ARTICLE IN PRESS
Journal of Thermal Biology 34 (2009) 220–225
Contents lists available at ScienceDirect
Journal of Thermal Biology
journal homepage: www.elsevier.com/locate/jtherbio
Critical thermal tolerance polygons of tropical marine fishes
from Sulawesi, Indonesia
John Eme a,, Wayne A. Bennett b
a
b
Ecology and Evolutionary Biology, University of California, Irvine, 321 Steinhaus Hall, Irvine, CA 92697-2525, USA
Department of Biology, University of West Florida, 11000 University Pkwy., Pensacola, FL 32514-5750, USA
a r t i c l e in f o
Article history:
Received 15 January 2009
Accepted 13 February 2009
Keywords:
CTM
CTMax
CTMin
Sulawesi
Temperature tolerance
Thermal tolerance polygon
Tropical fish
a b s t r a c t
1. Replicate thermal tolerance polygons were created using critical thermal methodology (CTM) and
statistically compared.
2. Reef-associated damselfish and cardinalfish displayed the smallest total and intrinsic polygon zones
and equal upper and lower acquired tolerance zones within species.
3. Two gobiids and a mullet species (resident and transient to tidepools, respectively) showed greater
total and intrinsic tolerance zones than reef-associated species.
4. These CTM-polygons assess the thermal biology of fishes in habitats sensitive to global climate
change and suggest that tropical Indo-Pacific fishes are likely to be affected by indirect consequences
of global climate change, rather than by direct temperature mortality.
& 2009 Elsevier Ltd. All rights reserved.
1. Introduction
The pervasive effect of temperature on fish physiology has
engendered a large body of thermal tolerance literature stretching
back over 120 years (Beitinger et al., 2000). The considerable
interest in the thermal physiology of fishes is evidenced not only
by the volume of literature produced but also by the progressive
increase in experimental sophistication and complexity. The
earliest studies focused on measuring single tolerance endpoints
for fishes, often without regard for previous thermal acclimation
history (Heath, 1884; Carter, 1887). As the importance of
acclimation history emerged, however, researchers began quantifying thermal tolerance values at multiple temperatures across a
species’ acclimation range. By the 1940s, Fry and colleagues were
using upper and lower tolerance values to create the first thermal
tolerance polygons—graphical representations outlining a fishes’
thermal niche. Early polygons were constructed using the
Incipient Lethal Temperature technique (ILT; Fry et al., 1942), in
which groups of fish were plunged into a series of high and low
temperatures to determine temperatures lethal to 50% of the
population (see Fry, 1967 for a complete description). Polygons
derived from ILT data are rather burdensome, requiring large
numbers of fish and equipment and have not been widely used
Corresponding author. Tel.: +1 949 824 2822; fax: +1 949 824 2181.
E-mail address: [email protected] (J. Eme).
0306-4565/$ - see front matter & 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtherbio.2009.02.005
since the early 1950s. Critical thermal methodology (CTM) has
largely replaced the ILT technique as a means of determining fish
thermal tolerance (Lutterschmidt and Hutchinson, 1997; Beitinger
et al., 2000), due in part to logistical and animal-care concerns.
Critical thermal tests require relatively few fish, less equipment
and provide a rapid, non-lethal assessment of thermal tolerance
(Fry, 1967; Beitinger et al., 2000). In 1997, Bennett and Beitinger
used CTM thermal tolerance values to build the first CTM-polygon.
Of the 25 complete fish polygons, five are CTM-based (Bennett
and Beitinger, 1997; Fangue and Bennett, 2003; Hernández and
Bückle, 2002; Ford and Beitinger, 2005); however, the statistical
fidelity with which these CTM-polygons reflect a fish’s thermal
ecology remains untested.
Attributes of thermal tolerance polygons provide important
insights into fish ecology and distribution and have been used
to identify temperature-related survival tactics (Bennett and
Beitinger, 1997), predict the spread of exotic species (Bennett
et al., 1997), quantify the thermal niche of endangered species
(Walsh et al., 1998) and determine optimal culture conditions
(Das et al., 2004). The usefulness of thermal tolerance polygons
lies in their ability to impart markedly more information
than tolerance endpoints alone. Overall polygon area (reported
as 1C2) provides a convenient and useful comparative index of
eurythermicity between species. In addition, polygons define
intrinsic thermal tolerance zones, i.e., tolerance independent of
previous thermal acclimation history, as well as upper and lower
acquired tolerance zones, i.e., thermal tolerance gained through
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J. Eme, W.A. Bennett / Journal of Thermal Biology 34 (2009) 220–225
acclimation (Beitinger and Bennett, 2000). These zones characterize the relationship between thermal acclimation strategy and the
thermal regimen of the fishes’ life history or environment
(Beitinger and Bennett, 2000; Fangue and Bennett, 2003).
Thermal tolerance polygons have been traditionally evaluated
using direct percentile comparisons (Beitinger and Bennett, 2000;
Fangue and Bennett, 2003), but stronger statistical inferences
would make polygonal zone comparisons between fishes more
meaningful. In this study, the efficacy of polygons to reflect the
thermal habitats that fish exploit in the Wakatobi Marine National
Park (WMNP: Banda Sea, Sulawesi, The Republic of Indonesia) was
tested. The park encompasses a wide array of intertidal habitat
subtypes, from thermally stable seagrass and patch reefs to
shallow, hyperthermal mangrove tidepools (mangals). These
habitats comprise a natural thermal gradient containing fishes
that, while in close physical proximity, are exposed to very
different thermal regimens. CTM-polygons were constructed and
compared for five fishes with disparate spatial and temporal usage
patterns of intertidal habitats in the WMNP. White-tailed humbug
(Dascyllus aruanus; Linnaeus, 1758) and Nine-banded cardinalfish
(Apogon novemfasciatus; Cuvier, 1828) inhabit patch reef and
seagrass areas, respectively, while avoiding insolated tidepools
(Myers, 1991). Squaretail mullet (Liza vaigiensis; Quoy & Gaimard,
1825) is a mangal transient that enters tidepools during nighttime
low-tide events (Hiatt and Strasburg, 1960). Common goby
(Bathygobius fuscus; Rüppell, 1830) and an undescribed sandflat
goby species (Bathygobius sp.; James Van Tassell, personal
communication) are mangal residents that never leave shallow
tidepools and encounter local temperatures that can exceed 40 1C
(Myers, 1991; Taylor et al., 2005). This study is the first to use
statistical comparisons of thermal tolerance polygons (interspecific) and acquired tolerance zones (intraspecific) to provide
assessment of fishes’ thermal ecology, and the results of these
polygons are presented in the context of sea surface temperatures
in the Indo-Pacific. In addition, we report various thermal tactics
used by fishes living within a coral reef thermal gradient as well
as exceptional heat tolerance in species that routinely encounter
temperatures near the upper biokinetic limit for vertebrate life.
2. Materials and methods
2.1. Collection, transport and maintenance of fishes
Experiments were conducted during a total of 20 weeks in the
WMNP from June to August in 2003, 2004 and 2005. Fishes were
collected from sites off Hoga Island (05127.53S, 123146.33E),
transported to the Hoga Marine Research Centre and transferred
to 190-L holding tanks filled with seawater at 2671.0 1C. Animals
were collected under Operation Wallaceas collection permit #OP
647-03 and treated according to University of West Florida Animal
Care and Use Committee protocol #2003-003.
2.2. Determination of thermal acclimation limits
Maximum and minimum acclimation temperatures were
determined using chronic lethal methodology (CLM; Beitinger
et al., 2000). Fish were randomly assigned to either CLmaxima
or CLminima treatments. Treatments consisted of three replicate
22-L acclimation aquaria containing six to eight fish each. Aquaria
were biologically filtered, and 20–25% of water changed daily
to assure good water quality. Fishes were fed TetraMins (Tetra
Werke; Melle, Germany) flake food daily. Temperatures were
increased or decreased from ambient at a rate of 1.670.3 1C day1
221
(mean7SD) until a temperature lethal to 50% of the group was
reached. Fishes used in CLM trials were not used in CTM trials.
2.3. Thermal acclimation and thermal tolerance determination
Critical thermal minimum (CTminimum) and Critical thermal
maximum (CTmaximum) were estimated using the critical
thermal methodology (Cox, 1974; Paladino et al., 1980; Beitinger
et al., 2000). All species were randomly assigned to one of five
temperature treatments across their acclimation range, except for
Nine-banded cardinalfish (seven treatments). Treatments comprised three, replicate 22-L acclimation aquaria containing six to
eight fish each. Aquaria were biologically filtered, and 20–25% of
water changed daily to assure good water quality. Fishes were fed
TetraMins flake food daily, but not fed 24 h prior to trials. Water
temperatures were increased or decreased from ambient by
1.5 1C day1 until the desired acclimation temperatures were
reached for each treatment. Fishes remained at each acclimation
set-point temperature for at least 14 days prior to CTM trials.
For each CTM trial, randomly selected fish were placed, one
each, into 250-ml Nalgenes beakers filled with clean seawater at
appropriate acclimation temperatures. Beakers were suspended
within a 60-L, insulated, recirculating water bath and provided
with moderate aeration to prevent thermal stratification.
A certified Fisherbrands NIST mercury thermometer monitored
temperature in each beaker. Temperatures in the CTM water bath
were heated or chilled using a 1500-W immersable heater
(custom made) or a 1/4 HP chiller (New Ocean, Universal Marine
Industries, CA) at a rate of 0.3170.08 1C min1 (mean7SD) until
final loss of equilibrium, LOE (inability to maintain dorso-ventral
orientation for at least 1 min; Beitinger et al., 2000), was reached.
This rate was slow enough to track body temperature, but
fast enough to prevent thermal acclimation (Cox, 1974;
Becker and Genoway, 1979). Following each trial, fish were
weighed (wet mass 70.01 g), measured (standard length
70.5 mm) and returned to acclimation temperature to recover.
Upper and lower thermal tolerance for each replicate treatment group was calculated as the mean of the CTminima or
CTmaxima trials. The grand mean of the collective replicate
endpoints was taken as the CTminimum or CTmaximum for the
population (Cox, 1974). Simple linear regression (SLR) analysis was
used to model the relationship of thermal tolerance on acclimation temperature for each species. Analysis of covariance
(ANCOVA) was performed on tolerance endpoint data within each
species, and least square mean (LSM) values used to assess
potential mass on tolerance effects.
2.4. Construction and interpretation of thermal tolerance polygons
Thermal tolerance polygons were constructed from the CTM
and CLM limits of each species using a modified version of the
methods described by Bennett and Beitinger (1997). Polygons
were created by connecting CLminima and CLmaxima with CTM
regressions to produce a quadrilateral figure expressed quantitatively using the areal units, 1C2. Polygons were divided into
an intrinsic tolerance zone (i.e., thermal tolerance independent
of previous thermal acclimation) and acquired tolerance zones
(i.e., thermal tolerance gained through acclimation) by dividing
polygons with horizontal lines from extrapolated CTminimum and
CTmaximum values at CLM limits. A one-way analysis of variance
(ANOVA) was used to compare total polygonal area, intrinsic
tolerance area and acquired tolerance areas between species, and
a Tukey’s Studentised Range (TSR) post-hoc test separated values
into statistically distinct subsets. Student’s t-test was used to
examine intraspecific differences between upper and lower
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Squaretail mullet (Liza viagiensis)
Common goby (Bathygobius fuscus)
50
0.13 (Acc Temp) + 37.74
R2= 0.883, P < 0.0001
39.1
Thermal Limit (°C)
40
40.1 40.4
41.6
Total = 829°C
2
20
12.3
0
9.5 9.2
7.3
13.5 13.8
11.0
43.4
44.5
45.3
37.9
30
Total = 823°C
2
20
16.1
16.9
13.8
11.2
10
9.9 10.0
0.24 (Acc Temp) + 4.55
R2 = 0.983 P < 0.0001
0.36 (Acc Temp) + 2.69
R2 = 0.965 P = 0.012
7.1
0
0
10
20
30
40
Acclimation Temperature (°C)
50
0
0.12 (Acc Temp) + 37.82
R2 = 0.930, P < 0.0001
40.6
39.8 40.1
40
30
R2 = 0.978, P < 0.0001
40
2
14.5 14.9
11.9
40
50
0.34 (Acc Temp) + 29.13
20
9.8 10.2
30
50
42.7 43.0
41.4 42.2
Total = 639°C
10
20
White-tailed humbug (Dascylus aruanus)
Thermal Limit (°C)
50
10
Acclimation Temperature (°C)
undescribed sandlfat goby
(Bathygobius sp.)
Thermal Limit (°C)
42.7
40.1 40.5
40
30
10
0.26 (Acc Temp) + 34.98
2
R = 0.995, P < 0.0001
41.3 42.4 42.6
Thermal Limit (°C)
50
12.8 12.8
41.4
40.0 40.5
38.0
35.6 36.0
35.3
30
Total = 442°C2
20
11.6 12.0
10
13.1
13.8
16.1
16.3
17.0
0.29 (Acc Temp) + 6.60
0.22 (Acc Temp) + 6.54
2
R = 0.973 P < 0.0001
2
R = 0.919 P < 0.0001
0
0
0
10
20
30
40
Acclimation Temperature (°C)
0
50
10
20
30
40
Acclimation Temperature (°C)
50
Nine-banded cardinalfish
(Apogon novemfasciatus)
50
0.35 (Acc Temp) + 28.32
R2 = 0.926, P < 0.0001
39.0*
35.2* 38.0*
Thermal Limit (°C)
40
34.8
30
40.1 40.9
35.1
Total = 408°C
2
20
18.7
17.7* 17.8
15.0*
12.6 12.9 13.4*
10
0.36 (Acc Temp) + 5.99
2
R = 0.936 P < 0.0001
0
0
10
20
30
40
50
Acclimation Temperature (°C)
Fig. 1. CTM-polygons for five tropical fish species from the Banda Sea, Sulawesi, Indonesia: (A) Common goby (Bathygobius fuscus); (B) Squaretail mullet (Liza vaigiensis);
(C) sandflat goby (Bathygobius sp.); (D) Nine-banded cardinalfish (Apogon novemfasciatus); (E) White-tailed humbug (Dascyllus aruanus). Each polygon displays the upper
and lower acquired tolerance zones (right triangles), the zone of intrinsic tolerance (rectangle) and total thermal tolerance (entire quadrilateral). Simple linear regression
models of CTmaxima and CTminima are also shown. Critical Thermal trials (K) were conducted with individuals randomly selected from three replicate tanks and have
95% confidence interval error bars. Select Nine-banded cardinalfish endpoints (*) are based on averages from six replicate tanks. The lowest and highest CTmaxima and
CTminima (J) are based on extrapolated regression lines, with upper and lower acclimation limits based on CLmaxima and CLminma, respectively.
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acquired polygonal areas. All statistical determinations were
based on a ¼ 0.05 (SAS System for Windows, Version 8).
3. Results
3.1. Chronic lethal thermal limits
Mangal residents (Bathygobiids) and transient (Squaretail
mullet) displayed higher upper acclimation limits than either
reef-associated species (Nine-banded cardinalfish and Whitetailed humbug). Bathygobiids and Squaretail mullet did not
survive chronic exposure to temperatures higher than 38.07
0.1 1C (mean7SD) or 38.970.7 1C, respectively. Nine-banded
cardinalfish and White-tailed humbug did not survive temperatures higher than 35.771.1 1C. Common goby, sandflat goby and
Squaretail mullet did not survive temperatures below 10.970.2,
16.070.4 and 11.270.1 1C, respectively. Chronic exposure to
temperatures lower than 17.371.10 1C was lethal to Nine-banded
cardinalfish and White-tailed humbug. These temperatures were
taken as respective upper and lower acclimation limits (Fig. 1).
3.2. Critical thermal limits
Comparison of LSM CTminima and CTmaxima values (derived
from ANCOVA) with uncorrected mean values for all species
revealed an average difference of 0.0170.03 1C (mean7SD), with
no difference greater than 0.1 1C. Therefore, it was concluded that
CTM data were unaffected by mass, and actual CTM values were
used for all subsequent comparisons and construction of thermal
tolerance polygons.
While all fishes exhibited CTmaxima greater than 34 1C and
CTminima less than 18 1C, regardless of their thermal acclimation
history (Fig. 1), mangal residents and transient Squaretail mullet
exhibited the highest CTmaxima and lowest CTminima. Squaretail
mullet displayed the highest CTmaximum value of 44.570.05 1C
(mean7SD) and Common goby the lowest CTminimum,
9.270.2 1C. Sandflat goby showed CTmaxima of 42.770.2 1C and
CTminima of 10.270.7 1C at the high and low ends of their
acclimation range, respectively. Both reef-associated species,
Nine-banded cardinalfish and White-tailed humbug, had CTmaxima of over 40 1C and CTminima under 13 1C at the respective high
and low ends of their thermal acclimation range. Bathygobiids and
Squaretail mullet displayed CTmaxima greater than 38 1C across
their entire acclimation range. However, reef-associated species,
Nine-banded cardinalfish and White-tailed humbug, showed
tolerance values of at least 38 1C only at acclimation temperatures
greater than 26 1C.
223
In addition, regression analysis showed that mangal residents
gained less tolerance with changes in acclimation temperature
than either Squaretail mullet or both reef-associated species.
Common and sandflat goby gained 0.13 and 0.12 1C of upper
tolerance, respectively, for every 1 1C change in acclimation but
gained 0.24 and 0.22 1C in low-temperature tolerance. In contrast,
Squaretail mullet displayed approximately twice the acclamatory
response, with changes in CTmaxima of 0.26 1C and CTminima of
0.36 1C for every 1 1C change in acclimation. Nine-banded
cardinalfish and White-tailed humbug also showed high levels
of upper (0.35 and 0.36 1C, respectively) and lower (0.34 and
0.29 1C, respectively) tolerance accruement. Regressions of CTminima and CTmaxima on acclimation temperature were significant
for all species (SLR, Pp0.012), with acclimation temperature
explaining between 88% and 99% of thermal tolerance variability
(Fig. 1).
3.3. Thermal tolerance polygons
Common goby exhibited the largest total polygonal area,
followed by Squaretail mullet, sandflat goby, White-tailed humbug and Nine-banded cardinalfish (Po0.0001; Table 1). Polygons
had areas ranging from 408.4 1C2 (Nine-banded cardinalfish) to
829.1 1C2 (Common goby). Common goby, sandflat goby and
Squaretail mullet displayed polygonal areas larger than 630 1C2, at
least 222 (54%) and 188 1C2 (43%) greater than reef-associated
Nine-banded cardinalfish or White-tailed humbug, respectively.
Common goby and Squaretail mullet had the largest intrinsic
polygonal area, followed by sandflat goby, White-tailed humbug
and Nine-banded cardinalfish (Po0.0001; Table 1). Squaretail
mullet acquired the greatest amount of upper and lower tolerance
through acclimation and sandflat goby the least upper tolerance
(Table 1).
4. Discussion
Critical thermal tolerance polygons convey important information regarding the thermal physiology of fishes from disparate
thermal habitats. Partitioning of a polygon into total, intrinsic and
acquired zones, as well as inter and intraspecific statistical
comparisons of these zones, provides important insights into
how each species mitigates problems associated with changing
environmental temperatures. Water temperatures in Hoga’s
mangals increase rapidly during daytime low tides, resulting in
episodic hyperthermal conditions that can become limiting to
fish. Both resident (Common and sandflat goby) and transient
mangal fishes (Squaretail mullet) showed substantially larger
Table 1
Areal values (1C2) of CTM-polygons for five tropical fishes from the Banda Sea, Sulawesi, Indonesia.
Species, common name
n
Wet
mass (g)
Mean (SD)
Standard
length (mm)
Mean (SD)
Total
tolerance (1C2)y
Mean (SD)
Intrinsic
tolerance (1C2)y
Mean (SD)
Upper acquired
tolerance (1C2)y
Mean (SD)
Lower acquired
tolerance (1C2)y
Mean (SD)
Bathygobius fuscus, Common goby
Liza vaigiensis, Squaretail mullet
Bathygobius sp., sandflat goby
Dascyllus aruanus, White-tailed humbug
Apogon novemfasciatus, Nine-banded cardinalfish
99
101
91
98
97
0.8 (0.4)
1.3 (0.7)
0.2 (0.1)
0.3 (0.3)
0.4 (0.3)
31 (5)
33 (7)
25 (3)
16 (4)
27 (5)
829.1 (2.2) A
823.1 (9.5) A
638.8 (0.6) B
442.7 (1.0) C
408.4 (1.1) D
694.5
582.6
545.9
336.8
295.9
48.1 (3.6) B
103.2 (4.3) A
35.8 (1.7) C
55.9 (3.8) B
56.7 (5.1) B
86.5 (3.4)* B
137.3 (8.2)* A
57.1 (6.3)* C
49.9 (3.8) C
55.9 (6.5) C
y
(2.1) A
(20.0) B
(5.1) C
(2.8) D
(9.3) E
Interspecific comparisons of each temperature tolerance feature are highlighted with letters and based on TSR post-hoc test. Different letters indicate significant
differences, and comparisons are made within columns. One-way ANOVA, F [4,10], TSR, a ¼ 0.05: total tolerance: F ¼ 5207.08, Po0.0001; intrinsic tolerance: F ¼ 822.19,
Po0.0001; upper acquired tolerance: F ¼ 132.40, Po0.0001; lower acquired tolerance: F ¼ 114.05, Po0.0001.
*
Intraspecific comparisons of replicate lower and upper acquired tolerance (t-test) indicate Common goby, sandflat goby and Squaretail mullet gain significantly less upper
tolerance through acclimation (t-value ¼ 13.59, DF ¼ 4, Po0.001; t-value ¼ 5.70, DF ¼ 4, Po0.01; and t-value ¼ 6.39, DF ¼ 4, Po0.01, respectively), whereas White-tailed
humbug and Nine-banded cardinalfish display no difference in upper and lower acquired tolerance zones (t-value ¼ 1.96, DF ¼ 4, P ¼ 0.122; and t-value ¼ 0.12, DF ¼ 4,
P ¼ 0.909, respectively).
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total and intrinsic polygonal areas than either reef-associated
fishes (Nine-banded cardinalfish and White-tailed humbug). In
addition, the bathygobiids and Squaretail mullet exhibited
reduced upper acquired tolerance zones compared to their lower
acquired zones, indicating these fishes maintain consistently high
levels of heat tolerance in response to predictable diel temperature extremes. Nine-banded cardinalfish and White-tailed humbug experience more limited thermal fluctuations and are less
eurythermic than both mangal resident and transient fishes.
These reef-associated fishes exhibit statistically identical upper
and lower acquired tolerance zones, along with a well-developed
acclimation potential. A polygonal profile of this type is well
suited to environments subject to limited diel temperature fluxes,
but seasonal or chronic shifts in sea temperatures may demand
readjustment in temperature tolerance.
The shape of each species’ CTM-polygon reflected its thermal
niche (Bennett and Beitinger, 1997), suggesting that polygons may
be potentially useful in several important areas of fish research.
Critical thermal minima have previously been used to estimate
the cold tolerance and overwintering potential of fish, including
piranha and lionfish (Bennett et al., 1997; Kimball et al., 2004).
Temperature tolerance data for endangered or threatened fishes
are necessary to understand population fluctuations, but baseline
data are often not present until the species’ status has been
recognised (Walsh et al., 1998). Fast, complete assessments of a
species’ thermal tolerance would be useful prior to policy
decisions, especially where a small number of individuals are
available for testing (forgoing chronic lethal measures). Polygonal
structure and zonal partitioning (i.e., acquired and intrinsic
tolerance attributes) could provide a baseline for thermal
aquaculture condition. Optimal culture conditions based on
temperature tolerance receive considerable attention in areas
where farm-raised fishes are a major food source, especially in
Southeast Asia (e.g., Das et al., 2004). Perhaps most importantly,
the size of intrinsic and acquired thermal tolerance zones can
provide an estimation of how well or poorly a fish may ameliorate
seasonal or chronic shifts in sea temperatures that may demand
readjustment in temperature tolerance.
All fishes studied showed noteworthy ultimate (most extreme)
tolerance to high and low temperatures. At the high temperature
end of their acclimation, each species acquired CTmaxima
exceeding 40 1C and at the low acclimation end, CTminima less
than 13 1C. Indo-Pacific sea surface temperatures between the
years 1981 and 2004 had mean levels of 27 1C (Richard Reynolds,
NOAA, personal communication; 351N to 301S, representing the
maximum northern and southern distribution of fishes in this
study). Although reef-associated Nine-banded cardinalfish and
White-tailed humbug showed a limited acclimation range (i.e.,
difference between upper and lower CLM; 18 1C) compared to
Common goby and Squaretail mullet (27 1C), the reef-associated
species appear able to survive long-term exposure to temperatures 7 1C above or 10 1C below mean Indo-Pacific sea surface
temperatures (27 1C). Extrapolated lower thermal limits of
Common goby and Squaretail mullet were less than 7.5 1C,
temperatures commonly associated with cooler climates. In fact,
these shallow-water tropical species displayed lower thermal
limits relatively close to critical thermal tolerances reported for
some temperate fishes (Beitinger et al., 2000).
Upper and lower thermal endpoints presented agree with
previous assessments of Indian and Pacific Ocean tropical
cardinalfish and goby critical thermal limits (Menasveta, 1981;
Mora and Ospina, 2001, 2002; Rajaguru, 2002; Ospina and Mora,
2004). Combined, these data show that many tropical marine fish
genera have CTmaxima approaching or greater than 40 1C and also
may survive in more temperate waters (Menasveta, 1981; Mora
and Ospina, 2001, 2002; Rajaguru and Ramachandran, 2001;
Rajaguru, 2002; Ospina and Mora, 2004; Eme and Bennett, 2008).
Interestingly, the exceptional CTmaxima of 44.5 1C we recorded
for Squaretail mullet acclimated to 35.9 1C was not unique for the
mullet family (Mugilidae). Greenback mullet (Liza subviridis)
acclimated to 29.5 or 28 1C exhibited CTmaxima of 42.0 and
44.5 1C, respectively (Menasveta, 1981; Rajaguru, 2002), and
White mullet (Mugil curema) acclimated to 26 1C had a CTmaxima
of 41 1C (Mora and Ospina, 2001). The remarkable upper
tolerance limits across Mugilidae genera are exceeded only by
the thermally tolerant cyprinodontids (Lowe and Heath, 1969;
Heath et al., 1993; Bennett and Beitinger, 1997), which at 45.3 1C
establish the upper biokinetic limit for vertebrate life (Bennett
and Beitinger, 1997). These cyprinodontid CTM values, however,
were achieved by fish acclimated to a cycling thermal regime near
or exceeding 40 1C, and future studies with mullet species
acclimated to cycling thermal regimes may bring their upper
tolerance limits closer to or higher than pupfishes’.
CTM-polygons may be useful indices of how a marine species
would respond to changes in the global climate. Monthly IndoPacific sea surface temperatures averaged 27 1C between 1981 and
2004; grand mean monthly high temperatures during those
23 years were 32.4 1C, and mean monthly high temperatures
ranged from 30.5 to 37.3 1C. On the other end of the thermal
spectrum, grand mean monthly low temperatures were 12.3 1C,
and mean monthly low temperatures ranged from 3.1 to 19.1 1C
(Richard Reynolds, NOAA, personal communication). There has
been much discussion over how fish populations might be
affected by global climate change (Perry et al., 2005; Portner
and Knust, 2007; Portner and Farrell, 2008). For both the mangal
and reef-associated fishes in this study, however, changes in sea
temperatures would have to be marked to provoke any direct
adverse effects. Nine-banded cardinalfish and White-tailed humbug show a limited acclimation range (i.e., difference between
upper and lower CLM; 18 1C). Nevertheless, these reef-associated
species appear able to survive long-term exposure to temperatures 7 1C above or 10 1C below current mean open-water
temperatures in the Indo-Pacific (27 1C), so long as the rate of
temperature change does not exceed the fishes’ acclimation rate.
Mangal-associated bathygobiids and Squaretail mullet tolerate
temperatures between about 38 and 16 1C, regardless of their
previous thermal acclimation, and greater extremes if given time
to acclimate. If other syntopic fishes show similar tolerance
profiles to those seen in this study, it would suggest that tropical
Indo-Pacific fishes are more likely to be affected by the indirect
consequences of global climate change (e.g., reef degradation or
changes in trophic structure) rather than direct temperature
mortality (Munday et al., 2008).
Acknowledgements
We thank D. Smith, T. Coles, B. Tiffany and the UWF Indonesia
research teams in 2003, 2004 and 2005. We also give special thanks
to R. Reynolds for help with Indo-Pacific sea temperature data and
to J. Van Tassell for assistance with goby identification. Operation
Wallacea, PADI Australia and UWF provided research funding.
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