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On the significance of structural vegetation elements for caterpillar thermoregulation in two peat bog butterflies: Boloria eunomia and B. aquilonaris
Journal of Thermal Biology 36 (2011) 173–180
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On the significance of structural vegetation elements for caterpillar thermoregulation in two peat bog butterflies: Boloria eunomia and B. aquilonaris Camille Turlure a,b,n, Viktoriia Radchuk a, Michel Baguette b,c, Hans Van Dyck a, Nicolas Schtickzelle a a
Universite´ catholique de Louvain, Earth and Life Institute, Biodiversity Research Centre, Place Croix du Sud, 4 – B-1348 Louvain-la-Neuve, Belgium Muse´um National d’Histoire Naturelle, UMR CNRS-MNHN 7204, Avenue du petit chˆ ateau, 1 - F-91800 Brunoy, France c ´cologie expe´rimentale du CNRS (Moulis), Route du CNRS, 4 - F-09200 Saint Girons, France CNRS USR 2936 Station d’e b
a r t i c l e i n f o
abstract
Article history: Received 18 August 2010 Accepted 3 February 2011 Available online 25 February 2011
Purpose: Temperature profoundly impacts on distribution and habitat-use of organisms. The development of ectothermous caterpillars does not depend on host plant quality only, but also on the availability of suitable thermal conditions. Selection for thermally favorable microclimates (i.e. behavioral thermoregulation) is a primary mechanism of temperature control, and caterpillars can be either (or alternately) temperature conformers (i.e. passively adopting ambient temperature conditions) or thermoregulators (i.e. able to some extent to elevate or decrease their body temperature relative to ambient temperature). Here, we addressed the functional significance of different structural vegetation elements for the behavioral thermoregulation by caterpillars of two butterfly species. Results: Weather conditions influenced the caterpillar detection probability within host plant patches, indicating that caterpillars can hide and use suitable microclimates provided by vegetation structures to cope with weather variations. This is why we (1) evaluated the heterogeneity in temperature conditions provided by these structures, (2) quantified the influence of ambient temperature and light intensity on caterpillar body temperature, and (3) tested how position on structure, substrate color and exposition influenced caterpillar body temperature. As expected, vegetation structures provided heterogeneous temperature and sun exposition conditions, while caterpillar body temperature was dependent on ambient temperature and light intensity. But body temperature was additionally influenced by the position on vegetation structures, substrate color and exposition. Conclusions: These results suggest that there is no unique and fixed structure in the vegetation subsuming the best thermal conditions for caterpillars. We argue that a better understanding of the thermal properties of vegetation structures is essential for correctly understanding caterpillar habitatuse and the behavioral mechanisms driving their body thermoregulation. Conceptually this means that thermal conditions should be included in the definition of a species’ functional habitat. Practically this may influence the choice of appropriate habitat management for species of conservation concern. & 2011 Elsevier Ltd. All rights reserved.
Keywords: Behavioral thermoregulation Climate change Ectothermous organisms Habitat management Microclimatic conditions Vegetation structure
1. Introduction All organisms have basic requirements for their environment (food, physical conditions) to successfully complete their development, including survival and reproduction. However, the precise identification of these basic requirements often remains far from self-evident. The higher the heterogeneity and variation of conditions and resources in their close environment, the more opportunities are offered to the organisms to find the resources they need under variable environmental conditions. For instance n Corresponding author at: Universite´ catholique de Louvain, Earth and Life Institute, Biodiversity Research Centre, Place Croix du Sud, 4 – B-1348 Louvain-la-Neuve, Belgium. Tel.: + 32 477 23 09 61; fax: +32 10 47 34 90. E-mail address: [email protected] (C. Turlure).
0306-4565/$ - see front matter & 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2011.02.001
in butterflies, caterpillar development usually depends on the quality and quantity of their host plant(s) (Hellmann, 2002; Stamp and Bowers, 1990; Weiss et al., 1988), but also on suitable micro-environmental conditions (Albanese et al., 2007, 2008; Alonso, 1997; Klok and Chown, 1999; Weiss et al., 1987). Taking into account that butterfly caterpillars are ectothermous organisms, one of the key micro-environmental resources should be temperature. As shown on several species, the ability to find suitable temperature conditions (or actively control body temperature) can be selected for under many circumstances (Alonso, 1997; Barghusen et al., 1997; Karban, 1998; Kukal et al., 1988; Rawlins and Lederhouse, 1981). Indeed, optimal growth rates are usually reached at optimal body temperatures (Stamp and Bowers, 1990; Alonso, 1997; Knapp and Casey, 1986), which in turn are associated with lower parasitism and predation risks,
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higher probability of the coincidence of host plant and insect phenology and, finally, higher adult fitness (Hellmann, 2002; Stamp and Bowers, 1990; Weiss et al., 1988). We thus expect that thermal effects will exert strong selective pressures on behavior, physiology and life history when environmental temperatures vary over space and time (Agilletta, 2009). This is particularly true for small ectothermous organisms like many insects. Regional climate, and particularly temperature, is filtered by vegetation structures, soil properties and substrates into particular microclimates with both spatial and temporal heterogeneity (Aschcroft et al., 2009; WallisDeVries and Van Swaay, 2006). Temperature conditions vary widely over different spatial scales, including the micro-scale at the within-vegetation structure level. Structural and, hence, thermal heterogeneity can be provided by the host plant itself (see Hellmann, 2002; Weiss et al., 1988; Alonso, 1997), by a substrate (like an apple providing warmer outer and colder inner part for feeding of Codling moth ¨ larva (Kuhrt et al., 2005)), or even by a leaf (see an example with leaf-miner insect in Pincebourde and Casas (2006)). Previous studies on two glacial relict butterfly species, Boloria eunomia (Esper 1799) and Boloria aquilonaris (Stichel 1908), showed that caterpillar presence was dependent on spatial habitat heterogeneity at meso- and micro-scale. Caterpillars of B. eunomia are confined to colder, darker and moister conditions within host plant patches (Turlure et al., 2009). Caterpillars of B. aquilonaris were more abundant in host plant patches characterized by more humid and cooler conditions (Turlure et al., 2010). These required micro-environmental conditions were typically provided by grass tussocks (of mainly Deschampsia cespitosa or Molinia caerulea) for B. eunomia and by Sphagnum hummocks for B. aquilonaris. Such structures provide thermal heterogeneity which in turn is expected to ensure higher survival of the caterpillars. Because caterpillars are ectothermous organisms, they do not principally rely on metabolic mechanisms for thermoregulation. The selection of thermally favorable microclimates is their primary behavioral mechanism of temperature control (Stevenson, 1985). Caterpillars can be either – or alternately – passive temperature conformers (i.e. passively adopting the ambient temperature conditions; e.g. Lymantria dispar (Knapp and Casey, 1986); Polygonia c-album and Vanessa atalanta (Bryant et al., 2000); Doratifera casta (Reader and Hochuli, 2003)) or active thermoregulators (i.e. able to some extent to elevate or decrease their body temperature relative to ambient temperature; e.g. Malacasoma americanum (Knapp and Casey, 1986); Euphydryas aurinia (Porter, 1982); Gynaephora groenlandica (Kukal et al., 1988); Euphydryas editha (Weiss et al., 1987); Gynaephora rossii (Kevan et al., 1982)). Some avoid overheating by moving into less exposed sites during the hottest period of the day (Casey, 1976; Frears et al., 1997; Nice and Fordyce, 2006). Thus, the most widely used thermoregulation type for caterpillars seems to be behavioral thermoregulation (e.g. moving to more suitable temperature conditions). In this paper, we used complementary observational and experimental studies to assess the functional significance of different structural vegetation elements at the micro-scale level for the behavioral thermoregulation by caterpillars of two peat bog butterfly species. As B. eunomia and B. aquilonaris are glacial relict species in NW Europe, a thorough functional understanding of the relation between vegetation structure and the microhabitat use of the caterpillars is of high conservation significance under global warming. We built on the following steps. 1. Through visual inspection of the vegetation, caterpillars can be found only when they are basking or eating, turning detection probability into a surrogate for these activities. So, we first analyzed to what extent caterpillars adjusted their behavioral activity according to weather conditions (temperature and
sunshine) by quantifying temporal variations in the detection probability of caterpillars under natural conditions. 2. Secondly, we analyzed how caterpillar body temperature varied across the day at different positions within different structural vegetation elements under semi-controlled conditions experiments. Caterpillars can be assumed to exploit the thermal heterogeneity of micro-environmental conditions on and around their host plants to thermoregulate and protect themselves against unsuitable thermal conditions. Specifically, B. eunomia caterpillars could move between differentially exposed parts of the tussock or between green P. bistorta leaves and brown withered leaves of the tussock, whereas B. aquilonaris caterpillars could alternatively use the external exposed side or the buffered microclimate of internal parts of the hummock. 3. We end with a discussion of the potential fitness rewards of high quality micro-sites for both species and how a better understanding of the thermal properties of vegetation structures will help drawing appropriate habitat management methods for conservation.
2. Materials and methods 2.1. Study species and sites The bog fritillary B. eunomia (formerly Proclossiana eunomia) is a specialist species of peat bogs and wet meadows. The cranberry fritillary B. aquilonaris is a glacial relict species of acid peat bogs and damp heaths. Both species have a boreo-alpine distribution with highly fragmented populations to the south (confined to the Ardenne and Lorraine regions in Belgium (Fichefet et al., 2008)). Both are of conservation concern and listed as ‘vulnerable’ in the Red Data Book of European butterflies (van Swaay and Warren, 2006). Caterpillars of B. eunomia are reddish-brown with short spines. Caterpillars of B. aquilonaris are dark brown, with light spines and a double yellow light line along the back. Observations and experiments were carried out in two peat bog nature reserves in South Belgium: the Fange de Pisserotte (50113’N 5147’E) and the Troufferies de Libin (49157’N 5119’E). Each reserve hosts one large and long-time established population of B. eunomia and one of B. aquilonaris. Their unique host plants (Polygonum bistorta and Vaccinium oxycoccos, respectively) occurred in high density within numerous patches in both reserves. P. bistorta is a rhizomatic perennial plant with leaves growing up to 20 cm that occurs in dense clusters. V. oxycoccos forms low creeping scrubs with evergreen leaves, growing up to 10 cm. Based on our earlier work on the larval ecology of both species, we assigned a low (LQ) or high (HQ) quality to each patch according to host plant density and presence of tussocks (mainly D. cespitosa) for B. eunomia, and to host plant density and presence of Sphagnum hummocks for B. aquilonaris (see Turlure et al., 2009, 2010; Goffart et al., 2010 for details about quantitatively defined habitat quality). 2.2. Do weather conditions affect caterpillar detection probability? In both study areas, we searched for last instar caterpillars of both species by visual inspection of all host plant patches (i.e. 40 P. bistorta patches covering in total 30.0 ha and 17 V. oxycoccos patches covering in total 16.4 ha) during the corresponding period of the life cycle from 2005 to 2007 (search time: B. eunomia: 198 h in May; B. aquilonaris: 79 h in June). For each host plant patch sampled, we recorded the sampling effort (in person-hours), air temperature and degree of cloud cover (three classes: no cloud, some clouds interspersed with bright intervals, hazy or cloudy sky). We also recorded for each caterpillar its activity (i.e. feeding on host plant or basking/resting),
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its position relative to tussock/hummock (i.e. on or near) and species and color of the plant on which it was found. Logistic regression with AIC-based model selection (Proc Genmod in SAS, with a binomial distribution and log link; Burnham and Anderson, 2002) was used to assess the importance of weather conditions for caterpillar detectability, for each species separately. Because caterpillar detectability is likely to be positively influenced by habitat quality and sampling effort, these two factors were added as covariates. We only used data from Pisserotte because all patches within it were sampled under a broader range of weather conditions, which was not the case for Libin. For regression models (here for the logistic regression model and also for following regression models), the statistical approach was to fit models corresponding to all possible combinations of the factors and select the best model according to its AIC value (Burnham and Anderson, 2002). 2.3. How do B. aquilonaris caterpillars exploit both air temperature and internal microclimate of Sphagnum hummock? B. aquilonaris caterpillars were mainly found on Sphagnum hummocks of various shapes (from elongated to cylindrical) and size (from 0.5 to 3 m mean diameter). As the interior part of this structure was shown to buffer external air temperature into a stable and cool environment compared to the exterior part experiencing fluctuating temperatures (van der Molen and Wijmstra, 1994), we hypothesized that caterpillars actively used this range of temperature conditions to find their optimal temperature and hence to thermoregulate. In Libin, we repeatedly measured body temperature of B. aquilonaris last instar caterpillars placed in semi-controlled conditions. Each caterpillar was free to move inside an individual cage (height: 20 cm, length: 40 cm, width: 4 cm) made of fine white mesh nylon with a wooden frame, containing a slice of a Sphagnum hummock (thickness: 4 cm), and deposited vertically in the center of a hummock in the field. Nine hummocks of similar height, shape and perimeter were selected, which is a trade-off between the number of replicates and limiting the detrimental effects associated with the experiment on the fragile ecosystem environment. Every 2 h a day, we removed the cage from the hummock, opened it for a short time and recorded the position and body temperature (using an IR thermometer; model Ibp Exato TS4; resolution: 0.1 1C, precision: 0.2 1C) of the caterpillar; we did it for each of the nine cages. Air temperature and light intensity at 40 cm height from the ground near each of the nine hummocks, and temperature at three different depths (0, 10, and 20 cm) within the nine hummocks were automatically recorded every minute by data loggers (Onset HOBO UA-002-64; www.onsetcomp.com). Firstly, to confirm the buffering effect of the hummock structures, we tested for correlation of temperature recorded at different positions within the hummock with air temperature and light intensity using values extracted every 5 min between 8:00 and 18:30. Secondly, we tested whether air temperature and light intensity influenced the position of the caterpillar (two classes: on or within Sphagnum hummock) using logistic regression with AIC-based model selection (Proc Genmod in SAS, with a binomial distribution and log link). Finally, we compared caterpillar body temperature between these two positions using one-way ANOVA. 2.4. Is B. eunomia caterpillar body temperature affected by position on the tussock and substrate color? B. eunomia caterpillars were mainly found on grass tussocks (i.e. small conic hillock of grass-like plants) of various sizes (range: 10–60 cm height), either on green or on withered (brown) leaves. As this variation provides some scope for thermoregulation by micro-
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site selection, we used two experiments with semi-controlled conditions to test how B. eunomia caterpillar body temperature was affected by (1) the color of the substrate (green or brown, to mimic the typical colors of fresh and withered leaves, respectively) and the position on the tussock, both (2) its height (three classes: top, middle and ground level) and (3) its exposition to the sun (the four points of the compass). Ideally, it would be nice to measure caterpillar body temperature in their natural conditions, but caterpillars are difficult to find within the vegetation so that it was impossible to perform such kind of factorial experiment from direct observations. Therefore, we used artificial substrates on which we placed caterpillars collected in the field. In a first experiment, we fixed two small wooden plates (10 cm 10 cm), one green and one brown, on a bamboo stick at three height positions (at 2, 15 and 30 cm from the ground, later referred to as ground, middle and top positions, respectively) around the tussock. Temperature and light intensity were recorded every minute at each position by a data logger (Onset HOBO UA-002-64; www.onsetcomp.com) placed on the hummock between the two plates. Six last instar caterpillars of similar size were put in a small portable fridge for a period of 15 min to reach an identical body temperature and then placed on the plates. Body temperature of each caterpillar was then recorded every minute using an IR thermometer (resolution: 0.1 1C; precision: 0.2 1C). The experiment was repeated three times over 2 days for about 1 h (sampling periods: 11:00–12:00, 16:00–17:00 and 17:30–18:30), using three different groups of six caterpillars. The temporal trends in external and caterpillar body temperature, reflecting natural variations throughout the day and according to weather conditions, were removed by standardizing all temperature measurements to a mean of zero (and standard deviation of 1) for each time step, leaving only the temperature differences between experimental conditions. The differences of standardized external temperatures between positions on the tussock were tested by one-way ANOVA. Effects of the position on the tussock, the color of substrate and the interaction effect on standardized caterpillar body temperatures were tested by a two-way ANOVA. In a second experiment, four brown plates were vertically fixed at the middle level of one tussock, each directed towards one point of the compass. As in the first experiment, temperature and light intensity were recorded every minute using data loggers (Onset HOBO UA-002-64; www.onsetcomp.com) fixed in front of each plate. One B. eunomia last instar caterpillar was placed on each plate; its size and temperature were controlled as in the first experiment. Body temperature of each of the four caterpillars was recorded every minute using an IR thermometer. The experiment was repeated twice a day for around 1 h (sampling periods: 11:20– 12:20 and 16:30–17:30) using two different groups of four caterpillars. The differences of standardized external and standardized caterpillar body temperatures (as previously described) between expositions on the tussock were tested by one-way ANOVA. Finally, data collected in these two experiments were combined and the impact of temperature and light intensity on caterpillar body temperature was assessed by linear regression with AIC-based model selection (Proc Genmod in SAS, with a normal distribution and identity link). The sampling period was used as a categorical covariate.
3. Results 3.1. Caterpillar detection probability in the field is affected by weather conditions For both B. eunomia and B. aquilonaris, temperature and cloud cover affected the probability to detect caterpillars in the field
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(see Appendix 1 (A) and (B) for model selection and Table 1 for parameter estimates using best model). Caterpillars were more likely to be found on a day when the air temperature was lower, under cloudless conditions in the case of B. eunomia, but under cloudy or partly cloudy conditions for B. aquilonaris. Among the 385 B. eunomia caterpillars detected, 332 (86%) were either feeding or basking on grass tussock and 53 were basking in the proximity of tussocks. Among the 165 B. aquilonaris caterpillars found, 154 (93%) were on Sphagnum hummock (either feeding on V. oxycoccos or simply basking) and 11 were near hummocks on Sphagnum carpets. The proportion of B. eunomia caterpillars observed basking on green leaves (46%) or on brown withered leaves (54%) was not significantly different (w2 ¼2.37, df¼1; P¼0.12).
3.2. Experimental demonstration that B. aquilonaris caterpillars use the buffered internal microclimate of Sphagnum hummocks to compensate for air temperature fluctuations Air temperature and light intensity ranged from 4.8 to 37.1 1C and from 1378 to 176,358 lx, respectively. The external temperature of Sphagnum hummocks ranged between 6.6 and 27.1 1C, while the interior part provided more buffered thermal conditions (between 10.5 and 17.2 1C). Temperature at each hummock position was positively correlated with external air temperature and light intensity (Pearson correlation tests: Po0.0001), but R2
Environmental factor Modalities
Intercept Air temperature
B. eunomia
B. aquilonaris
Estimate SE
Estimate SE
1.24 0.47
0.45 26.28 0.31 1.61
0.76 0.66
Cloud cover
No cloud 1.04 Bright interval 0.77 Cloudy 0
0.95 22.36 0.43 1.99 / 0
193,524.8 0.97 /
Habitat quality
High Low
0.47 /
0 /
2.01 0
24.85 0
Standardized ambient temperature
1.5 1 0.5 0 -0.5 -1
-1.5 Recorder position:
Ground Middle
Top
Standardized body temperature
Table 1 Factors affecting caterpillar detectability (estimated using best model from Appendix 1 (A) and (B)). For categorical variables, the estimate expresses the difference with the reference level (fixed to zero). B. eunomia caterpillars were more likely to be found under lower air temperature and in higher habitat quality patches (R2 ¼ 0.27). B. aquilonaris caterpillars were more likely to be found under lower air temperature and without clouds (R2 ¼ 0.42).
decreased from 65.7% to 32.5% for temperature and 16.4% to 4.2% for light intensity from top position to 20 cm depth in the hummock, illustrating the buffering of temperature occurring deeper in the hummock. Not a single B. aquilonaris caterpillar was observed deeper than 10 cm within the cage in the hummock. The probability of finding a caterpillar inside the Sphagnum hummock increased with light intensity only (R2 ¼ 32.54%; Appendix 1 (C)). Caterpillar body temperature was significantly lower inside than outside the hummock (one-way ANOVA: F1,54 ¼8.00; P¼0.0065; mean temperature and 95% confidence interval: 22.272.5 1C inside vs. 25.070.8 1C outside). Moreover, the excess of body temperature above ambient temperature ranged between 0.16 and 9.0 1C inside the hummock and reached larger values outside the hummock (up to 14 1C).
3.3. Experimental demonstration that B. eunomia caterpillar body temperature is affected by both the position on the tussock and the substrate color Temperature around the tussock was significantly different according to the position on the tussock (ANOVA: F2,245 ¼782.32, Po0.0001; Fig. 1A). Temperature decreased from the ground to the top (mean 795% confidence interval: 24.471.8 1C ground; 19.871.0 1C middle; 17.070.7 1C top). B. eunomia caterpillar body temperature ranged from 12.7 to 39.3 1C and from 12.4 to 36.3 1C on green and brown substrates, respectively. Two-way ANOVA analysis indicated that body temperature was affected by substrate color (greenobrown: F1,486 ¼106.11, Po0.001), height at which the caterpillar was located (ground4middle4top: F2,486 ¼157.87, Po0.001) and the interaction between both factors (F2,486 ¼13.43, Po0.001) (Fig. 1B). This interaction indicates that caterpillar body temperature on the green substrate was less dependent on the height at which the caterpillar was located than when it was on the brown substrate. Temperature and light intensity were significantly different relative to exposition side (one way ANOVAs; temperature: F3,231 ¼8921.4, Po0.0001, Fig. 2A; light intensity: F3,231 ¼64.5, Po0.0001, Fig. 2B). As expected, temperature (mean795% confidence interval) was highest towards the south (31.570.1 1C), intermediate towards the east (25.870.1 1C) and the west (25.470.2 1C), and lowest towards the north (21.9 70.1 1C). Light intensity (means795% confidence interval) decreased from the east (1997 14 lx), south (1627 11 lx), west (142 78 lx) to the north exposition (108 78 lx).
Substrate color:
Green
Brown
1.5 1 0.5 0 -0.5 -1 -1.5
Caterpillar Ground position:
Middle
Top
Fig. 1. (A) Standardized ambient temperature differed according to the position on the tussock (ground, middle and top level). (B) Standardized body temperature of B. eunomia differed according to position on tussock and substrate color (green: white dots and brown: black dots), as it was less dependent on the position on the tussock when located on the green support compared to the brown one. For both panels, values are means7 95% confidence interval.
a
1 0.5 0
b
c
-0.5 d
-1
-1.5 Recoder South East exposition:
West North
1.5
177
1.5 b
1 a
0.5
c
0
d
-0.5 -1
-1.5 Recorder South East exposition:
West North
Standardized body temperature
1.5
Standardized light intensity
Standardized airtemperature
C. Turlure et al. / Journal of Thermal Biology 36 (2011) 173–180
a
1 0.5 0 -0.5
b c
-1
-1.5 Caterpillar South East West North exposition:
Fig. 2. Standardized temperatures (A), light intensity (B), and body temperatures of B. eunomia caterpillars (C) differed according to exposition sides. Values are means7 95% confidence interval. Groups displayed with the same letter were not significantly different at the 0.05 level (Tukey–Kramer studentized range test).
Table 2 Factors affecting B. eunomia caterpillar body temperature (estimated using best model from Appendix 1 (D)). For categorical variables, the estimate expresses the difference with the reference level (fixed to zero). Caterpillar body temperature was (1) positively related to both air temperature and light intensity, (2) lower for the three first sampling periods, highest for the next sampling period and decreasing again for the last sampling period (R2 ¼ 0.57). Environmental factor
Modalities
Intercept Air temperature (1C) Light intensity (klx) Sampled periods
Estimate 23.76 0.13 0.10
11:00–12:00 11:20–12:20 16:00–17:00 16:30–17:30 17:30–18:30
10.02 3.82 5.17 7.22 0
SE 0.90 0.03 1.0 10 5 0.62 0.61 0.49 0.59 /
Caterpillar body temperature ranged from 21.2 1C in the north to 32.1 1C in the south, and differed significantly among the four directions (one-way ANOVA: F3,228 ¼108.52, Po0.001). Body temperature was highest for the south and east expositions, intermediate for the west exposition, and lowest for the north exposition (Fig. 2C). Overall, B. eunomia caterpillar body temperature was positively related to both temperature and light intensity (see Appendix 1 (D) for model selection and Table 2 for parameter estimates using best model). It was lowest in the morning (i.e. sampling period: 11.00–12:00; external temperature ranging from 11.5 to 31.7 1C; light intensity ranging from 64.6 to 55,111.5 lx), highest in the afternoon (i.e. sampling period: 16:00–17:00; external temperatures ranging from 13.2 to 32.1 1C, light intensity ranging from 64.6 to 44,089.2 lx), and decreasing again later in the afternoon (i.e. sampling period: 17:30–18:30; external temperature ranging from 15.9 to 35.6 1C; light intensity ranging from 1 to 22,045 lx).
4. Discussion 4.1. Influence of weather conditions on caterpillar detection probability Within habitat patches, caterpillars of B. eunomia and B. aquilonaris were easier to detect under weather conditions characterized by lower temperatures and specific cloud cover conditions: clearer sky for B. eunomia, (partly) clouded sky for B. aquilonaris. This suggests that during periods of inappropriate weather conditions, caterpillars stayed hidden inside the vegetation structures. For B. aquilonaris, this finding was experimentally
confirmed by the fact that caterpillars went inside in the hummock under increased light intensity. Defining the weather conditions that are favorable for caterpillar detection is important to optimize search efforts to find caterpillars (e.g. surveys or monitoring for conservation programs), and is essential for understanding correctly larval habitat-use and the behavioral mechanisms of caterpillar thermoregulation (Nice and Fordyce, 2006; Sherman and Watt, 1973). Caterpillar body temperature of both species was related to ambient temperature, and also to light intensity for B. eunomia. While the impact of ambient temperature on caterpillar body temperature has been reported by many studies, the positive influence of light intensity has not received as much attention yet (but see Porter, 1982; Klok and Chown 1999; Bryant et al., 2000 for examples). As predicted, the larval stages of B. eunomia and B. aquilonaris use suitable microclimates provided by structural vegetation elements (i.e. Sphagnum hummocks and grass tussocks, respectively) around the host plant in order to cope with variable weather conditions. 4.2. Use of suitable microhabitat Sphagnum hummocks provide a range of temperature conditions; the temperature of the external part of this structure was directly influenced by air temperature and light intensity, whereas the interior part provided stable and cool thermal conditions (Turlure et al., 2010; van der Molen and Wijmstra, 1994). Indeed, higher light intensity conditions are likely to induce warming up of local structural vegetation elements. This process depends on the water content of the hummocks due to relatively high thermal conductivity of water (van der Molen and Wijmstra, 1994) and decreased albedo – and correspondingly, energy reflectance – with higher moisture content (Nungesser, 2003). Additionally, the water content of hummocks may influence the temperature through a cooling effect of the latent heat flux of evapotranspiration. Here, we showed that the body temperature of B. aquilonaris caterpillars that were located on top of a hummock was higher than those that were located inside the hummock, which is probably due to the direct absorption of solar radiation. Our previous research showed that the survival of B. aquilonaris larvae was higher under lower temperature conditions (20 vs. 25 1C; Turlure et al., 2010). Therefore, we suggest that B. aquilonaris uses behavioral thermoregulation through micro-site selection, moving to different positions within the Sphagnum hummock. Inside the hummock, B. aquilonaris caterpillars adopted a temperature conformer strategy, at a lower but stable temperature, which is probably less physiologically costly (Knapp and Casey, 1986). When they reached the hummock surface to feed on the host plant, their body temperature increased above the ambient temperature exposing them to overheating and desiccation risks.
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Tussocks are cone-shaped structures, presenting a range of temperature conditions according to their shape and their exposition sides: temperature conditions were higher on the ground compared to the top, which can be related to the shelter properties of a tussock against the wind, and temperature was also higher on the south and east sides compared to the north and west sides. Body temperature of B. eunomia caterpillars decreased when changing the location from the plates located at ground level to the top of the tussock, and from the north to the south. From this experiment, we are not able to make a direct conclusion about the strategy B. eunomia individuals adopt for thermoregulation (i.e. conformer vs. active thermoregulator) as caterpillars were indeed not free to move on the tussock. Nevertheless, we hypothesize that caterpillars engage in behavioral thermoregulation as they were observed moving up and down on the tussocks during the day under natural conditions (C. Turlure, personal observation). Further, indirect evidence comes from the fact that B. eunomia caterpillars were difficult to find during cloudy periods; such conditions may hamper caterpillar basking behavior, making it more profitable or safe to stay inside the tussock structure than to move out. Both examples suggest that there is no unique and fixed ‘‘best quality microhabitat’’ in terms of thermal conditions within structural vegetation elements for the caterpillar stages. Microhabitat use is conditioned by both the environmental conditions and the internal state of the individual. So, requirements of caterpillars will change depending on the time of day and surrounding conditions, which may induce displacements to a place with beneficial conditions at a particular time (see Dennis and Sparks (2006) for a similar example for adult stages). Further experimental studies are now warranted to analyze how different thermal regimes that vary over time and micro-space affect development and survival (Barghusen et al., 1997; Bryant et al., 2000). However, the dependence of the caterpillar body temperature on the position within the peat bog vegetation structure indicates that these structures provide heterogeneous thermal conditions. Therefore, these structural elements should be considered an important resource, and hence an important habitat aspect of each species.
with plant tissue. A similar case was reported by Kukal et al. (1988) for G. groenlandica, which used the snow albedo to raise body temperature up to 20 1C above the ambient temperature. Previous research on the same study system showed that temperature did not affect caterpillar survival, but positively influenced caterpillar growth rate (Augem, 2007). Despite the benefit of the green substrate in terms of conferring elevated body temperatures, caterpillars were as likely to be found on both substrate colors. From a functional point of view, this suggests that there should be advantages and disadvantages associated with each color relative to the prevalent environmental conditions. A trade-off between adopting aposematic caterpillar body color but losing the possibility to thermoregulate optimally versus a dark body color that allows basking for elevation of body temperature but also increasing predation or parasitism risk has been reported for caterpillars in several other species (for examples, see Reader and Hochuli, 2003; Nice and Fordyce, 2006). Such potential interactions with background matching need further testing.
5. Conclusions Our field observations showed that both species are able to modify their position within the vegetation and their behavior depending on weather conditions. Moreover, our experiments demonstrated that caterpillars can actively use microclimatic gradients provided by structural vegetation elements to avoid thermal stress, which may occur on a daily basis due to temperature fluctuations. How these behavioral adaptations will allow these glacial relicts to cope with future climate warming remains still an open question. However, our results show that habitat management strategies aiming at the preservation of structural vegetation elements will be of the utmost importance for the survival of caterpillars, and, hence for the conservation of viable populations. These management measures should be planned rigorously taking into account ongoing and future climate changes.
Acknowledgments 4.3. Possible extra functions provided by structural vegetation elements Besides a diversity of thermal conditions, vegetation structures supply variation for other microclimatic variables as well. Hummocks are, for example, a valuable source of moisture for caterpillar development in B. aquilonaris (C. Turlure, personal observation). Other functions include providing cryptic color and conferring lower predation pressure, lower parasitism load (Karban (1998) reported the case of ‘behavioral fever’ for caterpillars of Platypteria virginalis, which elevate body temperature by basking on dead vegetation in order to cure themselves from parasitoids), or flooding avoidance (Coenonympha tullia climbs on the tussocks of Eriophorum vaginatum in order to avoid submergence during the winter (Joss et al., 1988; Joy and Pullin, 1997); in a similar manner, Sei and Porter (2003) described the vegetation types conferring higher survival from flooding for C. tullia nipisquit). Microhabitat use will hence be influenced by factors other than host plant use and thermoregulation, but still little is known about the factors that affect the selection of microhabitat for shelter (e.g. pupation or larval molting). In the case of B. eunomia, we observed that caterpillar body temperature was higher on a green substrate, which probably can be explained by the higher reflectance of green surfaces compared to the brown ones, even if wooden plates may have very different thermal properties (including specific heat capacity) compared
We thank Ame´lie Augem for her valuable help with field work, Jean Clobert for helpful discussions and an anonymous reviewer for his/her valuable comments. C.T. and V.R. were supported by a Ph.D. grant from the FRIA-fund. N.S. is Research Associate of the Fund for Scientific Research-FNRS. Reserves access and a permission to study these protected species in the field were granted by the Ministe re de la Re´gion Wallonne. This is publication BRC207 of the Biodiversity Research Centre at UCL. The funders had no rule in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Appendix 1 Modeling (A) B. aquilonaris caterpillar detectability, (B) B. eunomia caterpillar detectability, (C) B. aquilonaris caterpillar position (inside vs. outside Sphagnum hummock) and (D) B. eunomia caterpillar body temperature using linear or logistic regression models with AIC model selection. Are presented for each model: the list of covariates and variables considered, the number of estimated parameters, the AIC value and the difference (D) of AIC with the lowest-AIC model. Supported models (models with DAICo2) are indicated by nnn and selected best model is in bold (Table A1).
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Table A1 Species
Response variable
Model
Covariates
Variables in the model
(A) B. eunomia
Caterpillar detectability
Linear
Habitat quality + sampling effort
Cloud cover+ air temperature
(B) B. aquilonaris
(C) B. aquilonaris
(D) B. eunomia
Caterpillar detectability
Caterpillar position
Caterpillar body temperature
Linear
Logistic
Linear
Habitat quality + Sampling effort
/
Sampling period
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6
62.2
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8
64.13
1.93
4 5 3
65.41 67.81 72.51
3.21 5.61 10.31
nnn
2
44.19
0
Light intensity+ air temperaturennn Light intensity+ air temperature +(light intensity air temperature) Intercept only Air temperature
3 4
46.14 46.26
1.95 2.08
1 2
54.55 56.53
10.37 12.34
7
4156.53
6 6 5
4168.34 4188.26 4197.99
Light intensity
Ambient temperature+ light intensitynnn Light intensity Ambient temperature Intercept only
0 11.81 31.74 41.47
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Sherman, P.W., Watt, W.B., 1973. The thermal ecology of some Colias butterfly larvae. J. Comportemental Physiol. 83, 25–40. Stamp, N.E., Bowers, M.D., 1990. Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71, 1031–1039. Stevenson, R.D., 1985. The relative importance of behavioral and physiological adjustments controlling temperature in terrestrial ecotherms. Am. Nat. 126, 362–386. Turlure, C., Van Dyck, H., Schtickzelle, N., Baguette, M., 2009. Resource-based definition of the habitat, niche overlap and conservation of two glacial relict butterflies. Oikos 118, 950–960. Turlure, C., Choutt, J., Baguette, M., Van Dyck, H., 2010. Microclimate buffering and resource-based habitat of a relict butterfly species: significance for conservation under climate change. Global Change Biol. 16, 1883–1893.
van der Molen, P.C., Wijmstra, T.A., 1994. The thermal regime of hummock-hollow complexes on Clara bog, Co. Offaly. Biol. Environ.: Proc. R. Irish Acad. 94B, 209–221. van Swaay, C., Warren, M., 2006. Prime butterfly areas of Europe: an initial selection of priority sites for conservation. J. Insect Conserv. 10, 5–11. WallisDeVries, M.F., Van Swaay, C.A.M., 2006. Global warming and excess nitrogen may induce butterfly decline by microclimatic cooling. Global Change Biol. 12, 1620–1626. Weiss, S.B., Raymond, R.W., Dennis, D.M., Ehrlich, P.R., 1987. Growth and dispersal of larvae of the Checkerspot Butterfly Euphydryas editha. Oikos 50, 161–166. Weiss, S.B., Murphy, D.D., White, R.R., 1988. Sun, slope, and butterflies— topographic determinants of habitat quality for Euphydryas editha. Ecology 69, 1486–1496.
Contents lists available at ScienceDirect
Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio
On the significance of structural vegetation elements for caterpillar thermoregulation in two peat bog butterflies: Boloria eunomia and B. aquilonaris Camille Turlure a,b,n, Viktoriia Radchuk a, Michel Baguette b,c, Hans Van Dyck a, Nicolas Schtickzelle a a
Universite´ catholique de Louvain, Earth and Life Institute, Biodiversity Research Centre, Place Croix du Sud, 4 – B-1348 Louvain-la-Neuve, Belgium Muse´um National d’Histoire Naturelle, UMR CNRS-MNHN 7204, Avenue du petit chˆ ateau, 1 - F-91800 Brunoy, France c ´cologie expe´rimentale du CNRS (Moulis), Route du CNRS, 4 - F-09200 Saint Girons, France CNRS USR 2936 Station d’e b
a r t i c l e i n f o
abstract
Article history: Received 18 August 2010 Accepted 3 February 2011 Available online 25 February 2011
Purpose: Temperature profoundly impacts on distribution and habitat-use of organisms. The development of ectothermous caterpillars does not depend on host plant quality only, but also on the availability of suitable thermal conditions. Selection for thermally favorable microclimates (i.e. behavioral thermoregulation) is a primary mechanism of temperature control, and caterpillars can be either (or alternately) temperature conformers (i.e. passively adopting ambient temperature conditions) or thermoregulators (i.e. able to some extent to elevate or decrease their body temperature relative to ambient temperature). Here, we addressed the functional significance of different structural vegetation elements for the behavioral thermoregulation by caterpillars of two butterfly species. Results: Weather conditions influenced the caterpillar detection probability within host plant patches, indicating that caterpillars can hide and use suitable microclimates provided by vegetation structures to cope with weather variations. This is why we (1) evaluated the heterogeneity in temperature conditions provided by these structures, (2) quantified the influence of ambient temperature and light intensity on caterpillar body temperature, and (3) tested how position on structure, substrate color and exposition influenced caterpillar body temperature. As expected, vegetation structures provided heterogeneous temperature and sun exposition conditions, while caterpillar body temperature was dependent on ambient temperature and light intensity. But body temperature was additionally influenced by the position on vegetation structures, substrate color and exposition. Conclusions: These results suggest that there is no unique and fixed structure in the vegetation subsuming the best thermal conditions for caterpillars. We argue that a better understanding of the thermal properties of vegetation structures is essential for correctly understanding caterpillar habitatuse and the behavioral mechanisms driving their body thermoregulation. Conceptually this means that thermal conditions should be included in the definition of a species’ functional habitat. Practically this may influence the choice of appropriate habitat management for species of conservation concern. & 2011 Elsevier Ltd. All rights reserved.
Keywords: Behavioral thermoregulation Climate change Ectothermous organisms Habitat management Microclimatic conditions Vegetation structure
1. Introduction All organisms have basic requirements for their environment (food, physical conditions) to successfully complete their development, including survival and reproduction. However, the precise identification of these basic requirements often remains far from self-evident. The higher the heterogeneity and variation of conditions and resources in their close environment, the more opportunities are offered to the organisms to find the resources they need under variable environmental conditions. For instance n Corresponding author at: Universite´ catholique de Louvain, Earth and Life Institute, Biodiversity Research Centre, Place Croix du Sud, 4 – B-1348 Louvain-la-Neuve, Belgium. Tel.: + 32 477 23 09 61; fax: +32 10 47 34 90. E-mail address: [email protected] (C. Turlure).
0306-4565/$ - see front matter & 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2011.02.001
in butterflies, caterpillar development usually depends on the quality and quantity of their host plant(s) (Hellmann, 2002; Stamp and Bowers, 1990; Weiss et al., 1988), but also on suitable micro-environmental conditions (Albanese et al., 2007, 2008; Alonso, 1997; Klok and Chown, 1999; Weiss et al., 1987). Taking into account that butterfly caterpillars are ectothermous organisms, one of the key micro-environmental resources should be temperature. As shown on several species, the ability to find suitable temperature conditions (or actively control body temperature) can be selected for under many circumstances (Alonso, 1997; Barghusen et al., 1997; Karban, 1998; Kukal et al., 1988; Rawlins and Lederhouse, 1981). Indeed, optimal growth rates are usually reached at optimal body temperatures (Stamp and Bowers, 1990; Alonso, 1997; Knapp and Casey, 1986), which in turn are associated with lower parasitism and predation risks,
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higher probability of the coincidence of host plant and insect phenology and, finally, higher adult fitness (Hellmann, 2002; Stamp and Bowers, 1990; Weiss et al., 1988). We thus expect that thermal effects will exert strong selective pressures on behavior, physiology and life history when environmental temperatures vary over space and time (Agilletta, 2009). This is particularly true for small ectothermous organisms like many insects. Regional climate, and particularly temperature, is filtered by vegetation structures, soil properties and substrates into particular microclimates with both spatial and temporal heterogeneity (Aschcroft et al., 2009; WallisDeVries and Van Swaay, 2006). Temperature conditions vary widely over different spatial scales, including the micro-scale at the within-vegetation structure level. Structural and, hence, thermal heterogeneity can be provided by the host plant itself (see Hellmann, 2002; Weiss et al., 1988; Alonso, 1997), by a substrate (like an apple providing warmer outer and colder inner part for feeding of Codling moth ¨ larva (Kuhrt et al., 2005)), or even by a leaf (see an example with leaf-miner insect in Pincebourde and Casas (2006)). Previous studies on two glacial relict butterfly species, Boloria eunomia (Esper 1799) and Boloria aquilonaris (Stichel 1908), showed that caterpillar presence was dependent on spatial habitat heterogeneity at meso- and micro-scale. Caterpillars of B. eunomia are confined to colder, darker and moister conditions within host plant patches (Turlure et al., 2009). Caterpillars of B. aquilonaris were more abundant in host plant patches characterized by more humid and cooler conditions (Turlure et al., 2010). These required micro-environmental conditions were typically provided by grass tussocks (of mainly Deschampsia cespitosa or Molinia caerulea) for B. eunomia and by Sphagnum hummocks for B. aquilonaris. Such structures provide thermal heterogeneity which in turn is expected to ensure higher survival of the caterpillars. Because caterpillars are ectothermous organisms, they do not principally rely on metabolic mechanisms for thermoregulation. The selection of thermally favorable microclimates is their primary behavioral mechanism of temperature control (Stevenson, 1985). Caterpillars can be either – or alternately – passive temperature conformers (i.e. passively adopting the ambient temperature conditions; e.g. Lymantria dispar (Knapp and Casey, 1986); Polygonia c-album and Vanessa atalanta (Bryant et al., 2000); Doratifera casta (Reader and Hochuli, 2003)) or active thermoregulators (i.e. able to some extent to elevate or decrease their body temperature relative to ambient temperature; e.g. Malacasoma americanum (Knapp and Casey, 1986); Euphydryas aurinia (Porter, 1982); Gynaephora groenlandica (Kukal et al., 1988); Euphydryas editha (Weiss et al., 1987); Gynaephora rossii (Kevan et al., 1982)). Some avoid overheating by moving into less exposed sites during the hottest period of the day (Casey, 1976; Frears et al., 1997; Nice and Fordyce, 2006). Thus, the most widely used thermoregulation type for caterpillars seems to be behavioral thermoregulation (e.g. moving to more suitable temperature conditions). In this paper, we used complementary observational and experimental studies to assess the functional significance of different structural vegetation elements at the micro-scale level for the behavioral thermoregulation by caterpillars of two peat bog butterfly species. As B. eunomia and B. aquilonaris are glacial relict species in NW Europe, a thorough functional understanding of the relation between vegetation structure and the microhabitat use of the caterpillars is of high conservation significance under global warming. We built on the following steps. 1. Through visual inspection of the vegetation, caterpillars can be found only when they are basking or eating, turning detection probability into a surrogate for these activities. So, we first analyzed to what extent caterpillars adjusted their behavioral activity according to weather conditions (temperature and
sunshine) by quantifying temporal variations in the detection probability of caterpillars under natural conditions. 2. Secondly, we analyzed how caterpillar body temperature varied across the day at different positions within different structural vegetation elements under semi-controlled conditions experiments. Caterpillars can be assumed to exploit the thermal heterogeneity of micro-environmental conditions on and around their host plants to thermoregulate and protect themselves against unsuitable thermal conditions. Specifically, B. eunomia caterpillars could move between differentially exposed parts of the tussock or between green P. bistorta leaves and brown withered leaves of the tussock, whereas B. aquilonaris caterpillars could alternatively use the external exposed side or the buffered microclimate of internal parts of the hummock. 3. We end with a discussion of the potential fitness rewards of high quality micro-sites for both species and how a better understanding of the thermal properties of vegetation structures will help drawing appropriate habitat management methods for conservation.
2. Materials and methods 2.1. Study species and sites The bog fritillary B. eunomia (formerly Proclossiana eunomia) is a specialist species of peat bogs and wet meadows. The cranberry fritillary B. aquilonaris is a glacial relict species of acid peat bogs and damp heaths. Both species have a boreo-alpine distribution with highly fragmented populations to the south (confined to the Ardenne and Lorraine regions in Belgium (Fichefet et al., 2008)). Both are of conservation concern and listed as ‘vulnerable’ in the Red Data Book of European butterflies (van Swaay and Warren, 2006). Caterpillars of B. eunomia are reddish-brown with short spines. Caterpillars of B. aquilonaris are dark brown, with light spines and a double yellow light line along the back. Observations and experiments were carried out in two peat bog nature reserves in South Belgium: the Fange de Pisserotte (50113’N 5147’E) and the Troufferies de Libin (49157’N 5119’E). Each reserve hosts one large and long-time established population of B. eunomia and one of B. aquilonaris. Their unique host plants (Polygonum bistorta and Vaccinium oxycoccos, respectively) occurred in high density within numerous patches in both reserves. P. bistorta is a rhizomatic perennial plant with leaves growing up to 20 cm that occurs in dense clusters. V. oxycoccos forms low creeping scrubs with evergreen leaves, growing up to 10 cm. Based on our earlier work on the larval ecology of both species, we assigned a low (LQ) or high (HQ) quality to each patch according to host plant density and presence of tussocks (mainly D. cespitosa) for B. eunomia, and to host plant density and presence of Sphagnum hummocks for B. aquilonaris (see Turlure et al., 2009, 2010; Goffart et al., 2010 for details about quantitatively defined habitat quality). 2.2. Do weather conditions affect caterpillar detection probability? In both study areas, we searched for last instar caterpillars of both species by visual inspection of all host plant patches (i.e. 40 P. bistorta patches covering in total 30.0 ha and 17 V. oxycoccos patches covering in total 16.4 ha) during the corresponding period of the life cycle from 2005 to 2007 (search time: B. eunomia: 198 h in May; B. aquilonaris: 79 h in June). For each host plant patch sampled, we recorded the sampling effort (in person-hours), air temperature and degree of cloud cover (three classes: no cloud, some clouds interspersed with bright intervals, hazy or cloudy sky). We also recorded for each caterpillar its activity (i.e. feeding on host plant or basking/resting),
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its position relative to tussock/hummock (i.e. on or near) and species and color of the plant on which it was found. Logistic regression with AIC-based model selection (Proc Genmod in SAS, with a binomial distribution and log link; Burnham and Anderson, 2002) was used to assess the importance of weather conditions for caterpillar detectability, for each species separately. Because caterpillar detectability is likely to be positively influenced by habitat quality and sampling effort, these two factors were added as covariates. We only used data from Pisserotte because all patches within it were sampled under a broader range of weather conditions, which was not the case for Libin. For regression models (here for the logistic regression model and also for following regression models), the statistical approach was to fit models corresponding to all possible combinations of the factors and select the best model according to its AIC value (Burnham and Anderson, 2002). 2.3. How do B. aquilonaris caterpillars exploit both air temperature and internal microclimate of Sphagnum hummock? B. aquilonaris caterpillars were mainly found on Sphagnum hummocks of various shapes (from elongated to cylindrical) and size (from 0.5 to 3 m mean diameter). As the interior part of this structure was shown to buffer external air temperature into a stable and cool environment compared to the exterior part experiencing fluctuating temperatures (van der Molen and Wijmstra, 1994), we hypothesized that caterpillars actively used this range of temperature conditions to find their optimal temperature and hence to thermoregulate. In Libin, we repeatedly measured body temperature of B. aquilonaris last instar caterpillars placed in semi-controlled conditions. Each caterpillar was free to move inside an individual cage (height: 20 cm, length: 40 cm, width: 4 cm) made of fine white mesh nylon with a wooden frame, containing a slice of a Sphagnum hummock (thickness: 4 cm), and deposited vertically in the center of a hummock in the field. Nine hummocks of similar height, shape and perimeter were selected, which is a trade-off between the number of replicates and limiting the detrimental effects associated with the experiment on the fragile ecosystem environment. Every 2 h a day, we removed the cage from the hummock, opened it for a short time and recorded the position and body temperature (using an IR thermometer; model Ibp Exato TS4; resolution: 0.1 1C, precision: 0.2 1C) of the caterpillar; we did it for each of the nine cages. Air temperature and light intensity at 40 cm height from the ground near each of the nine hummocks, and temperature at three different depths (0, 10, and 20 cm) within the nine hummocks were automatically recorded every minute by data loggers (Onset HOBO UA-002-64; www.onsetcomp.com). Firstly, to confirm the buffering effect of the hummock structures, we tested for correlation of temperature recorded at different positions within the hummock with air temperature and light intensity using values extracted every 5 min between 8:00 and 18:30. Secondly, we tested whether air temperature and light intensity influenced the position of the caterpillar (two classes: on or within Sphagnum hummock) using logistic regression with AIC-based model selection (Proc Genmod in SAS, with a binomial distribution and log link). Finally, we compared caterpillar body temperature between these two positions using one-way ANOVA. 2.4. Is B. eunomia caterpillar body temperature affected by position on the tussock and substrate color? B. eunomia caterpillars were mainly found on grass tussocks (i.e. small conic hillock of grass-like plants) of various sizes (range: 10–60 cm height), either on green or on withered (brown) leaves. As this variation provides some scope for thermoregulation by micro-
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site selection, we used two experiments with semi-controlled conditions to test how B. eunomia caterpillar body temperature was affected by (1) the color of the substrate (green or brown, to mimic the typical colors of fresh and withered leaves, respectively) and the position on the tussock, both (2) its height (three classes: top, middle and ground level) and (3) its exposition to the sun (the four points of the compass). Ideally, it would be nice to measure caterpillar body temperature in their natural conditions, but caterpillars are difficult to find within the vegetation so that it was impossible to perform such kind of factorial experiment from direct observations. Therefore, we used artificial substrates on which we placed caterpillars collected in the field. In a first experiment, we fixed two small wooden plates (10 cm 10 cm), one green and one brown, on a bamboo stick at three height positions (at 2, 15 and 30 cm from the ground, later referred to as ground, middle and top positions, respectively) around the tussock. Temperature and light intensity were recorded every minute at each position by a data logger (Onset HOBO UA-002-64; www.onsetcomp.com) placed on the hummock between the two plates. Six last instar caterpillars of similar size were put in a small portable fridge for a period of 15 min to reach an identical body temperature and then placed on the plates. Body temperature of each caterpillar was then recorded every minute using an IR thermometer (resolution: 0.1 1C; precision: 0.2 1C). The experiment was repeated three times over 2 days for about 1 h (sampling periods: 11:00–12:00, 16:00–17:00 and 17:30–18:30), using three different groups of six caterpillars. The temporal trends in external and caterpillar body temperature, reflecting natural variations throughout the day and according to weather conditions, were removed by standardizing all temperature measurements to a mean of zero (and standard deviation of 1) for each time step, leaving only the temperature differences between experimental conditions. The differences of standardized external temperatures between positions on the tussock were tested by one-way ANOVA. Effects of the position on the tussock, the color of substrate and the interaction effect on standardized caterpillar body temperatures were tested by a two-way ANOVA. In a second experiment, four brown plates were vertically fixed at the middle level of one tussock, each directed towards one point of the compass. As in the first experiment, temperature and light intensity were recorded every minute using data loggers (Onset HOBO UA-002-64; www.onsetcomp.com) fixed in front of each plate. One B. eunomia last instar caterpillar was placed on each plate; its size and temperature were controlled as in the first experiment. Body temperature of each of the four caterpillars was recorded every minute using an IR thermometer. The experiment was repeated twice a day for around 1 h (sampling periods: 11:20– 12:20 and 16:30–17:30) using two different groups of four caterpillars. The differences of standardized external and standardized caterpillar body temperatures (as previously described) between expositions on the tussock were tested by one-way ANOVA. Finally, data collected in these two experiments were combined and the impact of temperature and light intensity on caterpillar body temperature was assessed by linear regression with AIC-based model selection (Proc Genmod in SAS, with a normal distribution and identity link). The sampling period was used as a categorical covariate.
3. Results 3.1. Caterpillar detection probability in the field is affected by weather conditions For both B. eunomia and B. aquilonaris, temperature and cloud cover affected the probability to detect caterpillars in the field
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(see Appendix 1 (A) and (B) for model selection and Table 1 for parameter estimates using best model). Caterpillars were more likely to be found on a day when the air temperature was lower, under cloudless conditions in the case of B. eunomia, but under cloudy or partly cloudy conditions for B. aquilonaris. Among the 385 B. eunomia caterpillars detected, 332 (86%) were either feeding or basking on grass tussock and 53 were basking in the proximity of tussocks. Among the 165 B. aquilonaris caterpillars found, 154 (93%) were on Sphagnum hummock (either feeding on V. oxycoccos or simply basking) and 11 were near hummocks on Sphagnum carpets. The proportion of B. eunomia caterpillars observed basking on green leaves (46%) or on brown withered leaves (54%) was not significantly different (w2 ¼2.37, df¼1; P¼0.12).
3.2. Experimental demonstration that B. aquilonaris caterpillars use the buffered internal microclimate of Sphagnum hummocks to compensate for air temperature fluctuations Air temperature and light intensity ranged from 4.8 to 37.1 1C and from 1378 to 176,358 lx, respectively. The external temperature of Sphagnum hummocks ranged between 6.6 and 27.1 1C, while the interior part provided more buffered thermal conditions (between 10.5 and 17.2 1C). Temperature at each hummock position was positively correlated with external air temperature and light intensity (Pearson correlation tests: Po0.0001), but R2
Environmental factor Modalities
Intercept Air temperature
B. eunomia
B. aquilonaris
Estimate SE
Estimate SE
1.24 0.47
0.45 26.28 0.31 1.61
0.76 0.66
Cloud cover
No cloud 1.04 Bright interval 0.77 Cloudy 0
0.95 22.36 0.43 1.99 / 0
193,524.8 0.97 /
Habitat quality
High Low
0.47 /
0 /
2.01 0
24.85 0
Standardized ambient temperature
1.5 1 0.5 0 -0.5 -1
-1.5 Recorder position:
Ground Middle
Top
Standardized body temperature
Table 1 Factors affecting caterpillar detectability (estimated using best model from Appendix 1 (A) and (B)). For categorical variables, the estimate expresses the difference with the reference level (fixed to zero). B. eunomia caterpillars were more likely to be found under lower air temperature and in higher habitat quality patches (R2 ¼ 0.27). B. aquilonaris caterpillars were more likely to be found under lower air temperature and without clouds (R2 ¼ 0.42).
decreased from 65.7% to 32.5% for temperature and 16.4% to 4.2% for light intensity from top position to 20 cm depth in the hummock, illustrating the buffering of temperature occurring deeper in the hummock. Not a single B. aquilonaris caterpillar was observed deeper than 10 cm within the cage in the hummock. The probability of finding a caterpillar inside the Sphagnum hummock increased with light intensity only (R2 ¼ 32.54%; Appendix 1 (C)). Caterpillar body temperature was significantly lower inside than outside the hummock (one-way ANOVA: F1,54 ¼8.00; P¼0.0065; mean temperature and 95% confidence interval: 22.272.5 1C inside vs. 25.070.8 1C outside). Moreover, the excess of body temperature above ambient temperature ranged between 0.16 and 9.0 1C inside the hummock and reached larger values outside the hummock (up to 14 1C).
3.3. Experimental demonstration that B. eunomia caterpillar body temperature is affected by both the position on the tussock and the substrate color Temperature around the tussock was significantly different according to the position on the tussock (ANOVA: F2,245 ¼782.32, Po0.0001; Fig. 1A). Temperature decreased from the ground to the top (mean 795% confidence interval: 24.471.8 1C ground; 19.871.0 1C middle; 17.070.7 1C top). B. eunomia caterpillar body temperature ranged from 12.7 to 39.3 1C and from 12.4 to 36.3 1C on green and brown substrates, respectively. Two-way ANOVA analysis indicated that body temperature was affected by substrate color (greenobrown: F1,486 ¼106.11, Po0.001), height at which the caterpillar was located (ground4middle4top: F2,486 ¼157.87, Po0.001) and the interaction between both factors (F2,486 ¼13.43, Po0.001) (Fig. 1B). This interaction indicates that caterpillar body temperature on the green substrate was less dependent on the height at which the caterpillar was located than when it was on the brown substrate. Temperature and light intensity were significantly different relative to exposition side (one way ANOVAs; temperature: F3,231 ¼8921.4, Po0.0001, Fig. 2A; light intensity: F3,231 ¼64.5, Po0.0001, Fig. 2B). As expected, temperature (mean795% confidence interval) was highest towards the south (31.570.1 1C), intermediate towards the east (25.870.1 1C) and the west (25.470.2 1C), and lowest towards the north (21.9 70.1 1C). Light intensity (means795% confidence interval) decreased from the east (1997 14 lx), south (1627 11 lx), west (142 78 lx) to the north exposition (108 78 lx).
Substrate color:
Green
Brown
1.5 1 0.5 0 -0.5 -1 -1.5
Caterpillar Ground position:
Middle
Top
Fig. 1. (A) Standardized ambient temperature differed according to the position on the tussock (ground, middle and top level). (B) Standardized body temperature of B. eunomia differed according to position on tussock and substrate color (green: white dots and brown: black dots), as it was less dependent on the position on the tussock when located on the green support compared to the brown one. For both panels, values are means7 95% confidence interval.
a
1 0.5 0
b
c
-0.5 d
-1
-1.5 Recoder South East exposition:
West North
1.5
177
1.5 b
1 a
0.5
c
0
d
-0.5 -1
-1.5 Recorder South East exposition:
West North
Standardized body temperature
1.5
Standardized light intensity
Standardized airtemperature
C. Turlure et al. / Journal of Thermal Biology 36 (2011) 173–180
a
1 0.5 0 -0.5
b c
-1
-1.5 Caterpillar South East West North exposition:
Fig. 2. Standardized temperatures (A), light intensity (B), and body temperatures of B. eunomia caterpillars (C) differed according to exposition sides. Values are means7 95% confidence interval. Groups displayed with the same letter were not significantly different at the 0.05 level (Tukey–Kramer studentized range test).
Table 2 Factors affecting B. eunomia caterpillar body temperature (estimated using best model from Appendix 1 (D)). For categorical variables, the estimate expresses the difference with the reference level (fixed to zero). Caterpillar body temperature was (1) positively related to both air temperature and light intensity, (2) lower for the three first sampling periods, highest for the next sampling period and decreasing again for the last sampling period (R2 ¼ 0.57). Environmental factor
Modalities
Intercept Air temperature (1C) Light intensity (klx) Sampled periods
Estimate 23.76 0.13 0.10
11:00–12:00 11:20–12:20 16:00–17:00 16:30–17:30 17:30–18:30
10.02 3.82 5.17 7.22 0
SE 0.90 0.03 1.0 10 5 0.62 0.61 0.49 0.59 /
Caterpillar body temperature ranged from 21.2 1C in the north to 32.1 1C in the south, and differed significantly among the four directions (one-way ANOVA: F3,228 ¼108.52, Po0.001). Body temperature was highest for the south and east expositions, intermediate for the west exposition, and lowest for the north exposition (Fig. 2C). Overall, B. eunomia caterpillar body temperature was positively related to both temperature and light intensity (see Appendix 1 (D) for model selection and Table 2 for parameter estimates using best model). It was lowest in the morning (i.e. sampling period: 11.00–12:00; external temperature ranging from 11.5 to 31.7 1C; light intensity ranging from 64.6 to 55,111.5 lx), highest in the afternoon (i.e. sampling period: 16:00–17:00; external temperatures ranging from 13.2 to 32.1 1C, light intensity ranging from 64.6 to 44,089.2 lx), and decreasing again later in the afternoon (i.e. sampling period: 17:30–18:30; external temperature ranging from 15.9 to 35.6 1C; light intensity ranging from 1 to 22,045 lx).
4. Discussion 4.1. Influence of weather conditions on caterpillar detection probability Within habitat patches, caterpillars of B. eunomia and B. aquilonaris were easier to detect under weather conditions characterized by lower temperatures and specific cloud cover conditions: clearer sky for B. eunomia, (partly) clouded sky for B. aquilonaris. This suggests that during periods of inappropriate weather conditions, caterpillars stayed hidden inside the vegetation structures. For B. aquilonaris, this finding was experimentally
confirmed by the fact that caterpillars went inside in the hummock under increased light intensity. Defining the weather conditions that are favorable for caterpillar detection is important to optimize search efforts to find caterpillars (e.g. surveys or monitoring for conservation programs), and is essential for understanding correctly larval habitat-use and the behavioral mechanisms of caterpillar thermoregulation (Nice and Fordyce, 2006; Sherman and Watt, 1973). Caterpillar body temperature of both species was related to ambient temperature, and also to light intensity for B. eunomia. While the impact of ambient temperature on caterpillar body temperature has been reported by many studies, the positive influence of light intensity has not received as much attention yet (but see Porter, 1982; Klok and Chown 1999; Bryant et al., 2000 for examples). As predicted, the larval stages of B. eunomia and B. aquilonaris use suitable microclimates provided by structural vegetation elements (i.e. Sphagnum hummocks and grass tussocks, respectively) around the host plant in order to cope with variable weather conditions. 4.2. Use of suitable microhabitat Sphagnum hummocks provide a range of temperature conditions; the temperature of the external part of this structure was directly influenced by air temperature and light intensity, whereas the interior part provided stable and cool thermal conditions (Turlure et al., 2010; van der Molen and Wijmstra, 1994). Indeed, higher light intensity conditions are likely to induce warming up of local structural vegetation elements. This process depends on the water content of the hummocks due to relatively high thermal conductivity of water (van der Molen and Wijmstra, 1994) and decreased albedo – and correspondingly, energy reflectance – with higher moisture content (Nungesser, 2003). Additionally, the water content of hummocks may influence the temperature through a cooling effect of the latent heat flux of evapotranspiration. Here, we showed that the body temperature of B. aquilonaris caterpillars that were located on top of a hummock was higher than those that were located inside the hummock, which is probably due to the direct absorption of solar radiation. Our previous research showed that the survival of B. aquilonaris larvae was higher under lower temperature conditions (20 vs. 25 1C; Turlure et al., 2010). Therefore, we suggest that B. aquilonaris uses behavioral thermoregulation through micro-site selection, moving to different positions within the Sphagnum hummock. Inside the hummock, B. aquilonaris caterpillars adopted a temperature conformer strategy, at a lower but stable temperature, which is probably less physiologically costly (Knapp and Casey, 1986). When they reached the hummock surface to feed on the host plant, their body temperature increased above the ambient temperature exposing them to overheating and desiccation risks.
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Tussocks are cone-shaped structures, presenting a range of temperature conditions according to their shape and their exposition sides: temperature conditions were higher on the ground compared to the top, which can be related to the shelter properties of a tussock against the wind, and temperature was also higher on the south and east sides compared to the north and west sides. Body temperature of B. eunomia caterpillars decreased when changing the location from the plates located at ground level to the top of the tussock, and from the north to the south. From this experiment, we are not able to make a direct conclusion about the strategy B. eunomia individuals adopt for thermoregulation (i.e. conformer vs. active thermoregulator) as caterpillars were indeed not free to move on the tussock. Nevertheless, we hypothesize that caterpillars engage in behavioral thermoregulation as they were observed moving up and down on the tussocks during the day under natural conditions (C. Turlure, personal observation). Further, indirect evidence comes from the fact that B. eunomia caterpillars were difficult to find during cloudy periods; such conditions may hamper caterpillar basking behavior, making it more profitable or safe to stay inside the tussock structure than to move out. Both examples suggest that there is no unique and fixed ‘‘best quality microhabitat’’ in terms of thermal conditions within structural vegetation elements for the caterpillar stages. Microhabitat use is conditioned by both the environmental conditions and the internal state of the individual. So, requirements of caterpillars will change depending on the time of day and surrounding conditions, which may induce displacements to a place with beneficial conditions at a particular time (see Dennis and Sparks (2006) for a similar example for adult stages). Further experimental studies are now warranted to analyze how different thermal regimes that vary over time and micro-space affect development and survival (Barghusen et al., 1997; Bryant et al., 2000). However, the dependence of the caterpillar body temperature on the position within the peat bog vegetation structure indicates that these structures provide heterogeneous thermal conditions. Therefore, these structural elements should be considered an important resource, and hence an important habitat aspect of each species.
with plant tissue. A similar case was reported by Kukal et al. (1988) for G. groenlandica, which used the snow albedo to raise body temperature up to 20 1C above the ambient temperature. Previous research on the same study system showed that temperature did not affect caterpillar survival, but positively influenced caterpillar growth rate (Augem, 2007). Despite the benefit of the green substrate in terms of conferring elevated body temperatures, caterpillars were as likely to be found on both substrate colors. From a functional point of view, this suggests that there should be advantages and disadvantages associated with each color relative to the prevalent environmental conditions. A trade-off between adopting aposematic caterpillar body color but losing the possibility to thermoregulate optimally versus a dark body color that allows basking for elevation of body temperature but also increasing predation or parasitism risk has been reported for caterpillars in several other species (for examples, see Reader and Hochuli, 2003; Nice and Fordyce, 2006). Such potential interactions with background matching need further testing.
5. Conclusions Our field observations showed that both species are able to modify their position within the vegetation and their behavior depending on weather conditions. Moreover, our experiments demonstrated that caterpillars can actively use microclimatic gradients provided by structural vegetation elements to avoid thermal stress, which may occur on a daily basis due to temperature fluctuations. How these behavioral adaptations will allow these glacial relicts to cope with future climate warming remains still an open question. However, our results show that habitat management strategies aiming at the preservation of structural vegetation elements will be of the utmost importance for the survival of caterpillars, and, hence for the conservation of viable populations. These management measures should be planned rigorously taking into account ongoing and future climate changes.
Acknowledgments 4.3. Possible extra functions provided by structural vegetation elements Besides a diversity of thermal conditions, vegetation structures supply variation for other microclimatic variables as well. Hummocks are, for example, a valuable source of moisture for caterpillar development in B. aquilonaris (C. Turlure, personal observation). Other functions include providing cryptic color and conferring lower predation pressure, lower parasitism load (Karban (1998) reported the case of ‘behavioral fever’ for caterpillars of Platypteria virginalis, which elevate body temperature by basking on dead vegetation in order to cure themselves from parasitoids), or flooding avoidance (Coenonympha tullia climbs on the tussocks of Eriophorum vaginatum in order to avoid submergence during the winter (Joss et al., 1988; Joy and Pullin, 1997); in a similar manner, Sei and Porter (2003) described the vegetation types conferring higher survival from flooding for C. tullia nipisquit). Microhabitat use will hence be influenced by factors other than host plant use and thermoregulation, but still little is known about the factors that affect the selection of microhabitat for shelter (e.g. pupation or larval molting). In the case of B. eunomia, we observed that caterpillar body temperature was higher on a green substrate, which probably can be explained by the higher reflectance of green surfaces compared to the brown ones, even if wooden plates may have very different thermal properties (including specific heat capacity) compared
We thank Ame´lie Augem for her valuable help with field work, Jean Clobert for helpful discussions and an anonymous reviewer for his/her valuable comments. C.T. and V.R. were supported by a Ph.D. grant from the FRIA-fund. N.S. is Research Associate of the Fund for Scientific Research-FNRS. Reserves access and a permission to study these protected species in the field were granted by the Ministe re de la Re´gion Wallonne. This is publication BRC207 of the Biodiversity Research Centre at UCL. The funders had no rule in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Appendix 1 Modeling (A) B. aquilonaris caterpillar detectability, (B) B. eunomia caterpillar detectability, (C) B. aquilonaris caterpillar position (inside vs. outside Sphagnum hummock) and (D) B. eunomia caterpillar body temperature using linear or logistic regression models with AIC model selection. Are presented for each model: the list of covariates and variables considered, the number of estimated parameters, the AIC value and the difference (D) of AIC with the lowest-AIC model. Supported models (models with DAICo2) are indicated by nnn and selected best model is in bold (Table A1).
C. Turlure et al. / Journal of Thermal Biology 36 (2011) 173–180
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Table A1 Species
Response variable
Model
Covariates
Variables in the model
(A) B. eunomia
Caterpillar detectability
Linear
Habitat quality + sampling effort
Cloud cover+ air temperature
(B) B. aquilonaris
(C) B. aquilonaris
(D) B. eunomia
Caterpillar detectability
Caterpillar position
Caterpillar body temperature
Linear
Logistic
Linear
Habitat quality + Sampling effort
/
Sampling period
References Agilletta, M.J., 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press, Oxford. Albanese, G., Vickery, P.D., Sievert, P.R., 2007. Habitat characteristics of adult frosted elfins (Callophrys irus) in sandplain communities of southeastern Massachusetts, USA. Biol. Conserv. 136, 53–64. Albanese, G., Vickery, P., Sievert, P., 2008. Microhabitat use by larvae and females of a rare barrens butterfly, frosted elfin (Callophrys irus). J. Insect Conserv.. Alonso, C., 1997. Choosing a place to grow. Importance of within-plant abiotic microenvironment for Yponomeuta mahalebella. Entomol. Exp. Appl. 83, 171–180. Aschcroft, M.B., Chisholm, L.A., French, K.O., 2009. Climate change at the ladscape scale: predicting fine-grain sptial heterogeneity in warming and potential refugia for vegetation. Global Change Biol. 15, 656–667. Augem, A., 2007. La se´lection de l’habitat et son influence sur le de´veloppement de deux espe ces de Le´pidopte res Rhopaloce res (Proclossiana eunomia et Lycaena helle). M.Sc. Thesis, Universite´ catholique de Louvain. Barghusen, L.E., Claussen, D.L., Anderson, M.S., Bailer, A.J., 1997. The effects of temperature on the web-building behaviour of the common house spider, Achaearanea tepidariorum. Funct. Ecol. 11, 4–10. Bryant, S.R., Thomas, C.D., Bale, J.S., 2000. Thermal ecology of gregarious and solitary nettle-feeding nymphalid butterfly larvae. Oecologia 122, 1–10. Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer-Verlag, New York. Casey, T.M., 1976. Activity patterns, body temperature and thermal ecology in two desert caterpillars. Ecology 57, 485–497. Dennis, R.L.H., Sparks, T.H., 2006. When is a habitat not a habitat? Dramatic resource use changes under differing weather conditions for the butterfly Plebejus argus. Biol. Conserv. 129, 291–301. Fichefet, V., Barbier, Y., Baugne´e, J.-Y., Dufrˆene, M., Goffart, P., Maes, D., Van Dyck, H., 2008. Papillons de jour de Wallonie (1985–2007). Publication du Groupe de Travail Papillons de jour Lycaena et du Centre de Recherche de la Nature, des Forˆets et du Bois (MRW-DGRNE), Gembloux. Frears, S.L., Chown, S.L., Webb, P.I., 1997. Behavioural thermoregulation in the mopane worm (Lepidoptera). J. Therm. Ecol. 22, 325–330. Goffart, P., Schtickzelle, N., Turlure, C., 2010. Conservation and management of the habitats of two relict butterflies in the Belgian Ardenne: Proclossiana eunomia & Lycaena helle. In: Habel, J., Assmann, T. (Eds.), Relict Species. Phylogeography and Conservation Biology. Springer, Berlin, pp. 357–370.
Number of parameters nnn
AIC
DAIC
6
164.13
0
(covariates only) nnn Cloud cover nnn Air temperature nnn Cloud cover+ air temperature +(cloud cover air temperature)
3 5 4 8
164.43 165 166.04 166.35
0.3 0.87 1.91 2.22
Cloud cover+ air temperaturennn
6
62.2
0
Cloud cover+ air temperature +(cloud cover air temperature)nnn Air temperature Cloud cover (covariates only)
8
64.13
1.93
4 5 3
65.41 67.81 72.51
3.21 5.61 10.31
nnn
2
44.19
0
Light intensity+ air temperaturennn Light intensity+ air temperature +(light intensity air temperature) Intercept only Air temperature
3 4
46.14 46.26
1.95 2.08
1 2
54.55 56.53
10.37 12.34
7
4156.53
6 6 5
4168.34 4188.26 4197.99
Light intensity
Ambient temperature+ light intensitynnn Light intensity Ambient temperature Intercept only
0 11.81 31.74 41.47
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