THE Common Thresher Shark, Alopias vulpinus, is a large (maximum total length 760 cm, body mass 348 kg) actively swimming pelagic species classified in the Family Alopiidae (Hart, 1973; Compagno, 2001; R. Froese and D. Pauly, unpubl., www.fishbase.org). The internal anatomy of the swimming musculature of A. vulpinus closely resembles that of the endothermic sharks (e.g., Shortfin Mako Shark, Isurus oxyrinchus) in the Family Lamnidae (Carey and Teal, 1969; Carey et al., 1971; Carey et al., 1985) in having the red aerobic muscle (RM) located in an axial position (i.e., closer to the vertebral column) and the circulation to this tissue is through a putative counter-current heat exchanger (retia; Bone and Chubb, 1983; Bernal et al., 2003; pers. obs.). Although morphological similarities between the Common Thresher Shark and the lamnids have been used to suggest that threshers are capable of regional endothermy, no in vivo temperature measurements exist for this species. The only two in vivo RM temperature measurements that exist for any alopiid shark were taken from two Bigeye Thresher Sharks (Alopias superciliosus; Carey et al., 1971), for which the RM temperature was warmer than ambient, in one specimen, and cooler than ambient in the other. Collectively, the inconclusive RM temperature data for the Bigeye Thresher (Carey et al., 1971) and the lack of temperature measurements for the other two thresher species (i.e., Common Thresher and Pelagic Thresher, Alopias pelagicus) presents the question as to whether this group is capable of RM endothermy as are the lamnid sharks. The objective of this communication is to present in vivo temperature measurements for the RM and white muscle (WM) of the Common Thresher Shark and to test whether this species is capable of elevating its RM temperature elevation above ambient, indicating regional endothermy.

Materials and Methods

Specimen collection.—

Twenty-four Common Thresher Sharks were captured off the coast of Southern California from 1999–2003. Seven sharks were captured using rod and reel techniques at depths from the surface (0 m) to 30 m, whereas 17 sharks were captured using a 4 km longline (O'Brien and Sunada, 1994) during the 1999 National Marine Fisheries Service (NMFS) shark indexing survey. Longline hook-depths ranged from 35–50 m and the thermal profile of the water column was recorded using manually launched expendable bathythermographs (XBT, Sippican, Inc.; Marion, MA). When possible, after recording morphological data (e.g., total length, estimated mass, sex) and the physical condition of the animal, the sharks were tagged with NMFS conventional spaghetti tags and released. Heavy fishing tackle (24 kg) was used to collect all sharks by rod and reel in an attempt to minimize the struggle and fight times associated with capture and once along side the boat. Rapid handling of the sharks allowed for the measurement of muscle temperatures within 1 min of the shark reaching the fishing vessel. Struggle time for longline captured fishes is unknown and may have ranged from a maximum of approximately 240 min (total gear soak time) to a minimum of 15 min (immediately prior to gear haul back).

Temperature measurements.—

Muscle temperature measurements were taken from sharks as they were brought alongside the fishing vessel but while still partially submerged in the water. A 0.5 cm incision was made using a surgical blade at 20–30% total length (TL; i.e., below the first dorsal fin) where the relative amount of RM is highest (Bernal et al., 2003). A thermocouple thermometer (Barnant model 600) was inserted transversely into the swimming musculature, approximately 2–4 cm beneath the skin and a temperature measurement of WM was recorded. Thermocouple trajectory is shown in Figure 1 and illustrates the path taken by temperature probe from the WM until reaching the RM. Immediately after the muscle temperatures were taken the thermocouple probe was immersed in the surrounding water to measure the SST during rod and reel collection and to confirm the SST obtained by the XBT during the longline operations.

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Statistical analyses.—

The mean RM and WM temperature elevations above SST were compared using a Student's Paired t-test and comparisons of mean temperature elevations for RM and WM between the different collection techniques were done with a Student's two sample t-test. A least-squares linear regression analysis was used to determine the presence of a significant relationship between RM temperature and fish length. All tests were performed using an α of 0.05.

Results

Red muscle temperature data were obtained from 24 Common Thresher Sharks ranging in TL from 134–382 cm (80–215 cm fork length, FL) and with an estimated body mass ranging from 3–150 kg. There was no significant relationship between body size (i.e., FL) and RM temperature elevation above SST (r² = 0.09, F = 2.24, P = 0.14, df = 1,22), but there was a significant relationship (r² = 0.23, F = 6.61, P = 0.017, df = 1,22) between FL and RM temperature elevation above WM (described by T_RM-WM = 0.0265 × FL− 1.28, where T_RM-WM is the RM temperature elevation above WM and FL is in cm). All but one of the Common Threshers had a RM temperature that was warmer than the ambient SST and all RM temperatures were warmer than those of the WM (Table 1). The mean (± SE) RM temperature for all threshers (21.47 ± 0.31 C) was significantly higher (t = 7.76, P < 0.001, df = 23) than the mean SST (19.13 ± 0.22 C), but there was no significant difference (t = 0.36, P = 0.71, df = 23) between the mean SST and the mean WM temperature (19.22 ± 0.30 C). The mean RM temperature elevation for all threshers was 2.33 ± 0.30 C above SST and 2.25 ± 0.35 C above WM, with Common Thresher #17 having the warmest relative RM temperature (i.e., 5.4 C above SST and 7.6 C above WM, Table 1, Fig. 2). There was no significant difference between the mean RM temperature elevation above SST (t = 1.38, P = 0.17, df = 22) for threshers caught by rod and reel (2.97 ± 0.54 C) and longline (2.07 ± 0.35 C) and no significant difference (t = 1.61, P = 0.11, df = 22) was determined between the RM temperature elevation above WM for sharks caught by rod and reel (3.10 ± 0.61 C) or by longline (1.89 ± 0.41 C). For seven rod and reel caught sharks, there was no significant relationship between the RM temperature elevation above SST and time spent struggling on the line (r² = 0.52, F = 5.59, P = 0.064, df = 1,5).

Table 1.  Red Muscle Temperature (T_RM), T_RM Elevation above Sea Surface Temperature (SST), and White Muscle Temperature (T_WM) for Common Thresher Sharks Captured off Southern California

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Sea surface temperatures (SST) ranged from 18–23 C with a mean of 19.5 ± 0.72 C during the rod and reel operations and 18.9 ± 0.09 C during the longline operations. In addition, the vertical thermal profile (i.e., surface to 40 m) data collected during the longline operations documents the thermocline depth at approximately 25 m and an associated decrease in the water temperature to 12.70 ± 0.19 C at 30 m (Fig. 3).

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Discussion

The present study tested the hypothesis that A. vulpinus is capable of significantly elevating the temperature of its aerobic red myotomal musculature (RM) above that of the sea surface temperature (SST). Temperature measurements of the RM, white muscle (WM), and ambient water for 24 live sharks show that A. vulpinus is capable of elevating its RM temperature significantly above that of SST.

How warm does a fish need to be in order to be considered endothermic? A review of fish muscle temperatures by Dickson (1994) noted that even very large active fish (i.e., Blue Marlin, Makaira nigricans) after an exhaustive struggle were not capable of elevating their internal body temperatures more than 2.7 C above SST. Dickson's (1994) study attributes temperature elevation in ectothermic fish to swimming activity level, large body size, and circulatory adjustments that decrease the rate of heat loss across the body. In the current study, we observed 10 Common Threshers with RM temperatures above Dickson's (1994) hypothesized endothermy threshold value of 2.7 C above SST (Table 1) suggesting the that the Common Thresher Shark is capable of RM endothermy.

Although the data presented in this study support the hypothesis of Common Thresher Shark RM endothermy, the RM temperatures recorded may have underestimated the true potential thermal excess (difference between RM temperature and surrounding water at depth) for this species. Recent studies on the movement of free-swimming Bigeye Thresher sharks documented repeated diurnal vertical movements (i.e., changes in depth), which correspond to fluctuations in the ambient temperature of up to 14–16 C (Nakano et al., 2003; Weng and Block, 2004). Similarly, recent archival tagging work on the Common Thresher Shark (D. Cartamil and C. Sepulveda, unpubl.) show that this species undergoes frequent vertical oscillations, spending significant portions of time below the thermocline. In addition, the coexistence of Common Thresher Sharks and Bigeye Thresher Sharks in the California drift gillnet fishery suggests that the Common Thresher may also have a vertical movement pattern that at least at times overlaps with that displayed by the Bigeye Thresher (Hanan et al., 1993). For this reason, it is important to consider that a comparison of the RM temperature to that of the ambient surface conditions may underestimate the true thermal excess ordinarily experienced by these sharks. For example, the warmest specimen in our study (i.e., Thresher #17, Fig. 2), which had a RM thermal excess of 5.4 C when compared to the SST (Table 1), would achieve a much higher thermal excess (11.1 C) when compared to the water temperature at the depth at which the shark was hooked (i.e., 30–35 m, water temperature 12.7 C, Fig. 3). For this reason, it may be more appropriate to compare the RM values to the temperature at which the fish was captured, and if not possible, to the coolest WM temperatures recorded rather than to the SST which is the most conservative measurement of thermal excess. Again, using Thresher #17 as an example, the thermal excess of 7.4 C above the WM, represents a value that is similar to those recorded in both lamind sharks and tunas, the only other groups documented to warm their RM (Carey et al., 1971; Carey, 1973; Anderson and Goldman, 2001).

Why are the temperature measurements for the threshers in this study so variable? The difficulty associated with capturing (i.e., length of time on the line) and handling large pelagic fish and the constraints of the methods employed in this study can probably account for some of the variability in the data. Although we found no effect of fight time (Table 1) on the RM temperature elevation above SST in rod and reel captured sharks, these data and the measurements reported for longline capture fish were taken from sharks that had undergone some degree of capture-related struggle, and it may be that these values do not reflect the natural in vivo temperature of this species, but rather values from fish that have undergone various degrees of exhaustion. For example, the effects of an increased swimming activity level on metabolic heat production may have altered RM temperature elevation. In general, an increase in aerobic activity (e.g., long, sustained capture-struggle events) should result in a higher rate of RM contraction, an elevated RM aerobic demand, and an enhanced RM blood supply (i.e., resulting from a higher cardiac output). Although this increased activity is also accompanied by an increase in metabolic heat production, the consequential increase in blood flow through the adjacent retia would decrease blood residence time in the vascular structure and result in a decreased heat-exchange efficiency because heat flux (i.e., heat exchange) is inversely correlated to the rate of blood flow (Graham, 1983; Brill et al., 1994). Hence, the aerobic demand forced upon a struggling fish (capture struggle) may translate into a decrease in RM temperature elevation, further suggesting that the temperature data presented in this study (all of which underwent some degree of capture-related struggle) may be lower than values for nonstressed fish. This hypothesis is supported by Carey at al. (1981) and Goldman (1997) who found that lamnid sharks that underwent the longest capture-related struggle exhibited the lowest visceral thermal excess (the viscera of lamnids is also served by a heat-exchanging retia). Resolving questions related to RM temperature elevation and swimming activity level requires future studies to focus on collecting RM temperature data from free-swimming sharks that undergo natural diving movements.

Although this work documents that the Common Thresher Shark is capable of RM endothermy, the degree to which the temperature is maintained and the possibility of physiological and behavioral thermoregulation remain unknown. In addition, the assumption that all members of the Alopiidae are capable of RM endothermy may be premature. Little is known about the other two thresher species (Alopias superciliosus and Alopias pelagicus) and although recent work has focused on the movements of free-swimming Bigeye Thresher Sharks (Nakano et al., 2003; Weng and Block, 2004), there is no information on their RM morphology and the presence or absence of a heat exchange system (retia) serving the RM. This precludes the generalization that RM endothermy is a synapomorphy of the Family Alopiidae and warrants future investigations aimed at describing the muscle morphology, vascular anatomy, and endothermic capacity of all three thresher shark species. Understanding the physiological and behavioral differences among the three thresher shark species may provide valuable information regarding their geographic distribution, habitat use, and possible niche overlap.