國立臺灣大學生命科學院生態學暨演化生物學研究所 碩士論文
Institute of Ecology and Evolutionary Biology College of Life Science
National Taiwan University Master Thesis
斯文豪氏攀蜥與黃口攀蜥之運動生理與溫度特性:
跨海拔之物種內、種間及性別間之比較
Thermal sensitivity of locomotor performance and thermal profiles in two agamid lizards in Taiwan: Intraspecific,
interspecific, intersexual comparisons across altitudes
陳哲豪 Che-Hao Chen
指導教授：林雨德 博士 Advisor: Yu-Teh Kirk Lin, Ph.D.
中華民國 103 年 6 月 June 2014
i
謝誌
鳳凰花開，只能選擇離開，短短兩年的碩士生涯，在不斷忙碌的過程中辛苦 渡過，或許無邪的笑容已經不再精彩，但有你們一路上的支持、幫助與鼓勵才能 完成這篇論文，在此致上我衷心的感激。
首先感謝林雨德老師願意指導我，在研究上提供支持與協助，也讓我有機會 可以去國外參加研討會，開拓視野。剛進研究所的時候，寫推薦信協助申請獎學 金，讓我能在沒有經濟壓力下能專心的進行研究。也感謝老師給我這個機會，讓 我在兩年內完成碩士論文，除了在生態領域的指導外，在面對人生想法及態度上，
讓我有了更進一步的成長。感謝動物生態研究室的各位夥伴們: 淑蕙學姊、邵閔學 長、威廷、善達、艾陵、佳倩、貝珊、柏翰、慶賀、威森、蟲子、文皓、雨珊、
凌軒、肥缺、林杰，在實驗上提供建議與人力上的協助，尤其是善達，在實驗的 架構上給了我很大的幫助，感謝你們這段時間在實驗室的陪伴。
感謝各位口試委員: 陳賜隆老師、何傳愷老師、蔡添順老師在百忙之中抽空閱 讀我的論文，找出問題並提供許多的建議與想法，也謝謝你們的鼓勵。感謝特有 生物中心的林德恩學長提供了實驗器材以及實驗上建議與協助，感謝毅倫和昱凱 在運送實驗器材及出差上的協助。感謝子榮不厭其煩得教我貝氏統計和 R 的編碼，
幫助我能順利分析完成。感謝小松和托托學長在作圖與統計上的諮詢。感謝閣桓、
玉米、渼晨、嚕嚕、長人、小汪協助我進行野外調查。感謝三重薛先生協助我完 成跑步台的零件。感謝宣雅常常在深夜送來溫馨宵夜，感謝台大男壘、台大植昆 系壘讓我在研究之餘，可以宣洩壓力、放鬆身心。感謝難波 5566 們在參加 ESJ 時，
一同留下美好的回憶。感謝在這段時間認識的朋友們，在生活中的噓寒問暖與鼓 勵。感謝每隻實驗的攀蜥都努力地向前衝刺與跳躍。
感謝身邊的好朋友們，有你們的鼓勵、歡笑和嘴砲，使我不畏艱辛地一直走 下去。感謝家人們這些年來的支持與包容，讓我不顧一切地進入生態學領域，完 成我的目標。最後，感謝那個每天努力奮鬥到深夜做實驗、寫論文的自己。
ii
摘要
外溫動物的生理表現隨著體溫變化，其中運動表現對個體的生存有重大的影 響，而研究同一物種在不同溫度環境中族群的運動生理表現可讓我們了解溫度生 理的適應性演化。本研究探討斯文豪氏攀木蜥蜴(Japalura swinhonis)與黃口攀木蜥 蜴(Japalura polygonata xanthostoma)的中海拔族群和低海拔族群在運動生理及溫度 特性上的差異，我測量攀木蜥蜴在六個溫度下的跑步速度與跳躍距離以畫出運動 表現的溫度敏感度曲線(thermal sensitivity curve)，並算出表現寬度(B80)及理想表現
溫度(To)。此外，我測量最高耐受溫度極限(CTmax)、最低耐受溫度極限(CTmin)及個
體在野外環境中的體溫(Tb)，並且透過室內選溫實驗測量蜥蜴的選溫偏好(Tsel)。結
果發現兩種攀蜥在不同海拔的族群在溫度生理上都有適應性演化，但不同的運動 型態的適應情形會隨著物種而不同，而雌雄在溫度生理上的差異只有在黃口攀蜥 發現。然而不同海拔族群或不同性別的攀木蜥蜴在溫度偏好上並無差異。本研究 顯示外溫動物族群在溫度生理上會適應不同的溫度環境。
關鍵字: 溫度敏感度、運動表現、溫度耐受極限、蜥蜴、海拔、雌雄差異
iii
Abstract
Physiological performance varies with body temperature in ectotherms, especially
the locomotor performance which may influence their survivorship. Whether lizard
populations in various thermal environments maintain similar thermal profiles and
thermal performance curves has been debated. In this study, I compared the thermal
characteristics between two populations from lowland and mid-altitude in Japalura
swinhonis and Japalura polygonata xanthostoma. I measured lizard sprint speed and
jump distance at 6 temperatures to calculate performance breadth (B80) and thermal
optimum (To). I also measured thermal tolerance limits (CTmax, CTmin), selected
temperature (Tsel) and field body temperature (Tb). Results showed that in both species
populations from different altitudes had different patterns of thermal sensitivity and
thermal tolerance. Sexual difference in thermal physiology was only found in
J.polygonata xanthostoma. However, there was no significant difference in Tsel between
two altitudinal populations or sexes in both species. My results support the labile view
on the evolution of thermal physiology for lizards.
Keywords: thermal sensitivity, locomotor performance, thermal tolerance, lizard,
altitude, sexual difference
iv
Contents
謝誌 ... i
摘要 ... ii
Abstract ... iii
Introduction ... 1
Materials and Methods ... 8
Study locations ... 8
Field temperatures (T
band T
e) and lizard collection ... 9
Laboratory housing ... 10
Thermal performance curve ... 10
Thermal tolerance ... 12
Selected body temperature (T
sel) ... 13
Morphological measurement ... 14
Constructing the thermal performance curve ... 15
Statistical analyses ... 16
Results ... 18
Thermal sensitivity of sprint speed ... 18
Thermal sensitivity of jump distance ... 18
Thermal tolerance ... 20
Thermal profiles ... 20
Discussion ... 21
v
Intraspecific comparison ... 23
Intersexual comparison ... 24
Interspecific comparison ... 26
Conclusion ... 29
References ... 30
Tables ... 37
Figures ... 57
Appendix ... 74
vi
Contents of Tables
Table 1. Parameters related to the thermal sensitivity of sprint speed in
J.swinhonis. ... 37
Table 2. Parameters related to the thermal sensitivity of sprint speed in J. polygonata xanthostoma ... 38
Table 3. Parameters related to the thermal sensitivity of jump distance in J.swinhonis. ... 39
Table 4. Parameters related to the thermal sensitivity of jump distance in J. polygonata xanthostoma ... 40
Table 5. The thermal tolerance of J. swinhonis.. ... 41
Table 6. The thermal tolerance of J. polygonata xanthostoma. ... 42
Table 7. The thermal profile of J. swinhonis. ... 43
Table 8. The thermal profile of J. polygonata xanthostoma. ... 44
Table 9. Statistical results of two-way ANOVAs using MCMCglmm examining the effects of altitude and sex on various parameters related to the thermal sensitivity of sprint speed in Japalura swinhonis. ... 45
Table 10. Statistical results of two-way ANOVAs using MCMCglmm examining the effects of altitude and sex on various parameters related to the thermal sensitivity of sprint speed in J.polygonata xanthostoma. ... 46
Table 11. Statistical results of two-way ANOVAs using MCMCglmm examining the effects of altitude and sex on various parameters related to the thermal sensitivity of jump distance in Japalura swinhonis. ... 47
Table 12. Statistical results of two-way ANOVAs using MCMCglmm
examining the effects of altitude and sex on various parameters
related to the thermal sensitivity of jump distance in J.polygonata
xanthostoma. ... 48
vii
Table 13. Statistical results of two-way ANOVAs using MCMCglmm examining the effects of altitude and sex on thermal tolerance in Japalura swinhonis. ... 49 Table 14. Statistical results of two-way ANOVAs using MCMCglmm
examining the effects of altitude and sex the thermal tolerance in J.polygonata xanthostoma. ... 50 Table 15. Statistical results of two-way ANOVAs using MCMCglmm
examining the effects of altitude and sex on various parameters related to the thermal profiles in Japalura swinhonis. ... 51 Table 16. Statistical results of two-way ANOVAs using MCMCglmm
examining the effects of altitude and sex on various parameters related to the thermal profiles in J.polygonata xanthostoma. ... 52 Table 17. Means and 95% confident intervals of the thermal sensitivity of
sprint speed in J.polygonata xanthostoma that showed interaction between altitude and sex. ... 53 Table 18. Means and 95% confident intervals of the thermal sensitivity of
jump performance in J.polygonata xanthostoma that showed interaction between altitude and sex. ... 54 Table 19. Comparison of field body temperature (T
b) and operative
temperature (T
e) at mid-altitude and lowland in two Japalura lizards. ... 55 Table 20. Comparison of performance breadth (B
80) between sprint speed
and jump performanceat in J.swinhonis. ... 56
viii
Contents of Figures
Figure 1. Concept map of the current study ... 57
Figure 2. The thermal sensitivity curves of sprint speed in J. swinhonis 58
Figure 3. The thermal sensitivity curves of sprint speed in J.polygonata xanthostom. ... 59
Figure 4. The thermal sensitivity curves of jump distance in J. swinhonis 60 Figure 5. The thermal sensitivity curves of jump distance in J.polygonata xanthostoma ... 61
Figure 6. The critical thermal maximum of J. swinhonis ... 62
Figure 7. The critical thermal minimum of J. swinhonis ... 63
Figure 8. The critical thermal maximum of J.polygonata xanthostoma .... 64
Figure 9. The critical thermal minimum of J.polygonata xanthostoma .... 65
Figure 10. The thermal profiles of mid-altitude J. swinhonis ... 66
Figure 11. The thermal profiles of lowland J.swinhonis ... 67
Figure 12. The thermal profiles of mid-altitude J.polygonata xanthostoma ... 68
Figure 13. The thermal profiles of mid-altitude J.polygonata xanthostoma ... 69
Figure 14. The monthly mean temperature at four study locations ... 70
Figure 15. The thermal profiles of J.swinhonis ... 71
Figure 16. The thermal profiles of J.polygonata xanthostoma ... 72
Figure 17. The contraption for measuring sprint speed of lizards ... 73
1
Introduction
For ectotherms, their physiology and behavior, including locomotion (Bennett,
1980; Hirano and Rome, 1984; Weinstein, 1998; Ojanguren and Brana, 2000), immune
function (Mondal and Rai, 2001), courtship (Navas and Bevier, 2001), foraging ability
(Greenwald, 1974; Ayers and Shine, 1997; Carriere and Boivin, 2001), and rate of
growth and development (Dutton et al., 1975; Kingsolver and Woods, 1997) are highly
sensitive to body temperature. The relationship between body temperature and
performance in ectotherms could be described by the thermal performance curve, or
thermal sensitivity curve (Huey and Stevenson, 1979). The characteristics of thermal
sensitivity curves reveal how organismal performance changes with body temperature.
They generally include thermal optimum (To)—the body temperature when
performance is at its maximum, performance breadth (B80)—the body temperature
range that performance is greater than or equal to 80% of the maximum level, and
critical thermal maximum (CTmax) and minimum (CTmin)—the highest and lowest body
temperature at which the organism loss its ability to perform.
Since environmental temperature may vary spatially and temporally, ectotherms
often use thermoregulation to cope with temperature heterogeneity. They regulate body
temperature within a specific range through behavioral, physiological, or morphological
changes to maintain high level of performance (Avery, 1982; Hutchison and Dupre,
2
1992). However, thermoregulation may incur costs, such as increased risk of predation
(Huey and Slatkin, 1976). In addition, thermoregulation may not be effective under
certain circumstances, such as constant low or highly fluctuating environmental
temperature or competition for basking perches among individuals. Ectotherms, thus,
may fail to maintain proper body temperature for daily activities, such as feeding,
reproduction, and escaping predators (Huey and Slatkin, 1976). Therefore, one would
expect ectotherms evolve to adapt to different thermal environments (Kingsolver and
Huey, 1998). Thermal adaptation should alter the parameters of thermal sensitivity
curves including To, B80, CTmax, or CTmin.
To understand thermoregulation and its evolution, one needs to know the thermal
profiles of ectotherms as well (Huey and Slatkin, 1976; Hertz et al., 1993), which
includes three important variables: the environmental temperature (Te, or operative
temperature); the field body temperature (Tb) that ectotherms achieve in the
environment; and the selected body temperature (Tsel) that ectotherms choose under
ideal thermal gradient conditions. Tb does not necessarily conform to Tsel, and may be
seen as the result of the compromise between the Tsel and Te.
Many types of individual performance could be examined to construct the thermal
performance curves. Among them, locomotor performance such as swimming, jumping,
and sprinting that involve whole-organism performance (Bennett, 1990) is often
3
adopted because it affects foraging efficiency, predator avoidance, survivorship, and
finally the fitness (Greenwald, 1974; Christian and Tracy, 1981; Jayne and Bennett,
1990; Robson and Miles, 2000; Husak, 2006). . The thermal sensitivity curves of
locomotor performance in association with thermal profiles have been estimated for
many species. For example, in Anolis lizards, the To for sprint speed was correlated with
field Tb, and both the 95% performance breadth (B95) and the thermal tolerance (CTmax
─ CTmin) were positively correlated with the range of field Tb (van berkum, 1986).
Similarly, Huey and Kingsolver (1993) conducted a comparative study on thermal
sensitivities for sprinting speed among iguanid lizards, and found that To was positively
correlated with field Tb, and with CTmax. These results indicated that evolutionary
responses to thermal environments (Te) have occurred. Previous studies on amphibians
have also shown similar patterns in thermal physiology. Navas (1996a, b, 1997)
compared thermal sensitivity curves of swimming among families: Dendrobatidae,
Hylidae, Bufonidae, and Leptodactylidae. He found that high-elevation species had
lower To and wider B80 than their congener from low-elevation.
These interspecific comparative studies in reptiles and amphibians indicated that
thermal sensitivity of locomotor performance could adapt to thermal variations along
the altitude or latitude cline (Huey et al., 1989). That is, many thermal physiological
parameters are labile, at least in some taxa. However, interspecific comparison may be
4
influenced by variables other than habitat differences (Pearson et al., 2002).
Intraspecific comparison is better than interspecific ones for inferring evolutionary
adaptation in response to changes in thermal environments or geographic variation in
climate (Van Damme et al., 1989; Huey and Kingsolver, 1993; Bennett and Lenski,
1999; Feder et al., 2000; Qualls and Shine, 2000; Angilletta et al., 2002; Kiefer et al.,
2005). Yet, few studies have been conducted that examined intraspecific comparisons.
For example, eastern fence lizard (Sceloporus undulatus) from two altitudinal
populations had identical To for sprinting speed despite the difference in field Tb
(Crowley, 1985). A research on the wall lizard (Podarcis tiliguerta) found that field Tb
differed between low- and high-elevation populations, but To and B80 for sprinting speed
were identical in both populations (Van Damme et al., 1989). These results indicate that
the evolution of thermal sensitivity of locomotor performance may be conservative
within species even though there exists great divergence in the thermal environment. In
contrast, a labile view of evolutionary thermal physiology has its support. For example,
Beuchat et al. (1984) found the Puerto Rican robber frog (Eleutherodactylus
portoricensis) in the montane area jumped poorly at high Tb while jumped well at low
Tb, compared to its lowland congener. In all, more intraspecific comparative studies
along latitude or altitude clines are needed to reveal the relationship between the
characteristics of thermal sensitivities and thermal environments. This is a major gap in
5 the studies of evolution of thermal physiology.
Another major gap is that most studies of evolution of thermal physiology have
ignored the intersexual difference within species. Sexual differences in life-history
(Shine, 2005), behavior, and activity (Kerr and Bull, 2006) have been studied in a few
reptilian species. They suggested that males and females might prefer different Tb, and
use different thermoregulatory strategies. Indeed, several studies have shown sex
differences in thermal tolerance (Lailvaux and Irschick, 2007), Tsel (Sievert and
Hutchison, 1989), field Tb (Brown and Weatherhead, 2000; Singh et al., 2002;
Fitzgerald et al., 2003), and sprint speed (Cullum, 1998; Lailvaux et al., 2003). These
results indicated that we should routinely consider sex a variable when conducting
studies on thermal physiology.
To fill the two gaps, I studied the thermal physiology of two agamid lizards,
Japalura swinhonis and Japalura polygonata xanthostoma. They are endemic species
and subspecies of Taiwan, respectively. J. swinhonis distributes the whole island, while
J. polygonata xanthostoma distributes in northern Taiwan. Both species occur from
lowland to mid-altitude (Ota, 1991; Hsiang, 1997; Kuo et al., 2007), and provide an
altitudinal cline for investigating intraspecific variation. Both Japalura lizards have
sexual dimorphism, especially J. swinhonis (Lin and Lu, 1982; Kuo et al., 2007; Kuo et
al., 2009). However, the two species dwell in different habitat types. J. swinhonis occurs
6
more often in human-inhabited areas, while J. polygonata xanthostoma in forested areas
(Shan, 2013). Since human-inhabited areas are generally more open, thus have higher
air temperatures than forested areas, the two species encounter different thermal
environments both within and across altitudes. It offers a great opportunity to examine
the inter-specific, intra-specific, and inter-sexual variations in thermal sensitivity curves,
thermal profiles, and their relationships. Overall, my research goals are as follows: (1)
To examine the evolutionary pattern of thermal physiology by comparing
intra-specifically between lowland and mid-altitude populations in both J. swinhonis
and J. polygonata xanthostoma; (2) To examine sexual difference in thermal physiology
in J. swinhonis and J. polygonata xanthostoma; and (3) To compare the extent of
thermal adaptation between J. swinhonis and J. polygonata xanthostoma. Figure 1 gives
the concept map of the current study.
To fulfill the goals, I compared the thermal sensitivity in locomotor performance
between lowland and mid-altitude populations as well as between two sexes in both J.
swinhonis and J. polygonata xanthostoma. I measured sprint speed and jump distance as
locomotor performance. Both types of locomotion are important for arboreal lizards
(Losos and Irschick, 1996; Irschick and Losos, 1998). I also measured the thermal
profiles: field body temperature (Tb), operative temperature (Te), and selected body
temperature (Tsel) of Japalura lizards. I tested the following hypotheses: (1)
7
Mid-altitude and lowland population lizards inhabit different thermal environments,
thus have different thermal sensitivity of locomotor performance and thermal tolerance.
(2) J. swinhonis and J. polygonata xanthostoma have sexual difference in thermal
sensitivity of locomotor performance, thermal tolerance and thermal profiles. (3) J.
swinhonis and J. polygonata xanthostoma have different extent of thermal adaptation
across altitudes.
8
Materials and Methods
Study locationsThe study was conducted, for each species, in one mid-altitude and two lowland
locations, each. The mid-altitude location for Japalura swinhonis was the Xi-Tou
Nature Education Area (23°67’N, 120°80’E) at an altitude of 1100–1150m. The mean
temperature from June to September is 20.42±0.43°C (data obtained from Xi-Tou
weather station, Experimental Forest of National Taiwan University, 2005-2013). The
survey trail was about 2 km in length. The lowland locations for Japalura swinhonis
were at the general area encompassed by the Fu-Yang Eco Park (25 °00’N, 121°33’E)
and Fu-Jou-Shan Park (25°10’N, 121°33’E) at an altitude of 25-40m and 20-55m,
respectively. The mean temperature from June to September is 28.48±1.09°C (data
obtained from Data Bank for Atmospheric Research, 1998-2010). The survey trail was
about 3 km in length.
The mid-altitude location for Japalura polygonata xanthostoma was the
Ming-Chih Forest Recreation Area (24°39’N, 121°28’E) at an altitude of 1150-1180m.
The mean temperature from June to September is 16.75±1.50°C (data obtained from the
Ecological and Environmental GIS database for Taiwan, Council of Agriculture,
1997-2010). The survey trail was about 2 km in length. The lowland locations for
Japalura polygonata xanthostoma was at the general area that covered Min-Jiu-Shan
9
Mountain Trail (25 °05’N, 121°37’E) at an altitude of 30-40m, and Jin-Mian-Shan
Hiking Trail (25 °09’N, 121°58’E) at an altitude of 25-30m. The mean temperature from
June to September is 27.68±1.36°C (data obtained from the Data Bank for Atmospheric
Research, 1998-2010). The survey trail was about 2 km in length.
Field temperatures (Tb and Te) and lizard collection
I sampled the lowland populations of Japalura swinhonis and Japalura polygonata
xanthostoma from June to October, and the mid-altitude populations from July to
September in 2013. I surveyed at least three times at each location. Generally, a survey
began at 0800~0830 in the morning or 1400~1430 in the afternoon, depending on
weather conditions. During surveys, I walked leisurely along trails, and captured lizards
by hand or noose. Each captured lizard was measured field body temperature (Tb)
immediately by inserting a thermocouple probe (DTM317, TECPEL, Inc., Taipei,
Taiwan) into their cloaca. The operative temperature (Te, or environmental temperature)
was recorded by measuring the substrate where the lizard was perching on using a
portable infrared thermometer (LS-E2006-01-A, OPTRIS, Inc., Berlin, Germany). I also
recorded species, sex, snout vent length, and initial perch height of the lizard. The lizard
was then put in a cloth bag, and brought back to the laboratory within 24 hrs. Lizards
that were pregnant, or had tail loss or injury were released at site.
10 Laboratory housing
Upon returning to the laboratory, I housed lizards individually in glass tanks
(L×W×H: 35×21×26 cm3) with 3-cm-depth potting soil substrate and a leaning rod for
perching. Tanks were maintained in growth chambers (CK-68E, CHANG-KUANG, Inc.,
Taipei, Taiwan) with a L:D=13:11 light cycle. The temperature was set at 30°C at light
and 25°C at dark for lowland populations; 26°C at light and 20°C at dark for
mid-altitude populations. The settings followed the average temperatures in the field. I
monitored the health of lizards daily, and provided two small crickets with calcium
powder and ad lib water to each lizard daily. Lizards from each population were
randomly divided into two groups: one is for measuring the locomotor performance:
sprint speed and jump distance; the other for measuring thermal tolerance and selected
body temperature (Tsel). The reason for dividing the lizards into two groups was to
reduce the housing period, and the potential for laboratory temperature acclimation. All
laboratory trials were completed within 10 days of capture of lizards.
Thermal performance curve
I obtained thermal performance curve (thermal sensitivity curve) by measuring the
sprint speed and jump distance of lizards in performance trials. I measured the sprint
11
speed by chasing lizards up a 10-cm-diameter rod. The rod was 250-cm in length, and
held at a 60° incline angle. Along the length of the rod, I set up eight pairs of photocells
at 10-cm intervals at the mid-section of the rod (Fig. 17). As a sprinting lizard crossed
the consecutive light beams of the photocells (Nine Section Photoelectric Timer,
POWCHUNG, Inc., Taipei, Taiwan), the time it crossed each bean would be recorded
by a photoelectric timer. I calculated the sprint speed from the travel distance and time
recorded. The sprint speed of each lizard was measured at six different body
temperatures: 20, 25, 27.5, 30, 32.5, 35°C in random order. In the beginning of a trial, I
placed a lizard in a growth chamber set at the target temperature for 1 hour. The lizard
was then removed from the growth chamber, its body temperature measured with a
thermocouple probe to be sure it reached the target temperature. Immediately, I placed
the lizard on the race rod, and chased the lizard up the rod. I measured lizard body
temperature immediately after the trial to ensure it did not deviate more than 1°C from
the target temperature. The sprint speed of each lizard was measured three times per
temperature with a 1-hour rest in the growth chamber between trials. The average sprint
speed measured for each individual at a given temperature entered the subsequent
analyses. The lizards get a full day’s rest between trials performed at different
temperatures. Overall, there were six average sprint speeds (one at each temperature) for
each lizard.
12
I measured the jump distance by probing lizards to jump from a platform (L×W×H:
10×10×9 cm3) in an arena (L×W×H: 98×30×30cm3). The platform was at one end of the
arena, and a shelter (a halved flowerpot) at the other end. Lizards were induced to jump
toward the shelter, and the jump distances were recorded by a video camera
(HDR-SR12, SONY, Inc., Tokyo, Japan). Similar to the procedures used for measuring
sprint speed, jump distance of each lizard was measured three times at each temperature
on the same days upon the completion of sprint speed trials. The maximum jump
distance measured for each individual at a given temperature entered the subsequent
analyses. Overall, there were six maximum jump distances (one at each temperature) for
each lizard.
Thermal tolerance
The two ends of a thermal performance curves are the critical thermal minimum
(CTmin) and the critical thermal maximum (CTmax). I determined the two critical values
by measuring the temperatures at which a lizard lost righting response (Lutterschmidt
and Hutchison, 1997a, b). In the beginning of a trial, a lizard, still in the housing tank,
would be moved from growth chamber and placed in room temperature for an hour to
allow the lizard adjust to the ambient temperature. To determine the CTmax, I inserted a
thermocouple probe into the lizard’s cloaca, then placed the lizards under a ceramic heat
13
lamp (7Z-JT-250W, ZOOLIFE, Inc., Taipei, Taiwan), and constantly checked its
righting response. By adjusting the distance between lizard and lamp, I raised the
lizard’s body temperature at approximately 1°C/min until it lost righting ability. I
followed similar procedures to determine the CTmin, except that the lizard was put in an
open ziplock bag and submerged in 1°C ice water. By adjusting the submerge time, I
lowered the lizard’s body temperature at approximately 1°C/min until it lost righting
ability. The CTmax and CTmin trials were conducted one day apart.
Selected body temperature (Tsel)
This experiment was conducted in a cold room in which temperature was
maintained at 18°C. I fitted four steel temperature gradient troughs (L×W×H:
98×30×30cm3) with 3-cm-depth potting soil substrate in the room. Two ceramic heat
lamps (250W and 150W, respectively) were suspended at one end and 1/4 length,
respectively, of each trough as heat sources, to create a thermal gradient ranged from 18
to 60°C. Lizards would be moved from growth chamber, and randomly placed into
troughs at 0700 hour, one in each. They were free to move around within troughs. At
1500 hour, I measured the body temperatures of lizards as their selected body
temperatures (Tsel), and replaced the lizards back to its housing chamber. The trial was
repeated on the second day, so the selected body temperature was measured twice for
14
each lizard. I used the mean of the two readings as the selected body temperature (Ji et
al., 1996; Ji et al., 1997; Xu et al., 1999; Du et al., 2000; Chen et al., 2003; Zhang and Ji,
2004).
Morphological measurement
I recorded 13 morphological variables for each lizard using an electronic vernier
caliper. I measured: head length (HL, measured from quadrate to the tip of snout), head
width (HW, the distance between jaw joints on each sides), head height (HH, measured
from lower dentary to the parietal), body width (BW, measured from the longest
distance between each side of body), body height (BH, longest distance between dorsal
and ventral), snout-ventral length (SVL, measured from the cloacal opening to the tip of
snout), tail length (TL, measured from cloacal opening to the tip of tail), right forelimb
length (Flimb, measured from the upper arm joint to wrist), right forelimb palm length
(Fpalm, measured from wrist to the base of longest toe), length of the longest toe of
right forelimb (Ftoe, measured from toe base to tip, claws were not included), right
hindlimb length (Hlimb, measured from the upper leg joint to ankle), right hindlimb
palm length (Hpalm, measured from wrist to the base of longest toe), length of the
longest toe of right hindlimb (Htoe, measured from toe base to tip, claws were not
included).
15 Constructing the thermal performance curve
There were six body temperature-specific average sprint speeds for each lizard.
First, I transformed the absolute average sprint speeds (cm/sec) into relative sprint
speeds (%) by dividing each value by the highest value. Ideally, the six relative sprint
speeds could be connected by a minimum convex polygon on a speed-by-temperature
space (van Berkum 1985). If a sprint speed fell inside the polygon, it would be
considered an underestimation, and replaced by a value interpolated from other values
that fitted the polygon (van Berkum 1985). After I connected the six relative sprint
speeds on the speed-by-temperature space, I joint them to thermal tolerance. Since the
lizards that I measured sprint speeds and those I measured thermal tolerance were not
the same individuals, I used universal CTmin and CTmax (mean CTmin and mean CTmax
per sex per population per species) as the two end points of all thermal performance
curves. After completing a thermal performance curve on the speed-by-temperature
space, I extracted the lower and higher bound of body temperature at which lizard can
sprint at 80% of its maximum (L80 and H80, respectively) and 95% of its maximum (L95
and H95, respectively). From them, I obtained two performance breadth readings: B80
and B95, calculated as the difference between L80 and H80, and between L95 and H95,
respectively. Finally, To, defined as the body temperature at which individual
16
performance is at maximum, was calculated as the midpoint of the B95. Following the
same procedures, I also constructed the thermal performance curve based on the six
body temperature-specific maximum jump distances for each lizard.
Statistical analyses
To test the effects of altitude and sex on the temperature-specific locomotor
performance, thermal tolerance, and thermal profiles, I conducted two-way ANOVAs
using Markov chain Monte Carlo (MCMC) generalized linear mixed models
(implemented in the R 3.0.2 package R2WinBUGS running WinBUGS 1.4.3). With
priors set at ‘uninformative’ and intercept set at ‘lowland female’, I ran three parallel
MCMC sampling chains of 30000 iterations each, and saved one per 15 iterations as
samples, a total of 6000 samples. Autocorrelation between successive stored iterations
for all chains were low (ACF < 0.1 in all chains). For all parameters (H95, L95, H80, L80,
B95, B80, To) I tested, the 3 chains (models) showed sufficient convergence (Rhat < 1.05
in all parameters). I carried out permutation t-tests (5000 permutations) to evaluate the
differences between two types of locomotion in parameters of thermal sensitivity. I also
used permutation t-tests (5000 permutations) to evaluate the differences between
thermal profiles (Tb, Te and Tsel).
I generated size-independent estimates of morphological traits by the following
17
procedures. First, I performed a principal component analysis that included 13
morphological variables (HL, HW, HH, BW, BH, SVL, TL, Flimb, Fpalm, Ftoe, Hlimb,
Hpalm, Htoe), and used the first principal component (PC1) to represent the overall
body size. I regressed each morphological variable against PC1, and used the residuals
against regression line as size-independent estimates of morphological traits
(standardized traits, hereafter). I used two-way ANOVAs to compare the standardized
traits between two altitudinal populations and sexes.
18
Results
Thermal sensitivity of sprint speedIn Japalura swinhonis, both B80 and B95 of mid-altitude population were broader
than those of lowland population (two-way ANOVAs, B80: pMCMC <0.01, B95:
pMCMC <0.05, Table 1 and 9, Fig. 2). In addition, H95, L95, H80, L80, and To (Table 1) of
mid-altitude population were lower than those of lowland population (pMCMC <0.001
in all cases, Table 9, Fig. 2). However, there was no sexual difference in thermal
sensitivity of sprint speed in J. swinhonis.
In Japalura polygonata xanthostoma, there was no difference in L95 and L80
between altitudes or sexes (two-way ANOVAs, Table 2 and 10, Fig. 3). There was no
altitude effect in B95 (pMCMC =0.94) or B80 (pMCMC =0.21, Table 10). Sexual
difference occurred in B95 (pMCMC <0.05), and marginally in B80 (pMCMC =0.06,
Table 10). B95 or B80 of males was broader than that of females (Fig. 3). Interactions
occurred between altitude and sex. In males, H95, H80, and To of mid-altitude population
were lower than those of lowland population (H95: pMCMC <0.001, H80: pMCMC
<0.001, To: pMCMC <0.01); whereas there was no altitudinal difference in
females(Table 17, Fig. 3).
Thermal sensitivity of jump distance
19
In J. swinhonis, there was no difference in L95, B95, and B80 between altitudes or
sexes (Table 3 and 11, Fig. 4). H95, H80, L80, and To of mid-altitude population were
lower than those of lowland population (two-way ANOVAs, H95: pMCMC <0.01, H80:
pMCMC <0.01, L80: pMCMC <0.05, To: pMCMC <0.05, Table 11, Fig. 4). There was no
sexual difference in jump distance (Table 11, Fig. 4).
In J. polygonata xanthostoma, L80, L95, and To of mid-altitude population were
lower than those of lowland population (two-way ANOVA, L80: pMCMC <0.01, L95:
pMCMC <0.001, To: pMCMC <0.01, Table 4 and 12, Fig. 5); L80 of males was lower
than that of females (pMCMC <0.05, Table 12, Fig. 5). B80 of mid-altitude population
was broader than that of lowland population (pMCMC <0.001, Table 12, Fig. 5); B80 of
males was broader than that of females (pMCMC <0.01, Table 12, Fig. 5). There were
interactions between altitude and sex in H95 and B95 (H95: pMCMC <0.05, B95: pMCMC
<0.05, Table 12, Fig. 5). In males, H95 of mid-altitude population was lower than that of
lowland population; whereas there was no altitudinal difference in females (Table 18,
Fig. 5). B95 of mid-altitude population was broader than that of lowland population in
males; whereas there was no altitudinal difference in females (Table 18, Fig. 5). There
was no significant difference in H80 between altitudes or sexes (Table 12, Fig. 5).
Thermal tolerance
20
There was a significant difference in CTmax between altitudes in J. swinhonis
(Table 5). CTmax of lowland population was higher than that of mid-altitude population
(ANOVA, pMCMC <0.05, Table 13, Fig. 6). In J. polygonata xanthostoma (Table 6),
CTmax of males was higher than that of females, and CTmin of mid-altitude population
was lower than that of lowland population (ANOVA, CTmax: pMCMC <0.01, CTmin:
pMCMC<0.001, Table 14, Fig. 8, Fig. 9).
Thermal profiles
Field Tb and Te of mid-altitude population were lower than those of lowland population
in J. swinhonis (Two-way ANOVAs, Tb: pMCMC <0.001, Te: pMCMC<0.001, Table 7
and 15). J. polygonata xanthostoma had a similar pattern. Field Tb and Te of
mid-altitude population were lower than those of lowland population (Tb: pMCMC
<0.001, Te: pMCMC <0.01, Table 8 and 16). However, in both species, there was no
sexual difference in Tb or Te (Table 15 and 16). In both species, there was no difference
between altitudes or sexes in Tsel (Table 15 and 16).
21
Discussion
In Taiwan, both Japalura swinhonis and J. polygonata xanthostoma can be found
in drastically different thermal environments. The mid-altitude populations inhabit
thermal environments that have much lower and more variable mean temperatures
(20.42±0.43 and 16.75±1.50°C, respectively) than those of lowland populations
(28.48±1.09 and 27.68±1.36 °C, respectively). Ectotherms in low body temperature
states would have low level of locomotor performance. The impairment of locomotor
performance might result in serious consequences for capturing prey (Greenwald, 1974;
Avery et al., 1982), escaping predation (Webb, 1976; Christian and Tracy, 1981; Hirano
and Rome, 1984), and other fitness-related functions. I observed that both Japalura
species thermo-regulated by choosing micro thermal habitats (Te, 25.09±2.49 and
30.08±1.29°C for mid-altitude and lowland habitats, respectively, for J. swinhonis;
25.34±5.21and 28.72±2.25°C for mid-altitude and lowland habitats, respectively, for J.
polygonata xanthostoma, Table 19) that had much higher temperature than the general
areas could offer. They obtained field body temperatures (Tb) that were in fact
significantly higher than Te, which indicated the two species likely thermo-regulated not
only behaviorally, but also physiologically. However, only the lowland individuals were
able to reach Tbs that were close to the preferred body temperatures (Tsel, 31.19±2.35
and 31.67±2.14°C for mid-altitude and lowland habitats, respectively, for J. swinhonis;
22
29.82±2.10 and 29.86±1.88°C for mid-altitude and lowland habitats, respectively, for J.
polygonata xanthostoma, Table 7 and 8), which were similar between populations and
sexes (Table 15 and 16) within species. Nevertheless, mid-altitudinal populations in
both species have adapted their thermal physiology toward their respective thermal
environments by changing the thermal sensitivity curves and critical temperature limits
(Fig. 2–5). The hypothesis that mid-altitude and lowland population lizards have
different thermal sensitivity of locomotor performance and thermal tolerance is
supported.
While previous studies have failed to find intraspecific difference (Crowley, 1985;
Van Damme et al., 1989), a study on eastern fence lizard, Sceloporus undulates,
suggested that high level of insect densities in high-altitude may allow successful
foraging despite the impairment of locomotor performance (Crowley, 1985). Moreover,
the reduced predator pressure enhanced the survivorship at high elevations and latitudes
in lizards may also contribute to different strength of the relationships between
locomotor performance and fitness among populations (Tinkle, 1969; Pianka, 1970;
Ballinger et al., 1979; Schall and Pianka, 1980). My results suggest that J. swinhonis
and J. polygonata xanthostoma in mid-altitude and lowland might have same prey
availability and predator pressure. Hence, they evolve adaptive thermal sensitivity of
locomotor performance under mid-altitude thermal habitat where temperature is lower
23 and variable.
Intraspecific comparison
I found that generally, several, if not all, parameters of the thermal sensitivity
curves and critical temperature limits of the mid-latitude populations are lower (in H80 ,
H95 , L80 , L95 , To, CTmax and CTmin) and/or broader (in B80 and B95) than those of the
lowland populations. This is particularly true in J. swinhonis. Both in sprinting and
jumping, thermal optimum (To) of mid-altitude J. swinhonis population is lower than
that of lowland population. Moreover, performance breadth (B80) of mid-altitude
population not only shifts to the cold end of thermal sensitivity curve, but also is
broader than that of lowland population. The effect of altitude on B80 occurs
significantly in sprinting (Table 9), but not jumping (Table 11), while the trends are in
the same direction (Table 1 and 3). Since B80 of jumping is generally broader than that
of sprinting (Table 20), it indicates that jumping is less sensitive to body temperature
than sprinting is in J. swinhonis. This is likely due to the weak influence on fitness by
jumping (Huey and Kingsolver, 1993), and may contribute to different evolutionary
patterns between sprinting and jumping.
Compared to J. swinhonis, J. polygonata xanthostoma showed a different pattern
of the thermal sensitivity of locomotor performance. The effect of altitude is not as
24
ubiquitous on the former as on the latter species. In sprinting, mid-altitude population
has lower To than lowland population only in males (Table 10). In jumping, on the other
hand, mid-altitude population has broader B80 and lower To than those of lowland
population in both sexes (Table 12). It seems that in J. polygonata xanthostoma thermal
sensitivity of jump distance is more adaptive than sprint speed to the thermal
environment. It has been suggested that lizards prefer different types of locomotion
when temperature resource is limited (Ibarguengoytia et al., 2007; Aguilar and Cruz,
2010; Fernandez et al., 2011). J. polygonata xanthostoma might prefer jumping to
sprinting while the thermal quality of habitat is low. I expect that J. polygonata
xanthostoma use more jumping movements in the mid-altitude than lowland habitats.
Unfortunately, the frequency of each types of locomotion which J. polygonata
xanthostoma used in natural circumstances is unclear to test such a prediction.
Intersexual comparison
Both J. swinhonis and J. polygonata xanthostoma are sexually dimorphic, with
males having larger body sizes than females, particularly in the former species.
Individuals with large body size have a small volume to surface area ratio, the thermal
inertia of the bodies (trend of a body to resist to changes in its temperature) should be
high. That is, they take longer to reach desired body temperature from exterior heat
25
source, yet could retain body heat longer. Thus, I expect male lizards, being larger, may
be able to thermo-regulate more effectively than females. Regardless of body size
differences, different sexes could also have different physiological abilities and vary in
thermoregulation needs due to differences in reproductive roles (Huey & Pianka 2007).
For example, males are territorial and often fight between individuals. Previous studies
revealed that dominance correlates with activity level in lizards (Brackin, 1978) and
activity level are related to locomotor performance (Bennett et al., 1984; Hertz et al.,
1988; Garland et al., 1990). Thus, males and females could have different field body
temperatures (Tb) and Tsel, and thermal sensitivities.
Although I did not detected sexual difference in Tb or Tsel, I did observe sexual
differences in thermal sensitivity. As stated above, in J. polygonata xanthostoma, I
found altitudinal difference in To of sprint speed occurred only in males. In addition,
males have broader B80 in both sprint speed (though marginally) and jump distance
(Table 10 and 12), and higher CTmax than those of females in both altitudinal
populations (Table 14). It suggested that the adaptation of thermal sensitivity to local
thermal environments is likely constrained for J. polygonata xanthostoma females,
especially in mid-altitude. Therefore, females potentially use different strategies or
change active period for daily activities (Lailvaux et al., 2003). Interestingly, J.
swinhonis, with a much stronger sexually dimorphism than J. polygonata xanthostoma,
26
did not show any sexual difference in thermal physiology. Both males and females have
the same thermal sensitivity of locomotor performance (in both sprinting and jumping)
and thermal tolerance (Table 9, 11 and 13). Since all body parts of males are larger than
those of females (Kuo et al., 2009), enabling males run faster and jump farther than
females. Overall, the hypothesis that J. swinhonis and J. polygonata xanthostoma have
sexual difference in thermal sensitivity of locomotor performance, thermal tolerance
and thermal profiles is partially supported.
Interspecific comparison
As I have discussed in previous paragraphs, J. swinhonis and J. polygonata
xanthostoma revealed different patterns in thermal sensitivity of locomotor performance.
Generally, J. swinhonis has adaptive thermal physiological changes in sprinting while J.
polygonata xanthostoma has changes in jumping. Such a difference could be explained
by different habitat types (Shan, 2013) which may affect locomotor ability (Losos and
Sinervo, 1989; Spezzano and Jayne, 2004). J. swinhonis occurs in wooded areas with
abundant canopy gaps, while J. polygonata xanthostoma in forested areas with
relatively closed canopy (Tao, 2013). Although sprinting is important to both arboreal
lizards for escaping predation and foraging on the trunk, J. polygonata xanthostoma has
more opportunity to use jump ability in its forested habitats, which often have shrubby
27 undergrowth.
The patterns of thermal tolerance differ between the two species. Mid-altitude J.
polygonata xanthostoma has lower critical thermal minimum (CTmin) than that of
lowland population (Table 14), whereas J. swinhonis has no difference in CTmin between
two altitudinal populations (Table 13). It might be attributed to the fact that the mean
temperature in Mingchih Forest Recreation Area from December to March can drop
below the CTmin of J. polygonata xanthostoma. The winter temperature can be a strong
selective force. In contrary, J. swinhonis has higher CTmax of lowland population than
mid-altitude population. J. swinhonis prefer relatively open areas which have high
temperature, particularly during the breeding season. The species in lowland might be
often confronted by environmental temperatures that are very close to CTmax. Hence, an
adaptive shift in CTmax is important to J. swinhonis. Such a finding of geographic
difference in thermal tolerance is also found in several studies (Miller and Packard,
1977; Hertz, 1979a; Hertz et al., 1979; Hertz and Huey, 1981), but not others (Huey and
Webster, 1976; Hertz, 1979b; Gvozdik and Castilla, 2001). Nevertheless, thermal
tolerance may respond to not only habitat temperature but also other factors such as
microclimate, seasonal cycle and diet (Lutterschmidt and Hutchison, 1997b; Leal and
Gunderson, 2012), and should be explored further.
Regarding thermal profiles, J. swinhonis has higher selected body temperature (Tsel)
28
and Tb compared to those of J. polygonata xanthostoma (Table 23, 24, 25 and 26). It
indicates that J. swinhonis prefer higher temperature than J. polygonata xanthostoma. It
conforms to the fact that J. swinhonis often occurs in relatively open areas. Although
both J. swinhonis and J. polygonata xanthostoma have changed thermal sensitivity
curves of locomotor performance to compensate for the challenge of mid-altitude, there
is no difference in Tsel between mid-altitude population and lowland population (Table
15 and 16). Numerous species of reptiles have been reported that temporal, spatial
variation and individual status may affect Tsel (Gatten, 1974; Ellner and Karasov, 1993;
Christian and Bedford, 1995; Andrews, 1998; Firth and Belan, 1998). Why is there no
intraspecific difference in Tsel despite different thermal habitats? A possibility is that
lizards selected their preferred body temperature may not only consider the locomotor
performance but other physiological functions which might have different thermal
sensitivity curve, such as food assimilation and immune function (Van Damme et al.,
1991; Ji et al., 1996; Angilletta et al., 2002). Overall, the hypothesis that J. swinhonis
and J. polygonata xanthostoma have different extent of thermal adaptation across
altitudes is supported.
Conclusion
29
In this thesis, I reported interspecific, intraspecific, and sexual variations in thermal
physiology of J. swinhonis and J. polygonata xanthostoma. The results strongly support
the labile view of the evolution of thermal physiology in ectotherms. Environmental
temperatures have strongly influenced thermal physiology of J. swinhonis and J.
polygonata xanthostoma, shaping their thermal sensitivity curve of locomotor
performance and thermal tolerance. The extent of adaptation between different types of
locomotion may vary with species and sex. Future work should focus on the escape and
foraging behavior in the field environment to evaluate the differences between sexes,
species and population. Furthermore, other environmental factors, prey availability and
predator pressure of habitat should be taken into consideration.
30
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