ARTICLE IN PRESS
Journal of Thermal Biology 33 (2008) 62–66
www.elsevier.com/locate/jtherbio
Low temperature as a limiting factor for introduction and distribution
of Indo-Pacific damselfishes in the eastern United States
John Emea,, Wayne A. Bennettb
a
Department of Ecology and Evolutionary Biology, University of California, Irvine, 321 Steinhaus Hall, CA 92697-2525, USA
b
Department of Biology, University of West Florida, 11000 University Pkwy., Pensacola, FL 32514-5750, USA
Received 10 April 2007; accepted 31 October 2007
Abstract
1. Distribution and reproduction of marine tropical fishes accidentally introduced along the United States’ east coast and Gulf of
Mexico are likely limited by low winter temperatures.
2. Mean minimum acclimation temperature, minimum feeding cessation temperature and critical thermal minima for eight Indo-Pacific
damselfishes (family: Pomacentridae) were less than or equal to 19.3, 18.6 and 15.2 1C, respectively.
3. These data suggest that Indo-Pacific damselfishes could survive winter temperatures and establish permanent populations if
introduced south of Cape Canaveral, Florida, USA.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Critical thermal minimum; Feeding cessation; Tropical fish introduction; Cold tolerance
1. Introduction
The past 50 years have seen a dramatic increase in the
number of exotic fish introductions into North America,
and such invasions are a well-recognized threat to the
biological diversity of American waters (Carlton, 1989;
Wilcove et al., 1998). Some species were established
purposely as a source of food or sport (Randall, 1987),
but the majority were accidental introductions. Of
approximately 645 successful non-native fish introductions
worldwide, 102 are marine or brackish fishes (Froese and
Pauly, 2006). Since 1999, no less than 16 exotic tropical
marine fishes have been reported from the southeastern
Atlantic coast of the United States (Semmens et al., 2004;
not included in Froese and Pauly, 2006). Escape from the
aquarium trade or aquarium releases were the likely cause
of these introductions; however, common aquarium fishes
have received scant attention in ecological or physiological
literature (Randall, 1987; Whitfield et al., 2002; Kimball
et al., 2004; Semmens et al., 2004).
Corresponding author. Tel.: +1 949 824 2822; fax: +1 949 824 2181.
E-mail address: [email protected] (J. Eme).
0306-4565/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtherbio.2007.10.003
Many marine fishes in the aquarium trade originate from
tropical locations in the Indo-Pacific, and temperature
should limit their northern distribution along the southeast
coast of the US (Brett, 1956; Kimball et al., 2004).
Numerous tropical marine aquarium fishes, however, have
wide geographic distributions (Myers, 1991) that often
extend into relatively cool waters. These include the
popular and brightly colored damselfishes of the IndoPacific (family: Pomacentridae) of which various genera
can be found in cool subtropical habitats around Taiwan,
Japan, southern Australia or northeast Africa (Allen,
1991). In the event of an accidental introduction, baseline
thermal tolerance data of trafficked fishes will be essential
for appropriate management and mitigation (Kimball
et al., 2004).
Damselfishes play a key role in shaping the ecology and
faunal distribution of subtropical and tropical coral reefs
worldwide (Williams, 1980; Hixon and Brostoff, 1983;
Lieske and Myers, 1999). Tropical Indo-Pacific Pomacentrids in particular are an extremely speciose group. The
Republic of Indonesia alone boasts 123 damsel species
(38% of all Pomacentrids). In contrast, the relatively young
Atlantic basin is habitat to 16 damsel species that can be
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J. Eme, W.A. Bennett / Journal of Thermal Biology 33 (2008) 62–66
found on reefs from Florida to the Bahamas and into the
northern Caribbean (Allen, 1991). Habitat overlap between
syntopic damselfishes can be high, and many damsels are
intensely territorial, directly competing for space and
resources with conspecifics or other fish species (Allen,
1991). In addition, some damsels maintain and defend algal
gardens, which can have indirect effects on both corals and
fishes (Birkeland, 1977; Hixon and Brostoff, 1983). In light
of their hardy nature and popularity with aquarists, exotic
introductions of damselfishes along the southeastern
Atlantic coast or Gulf of Mexico are possible and could
have adverse consequences if populations should become
permanently established.
The purpose of our study was to determine lowtemperature responses of selected Indo-Pacific damselfishes
and discuss the likelihood and implications of their
becoming permanent residents in the southeast US.
Specifically, we estimated minimum feeding cessation
temperature, minimum acclimation temperature and critical thermal minimum of eight common Indo-Pacific
damselfishes collected around Hoga Island in the Wakatobi Marine National Park, Sulawesi, Indonesia. The
species were blackspot sergeant (Abudefduf sordidus),
two-spot demoiselle (Chrysiptera biocellata), blue devil
(Chrysiptera cyanea), one-spot demoiselle (Chrysiptera
unimaculata), white-tailed humbug (Dascyllus aruanus),
palespot damsel (Dischistodus chrysopoecilus), white damsel (Dischistodus perspicillatus) and three-spot damsel
(Pomacentrus tripunctatus). Each species displays territorial
guarding behavior, resides in seagrass, rubble, patch reef
and/or reef environments and relies in part or wholly on
algae as a food source. Blackspot sergeant are also
63
commonly found in shallow, isolated tidepools (Allen,
1991; Myers, 1991). With exception of three-spot damsel,
each species has been utilized in the aquarium trade (Allen,
1991), and white-tailed humbug, two-spot demoiselle, blue
devil and blackspot sergeant are easily obtained (Allen,
1991).
2. Materials and methods
2.1. Collection, transport and maintenance of fishes
All experiments were conducted during a 10-week
expedition to the Wakatobi Marine National Park from
June to August 2005. Fishes were collected from patch reef,
reef rubble and tidepool sites adjacent to Hoga Island
(05127.53S, 123146.33E; Fig. 1) and transported to the
Hoga Marine Research Centre where they were transferred
to 22-L holding aquaria filled with seawater at 2571.0 1C.
All holding and treatment aquaria were individually
biologically filtered, and 20–25% of water changed daily
to assure good water quality. Fishes were fed TetraMins
flake food daily, ad libitum; however, fishes were not fed
24 h prior to, or during, temperature tolerance trials. Fish
behavior and health were carefully monitored during each
day of experimentation or acclimation.
2.2. Determining minimum feeding cessation temperature,
minimum acclimation temperature and critical thermal
minimum
For each trial, between four and nine fish of each species
were randomly assigned to three (six for white-tailed
Fig. 1. Damselfish collection site locations around Hoga Island, Wakatobi Marine National Park, Banda Sea, Sulawesi, Republic of Indonesia.
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J. Eme, W.A. Bennett / Journal of Thermal Biology 33 (2008) 62–66
humbug), replicate 22-L aquaria. Due to space and
equipment constraints, two species were housed in
each replicate aquarium. While density and species
composition in aquaria did not precisely mimic reef
conditions, all damselfishes tested occurred in high
numbers and in close proximity to one another on
patch-reef collection sites. Minimum feeding cessation
temperatures were determined using a modification of
the chronic lethal methodology proposed by Beitinger
et al. (2000). Briefly, water temperatures were decreased
(Aqua Medics T1500, 12HP chiller) from ambient at a
rate of 1.370.16 1C d1 (mean7SD) until all fishes
ceased eating. Fishes were then held at this temperature
for between 48 and 72 h, during which time food
was presented several times each day to confirm initial
feeding cessation observations. The grand mean of mean
replicate aquaria temperatures was taken as the feeding
cessation temperature for the species. Temperatures were
then increased until feeding resumed (approximately
0.6–1.0 1C above feeding cessation temperature). We
defined this higher temperature as the minimum acclimation temperature. The grand mean of mean replicate
aquaria temperatures at which feeding resumed was
taken as the minimum acclimation temperature for the
population.
Fish were held at the minimum acclimation set-point
temperature for at least an additional 10 d, after which
dynamic minimum thermal tolerance (critical thermal
minimum or CTminimum) was estimated using critical
thermal methodology (CTM; Cox, 1974; Paladino et al.,
1980; Beitinger et al., 2000). For each CTminimum trial,
randomly selected fish were placed, one each, into 250-mL
Nalgenes beakers filled with clean seawater at the
appropriate acclimation temperature. Beakers were suspended within a 10-L, insulated, recirculating CTM
water bath at acclimation temperature, and moderate
aeration of individual test beakers prevented thermal
stratification. Water temperature in the CTM chamber
was then decreased (12HP chiller) at 0.3470.057 1C min1
until final loss of equilibrium (LOE) was observed. This
rate of temperature change has been shown to be slow
enough to track body temperature, but fast enough to
prevent thermal acclimation for fish within the size range
we used (Cox, 1974; Becker and Genoway, 1979). In our
experiments, LOE was defined as inability of fish to
maintain dorso-ventral orientation for at least 1 min
(Beitinger et al., 2000). An LOE endpoint was used because
onset of muscle spasms, preferred by some authors, was
not observed for fishes during trials. As LOE was reached,
water temperature in the beaker was taken with a certified
Fisherbrands NIST mercury thermometer, fish were then
weighed (wet mass70.01 g), measured (standard
length70.5 mm) and returned to minimum acclimation
temperature to recover. Critical thermal minimum was
determined as the grand mean of mean replicate temperatures at which LOE was observed for each species
(Cox, 1974).
2.3. Statistical comparisons
A one-way analysis of variance (ANOVA) was used to
compare mean mass between species, and a Student–
Newman–Keuls (SNK) test separated values into statistically
distinct subsets. An analysis of covariance (ANCOVA) was
performed on CTM endpoint data, and least-square mean
(LSM) values were used to assess potential effects of mass on
CTminima. Nested ANOVA compared CTminima between
species with replicate aquaria nested within species, and a
SNK test separated values into statistically distinct subsets.
All statistical determinations were based on a ¼ 0.05.
3. Results
3.1. Minimum feeding cessation temperature and minimum
acclimation temperature
Damselfishes in our study stopped eating at temperatures between 17.0 and 18.6 1C, but resumed feeding,
moving aquaria substrate and chasing behaviors as
temperatures were increased slightly (Table 1). White
damsels and palespot damsels were the most sensitive to
low temperatures, with minimum feeding cessation temperatures values of 18.4 1C. Nine of 15 white damsels
(60%) and 13 of 16 palespot damsels (81%) died after 72 h
of exposure to 18.4 1C; however, surviving fish resumed
feeding at 19.2 1C and were included in CTminima comparisons. Blue devil and three-spot damsels stopped eating at
18.6 1C, but all fish survived 48 h exposure at this
temperature. Both fishes resumed food consumption at a
minimum acclimation temperature of 19.3 1C. White-tailed
humbug, one-spot demoiselle, two-spot demoiselle and
blackspot sergeant were the most cold tolerant of the fishes
we tested. White-tailed humbug and two-spot demoiselle
exhibited minimum feeding cessation temperature of
17.0 1C, and blackspot sergeant and one-spot demoiselle
had feeding cessation temperature of 17.4 1C; all fish in
these respective groupings survived for 72 and 48 h at
feeding cessation temperatures. Resumption of feeding was
observed at approximately 18 1C in all four species, and the
appropriate grand mean values were taken as their
minimum acclimation temperature.
3.2. Critical thermal minima
Critical thermal minima for damselfishes held at least
10 d at minimum acclimation temperatures ranged from
12.2 1C in white-tailed humbug to 15.2 1C for palespot
damsel (Table 1), with a mean value across all species of
13.471.00 1C. Highly significant differences between damselfish CTminima were identified (nested ANOVA;
F7,19 ¼ 37.98, Po0.0001), with palespot damsels and white
damsels each forming statistically distinct subsets, and all
other species exhibiting various degrees of statistical
overlap (SNK, a ¼ 0.05; Table 1). Mean mass values
varied from 0.48 to 4.56 g, and while significant differences
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65
Table 1
Number, wet mass, standard length, minimum acclimation (AT) and feeding cessation (FC) temperatures, as well as critical thermal minimum values
(CTminimum) for eight damselfishes from Banda Sea, Sulawesi, Indonesia
Species
Common name
Dascyllus aruanus
White-tailed humbug
Chrysiptera biocellata
Two-spot demoiselle
Dischistodus perspicillatus
White damsel
Dischistodus chrysopoecilus
Palespot damsel
Chrysiptera cyanea
Blue devil
Pomacentrus tripunctatus
Three-spot damsel
Abudefduf sordidus
Blackspot sergeant
Chrysiptera unimaculata
One-spot demoiselle
n
Wet mass (g)
Mean (SD)
Length (mm)
Mean (SD)
Minimum AT ( 1C)
Mean (SD)
Minimum FC (1C)
Mean (SD)
CTminimum (1C)
Mean (SD)
23
0.48 (0.535)
18.5 (6.12)
18.1 (0.08)
17.0 (0.40)
12.2 (0.51)E
17
4.56 (4.679)
40.5 (9.60)
18.0 (0.07)
17.0 (0.40)
12.4 (0.41)DE
15/6a
1.32 (0.628)
31.4 (4.87)
19.2 (0.08)
18.4 (0.10)
14.3 (0.52)B
16/3a
0.84 (0.089)
28.0 (0.40)
19.2 (0.08)
18.4 (0.10)
15.2 (0.85)A
27
0.20 (0.119)
18.7 (2.67)
19.3 (0.14)
18.6 (0.33)
12.9 (0.59)DE
17
0.12 (0.030)
16.7 (1.02)
19.3 (0.14)
18.6 (0.33)
13.7 (0.58)C
17
0.74 (0.712)
24.5 (4.78)
18.0 (0.39)
17.4 (0.24)
13.0 (0.06)D
14
1.08 (0.405)
31.3 (3.58)
18.0 (0.39)
17.4 (0.24)
13.2 (0.20)DC
Critical thermal minimum values with like superscripts indicate statistically similar groups (nested ANOVA; F7,19 ¼ 37.98, Po0.0001).
a
Dual numbers for white and palespot damsels represent number of fish used to determine FC temperatures, and number of surviving fish acclimated
and used in CTminimum determinations, respectively.
were apparent between species (one-way ANOVA;
F7,116 ¼ 11.39, Po0.0001), ANCOVA revealed that uncorrected CTminima for six of the eight damselfishes varied
by less than 0.6 1C and no species differed by more than
1.4 1C from least-square adjusted CTminimum estimates. We
concluded, therefore, that effect of mass on CTminima was
minimal (Ospina and Mora, 2004), and only actual
CTminimum values are presented and were used for
comparisons and interpretations.
4. Discussion
Previous data on minimum survivable temperatures of
tropical Indo-Pacific fishes are limited to a single study in
lionfishes, Pterois volitans/miles complex (Kimball et al.,
2004). Based on a lethal minimum temperature of 10.0 1C,
Kimball and coauthors proposed Cape Hatteras, North
Carolina, as the northern limit for introduced lionfishes, a
zone corresponding to the 12 1C isothermal line in the
south Atlantic Bight (Blanton et al., 2003). Minimum
acclimation and feeding cessation temperatures for lionfish,
however, were between 14 and 15 1C (Kimball et al., 2004),
suggesting that these fish may not persist at temperatures
below 14 1C. Damselfish in our study were not as cold
tolerant as lionfish, displaying minimum acclimation
temperatures p19.3 1C and feeding cessation at temperatures p18.6 1C. Differences in minimum thermal tolerance
between Indo-Pacific damselfishes and lionfish are likely
related to habitation depth and not necessarily latitudinal
distribution. The approximate latitudinal distribution of
351N to 351S for Pterois spp. studied is quite similar to six
damselfishes used in our experiments (Allen, 1991; Froese
and Pauly, 2006). However, with the exception of the
white-tailed humbug—which inhabit waters up to 20 m
deep—damselfish in our study inhabit warmer, shallow
waters less than 10 m deep (Allen, 1991), whereas lionfishes
are found at depths of up to 50 m in the Indo-Pacific
(Schultz, 1986) and up to 80 m in introduced Atlantic sites
(Whitfield et al., 2002; Kimball et al., 2004).
Minimum acclimation and feeding cessation temperatures
of the eight tropical damselfishes tested suggest a minimum
ecological thermal limit of between 17 and 19 1C. Based on
these data, we propose that Cape Canaveral, Florida,
represents the approximate northern Atlantic limit for
potential US introduction of Indo-Pacific Pomacentrids.
Near-shore waters adjacent to and south of Cape Canaveral
have remained above 18–20 1C since 1950 (Blanton et al.,
2003), well within the damselfishes’ minimum acclimation
range. Furthermore, CTminima estimates indicate that these
damsels could endure short-term drops in temperature to
approximately 12–15 1C, depending on species (Table 1).
Although no damselfish studied exhibited CTminima below
12.2 1C, average minimum sea surface temperatures of
12.8 1C have been recorded near the limits of their range
(NOAA temperature data, 1981–2004; Richard Reynolds,
personal communication), and populations from these areas
may be more cold hardy than the individuals we studied.
Additionally, each damselfish studied is commonly found in
a zone at least 201 north and south of the equator (Froese
and Pauly, 2006), indicating that seasonal high temperatures
would not limit southern expansion into the Florida Keys,
southern Gulf of Mexico and northern Caribbean (Briggs,
1974; Kimball et al., 2004). Indeed, establishment of
permanent breeding populations in warmer areas of the
Atlantic and Gulf of Mexico is more likely to be limited by
lack of suitable habitat or interactions with native species
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than by temperature. Site of introduction, propagule
pressure and timing would be key elements in determining
success and extent of any introduction and release along the
southeast US coast. Local oceanic currents (Randall, 1987;
Kimball et al., 2004; Semmens et al., 2004) would likely
result in northward dispersal of fishes and any larvae
(Pomacentrids have pelagic larvae). Consequently, direct
introductions would likely be necessary for establishment of
these damsels in the Florida Keys, coastal southern Gulf of
Mexico, Caribbean Sea, coastal Brazil or the Bahamas
(Kimball et al., 2004).
The import of exotic fish into the US with little or no
understanding of how their accidental release would affect
native ecosystems is a widespread problem (Bennett et al.,
1997). Driven by an annual economic influx of over 300
million dollars (US), the global aquarium export trade in
marine ornamentals will likely continue to expand in
developing tropical countries (Shuman et al., 2004). Froese
and Pauly (2006) have catalogued approximately 3400
Indo-Pacific fishes as aquarium species, and nearly 3000
species as meeting the bulk of worldwide demand for these
fishes. Export of marine ornamental animals from the
Republic of Indonesia and Republic of the Philippines to
the US accounts for approximately 80% of the global
annual total (Shuman et al., 2004), and evidence already
exists that southeast Florida is a hotspot of exotic marine
aquarium fish introductions (Semmens et al., 2004). It is
likely that additional Indo-Pacific species will be released
into southeast American waters, either through accidental
aquarium releases or through shipping mishaps. Given the
proclivity of Pomacentrids to affect reef structure and
compete for space with other fish (Birkeland, 1977; Potts,
1977; Williams, 1980; Hixon and Brostoff, 1983; Choat,
1991; Itzkowitz et al., 2000), establishment of a reproducing Indo-Pacific damselfish population in southeast
American waters could have consequences for endemic
reef fishes as well as other fauna (Randall, 1987).
Acknowledgments
We thank B. Tiffany, D. Smith, A. Powell and the 2005
Operation Wallacea staff and volunteers for assistance in
data collection and F. Barreto for reviewing a manuscript
draft. Research funding for this project was provided by
Operation Wallacea and the University of West Florida,
College of Arts and Sciences. All animals were collected
under Operation Wallacea collection permit #OP 647-03 and
treated in accordance with guidelines established by Operation Wallacea and the Animal Care and Use Committee at
the University of West Florida, protocol #2003-002.
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