven Miller, Michael Smith Department of Biological Sciences, State University of New York at Cortland, Cortland, NY 13045, USA
a r t i c l e i n f o
abstract
Article history: Received 12 March 2012 Accepted 30 July 2012 Available online 11 August 2012
The extent to which the small tents of the early instars of Malacosoma americanum warmed when irradiated by sunlight was investigated by continuous electronic monitoring of field colonies for 137 colony-days. Tent temperatures exceeded the threshold for larval growth of 15 1C on 88–96% of the study days, exceeding in degree-minutes the ambient excess-over-threshold by a factor of approximately five. In still air, tents constructed by third instar caterpillars achieved greater temperature excesses over ambient than did a model of a tightly sealed glass house, but smaller tents and tents exposed to simulated wind did not perform as well. Tents of M. americanum warmed more rapidly and to a high temperature than silk nests of markedly different design constructed by other species. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Thermoregulation Social caterpillars Silk Basking
1. Introduction The communal silk nests of social caterpillars are multifunctional structures. They serve to shield caterpillars from predators and parasitoids, enclose moist internal microclimates conducive to molting, provide resting areas from which intermittent forays in search of food are launched, act in some species as communication centers from which nest mates are recruited to food finds, and facilitate en masse thermoregulation (Fitzgerald, 1993 and references therein; Fitzgerald, 1995; Rehnberg, 2002, 2006; Ruf and Fiedler, 2002). It is the latter function that has drawn the attention of most researchers. The nests of different species of caterpillars vary markedly in size, shape, and in the density of their walls, but all show marked temperature gains when exposed to solar radiation (Knapp and Casey, 1986; Joos et al., 1988; Casey et al., 1988; Fitzgerald and Underwood, 2000; Ruf and Fiedler, 2002; Fitzgerald et al., 2003; Rehnberg, 2002, 2006). The best studied of these structures are those of the lasiocampid caterpillars, the nests of which are referred to as tents. Lasiocampids in the genera Malacosoma and Eriogaster construct their tents by laying down new strands of silk over existing tent walls during intermittent en masse spinning bouts. The strands are stretched slightly before they are attached and their subsequent axial retraction causes sheets of newly spun silk to tighten and lift from subjacent silk surfaces (Fitzgerald and Willer, 1983; Fitzgerald et al., 1991). Successive episodes of spaced spinning bouts result in the creation of a structure that consists
n
Corresponding author. Tel.: þ1 607 756 4504; fax: þ1 607 753 2927. E-mail address: fi[email protected] (T.D. Fitzgerald).
0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2012.07.010
of multiple layers of silk separated by air-filled gaps. When exposed to solar radiation, the layered structure of the tent creates a thermally heterogeneous environment within which the caterpillars thermo regulate by moving between warmer and cooler layers (Casey et al., 1988; Ruf and Fiedler, 2002). Eastern tent caterpillars (M. americanum) are widely distributed throughout eastern North America (Stehr and Cook, 1968). They typically eclose from their eggs in mid-April and initiate the construction of a tent in the branches of the host tree shortly thereafter (Fitzgerald, 1995). Basking on or in the tent is essential to the growth of the caterpillars because ambient air temperatures in the early spring are often too low to allow the caterpillars to digest their meals. Both the forest tent caterpillar M. disstria (Hodson, 1941; Ives, 1973) and M. americanum (Knapp and Casey, 1986; Casey et al., 1988) grow little if at all when their Tb’s (body temperatures) fall below approximately 15 1C. On cold mornings, eastern tent caterpillars are commonly found clustered just under the surface of their tent on the side that faces the morning sun. Their dark bodies absorb solar radiation and the walls of the tent limit convective heat loss, resulting in significant gains in Tb over Ta (air temperature). This enables the caterpillars to process food collected during their overnight forays (Knapp and Casey, 1986; Casey et al., 1988; Joos et al., 1988; Fitzgerald, 1995). Although spot measurements of clusters of early instar eastern tent caterpillars by Knapp and Casey (1986) showed that the small caterpillars had Tb’s in excess of Ta, all previous studies of the ability of lasiocampid tents to gain heat when irradiated have focused on the large, many-layered structures of the maturing caterpillars (Casey et al., 1988; Joos et al., 1988; Ruf and Fiedler, 2002). Heat trapping by the relatively thin and airy tents inhabited by the caterpillars during their first several stadia, however,
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is likely to be even more important to the growth and survival of the caterpillars. This is the case because the caterpillars are among the earliest to emerge in the spring and during the first few weeks of their lives ambient temperatures commonly fall below freezing. During early spring, basking is essential not only to growth but to survival as well and whole populations of M. americanum have perished during their first stadium when persistent cloudy and cold weather prevented the caterpillars from processing food (Blackman, 1918; personal observation). Ruf and Fiedler (2005) also determined that the inability of the caterpillars of Eriogaster lanestris to build an initial tent or their failure to maintain an existing tent were the most important factors affecting colony survival. We report here the results of a study of the small tents of first to third instar eastern tent caterpillars undertaken to determine their effectiveness in creating a thermal environment which fosters the growth and development of the caterpillars.
2. Materials and methods 2.1. Field study site and host species Field studies were conducted at the State University of New York at Cortland on the Hoxie Gorge campus (42 degree 32 min 48 s N, 76 degree 4 min 32 s W). The study site, at an elevation of approximately 425 m, consists of an old field succession containing numerous apple (Malus pumila) and cherry trees (Prunus serotina and Prunus. virginiana), ovipositional host species for the caterpillars. 2.2. Field studies A study to determine the extent to which the inhabited tents of the eastern tent caterpillar warmed when exposed to sunlight was conducted at the study site from April 20 to May 21, 2005. Tent caterpillars began to eclose on April 13 and small tents were evident by April 20. On the latter date, thermistor sensors 3.2 mm in diameter by 18 mm long attached to Hobo Stowaway temperature data loggers (Onset Computer Co., Bourne, Massachusetts, USA.) were inserted into each of two, naturally occurring tents, approximately 1 cm below their south-facing surfaces. As the tents grew in size, the sensors were moved to maintain this approximate position. Care was taken to minimize disruption of the tent silk during this process and new silk was soon added by the caterpillars, fully embedding the sensors in the new positions. The loggers were programmed to record temperature every 15 min. The caterpillars moved in an out of the compartments of the tents fitted with the sensors so the temperatures were recorded though the whole range of tent occupancy. An additional thermistor sensor was encased in an RS1 solar radiation shield (Onset Computer Co.) and situated near the tents to record ambient temperature. Loggers were downloaded to a shuttle every 48 h and the data compiled with Boxcar Pro software (Onset Computer Corporation). In 2008, three additional tents were monitored in the same manner at this same site. In 2008, eclosion occurred on April 21 and recording began when thermistors were placed in the tents on April 25. Recording continued uninterrupted until May 20. 2.3. Laboratory studies 2.3.1. Temperature gain in occupied tents A study was conducted in the laboratory to obtain measurements of temperature gain in occupied tents and isolated caterpillars when both were exposed to an infrared lamp. Nine tents
Fig. 1. Left to right: second instar tent of M. americanum, third instar tent of M. americanum, third instar nest of E. socialis, third instar nest of E. psidii.
constructed by second–third instar colonies of tent caterpillars (Fig. 1) were collected from the field and held overnight in a refrigerator at approximately 2 1C. To conduct the study, a tent was transferred to a walk-in cooler having an average ambient temperature of 6.970.19 1C (SE). A 30-gauge copper-constantan thermocouple connected to a BAT-12 thermometer (Sensortek, Inc., Clifton, New Jersey) was inserted approximately 1 cm below the light-facing surface of the tent which was situated 50 cm from the front surface of a 250 W heat lamp (Extralife IR Lamp LR 48263) and the temperature gain of the tent recorded over 15 min. Another thermocouple wire was inserted into a recently killed third instar caterpillar and placed in the path of the infrared light at the same distance as the tent to determine the ability of a solitary, exposed caterpillar to gain heat. IR heat lamps have been previously used in this manner to irradiate tents in studies conducted by Breuer and Devkota (1990), Fitzgerald and Underwood (2000), Rehnberg (2002), and Fitzgerald et al. (2003). Temperature readings from the irradiated tent and exposed caterpillars were taken at 30 s intervals for the first minute and at 1 min intervals thereafter for a total of 15 min. The cooler’s fan created weak air movement in the chamber throughout the study period causing a slight fluttering of loose silk strands at the tent surface.
2.3.2. Temperature gain in unoccupied tents and comparison with glass house Two previous studies reported that tents devoid of the thermal mass afforded by the enclosed caterpillars warmed little when exposed to sunlight (Knapp and Casey, 1986; Ruf and Fiedler, 2002) while another reported that the temperatures of empty tents rose significantly in sunlight (Joos et al., 1988). Moreover, Joos et al. (1988) reported that tents of M. americanum functioned like miniature glass houses while Ruf and Fiedler (2002) stated that this was not the case for tents of similar design constructed by E. lanestris. To further investigate these conflicting reports, the extent to which 11 tents of first–second instars, devoid of caterpillars, and a model of a glass house gained heat when exposed to an IR light source was investigated. The tents used in this study were collected from the field and were different tents than those used in the study outlined above. They were markedly smaller and had thinner silk walls than those of the third instars. In the laboratory, caterpillars were collected while feeding off the tents to evacuate them. Stragglers were manually removed from the tents. A thermocouple was inserted through a small hole drilled into a branch supporting a tent to gain access to the interior without tearing the fragile silk of the small structure.
T.D. Fitzgerald et al. / Journal of Thermal Biology 37 (2012) 615–624
The glass house was constructed with 0.15 mm thick glass and was box-shaped with a volume of approximately 303 cm, approximating that of an average experimental tent. Four sections of cherry branches, 4 cm-long 4–5 mm diameter were enclosed in the house to provide thermal mass similar to that enclosed by the tent. A thermocouple wire was suspended in the air at the center of the house. The house was tightly sealed with transparent tape on all edges. Temperature gain was recorded at 30 s intervals for the first minute, then at 1 min intervals for a total of 15 min. The IR source was then turned off and the cool-down of the structures recorded for an additional 10 min. For statistical analysis, the maximum temperatures achieved by each of the 11 tents were compared to the mean maximum temperature obtained by the glass house with a One-Sample t-test.
2.3.3. Temperature gain of fully formed third-instar tents vs glass house in still and moving air This glass house study detailed above was repeated with the larger, fully-formed tents of third instar colonies using a procedure identical to that detailed above except that the structures were exposed to the IR lamp for 30 min before cooling down. To obtain tents for this study, laboratory colonies of newly eclosed caterpillars were situated at the centers of wooden frames and allowed to construct their tents (Fig. 2). Food was provided at the ends of bridges that extended from the frames. Before the caterpillars initiated tent construction, thermocouples were attached to the center supports of the frames, following the procedure of Casey et al. (1988), such that they would be at the approximate centers of the fully constructed tents. The caterpillars were allowed to build tents until they reached the end of their third instar when they were removed from the tents as described above. A total of five tents were prepared in this manner. A larger glass house than used in the previous experiment was used in this study to more nearly approximate the size of the larger tents. The box shaped house was constructed with glass walls 2.4 mm thick and enclosed a volume of approximately 172 cm3. Four sections of cherry branches, 6 cm long 5–7 mm diameter were enclosed to add thermal mass. This study was also replicated using the identical procedure and the same tents except that a fan was employed through the duration of each of the 30 min trials to simulate the effect of an approximate 8 km/h wind on the thermodynamics of the structures. For both of these studies, each trial consisted of running one tent along side the glass house. For statistical analysis, the maximum temperature achieved by each of the five tents was compared to the mean
maximum temperature obtained by the glass house over the five runs with a One-Sample t-test. 2.3.4. Comparison of temperature gain of tent caterpillar nests to nests of different design The silk nests of caterpillars of different species vary markedly in size, shape, and density and would be expected to be adapted to perform differently when irradiated. However, there have been no previous attempts to compare the performance of these nests. Nor has there been an agreed upon standard procedure for assessing thermal performance that would allow for comparisons across space and time. A preliminary attempt at obtaining such comparative data was made during the present study. Using the procedure outlined above for assessing the performance of tents when irradiated in the laboratory, we compared the relative performance of nests constructed by M. americanum up to the end of the third instar, and nests of comparable volume constructed by Eucheria socialis (Pieridae) and the lasiocampid Eutachyptera psidii. All nests were devoid of caterpillars and the thermocouples were placed near the centers of the structures. Nests of these species were chosen because they are fundamentally different in overt form and construction (Fig. 1). The study was replicated with seven different field collected nests of each type, all devoid of caterpillars. 2.4. Data analysis Temperature data were graphed and analyzed with SigmaPlot, ProStat and SigmaStat software. Data were analyzed by t-tests, One-Sample t-tests or by One-Way ANOVA’s. If normality or equal variance considerations precluded a parametric test, a Kruskal– Wallis One Way ANOVA followed by a Tukey test for multiple comparisons was performed.
3. Results 3.1. Field studies In 2005 and 2008 ambient temperature exceeded the threshold for growth of 15 1C on 48% and 56% of the study days, respectively (Table 1). Temperature probes in tents exceeded the growth threshold on 87% of the days in 2005 and from 88% to 96% of the days in 2008. Ambient temperature probes took Table 1 Number of days during the study periods when ambient and tent temperatures exceeded the threshold for caterpillar growth of 15 1C, time between initial sunstrike and the achievement of threshold, and time relative to ambient to reach 15 1C. Means in each year followed by a different letter are significantly different po 0.05. Year and study duration (days) 2005 (31) Ambient Tent 1 2005 Tent 2 2005 2008 (25) Ambient Tent 1 Tent 2 Tent 3
Fig. 2. Tent constructed in the laboratory on a dowel frame by a colony of M. americanum caterpillars.
617
a
Number days Z 15 1C)
Mean7 SE minutes Mean7 SE minutes after 0700 h to achieve earlier than ambient to reach 15 1Ca 15 1C
15 27
3107 34a 184 734b
– 206 735
27
166 735b
221 738
14 24 23 22
3107 42a 161 725b 185 726b 158 740b
– 209 731 194 726 239 731
Data only for days when ambient temperature reached 15 1C.
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Fig. 3. Daily records of tent (grey) and ambient temperatures for two colonies of M. americanum monitored in 2005.
Fig. 4. Daily records of tent (grey) and ambient temperatures for three colonies of M. americanum monitored in 2008.
T.D. Fitzgerald et al. / Journal of Thermal Biology 37 (2012) 615–624
approximately 2 h to 2.5 h longer to reach the growth threshold than did temperature probes inserted into tents in both 2005 (ANOVA, F¼3.83, df¼2, p ¼0.0268) and 2008 (Kruskal–Wallis one way ANOVA, H¼12.06, df¼3, p ¼0.007). On those days when ambient temperatures reached 15 1C, (15 of the 31 study days in 2005 and 14 of the 25 study days in 2008) tent probes reached the growth threshold approximately 3–4 h sooner (Table 1). Although sunrise occurred at approximately 0545 h during the study periods, sunlight did not strike the tents until approximately 0700 h. Both ambient and tent temperatures typically achieved their daily maxima between 1300 h and 1400 h. Daily ambient and tent temperatures for tents monitored in 2005 and 2008 are shown in Figs. 3 and 4. On cloudless mornings, the temperatures of the irradiated tents rose precipitous (Fig. 5) with the greatest rate of change typically occurring between 0700 h and approximately 1000 h. During this period for all study days in 2005 and 2008, regardless of the extent of early morning cloud cover, the mean rate at which tents gained temperature greatly exceeded the rate of ambient temperature increase (Table 2, 2005: Kruskal–Wallace test, H¼24.7, df¼2. po 0.001; 2008: H¼9.1, df ¼3, p ¼0.03). The maximum rate of heat gain recorded during the whole of the study occurred during this 3 h interval on sunny days in mid-May in both 2005 and 2008. The maximum overall rate of change occurred on the morning of May 13, 2008. On that day the temperature of tent 1 at 1000 h was 42.9 1C greater than its temperature at 0700 h, an average rate of increase of 14.3 1C/h, exceeding at that time ambient temperature by 31.0 1C. The most precipitous rate of change recorded over any 1 h period was for tent 1 on May 14, 2005 between 0930 h and 1030 h (Fig. 5). During this period, the internal temperature of the tent increased at an average rate of 0.42 1C/min, a rate 8.4 times greater than that recorded for ambient temperature during this same period. The maximum temperature achieved by a tent during both study years occurred on May 6 and 13, 2008 when tent 1 reached 49.5 1C. Though the tents warm rapidly to high temperatures, they are poorly insulated against heat loss. Their internal temperatures are sustained above ambient only during the period of irradiation and decline rapidly to the ambient temperature as sunset approaches (Fig. 5). Table 3 and Figs. 6 and 7 compare the number of degreeminutes in excess of 15 1C registered by tent and ambient temperature probes for the whole of the 2005 and 2008 study periods. To calculate degree-minutes, the average temperature
619
Table 2 Rate of warming of ambient and tent probes between 0700 h and 1000 h. Means within the same year followed by different letters are significantly different (po 0.05). Study year 2005 Ambient Tent 1 Tent 2 2008 Ambient Tent 1 Tent 2 Tent 3
Number of days monitored
Mean7SE (1C/h)
31 28 31
1.87 0.2a 5.27 0.6b 4.97 0.5b
25 25 25 25
1.77 0.3a 4.47 0.7b 3.37 0.5b 3.97 0.6b
Table 3 Degree-minutes in excess of the threshold for growth of 15 1C for ambient and tent thermal probes. Means in each year followed by different letters are significantly different (p o0.05). Year
2005 Ambient Tent 1 Tent 2 2008 Ambient Tent 1 Tent 2 Tent 3
Days Mean 7SE degreemonitored minutes in excess of 15 1C/day
Total degree-minutes in excess of 15 1C for entire study periods
31 28 31
835.7 7 321.0a 4573 7 824b 4159 7 757b
26,465 123,478 128,918
26 26 26 26
727 7 253a 2597 7 534b 3555 7 635b 3699 7 700b
18,903 67,527 92,423 96,181
between two successive readings was calculated then multiplied by the number of minutes in the interval between readings to obtain degree-minutes. Only mean temperature values in excess of 15 1C were used in these calculations. For both years, daily and total degree-minutes in excess of the threshold value were significantly greater for tent than ambient probes (Table 3, 2005: Kruskal–Wallace Test, H¼ 22.8 df¼2, po0.001, 2008: H¼21.3, df¼3, p ¼ o0.001). Daily and total values for tents exceeded ambient values by a factor of approximately 5 with the exception of tent 1-2008, which exceed ambient values by a factor of approximately 3.5. The greatest excesses of tent over ambient in degree-minutes were registered on May 10, 2005 (for tents 1 and 2, 6429 and 7329 degree min, respectively) and on May 13, 2008 (for tents 1–3, 7775, 11577 and 9536 degree min, respectively). 3.2. Laboratory studies 3.2.1. Temperature gain in occupied tents Under laboratory conditions, when irradiated by an IR lamp, third instar tents containing caterpillars warmed rapidly, achieving a maximum average temperature in excess of ambient of 21.571.5 1C. Caterpillar models also warmed above ambient but to lesser extent than the tents, achieving a maximum average temperature in excess of ambient of 9.670.74 1C (t-test, t ¼14.42, df¼8, p o0.0001, Fig. 8).
Fig. 5. Five day record of the temperature of tent 1-2005 (black line) and ambient temperature. Rectangles indicate daylight hours between local sunrise and sunset.
3.2.2. Temperature gain in unoccupied tents and comparison with glass house Eleven unoccupied tents constructed by first to second instar caterpillars heated well above ambient in laboratory tests (Fig. 9) but the maximum average temperature achieved (14.970.65 1C)
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Fig. 6. Degree-minutes per day in excess of 15 1C for two tents of M. americanum (grey) monitored in 2005 and the corresponding ambient excess. Temperature data were not collected on days indicated by (x) due to recorder malfunction.
was approximately 7 1C less than the maximum temperature achieved by the larger, occupied tents of third instar caterpillars used in the study reported above. Both the denser walls of the larger tents and their greater thermal mass, due to the presence of caterpillars, likely contributed to their achieving higher final temperatures. The average maximum temperature achieved by the 11 tents was also significantly less than that of the glass house (19.0 1C, One-Sample t-test, t ¼6.24, p o0.001, Fig. 9). The difference between the two is most likely attributable to the stronger negative effect of convective air flow on the small, thin-walled tents than on the tightly sealed glass house. The performance of four, first instar tents, from which the caterpillars had been removed, measured under field conditions, confirms the results of these laboratory tests showing that the interior of empty tents warms well above ambient (Fig. 10).
3.2.4. Comparison of temperature gain of tent caterpillar nests to nests of different design The performance of the tents of third instar M. americanum is compared to that of the nests of two other species in Fig. 12. When exposed to an IR light source in the laboratory, the nests of the tent caterpillar rose much more precipitously and achieved significantly higher maximum temperatures (26.972.3 1C) than the nests of E. socialis (15.171.2 1C) or E. psidii (10.7 71.0 1C, Kruskal–Wallace Test, H¼14.95 df ¼2 po0.001). Although the nests of E. socialis achieved higher temperatures than those of E. psidii at all measurement points, Tukey’s multiple comparison test indicated that there was no significant difference in the maximum temperatures they achieved (p 40.05).
4. Discussion 3.2.3. Temperature gain of fully formed third-instar tents vs glass house in still and moving air In contrast to the performance of the tents of first–second instar caterpillars, the maximum average temperature achieved by the empty tents of third instar caterpillars in still air (26.270.72 1C), was significantly greater than that of the glass house (22.1 1C, OneSample t-test, t¼5.65, p¼0.005, Fig. 11). However, when the structures were subjected to air moving at approximately 8 km/h both the tents and the glass house achieved lower maximum temperatures (17.370.87 1C and 18.3 1C) which were not significant different from each other (One-Sample t-test, t¼ 1.26. p¼0.27). The greater average temperature drop for the tents (34%) than for the glass house ( 17%) in moving air can be attributed to greater convective heat loss in the former.
Our study shows that the small tents of M. americanum constructed during the first several stadia of larval life effectively facilitate larval thermoregulation. On most of our study days, the tents warmed to temperatures well above the threshold for digestion by 1000 h. Daily temperature excesses of most tents measured in degree-minutes above the threshold for growth exceeded ambient excesses calculated in the same manner by a factor of approximately five, the same value previously calculated by Knapp and Casey (1986) for the basking later instars. Under permissive field conditions, tent caterpillars forage at dusk, at dawn, and in the mid-afternoon (Fitzgerald et al., 1989) packing their foreguts with leaves. In the early spring, the caterpillars are likely to be too cold to fully process food collected during either their dusk or dawn forays, and their ability to
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Fig. 7. Degree-minutes per day in excess of 15 1C for three tents of M. americanum (grey) monitored in 2008 and the corresponding ambient excess.
elevate their Tb’s after sunrise by basking on or in the tent is essential to their growth and development. Prolonged basking at elevated Tb’s also assures that the foreguts of the caterpillars are fully empty at the start of their afternoon foray, maximizing the amount of food that can be collected and subsequently processed at the milder temperatures likely to occur in the afternoon. Past studies of themoregulation in lasiocampid caterpillars have been based largely on measurements taken within the mass of caterpillars basking in or on the tent (Knapp and Casey, 1986; Ruf and Fiedler, 2002). These investigators reported that the large tents of maturing colonies, devoid of the thermal mass afforded by the aggregated caterpillars, had little ability to warm above ambient. Small tents, however, enclose host tree branches to a much greater extent on a per unit volume basis than larger tents (Fig. 1) and the dark colored branches readily absorb and emit captured heat. As tents are expanded, the thermal storage afforded by enclosed branches decreases relative to small tents
not only because of their greater volume but also because the branches are shielded from the sun by a greater number of silk layers. As Ruf and Fiedler (2002) observed, the silk layers of the tent are only semi-trasparent to short wavelengths and their study indicated that even a thin layer of tent silk blocks a significant fraction of the incoming radiation. Both Knapp and Casey (1986) and Ruf and Fiedler (2002) reported that when devoid of caterpillars, large, irradiated tents warmed to only 2–5 1C above ambient. The differing results of our study, showing that tents devoid of caterpillars had much greater temperature gains over ambient, may reflect in part the relative importance of encased, non-caterpillar thermal mass. This does not explain, however, why Knapp and Casey (1986) also reported that areas of the small tents of early instar tent caterpillars only a centimeter or so distant from the caterpillar mass had temperatures that were not significantly different from ambient. Moreover, the results of a study by Joos et al. (1988) stand in marked
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Fig. 8. Mean temperature of nine tents (black circles) and nine caterpillar models (triangles) of M. americanum irradiated with an infrared light source.
Fig. 9. Performance of 11 empty tents of first to second instar M. americanum (open circles) and a glass house in still air under laboratory conditions.
disagreement with these earlier reports. Their study showed temperature excesses (Tb–Ta) as great as 23 1C at the center of an empty, full-sized tent. Two undocumented variables may account for these discrepancies. None of the investigators reported wind velocity at the time their measurements were made nor did they note the depth within the tent at which their measurements were made. As shown in this study, even a slight breezes strips a tent of heat and the effect might be even more
marked near the surface of larger tents whose internal, noncaterpillar thermal mass may have less of a buffering effect than that of small tents. Rehnberg (2002) also document the profound negative affects of convective currents on the ability of the irradiated nests of Hyphantria cunea to retain heat. Ruf and Fiedler (2002) performed photospectronic studies showing that the tent silk of E. lanestris effectively blocked incoming light such that less than 4% of the incident radiant energy penetrated to the deepest layers of tents. They thus took issue with the observations of Joos et al. (1988) that the tents function as miniature glass-houses since the latter, in contrast to the walls of the tent, are highly transparent to short wave radiation. They also stated that glass-houses differ from tents in that glass blocks infrared radiation, trapping and preventing the escape of heat. Nonetheless, our empirical studies comparing third instar tents to a miniature glass-house showed that their performance exceeded that of a glass house in still air (Fig. 11). In still air, when the radiation source was removed, the loss of heat from the glass model occurred as precipitously as loss from the tent, indicating that any trapping effect that the glass might have on infrared radiation gave it no advantage over the tent. While the loss of heat from the tent can be largely attributable to convective currents, heat loss from the glass house can be attributable to conduction across the glass since the house was impervious to convective losses. Thus, the ability of the glass house to retain heat would be expected to vary depending on the thickness of the glass. In the absence of a radiant heat source, the body temperatures of aggregated social caterpillars may be several degrees centigrade above ambient temperature. This phenomenon was first reported by Mosebach-Pukowski (1937) in Vanessa caterpillars. Subsequently, Breuer and Devkota (1990) noted that the shelter of the pine processionary caterpillar Thaumetopoea pityocampa rose 2–3 1C when occupied by the caterpillars and cooled down when they left the structure to feed. Recently, Ruf and Fiedler (2000) made careful measurements that showed that when the caterpillars of E. lanestris aggregate in their tent, the internal temperature of the structure exceeded ambient temperature by as much as 6.7 1C, though the average temperature gain of 2–3 1C was in line with that reported by previous investigators for other species. The thermal gains appear attributable to the trapping of the metabolic heat generated by the caterpillars as they process food. As Ruf and Fiedler (2000) noted, even the small temperature gains attributable to the metabolic heat generated by aggregated caterpillars may facilitate growth but as yet there are no data from field populations of any species that bear on this possibility. The thermal performance of the nests of only a small number of species of lepidopterous caterpillars has been previously assessed. Studies have been conducted on the nests of H. cunea (Rehnberg, 2002, 2006), E. lanestris (Ruf and Fiedler, 2002), T. pityocampa (Breuer et al., 1989; Breuer and Devkota, 1990; Fitzgerald et al., 2003) and E. socialis (Fitzgerald and Underwood, 2000), all showing that the nests experience varying degrees of temperature gain when irradiated. The nests of these species, and those observed in the present study, can be sorted into three categories based on their overt structure. (1) The nests of M. americanum, E. lanestris and H. cunea are thinly spun structures consisting of definitive layers of silk which in the former two species alternate in a regular way with air-filled spaces. (2) Those of T. pityocampa, and E. psidii are dense, with a mop-like arrangement of their silk having no definitive internal structure. (3) That of E. socialis is unique in consisting of an external shell of densely woven silk enclosing a largely hollow internal space that contains branches and the resting caterpillars. The results of previous studies of caterpillars whose nests are of the first category and data from the present study (Fig. 12) show that they warm
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Fig. 10. Temperature gains of four empty tents of first instar M. americanum (filled circles) exposed outdoors to the morning sun on different days and corresponding ambient temperatures (open circles). (A) data for two tents, (B) data for one tent at the center (grey circles) and one-cm below the surface (black circles). Arrows in (B) and (C) indicate time when the tents were shaded from the sun.
quickly when exposed to sunlight and reach maximum temperatures far in excess of ambient. Indeed, the temperature of these nests may warm to an extent that renders them uninhabitable. When this occurs, the caterpillars of Malacosoma and Eriogaster evacuate the structures and may hang by their prolegs from the shaded back side, cooling their bodies by both minimizing contact with the surface of the tent and maximizing convective heat loss to the surrounding air (Joos et al., 1988; Fitzgerald, 1995; Ruf and Fiedler, 2002). Larvae of the fall webworm are not known to behave in this manner but move to cooler areas of their expansive nests to avoid intense solar radiation during the hottest part of the day (personal observations). The nests of caterpillars belonging to the second category are also capable of heating to well above ambient on hot, cloudless days under prolonged exposure to sunlight (Fitzgerald et al., 2003) but, as shown in Fig. 12, are slower to warm and do not reach temperatures as great as those of category 1 nests under identical levels of irradiation. This is the case because the
structures consist of densely packed silk which more effectively blocks solar radiation than the loosely packed silk of the nests in the first category. The single nest in the third category, that of E. socialis, is also capable of warming well above ambient after exposure to sunlight (Fitzgerald and Underwood, 2000) in its native habitat. But the extremely dense and brilliantly white outer shell of silk is an effective barrier to sunlight. The nests used in this study were collected at approximately 2600 m and 24 degree N latitude and it is likely that their structure is adapted to deal with the higher solar radiation that occurs at high altitude in this southerly habitat. Both E. socialis, E. psidii, and T. pityocampa forage only at night and their nests form secure retreats during the heat of the day because they do not warm to the extent that would require their evacuation (Fitzgerald and Underwood, 2000) list—please make the list complete or remove the reference from the text: ‘‘Fitzgerald and Underwood (2000)’’. –>; Fitzgerald et al., 2003). The palatability of the leaves of the host trees of M. americanum decline rapidly (Fitzgerald, 1995) and it may be that
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Acknowledgments The U. S. Department of Agriculture APHIS issued permits to import the nests of E. socialis (951340) and E. psidii (P526P-0900995). Thanks are extended to Alfonso Pescador-Rubio for collecting the nests of E. psidii used in this study and to Daniel Davis for his helping in collecting data. Merle Canfield and Haim Bar provided assistance with the statistical analysis of the data.
References
Fig. 11. Performance of five empty tents of third instar M. americanum (black circles) and a glass house (open circles) in still air under laboratory conditions.
Fig. 12. Performance of empty tents of third instar M. americanum (black circles), Eucheira socialis (open circles) and E. psidii (black triangles) in still air under laboratory conditions.
the caterpillar sacrifices the security afforded by a structure that never requires evacuation for the speed in growth afforded by one that heats rapidly to temperatures that facilitate digestion and maximize the rate of larval development.
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