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Vol. 26: 1–14, 2017 AQUATIC BIOLOGY Published online February 6 doi: 10.3354/ab00668 Aquat Biol OPENPEN ACCESSCCESS Thermal ecology of red lionfish Pterois volitans from southeast Sulawesi, Indonesia, with comparisons to other Scorpaenidae Theresa F. Dabruzzi1,*, Wayne A. Bennett2, Nann A. Fangue1 1Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, California 95616, USA 2Department of Biology, University of West Florida, Pensacola, Florida 32514, USA ABSTRACT: Scorpionfishes (family Scorpaenidae) occupy a wide range of thermal environments, yet little is known about the group’s thermal ecology. Recent invasions by red lionfish Pterois volitans and devil firefish P. miles into the Atlantic Ocean and Mediterranean Sea have stimulated interest in the ability of these species to withstand thermal extremes, but current temperature data are limited to cold tolerance estimates, or employ nonstandard techniques, making it difficult to compare values across studies. Using standardized methodologies, we quantified metabolic, physiological, and behavioral thermal responses of red lionfish from the Banda Sea, Sulawesi, Indonesia, and interpret the data in light of the group’s diversity and range of thermal habitats. Red lionfish acclimated at temperatures between 13 and 32°C exhibit a thermal scope of nearly 25°C. The resulting thermal niche is moderately large, allowing lionfish to exploit a wide range of thermal habitats, from mid-Atlantic coastal waters to hyperthermal tropical mangroves and tide- pools. Although lionfish prefer temperatures of ~23°C, they acclimate to the high temperature of a cycling thermoperiod. This feature, along with their comparatively low temperature sensitivity (metabolic temperature quotient <2), likely permits lionfish to limit energetic costs during forays into warmer waters. Although lionfishes are considered to be a tropical group, they exhibit a num- ber of thermal tolerance characteristics that allow them to persist in some surprisingly cool environments. Modeling thermal strategies used by red lionfish may provide new insights to the range and variability of thermal adaptations of scorpaenid fishes in general. KEY WORDS: Thermal tolerance polygon · Temperature quotient · Temperature preference · Metabolic rate · Critical thermal methodology INTRODUCTION covered by protective ridges and spines. Protective spines are also prominent on the dorsal, pelvic, and Scorpionfishes (family Scorpaenidae) are a diverse anal fins of many species, and are often venomous, and widespread group with representatives in the capable of delivering powerful defensive stings. Red Sea, western and southern Pacific Ocean, eastern Scorpaenids are proficient top predators that play a Atlantic Ocean, and Caribbean Sea (Nelson 2006). vital role in nutrient cycling and shaping prey assem- Scorpaenid systematics have undergone substantial blages in their respective habitats (Hixon & Beets revision over the last decade, and while some areas 1993). Lionfishes, firefishes, and turkey fishes (sub- remain unresolved, the most recent work by Esch - family Pteroinae), for example, are indiscriminant meyer et al. (2016) lists 376 valid species in the suction feeders that prey on a wide variety of small, family. Most scorpionfishes exhibit a somewhat com- midwater crustaceans and fish (Morris & Akins 2009, pressed body form with distinctively large heads Eddy et al. 2016, Harms-Tuohy et al. 2016), whereas © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Aquat Biol 26: 1–14, 2017 the crouchers (subfamily Caracanthinae), stone- 3% of scorpaenids regularly enter brackish environ- fishes, and scorpionfishes (subfamily Scorpaeninae) ments (Eschmeyer et al. 2016), with some species are cryptic ambush predators that consume a broad tolerating salinities as low as 5‰ (Jud et al. 2015, range of smaller, benthic prey. By limiting overall Schofield et al. 2015). Juvenile red lionfish, for exam- prey abundance, scorpionfishes indirectly influence ple, may use brackish seagrass or mangrove habitats other large predator populations (Albins & Hixon as nursery refugia during development (Barbour et 2013, Ingeman 2016). al. 2010, Claydon et al. 2012), and in some locations, While scorpaenids play a key ecological role in adults can be found feeding in low salinity intertidal their native environments, introductions into habitats zones on small fish and crustaceans (Vijay Anand & outside their native range can have deleterious Pillai 2007, Kulbicki et al. 2012, Pimiento et al. 2012, effects on the local ecology (Albins & Hixon 2008, Jud et al. 2015). No study to date has quantified Lesser & Slattery 2011, Hackerott et al. 2013). At least salinity tolerance of lionfish egg masses or larvae, 3 scorpaenid species are known to have successfully although Johnston & Purkis (2015) presented con- colonized novel habitats. The black scorpionfish vincing evidence that hurricanes are responsible for Scorpaena porcus from the Red Sea has established breaching the strong northerly flow of the Florida reproducing populations in the Mediterranean fol- Current, thereby allowing genetic mixing between lowing the opening of the Suez Canal (Spanier 2000, Floridian and Bahamian populations. If hurricanes Zenetos et al. 2005, Arculeo & Brutto 2014), and are indeed a vector for spreading invasive lionfish aquarium-released red lionfish Pterois volitans and from Florida to the Bahamas, then it might be reason- devil firefish P. miles have established permanent able to assume that eggs and larvae must also be populations along the US Eastern Seaboard, Gulf of somewhat tolerant of low salinity if they are to sur- Mexico, Caribbean Sea, and the eastern coasts of vive inundation by rainwater during transport. Scor- Central and South America over the last 30 yr pionfishes are also distributed over a wide range of (Schofield 2009). Introduced lionfish have dramati- depths, from rocky intertidal pools that become iso- cally reduced the abundance of benthic inverte- lated during low tide (Beckley 2000), to soft-bottom brates (Layman et al. 2014), as well as forage and deep-sea zones (Kulbicki et al. 2012, Nuttall et al. predator fish populations (Albins & Hixon 2008, 2014) over 800 m below the surface (Hureau & Litvi- Green et al. 2012, Albins & Hixon 2013). Further- nenko 1986). Ichthyofaunal surveys and field guides more, red lionfish on some Caribbean reefs have often list depths over which various scorpionfish spe- attained densities much higher than those seen in cies may be found (e.g. Paulin 1982, Steene 2003, their native range (Green & Côté 2009, Darling et al. Butler et al. 2012), but annotations of water tem - 2011). Higher lionfish concentrations in the Carib- peratures are seldom if ever reported (Whitfield et bean have been attributed to increased growth rates al. 2014). (Jud & Layman 2012, Albins & Hixon 2013, Pusack et Early fossil records suggest that scorpionfishes ori- al. 2016), iterative spawning (Edwards et al. 2014), ginated in warm marine waters sometime during the and early onset of reproduction (Edwards et al. 2014), Paleogene Period 65 to 23 million years ago (Berg all of which are likely to be exacerbated by rising sea 1958). While the greatest diversity of contemporary surface temperatures (Raitsos et al. 2010). The detri- scorpionfishes is still found on tropical reef or reef- mental effects on prey populations from lionfish associated habitats (Eschmeyer et al. 2016, also see introductions into novel ecosystems are widespread Motomura et al. 2011), several hypothermic scor- and thought to be related to increased predatory effi- paenids regularly exploit cool or even cold-water ciency due to prey naivety (Albins & Lyons 2012, zones in various seas and oceans. The California Lönn stedt et al. 2014), and a lack of predators actively scorpionfish Scorpaena guttata, for example, spends feeding on introduced populations (Allen & Esch - its entire life in cold waters along the southern Baja meyer 1973, Pimiento et al. 2012). California Sur (Eschmeyer et al. 1983, Love et al. The ability of scorpaenid fishes to occupy a variety 1987) at temperatures as low as 12.5°C (Norton & of habitat types, both native and novel, is due in large Mason 2003). Similarly, the black scorpionfish found part to their ability to tolerate a wide range of envi- on cold rocky bottoms at depths to 800 m in the eastern ronmental conditions (Cure et al. 2014, Schofield et Atlantic, Black Sea, and Mediterranean Sea (Hureau al. 2014). While sculpins were at one time included as & Litvinenko 1986) has been collected in winter at part of the Scorpaenidae (Nelson 2006), the current temperatures of 8.8°C (Bilgin & Çelik 2009), making classification scheme by Eschmeyer et al. (2016) in - it one of the most cold-tolerant scorpionfishes known. cludes no wholly freshwater members. Approximately Even some tropical scorpaeanid populations may Dabruzzi et al.: Red lionfish thermal ecology 3 regularly encounter cold water in parts of their natu- group (Hamner et al. 2007, Freshwater et al. 2009, ral or introduced range. Red lionfish, luna lionfish P. Betancur-R. et al. 2011) may not reflect novel ther- lunulata, and peppermint lionfish Dendrochirus bellus mal features seen in tropical wild-stock populations (= Brachirus bellus), for

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