Next Article in Journal
Optimization of Cyanine Dye Stability and Analysis of FRET Interaction on DNA Microarrays
Previous Article in Journal
Fish Immunoglobulins
Article Menu

Export Article

Biology 2016, 5(4), 46; https://doi.org/10.3390/biology5040046

Article
Thermal Resilience of Feeding Kinematics May Contribute to the Spread of Invasive Fishes in Light of Climate Change
Department of Biological Sciences, Florida Institute of Technology, 150 West University Boulevard, Melbourne, FL 32901, USA
*
Author to whom correspondence should be addressed.
Academic Editor: Chris O’Callaghan
Received: 30 September 2016 / Accepted: 17 November 2016 / Published: 25 November 2016

Abstract

:
As a consequence of global warming, tropical invasive species are expected to expand their range pole-ward, extending their negative impacts to previously undisturbed, high-latitude ecosystems. Investigating the physiological responses of invasive species to environmental temperature is important because the coupled effects of climate change and species invasion on ecosystems could be more alarming than the effects of each phenomenon independently. Especially in poikilotherms, the rate of motion in muscle-driven biomechanical systems is expected to double for every 10 °C increase in temperature. In this study, we address the question, “How does temperature affect the speed of jaw-movement during prey-capture in invasive fishes?” Kinematic analysis of invasive-fish prey-capture behavior revealed that (1) movement velocities of key components of the feeding mechanism did not double as water temperature increased from 20 °C to 30 °C; and (2) thermal sensitivity (Q10 values) for gape, hyoid, lower-jaw rotation, and cranial rotation velocities at 20 °C and 30 °C ranged from 0.56 to 1.44 in all three species. With the exception of lower-jaw rotation, Q10 values were significantly less than the expected Q10 = 2.0, indicating that feeding kinematics remains consistent despite the change in environmental temperature. It is conceivable that the ability to maintain peak performance at different temperatures helps facilitate the spread of invasive fishes globally.
Keywords:
global warming; prey-capture; suction feeding; organismal performance; thermal tolerance

1. Introduction

Projected variations in global temperature as a consequence of climate change have underscored renewed interest in addressing questions about temperature-dependent organismal performance [1,2,3,4,5]. The re-emergence of emphasis on ecological physiology of organisms is rooted in the notion that physiological traits are strong determinants of species response to climate change [6,7,8,9,10,11,12,13]. In light of the climate change phenomenon, what mechanisms underlie organismal response to environmental temperature variations? In an attempt to establish the foundation for continuing investigations addressing this central question, this study was designed to explore the effects of temperature on whole-organism performance, specifically prey-capture kinematics, in three orders of invasive-teleost fishes. To our knowledge, these are the first three invasive species used to investigate the effects of environmental temperature on feeding kinematics in light of climate change. The use of invasive fishes to examine temperature-dependent performance increases the relevance of this study because of the belief that the coupled effects of climate change and species invasion on ecosystems are more alarming than the effects of each taken independently [14]. It is predicted that, as a consequence of global warming, tropical invasive species expand their range poleward, thus, extending their well-known negative biological impacts to previously undisturbed, high-latitude ecosystems [14,15,16].
The effects of environmental temperature on physiological processes are widespread in both animals and plants, but in fishes its effects on skeletal-muscle performance and property have been the focus of most basic and applied physiological studies. It is expected that the direct effects of environmental temperature on body temperature mediate physiological processes, most especially metabolic rate. In fishes, as with any poikilothermic vertebrate, physiological performance peaks at a narrow range of body temperature, and environmental temperature remains a major constraint in their range of distribution [4,5,17,18,19,20]. Metabolic rate, in general, and contraction rate of skeletal muscle fibers, in particular, increase with environmental temperature until a threshold level is achieved, after which these rates decline with further increase in environmental temperature [18,21,22,23,24,25,26]. The ability of an individual to perform a certain task (e.g., prey capture) driven by a temperature-dependent process (e.g., rate of contraction of buccal-expansion muscles) is constrained by the reduction in biological rates as a consequence of decrease in environmental temperature. Furthermore, the expression of temperature-induced changes in fish-muscle physiology varies according to different temporal scales (i.e., daily, seasonal, or life-history, developmental time scales) and levels of organization (i.e., from molecular to organismal to ecosystem) [27]. For example, intracellular and extracellular ionic concentration and acid balance are destabilized by instant changes in environmental temperature [28]. Seasonal temperature change may induce modifications of the properties and composition of the contractile elements of the muscle fiber [27]. This time scale may allow fish to acclimate to the new ambient temperature and drive plastic response in muscle-fiber phenotypes and trigger behavioral and other mechanisms that buffer temperature effects and maintain homeostasis [28,29,30]. At the whole-organism level, responses to environmental temperature change may be taxon- and ontogenetic- specific. Indeed, environmental temperature has a profound influence on the fish’s ability to successfully accomplish relevant tasks such as swimming, feeding, mating, and escaping from predators.
Interestingly, previous studies investigating temperature effects on whole-organism performance in fishes have revealed mixed results. The kinematics of routine-swimming in teleost fishes have been largely consistent with physiological expectations. For example, swimming velocity doubles in response to a 10 °C increase in environmental temperature, that is, Q10 values are at least 2.0 [31,32,33,34]. The physiological quotient (Q10 value) indicates the magnitude of change in biological rates (e.g., swimming speed) for every 10 °C change in temperature [31,32,33,34]. An attempt to arrive at a consensus on the effects of temperature on feeding kinematics in teleost fishes remains unsuccessful perhaps because of the differences in the experimental design employed by the relatively few studies investigating this subject matter. In investigating how decrease or increase in environmental temperature, between 18 °C and 24 °C, affect prey-capture performance, Wintzer and Motta [19] concluded that it took bluegill (Lepomis macrochirus) longer to achieve maximum gape and lower-jaw rotation as water temperature decreased. DeVries and Wainwright [20] found that a 15 °C decrease in temperature caused only the time to reach maximum gape, among all timing parameters that underlie suction feeding performance in largemouth bass (Micropterus salmoides), to slightly increase. In Sloan and Turingan [35], and Turingan and Sloan [36], Repeated Measures Multivariate Analysis of Covariance revealed that environmental temperature, raised from 20 °C to 30 °C at a rate of 1 °C daily, had no effect on the magnitude and timing of prey-capture kinematics of nonnative teleost fishes in Florida, USA. Considering that the ability to successfully capture prey determines individual survivorship, it is imperative to elucidate how environmental temperature mediates prey-capture performance in organisms.
Three invasive Florida fishes—Pike killifish, Belonesox belizanus (Cyprinidontiformes); lionfish, Pterois volitans (Scorpaeniformes); and Mayan cichlid, Cichlasoma urophthalmus (Perciformes)—were used to determine how variable or consistent whole-organism response is, particularly in invasive species, to environmental temperature. Consistent with the prediction of climate-driven range expansion of invasive-species poleward, these invasive fishes have continued to extend their distribution northward from where they were introduced in south Florida [37,38,39,40]. The average annual temperature within the current distribution of these invasive fishes ranges between 20 °C and 30 °C [41]. This is used as the basis for the selection of experimental temperatures in this study.
Identified as one of the most abundant nonnative fishes in Florida, Belonesox belizanus is native to waters (temperature is 25–37 °C) in Mexico and Central America, and was introduced into a ditch in south Florida in the late 1950s [37,38,39,40,41,42,43]. It is a specialist predator, feeding on small fishes using a feeding mechanism that is well designed for piscivory. This piscivore is capable of achieving a large gape with its elongated premaxillae and mandibles lined with large teeth [44,45,46]. The ability of pike killifish to independently rotate its premaxilla posterodorsally, facilitated by the premaxillomandibular ligament and a twisting maxilla, further enhances gape formation [45].
Pterois volitans is native to the Indo-Pacific Ocean (temperature is 22–28 °C) [47]. After its initial introduction in south Florida in the early 1990s, it has rapidly expanded its invasive population southward to the Caribbean and northward along the Atlantic coast of the USA [48,49,50,51]. The invasive lionfish has been identified as the likely worst threat to marine biodiversity in the Mid-Atlantic, Gulf of Mexico, and Caribbean regions [48,49,50,51]. This invasive predator feeds on a diverse group of fishes in the region, including 21 families and 41 species of teleost fishes, the majority of which have commercial, recreational, and ecological importance [50,52]. The predatory success of the lionfish is perhaps enhanced by its ability to modulate its suction-feeding repertoire, including a characteristic rapid-strike on more mobile, elusive fish and crustacean prey [53].
The native distribution of Cichlasoma urophthalmus ranges from eastern Mexico to Nicaragua (temperature is 22–39 °C) [54]. Following its introduction into south Florida in the 1980s, it has spread into north Florida and the Florida Bay regions [55,56,57]. Perhaps among the traits that enable the invasive Mayan cichlid to spread northward in Florida is its tolerance to extreme variations in salinity [55,56,57,58] and temperature [56,58]. In addition, the invasive Mayan cichlid has a generalist diet, feeding on detritus, plants, invertebrates and fish [59,60,61,62]. Its feeding apparatus includes an oral-jaw mechanism for prey capture and a well-developed pharyngeal-jaw apparatus for prey-processing [63].
This study was designed to test the hypothesis that the velocity of prey-capture kinematics, particularly buccal expansion and compression behaviors powered by skeletal-muscle in teleost fishes doubles when ambient-water temperature is raised by 10 °C.

2. Materials and Methods

Four B. belizanus, collected from the Florida Everglades National Park, four C. urophthalmus, collected from Merritt Island, Florida, and four P. volitans, collected from Port St. Lucie, Florida were acclimated to 20 °C water temperature and trained for high-speed video in the fish ecophysiology laboratory at Florida Institute of Technology for two weeks before the experiment was initiated. Each fish was housed in 38 L filming tanks filled with water that matched their Florida habitats: 0 ppt for B. belizanus; 24 ppt for C. urophthalmus, and 35 ppt for P. volitans. The twelve fishes were subjected to a repeated measures experimental design, in which, each fish was filmed successively in each of the three experimental temperatures 20 °C, 25 °C and 30 °C (Figure 1). Temperature in each filming tank was raised from 20 °C to the higher filming temperatures at a rate of 1 °C daily using a water heater. Once the experimental temperature was achieved, feeding sessions were recorded every other day from each fish. Each fish was filmed using a RedLake High-Speed Motionscope 2000S camera with a shutter speed of 1/1000 s at 250 frames per second while feeding on live mosquitofish (Gambusia holbrooki) prey at 20 °C, 25 °C and 30 °C. Prey was maintained at 20 °C ambient-room temperature. Prey girth was about 80% of peak gape of each fish; previous analyses of feeding kinematics in these fishes indicated that this relative prey-size elicited maximum prey-capture performance in fish [35,36,46]. The effects of temperature on the prey was not investigated in this study. Experimental fish was not fed 1–2 days before each recording session to ensure fish was motivated to eat and exhibit maximum performance during feeding trials [19,20].
Each fish was filmed until at least 10 feeding bouts were recorded in which the fish was perpendicular to the camera and exhibited maximum prey-capture performance. The best four films were analyzed per fish at each of the three experimental temperatures using MaxTRAQ (Version 2.2.4.1 Innovision Systems, Inc., Columbiaville, MI, USA). Each film was played back frame-by-frame to measure maximum gape (mm), hyoid depression (mm), lower-jaw rotation (degree), and cranial rotation (degree), as well as the time (ms) to reach each of these maximum kinematic-displacement variables. Time to reach each of these maximum kinematic-displacement variables was calculated using the frame prior to mouth opening as time = 0. Reference points (i.e., kinematic hotspots) used to measure these variables are illustrated in Figure 2. Average velocity was calculated as the value of the maximum kinematic-displacement variable divided by the corresponding time to reach this maximum displacement: Gape Velocity = Maximum Gape ÷ Time to Reach Maximum Gape; Hyoid Velocity = Maximum Hyoid Depression ÷ Time to Reach Maximum Hyoid Depression; Lower-Jaw Rotation Velocity = Maximum Lower-Jaw Rotation ÷ Time to Reach Maximum Lower-Jaw Rotation; Cranial Rotation Velocity = Maximum Cranial Rotation ÷ Time to Reach Maximum Cranial Rotation. Physiological quotient (Q10) was calculated for each of the kinematic-velocity variables as Q10 = (Kinematic Velocity at 30 °C/Kinematic Velocity 20 °C) (modified from Schmidt-Nielsen [64]).
Each of the four kinematic-velocity variables was subjected to a Model I least-squares regression against temperature to define the model y = a + bx; where y = kinematic velocity, a = intercept, b = slope, and x = environmental temperature (=20 °C, 25 °C, and 30 °C). To test the hypothesis that the Q10 of each of the kinematic-velocity variables was different from 2.0, a series of Paired t-Tests were conducted to compare the empirical Q10 values with the theoretical Q10 value of 2.0. All statistical tests were conducted using R.
After the experiment, each fish was sacrificed using an overdose of MS-222 solution, fixed in 10% formalin solution, and then stored in 75% ethanol solution. All specimens have been stored appropriately in the fish ecophysiology and evolution laboratory at Florida Institute of Technology for use in current and future teaching and research. All procedures for housing, maintaining and sacrificing experimental fishes strictly followed the guidelines and procedures of the Institutional Animal Care and Use Committee (IACUC) of the Florida Institute of Technology (IACUC Approval # 101202).

3. Results

The three Florida invasive-fish species fed voraciously upon introduction of the prey during feeding-recording sessions at each of the three environmental temperatures, 20 °C, 25 °C, and 30 °C (Figure 3). Examination of the films revealed that the feeding behavior of each fish was consistent with previous studies [35,36,46,53]. The pike killifish stalked its prey and within a very short distance between the predator and the prey, the fish lunged toward the prey, opened its mouth widely and snapped at the prey. The lionfish used its pectoral fins to herd the prey closer to its mouth before suction feeding to capture prey. The Mayan cichlid behaved more aggressively; as soon as the prey was introduced into the filming tank, the cichlid rapidly swam toward the prey and suction-fed on it instantaneously.
Linear regression models indicated that the average velocity of kinematic events during feeding in all three invasive species remained consistent across environmental temperatures, with the exception of the average velocity of hyoid depression in the Mayan cichlid and average velocity of lower-jaw rotation in the lionfish. Species-specific variation in elevation (=y-intercept, a) is apparent, but, the slopes of the regression, b, were not statistically different from zero, indicating that kinematic velocities were unaffected by environmental temperature (Table 1 and Figure 4).
The mean Q10 values of each of the kinematic velocities were significantly less than the expected Q10 value of 2.0, with the exception of the average velocity of lower-jaw rotation in the lionfish and Mayan cichlid (Table 2 and Figure 5).

4. Discussion

Empirical evidence of how organismal performance is affected by environmental change advances our understanding of the consequences of climate change and invasion of nonnative species. Investigations into the combined effects of both phenomena on native-community structure and dynamics, as well as range expansion of invasive species, are especially important considering that their combined effects are perhaps more devastating than each taken independently ([64], www.invasivespecies.gov.). It has been predicted that as a consequence of the pole-ward warming of the earth, tropical-invasive species will continue to expand their range toward higher-latitude ecosystems at alarming rates [14,65]. Well known characteristics of invasive species that enable them to impart damage in the stability of native ecosystems include: (1) they have high propensity to introduce and spread diseases [66,67,68]; (2) they alter community and food web structure through competition and predation [38,69,70,71,72,73]; (3) they hybridize with native species [74,75,76]; and (4) they outcompete native species and ultimately displace and even drive native species to extinction [1,2,67,69]. The latter results in the reduction of biodiversity and may even lead to biological homogenization. Although empirical evidence demonstrating the direct and indirect interactions between invasive and native species, as well as the cause-effect mechanism underlying post-invasion changes in community structure of invaded ecosystems, are elusive, it is hypothesized that climate change exacerbates the negative impacts of invasive species to ecology and society [77,78]. In our attempt to contribute to the advancement of our understanding of the impacts of the invasive species and climate change coupling to ecosystem dynamics, our discussion of the results of this study centers on the question, “How do invasive fishes deal with variations in temperature within their invasive range?”
As poikilotherms, the feeding performance of invasive fishes are expected to conform with the known effects of temperature on the physiology and ecology of heterothermic, aquatic animals [79]. For example, first, the velocity of fin propulsion during swimming and mouth-opening during feeding, behaviors fueled by skeletal-muscle contraction and relaxation, are expected to double when ambient temperature is increased by 10 °C. This is because at the physiological level of analysis, there is a two-fold increase in the rate of muscular contraction and relaxation for every 10 °C increase in temperature (i.e., Q10 = 2.0) [18,21,22,23,24,31]. Second, at the ecological level of analysis, predictable seasonal cooling and warming of lakes and rivers have contributed to the evolution of acclimatization in teleost fishes [80,81,82]. Third, the food habit of some temperate fishes, such as largemouth bass, Micropterus salmoides, and pumpkinseed sunfish, Lepomis gibbosus, change seasonally, consistent with the seasonal cooling and warming of lakes or rivers in temperate ecosystems [80,81,82].
Results of this study, as well as those of Sloan and Turingan [35] and Turingan and Sloan [36] underscore the thermal independence of prey-capture performance in invasive-teleost fishes. Suction-feeding, which is the most dominant and generalized mode of prey-capture in teleost fishes, relies primarily on the high-speed movement of cranial elements such as the jaws, hyoid, suspensorium, and cranium during mouth opening and closing (see Figure 3; [46,83,84,85,86,87,88,89]). A successful strike and capture of prey relies heavily on the almost simultaneous and rapid expansion of the buccal cavity to generate subambient-pressure in the buccal chamber and mouth opening [83,84,85]. These kinematic events are accomplished primarily by the posterodorsal rotation of the cranium, depression of the hyoid apparatus, lateral extension of the suspensorial and opercular bones, and the posteroventral rotation of the lower-jaws [83,84,85,86,87,88,89]. These cranial movements are driven by skeletal muscles including the epaxialis, sternohyoideus, retractor arcus palatini, levator operculi, and dilator operculi [83,84,85,87]. It is well known that the rate of contraction of skeletal muscle is expected to at least double for every 10 °C increase in environmental and body temperature in ectotherms such as teleost fishes [20,31,33,34,90,91,92]. However, temperature has no significant effects on the velocity of movement of the key elements of the prey-capture mechanism in the three contrasting models of invasive species reported here. Although, on average, prey-capture kinematics significantly differ among the three invasive species, the absence of a temperature-induced change in kinematic velocity is evident in all three invasive species [35,36].
Thermal independence of fast-start behaviors and kinematics has been found in other vertebrate animals. Navas et al. [93] concluded that the Q10 for “jump take-off velocity and mean swimming velocity” in the frog Rana temporaria was lower than Q10 = 2.0. “Running velocity during burst activity” in several species of lizards were less affected by temperature, as evident in the low Q10 values for this behavior [94,95,96]. “Ballistic mouth opening and tongue projection dynamics” in toads (Bufo terrestris) were thermally independent [91]. Lack of temperature-induced variation in the dynamics of “ballistic mouth opening” was also evident in the frog Rana pipiens [96].
It is noteworthy that our results do not agree with the conclusions of the only two papers reporting the effects of temperature on the feeding kinematics of native teleost fishes. Prey-capture kinematics in North American native centrarchid fishes, bluegill Lepomis microchirus, and largemouth bass Micropterus salmoides, responded to environmental-temperature change in a manner that is consistent with physiological predictions [19,20]. Among other feeding-kinematic variables that were affected by temperature, it took longer for fishes to reach peak gape in colder than in warmer temperatures [19,20]. The prevalence of thermally independent prey-capture kinematics in invasive teleost fishes underscores the need to address how they compensate for the effects of temperature on the contractile properties and contraction velocity of skeletal muscles. A direct comparison between any of the invasive fishes in this study and an ecologically relevant (e.g., as a competitor or prey) native species in Florida is imperative, given the need to address the direct impacts of invasive on native species.
Translation of the physiological effects of temperature on muscle contractile properties to whole-animal performance may be mitigated by the central nervous system [27,97,98,99]. Central nervous-system governed compensatory mechanisms may allow whole animals to perform at optimum levels despite variation in environmental and body temperatures [100,101,102]. Such compensatory mechanisms likely include (1) plasticity in the recruitment of muscle fiber types [102,103,104,105]; (2) involvement of elastic strain energy storage and recovery in muscular and tendinous tissue [106,107]; (3) occurrence of temperature-induced change in acid-base balance in muscle fiber [107,108]; (4) plasticity of thermal sensitivity of myofibrillar ATPase activity [107,108]. For example, Rome et al. [104] concluded that at lower temperatures, carp (Cyrprinus carpio) recruited more fast-contracting (fast anaerobic) muscle fibers when environmental temperature was lower than ambient. Navas et al. [93] found that at 10 °C, optimal whole animal performance was accomplished by only 34% of muscle-power output. In the sartorius muscle of the toad Bufo bufo, Renaud and Stevens [107] demonstrated that short-term change in intracellular pH associated with decrease in water temperature from 25 °C to 5 °C was enough “to increase maximum force and, hence, power during isotonic shortening of muscle fiber, providing a short-term mechanism for compensation to low temperature”.
Global-climate change in general and global-temperature change in particular have important consequences for the performance of invasive species because of (1) the temperature-induced effects on physiological and mechanical processes [79,108]; (2) the likelihood that these physiological effects extend to whole-organism performance (e.g., [19,20]); and (3) the resilience of invasive species and the resistance of whole-organism performance to temperature change ([35,36]; this study]). These plausible avenues where the interplay between climate-change and invasive-species phenomena may be demonstrated need further investigation and confirmation.

5. Conclusions

The velocity of jaw movements during prey capture in the invasive fishes, Belonesox belizanus, Pterois volitans, and Cichlasoma urophthalmus, were statistically unaffected by water temperature. Within the range of temperature used in this study, all invasive fishes successfully captured their prey using a stereotypical suction-feeding kinematic pattern that is unaltered by temperature. It is plausible that this seemingly temperature-resilient behavior will facilitate the successful expansion of the invasive range of these tropical-fish species as a consequence of global warming.

Acknowledgments

We thank Brian Bement for illustrating Figure 2. Lisa Young, Chelsea Harms, Benjamin Compton, Kayla Chapman, Brian Bement, and Matthew Sonnefeld helped with the recording of fish-feeding. This study was partially funded by Florida Sea Grant and Sigma Xi.

Author Contributions

Ralph Turingan conceived of the idea and wrote the manuscript. Tyler Sloan conducted all statistical analyses. Turingan and Sloan designed and conducted the experiments.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Davis, M.B.; Shaw, R.G. Range shifts and adaptive responses to Quaternary climate change. Science 2001, 292, 673–679. [Google Scholar] [CrossRef] [PubMed]
  2. Baker, C.; Starger, C.J.; McClanahan, T.R.; Glynn, P.W. Coral reefs: Corals’ adaptive response to climate change. Nature 2004. [Google Scholar] [CrossRef] [PubMed]
  3. Portner, H.O.; Farrell, A.P. Physiology and climate change. Nature 2008, 322, 690–692. [Google Scholar]
  4. Portner, H.O. Integrating climate-related stressor effects on marine organisms: Unifying principles linking molecule to ecosystem-level changes. Mar. Ecol. Prog. Ser. 2012, 470, 273–290. [Google Scholar] [CrossRef]
  5. Huey, R.B.; Kingsolver, J.G. Evolution of resistance to high temperature in ectotherms. Am. Nat. 1993, 142, S21–S46. [Google Scholar] [CrossRef]
  6. Chown, S.L.; Gaston, K.J.; Robinson, D. Macrophysiology: Large-scale patterns in physiological traits and their ecological implications. Func. Ecol. 2004, 18, 159–167. [Google Scholar] [CrossRef]
  7. Helmouth, B.; Kingsolver, J.G.; Carrington, E. Biophysics, physiological ecology, and climate change: Does mechanism matter? Ann. Rev. Physiol. 2005, 67, 177–201. [Google Scholar] [CrossRef] [PubMed]
  8. Deutsch, C.A.; Tewksbury, J.J.; Huey, R.B.; Sheldon, K.S.; Ghalambor, C.K.; Haak, D.C.; Martin, P.R. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl. Acad. Sci. USA 2008, 105, 6668–6672. [Google Scholar] [CrossRef] [PubMed]
  9. Huey, R.B.; Deutsch, C.A.; Tewksbury, J.J.; Vitt, L.J.; Hertz, P.E.; Perez, J.A.; Garland, T. Why tropical forest lizards are vulnerable to climate warming. Proc. R. Soc. B 2009, 276, 1939–1948. [Google Scholar] [CrossRef] [PubMed]
  10. Kearney, M.R.; Porter, W.P. Mechanistic niche modeling: Combining physiological and spatial data to predict species ranges. Ecol. Lett. 2009, 12, 334–350. [Google Scholar] [CrossRef] [PubMed]
  11. Dillion, M.E.; Wang, G.; Huey, R.B. Global metabolic impacts of recent climate warming. Nature 2010, 467, 704–706. [Google Scholar] [CrossRef] [PubMed]
  12. Doak, D.F.; Morris, W.F. Demographic compensation and tipping points in climate-induced range shifts. Nature 2010, 467, 959–962. [Google Scholar] [CrossRef] [PubMed]
  13. Smith, A.L.; Hewitt, N.; Klenk, N.; Bazely, D.R.; Yan, N.; Wood, S.; Henriques, I.; MacLellan, J.I.; Lipsig-Mumme, C. Effects of climate change on the distribution of invasive alien species in Canada: A knowledge synthesis of range change projections in a warming world. Environ. Rev. 2012, 20, 1–16. [Google Scholar] [CrossRef]
  14. Perrings, C.; Dehnen-Shmutz, K.; Touza, J.; Williamson, M. How to manage biological invasions under globalization. Trends Ecol. Evol. 2005, 20, 212–215. [Google Scholar] [CrossRef] [PubMed]
  15. Hellmann, J.J.; Byers, J.E.; Bierwagen, B.G.; Dukes, J.S. Five potential consequences of climate change for invasive species. Conserv. Biol. 2008, 22, 534–543. [Google Scholar] [CrossRef] [PubMed]
  16. Shafland, P.L.; Pestrak, J.M. Lower lethal temperatures for fourteen nonnative fishes in Florida. Environ. Biol. Fishes 1982, 7, 149–156. [Google Scholar] [CrossRef]
  17. Rome, L.C.; Sosnicki, A.A. The influence of temperature on mechanics of red muscle in carp. J. Physiol. 1990, 427, 151–169. [Google Scholar] [CrossRef] [PubMed]
  18. Wintzer, A.P.; Motta, P.J. The effects of temperature on prey-capture kinematics of the bluegill (Lepomis macrochirus): Implications for feeding studies. Can. J. Zool. 2004, 82, 794–799. [Google Scholar] [CrossRef]
  19. DeVries, M.S.; Wainwright, P.C. The effects of acute temperature change on prey capture kinematics in largemouth bass, Micropterus salmoides. Copeia 2006, 3, 437–444. [Google Scholar] [CrossRef]
  20. Cossins, A.R.; Bowler, K. Temperature Biology of Animals; Chapman and Hall (Methuen): New York, NY, USA, 1987. [Google Scholar]
  21. Clarke, A.; Johnston, N.M. Scaling of metabolic rate with body mass and temperature in teleost fish. J. Anim. Ecol. 1999, 68, 893–905. [Google Scholar] [CrossRef]
  22. Gillooly, J.F.; Brown, J.H.; West, G.B.; Savage, V.M. Effects of size and temperature on metabolic rate. Science 2001, 293, 2248–2251. [Google Scholar] [CrossRef] [PubMed]
  23. Josephson, R.K. Contraction dynamics and power output of skeletal muscle. Annu. Rev. Physiol. 1993, 55, 527–546. [Google Scholar] [CrossRef] [PubMed]
  24. Watabe, S. Temperature plasticity of contractile proteins in fish muscle. J. Exp. Biol. 2002, 205, 2231–2236. [Google Scholar] [PubMed]
  25. Malek, R.L.; Sajadi, H.; Abraham, J.; Grundy, M.A.; Gerhard, G.S. The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2004, 138, 363–373. [Google Scholar] [CrossRef] [PubMed]
  26. Johnston, I.A.; Temple, G.K. Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behavior. J. Exp. Biol. 2002, 205, 2305–2322. [Google Scholar] [PubMed]
  27. Crawshaw, L.I.; Ackerman, R.A.; White, F.N.; Heath, M.E. Metabolic and acid-base changes during selection of warmer water by cold-acclimated fish. Am. J. Physiol. 1982, 242, R157–R161. [Google Scholar] [PubMed]
  28. Lemons, D.E.; Crawshaw, L.I. Behavioral and metabolic adjustments to low temperatures in largemouth bass (Micropterus salmoides). Physiol. Zool. 1985, 58, 175–180. [Google Scholar] [CrossRef]
  29. Clark, D.S.; Green, J.M. Seasonal variation in temperature preference of juvenile Atlantic cod (Gadus morhua), with evidence supporting an energetic basis for their diel vertical migration. Can. J. Zool. 1991, 69, 1302–1307. [Google Scholar] [CrossRef]
  30. Rome, L.C.; Swank, D.M.; Coughlin, D.J. The influence of temperature on power production during swimming. II. Mechanics of red muscle fibers in vivo. J. Exp. Biol. 2000, 203, 333–345. [Google Scholar] [PubMed]
  31. Herbing, I. Effects of temperature on larval fish swimming performance: The importance of physics to physiology. J. Fish Biol. 2002, 61, 865–876. [Google Scholar] [CrossRef]
  32. Lee, C.G.; Farrell, A.P.; Lotto, A.; MacNutt, M.J.; Hinch, S.G.; Healey, M.C. The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J. Exp. Biol. 2003, 206, 3239–3251. [Google Scholar] [CrossRef] [PubMed]
  33. Green, B.S.; Fisher, R. Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. J. Exp. Mar. Biol. Ecol. 2004, 299, 115–132. [Google Scholar] [CrossRef]
  34. Sloan, T.J.; Turingan, R.G. Invariant feeding kinematics of two trophically distinct invasive Florida fishes, Belonesox belizanus and Cichlasoma urophthalmus across environmental temperature regimes. Int. J. Biol. 2012, 4, 117–126. [Google Scholar] [CrossRef]
  35. Turingan, R.G.; Sloan, T.J. Modeling the relationship between environmental temperature and feeding performance in Florida (USA) nonnative fishes, with implications for invasive-species response to climate change. Annu. Rev. Res. Biol. 2014, 4, 121–132. [Google Scholar] [CrossRef]
  36. Belshe, J.F. Observations of an Introduced Tropical Fish (Belonesox belizanus) in Southern Florida; University of Miami: Coral Gables, FL, USA, 1961. [Google Scholar]
  37. Miley, W.W. Ecological Impact of the Pike Killifish, Belonesox belizanus, Kner, (Poeciliidae) in Southern Florida. Master Thesis, Florida Atlantic University, Boca Raton, FL, USA, 1978. [Google Scholar]
  38. Anderson, R. Geographic variation and aspects of the life history of Belonesox belizanus Kner (Pisces: Poeciliidae) from Central America. Master Thesis, University of Central Florida, Orlando, FL, USA, 1980. [Google Scholar]
  39. Kerfoot, J.R.; Lorenz, J.J.; Turingan, R.G. Environmental correlates of the abundance and distribution of Belonesox belizanus in a novel environment. Environ. Biol. Fish 2011, 92, 125–139. [Google Scholar] [CrossRef]
  40. Florida Wildlife Commission. Available online: http://myfwc.com/ (accessed on 15 December 2012).
  41. National Oceanic and Atmospheric Administration. National Oceanographic Data Center. Available online: http://www.nodc.noaa.gov/dsdt/cwtg/all.html (accessed on 15 December 2012).
  42. Hubbs, C. Fishes of the Yucatan Peninsula. Carnegie Inst. Wash. Publ. 1936, 457, 157–287. [Google Scholar]
  43. Rosen, D.E.; Bailey, R.M. The poeciliid fishes (Cyprinodontiformes): Their structure, zoogeography, and systematics. Bull. Am. Mus. Nat. Hist. 1963, 126, 1–146. [Google Scholar]
  44. Greven, H.; Brenner, M. Further notes on dentition and prey capture of the Pike killifish Belonesox belizanus (Poeciliidae). Bull. Fish Biol. 2008, 10, 97–103. [Google Scholar]
  45. Ferry-Graham, L.A.; Hernandez, L.P.; Gibb, A.; Pace, C. Unusual kinematics and jaw morphology associated with piscivory in the poeciliid, Belonesox belizanus. Zoology 2010, 113, 140–147. [Google Scholar] [CrossRef] [PubMed]
  46. Harms, C.A.; Turingan, R.G. Dietary flexibility despite behavioral stereotypy contributes to successful invasion of the pike killifish, Belonesox belizanus, in Florida, USA. Aquat. Invasions 2012, 7, 547–553. [Google Scholar] [CrossRef]
  47. FishBase Species Database. Available online: www.FISHBASE.org (accessed on 15 December 2012).
  48. Whitfield, P.E.; Hare, J.A.; David, A.W.; Harter, S.L.; Munoz, R.C.; Addison, C.M. Abundance estimates of the Indo-Pacific lionfish Pterois volitans/miles complex in the western North Atlantic. Biol. Invasions 2007, 9, 53–64. [Google Scholar] [CrossRef]
  49. Hamner, R.M.; Freshwater, D.W.; Whitfield, P.E. Mitochondrial cytochrome b analysis reveals two invasive lionfish species with strong founder effects in the western Atlantic. J. Fish Biol. 2007, 71, 214–222. [Google Scholar] [CrossRef]
  50. Morris, J.A.; Akins, J.L. Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environ. Biol. Fishes 2009, 86, 389–398. [Google Scholar] [CrossRef]
  51. Morris, J.A. The biology and ecology of Indo-Pacific lionfish. Dissertation, North Carolina State University, Raleigh, NC, USA, 2009. [Google Scholar]
  52. Albins, M.A.; Hixon, M.A. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar. Ecol. Prog. Ser. 2008, 367, 233–238. [Google Scholar] [CrossRef]
  53. Pfeiffenberger, J.A. Modulation and Scaling of Prey Capture Kinematics Through Ontogeny in Invasive Indo-Pacific Lionfish, Pterois volitans/miles complex. Ph.D. Thesis, Florida Institute of Technology, Melbourne, FL, USA, 2012. [Google Scholar]
  54. Miller, R.R. Geographical distribution of Central American freshwater fishes. Copeia 1966, 4, 773–802. [Google Scholar] [CrossRef]
  55. Martinez-Palacios, C.A.; Ross, L.G.; Rosado-Vallado, M. The effects of salinity on the survival and growth of juvenile Cichlasoma urophthalmus. Aquaculture 1990, 91, 65–75. [Google Scholar] [CrossRef]
  56. Stauffer, J.R.; Boltz, S.E. Effect of salinity on the temperature preference and tolerance of age-0 Mayan cichlids. Trans. Am. Fish. Soc. 1994, 123, 101–107. [Google Scholar] [CrossRef]
  57. Schofield, P.J.; Loftus, W.F.; Fontaine, J.A. Salinity effects on behavioural response to hypoxia in the non-native Mayan cichlid Cichlasoma urophthalmus from Florida Everglades wetlands. J. Fish Biol. 2009, 7, 149–156. [Google Scholar]
  58. Martinez-Palacios, C.A.; Ross, L.G. The feeding ecology of Central American cichlid Cichlasoma urophthalmus (Gunther). J. Fish Biol. 1988, 33, 665–670. [Google Scholar] [CrossRef]
  59. Bergmann, G.T.; Motta, P.J. Diet and morphology through ontogeny of the nonindigenous Mayan cichlid “Cichlasoma (Nandopsis)urophthalmus (Gunther 1862) in southern Florida. Environ. Biol. Fishes 2005, 72, 205–211. [Google Scholar] [CrossRef]
  60. Chavez-Lopez, R.; Peterson, M.S.; Brown-Peterson, N.; Morales-Gomez, A.A.; Franco-Lopez, J. Ecology of the Mayan cichlid, Cichlasoma urophthalmus, in the Alvarado Lagoonal system, Veracruz, Mexico. Gulf Caribb. Res. 2005, 17, 123–131. [Google Scholar] [CrossRef]
  61. Hellig, C.J.; Kerschbaumer, M.; Sefc, K.M.; Koblmuller, S. Allometric shape change of the lower pharyngeal jaw correlates with a dietary shift to piscivory in a cichlid fish. Naturwissenschaften 2010, 97, 663–672. [Google Scholar] [CrossRef] [PubMed]
  62. Hulsey, C.D. Function of a key morphological innovation: Fusion of the cichlid pharyngeal jaw. Proc. R. Soc. B 2006, 273, 669–675. [Google Scholar] [CrossRef] [PubMed]
  63. Schmidt-Nielsen, K. Animal Physiology: Adaptation and Environment; Cambridge University Press: Cambridge, UK, 1997. [Google Scholar]
  64. Invasive Species and Climate Change. Available online: www.invasivespecies.gov (accessed on 15 December 2012).
  65. Rahel, F.J.; Olden, J.D. Assessing the effects of climate change on aquatic invasive species. Conserv. Biol. 2008, 22, 521–533. [Google Scholar] [CrossRef] [PubMed]
  66. Crowder, L.B. Character displacement and habitat shift in a native cisco in Southeastern Lake Michigan: Evidence for competition? Copeia 1984, 4, 878–883. [Google Scholar] [CrossRef]
  67. Douglas, M.E.; Marsh, P.C.; Minckley, W.L. Indigenous fishes of western North America and the hypothesis of competitive displacement: Medafulgida (Cyprinidae) as a case study. Copeia 1994, 1, 9–19. [Google Scholar] [CrossRef]
  68. Gozlan, R.E.; St-Hilaire, S.; Feist, S.W.; Martin, P.; Kent, M.L. An emergent infectious disease threatens European fish biodiversity. Nature 2005. [Google Scholar] [CrossRef] [PubMed]
  69. Ogutu-Ohwayo, R. The decline of the native fishes of lakes Victoria and Kyoga (East Africa) and the impact of introduced species, especially the Nile perch, Lates niloticus, and the Nile tilapia, Oreochromis niloticus. Environ. Biol. Fish 1990, 27, 81–96. [Google Scholar] [CrossRef]
  70. Mooney, H.A.; Cleland, E.E. The evolutionary impact of invasive species. Proc. Natl. Acad. Sci. USA 2001, 98, 5446–5451. [Google Scholar] [CrossRef] [PubMed]
  71. Perry, W.L.; Lodge, D.M.; Feder, J.L. Importance of hybridization between indigenous and nonindigenous freshwater species: An overlooked threat to North American biodiversity. Syst. Biol. 2002, 51, 255–275. [Google Scholar] [CrossRef] [PubMed]
  72. Singh, A.K.; Pathak, A.K.; Lakra, W.S. Invasion of an exotic fish—Common carp, Cyprinuscarpio L. in the Ganga River, India and its impacts. Acta Inchthyol. Piscat. 2010, 40, 11–19. [Google Scholar] [CrossRef]
  73. Sato, M.; Kawaguchi, Y.; Nakajima, J.; Mukai, T.; Shimatani, Y.; Onikura, N. A review of the research on introduced freshwater fishes: New perspectives, the need for research, and management implications. Landsc. Ecol. Eng. 2010, 6, 99–108. [Google Scholar] [CrossRef]
  74. McKinney, M.L.; Lockwood, J.L. Biotic homogenization: A few winners replacing many losers in the next mass extinction. Trends Ecol. Evol. 1999, 14, 450–453. [Google Scholar] [CrossRef]
  75. Bacheler, N.M.; Neal, J.W.; Noble, R.L. Diet overlap between native bigmouth sleepers (Gobiomorus dormitory) and introduced predatory fishes in a Puerto Rico reservoir. Ecol. Freshwater Fish 2004, 13, 111–118. [Google Scholar] [CrossRef]
  76. Rahel, F.J. Biogeographic barriers, connectivity and homogenization of freshwater faunas: It’s a small world after all. Freshwater Biol. 2007, 52, 696–710. [Google Scholar] [CrossRef]
  77. Weinstein, M.R.; Litt, M.; Kertesz, D.A.; Wyper, P.; Rose, D.; Coulter, M.; McGreer, A.; Facklam, R.; Ostach, C.; Willey, B.M.; et al. Invasive infections due to a fish pathogen, Streptococus iniae. S. iniae study group. N. Engl. J. Med. 1997, 337, 589–594. [Google Scholar] [CrossRef] [PubMed]
  78. Britton, J.R.; Davies, G.D.; Brazier, M.; Pinder, A.C. A case study on the population ecology of a topmouth gudgeon (Pseudorasbora parva) population in the UK and the implications for native fish communities. Aquat. Conserv. 2006, 17, 749–759. [Google Scholar] [CrossRef]
  79. Hochachka, P.W.; Somero, G.N. Biochemical Adaptation: Mechanisms and Processes in Physiological Evolution; Oxford University Press: Oxford, UK, 2002. [Google Scholar]
  80. Adams, S.M.; McLean, R.B.; Parrotta, J.A. Energy partitioning in largemouth bass under conditions of seasonality of seasonally fluctuating prey availability. Trans. Am. Fish. Soc. 1982, 111, 549–558. [Google Scholar] [CrossRef]
  81. Cochran, P.A.; Adelman, I.R. Seasonal aspects of daily ration and diet of largemouth bass, Micropterus salmoides, with an evaluation of gastric evacuation rates. Environ. Biol. Fishes 1982, 7, 265–275. [Google Scholar] [CrossRef]
  82. Garcia-Berthou, E.; Moreno-Amich, R. Food of introduced pumpkinseed sunfish: Ontogenetic diet shift and seasonal variation. J. Fish Biol. 2000, 57, 29–40. [Google Scholar] [CrossRef]
  83. Liem, K.F. Modulatory multiplicity in the functional repertoire of the feeding mechanism in cichlids. I. Piscivores. J. Morphol. 1978, 158, 323–360. [Google Scholar] [CrossRef]
  84. Liem, K.F. Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am. Zool. 1980, 20, 295–314. [Google Scholar] [CrossRef]
  85. Lauder, G.V. Patterns of evolution in the feeding mechanism of actinopterygian fishes. Am. Zool. 1982, 22, 275–285. [Google Scholar] [CrossRef]
  86. Wainwright, P.C.; Lauder, G.V. Feeding biology of sunfishes: Patterns of variation in the feeding mechanism. Zool. J. Linn. Soc. 1986, 88, 217–228. [Google Scholar] [CrossRef]
  87. Turingan, R.G.; Wainwright, P.C. Morphological and functional bases of durophagy in the queen triggerfish, Balistes vetula (Pisces, tetraodontiformes). J. Morphol. 1993, 215, 101–118. [Google Scholar] [CrossRef]
  88. Ferry-Graham, L.A.; Lauder, G.V. Aquatic prey capture in ray-finned fishes: A century of progress and new directions. J. Morphol. 2001, 248, 99–119. [Google Scholar] [CrossRef] [PubMed]
  89. Westneat, M.W. Evolution of levers and the linkages in the feeding mechanism of fishes. Integr. Comp. Biol. 2004, 44, 378–389. [Google Scholar] [CrossRef] [PubMed]
  90. Deban, S.M.; Lappin, A.K. Thermal effects on the dynamics and motor control of ballistic prey capture in toads: Maintaining high performance at low temperature. J. Exp. Biol. 2011, 214, 1333–1346. [Google Scholar] [CrossRef] [PubMed]
  91. Deban, S.M.; Richardson, J.C. Cold-blooded snipers: Thermal independence of ballistic tongue projection in the salamander Hydromantes platycephalus. J. Exp. Zool. 2011, 315, 618–630. [Google Scholar] [CrossRef] [PubMed]
  92. Navas, C.A.; James, R.S.; Wakeling, J.M.; Kemp, K.M.; Johnston, I.A. An integrative study of the temperature dependence of whole animal and muscle performance during jumping and swimming in the frog Rana temporaria. J. Comp. Physiol. B 1999, 169, 588–596. [Google Scholar] [CrossRef] [PubMed]
  93. Christian, K.A.; Tracy, C.R. The effect of thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia 1981, 49, 218–223. [Google Scholar] [CrossRef]
  94. Bennett, A.F. Thermal dependence of muscle function. Am. J. Physiol. 1984, 247, R217–R229. [Google Scholar] [PubMed]
  95. Marsh, R.L.; Bennet, A.F. Thermal dependence of contractile properties of skeletal muscle from the lizard, Sceleporus occidentalis with comments on the methods for fitting and comparing force-velocity curves. J. Exp. Biol. 1986, 126, 63–77. [Google Scholar] [PubMed]
  96. Sandusky, E.P.; Deban, S.M. Temperature effects on the biomechanics of prey capture in the frog Rana pipiens. J. Exp. Zool. 2012, 317A, 595–607. [Google Scholar] [CrossRef] [PubMed]
  97. Dickinson, M.H.; Farley, C.T.; Full, R.J.; Koehl, M.A.R.; Kram, R.; Lehman, S. How animals move: An integrative view. Science 2000, 288, 100–106. [Google Scholar] [CrossRef] [PubMed]
  98. Grimby, L.; Hannerz, J.; Hedman, B. The fatigue and voluntary discharge properties of single motor units in man. J. Physiol. 1981, 316, 545–554. [Google Scholar] [CrossRef] [PubMed]
  99. Aagaard, P.; Simonson, E.B.; Andersen, J.L.; Magnusson, P.; Dyhre-Poulsen, P. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J. Appl. Physiol. 2002, 93, 1318–1326. [Google Scholar] [CrossRef] [PubMed]
  100. Johnston, I.A.; Davison, W.; Goldspink, G. Energy metabolism of carp swimming muscles. J. Comp. Physiol. 1997, 114, 203–216. [Google Scholar] [CrossRef]
  101. Rome, L.C.; Loughna, P.T.; Golspink, G. Muscle fibre recruitment as a function of swim speed and muscle temperature in carp. Am. J. Physiol. 1984, 247, R272–R279. [Google Scholar] [PubMed]
  102. Rome, L.C. Influence of temperature on muscle recruitment and muscle function in vivo. Am. J. Physiol. 1990, 259, R210–R222. [Google Scholar] [PubMed]
  103. Peplowski, M.M.; Marsh, R.L. Work and power output in the hindlimb muscles of Cuban tree frogs Oesteopilu septentrionalis during jumping. J. Exp. Biol. 1997, 200, 2861–2870. [Google Scholar] [PubMed]
  104. Bojsen-Moller, J.; Magnusson, S.P.; Rasmussen, L.R.; Kjaer, M.; Aagaard, P. Muscle performance during maximal isometric and dynamic contractions is influenced by the stiffness of the tendinous structures. J. Appl. Physiol. 2005, 99, 986–994. [Google Scholar] [CrossRef] [PubMed]
  105. Konow, N.; Azizi, E.; Roberts, T.J. Muscle power attenuation by tendon during energy dissipation. Proc. R. Soc. B 2012, 279, 1108–1113. [Google Scholar] [CrossRef] [PubMed]
  106. Boutilier, R.G.; Glass, M.L.; Heisler, N. Blood gases, and extracellular/intracellular acid-base status as a function of temperature in the anuran amphibian Xenopus laevis and Bufo marinus. J. Exp. Biol. 1987, 130, 13–25. [Google Scholar]
  107. Renaud, J.M.; Stevens, E.D. The extent of short-term and long-term compensation to temperature shown by frog and toad Sartorius muscle. J. Exp. Biol. 1984, 108, 57–75. [Google Scholar]
  108. Vogel, S. Life in Moving Fluids, the Physical Biology of Flow, 2nd ed.; Princeton University Press: Princeton, NJ, USA, 1994; p. 467. [Google Scholar]
Figure 1. Diagram depicting the experimental design investigating the effects of environmental temperature on the kinematic velocity to reach maximum gape, hyoid depression, cranial rotation, and lower-jaw rotation. Four individuals of each invasive species Belonesox belizanus, Pterois volitans, and Cichlasoma urophthalmus were filmed while feeding on live-fish prey at 20 °C, 25 °C, and 30 °C using high-speed video. The best four films of each individual feeding at each temperature were digitized to measure the four kinematic velocities stated above and to calculate Q10 values. Kinematic velocities and Q10 values were subjected to the appropriate statistical tests to determine the effects of temperature on prey-capture performance.
Figure 1. Diagram depicting the experimental design investigating the effects of environmental temperature on the kinematic velocity to reach maximum gape, hyoid depression, cranial rotation, and lower-jaw rotation. Four individuals of each invasive species Belonesox belizanus, Pterois volitans, and Cichlasoma urophthalmus were filmed while feeding on live-fish prey at 20 °C, 25 °C, and 30 °C using high-speed video. The best four films of each individual feeding at each temperature were digitized to measure the four kinematic velocities stated above and to calculate Q10 values. Kinematic velocities and Q10 values were subjected to the appropriate statistical tests to determine the effects of temperature on prey-capture performance.
Biology 05 00046 g001
Figure 2. Diagram of the pike killifish, Belonesox belizanus (top), lionfish, Pterois volitans (middle), and Mayan cichlid, Cichlasoma urophthalmus (bottom) showing the homologous hotspots used to measure peak gape (= maximum distance measured from the anteriormost tip of the premaxilla (A) to the anteriormost tip of the dentary (C)), peak hyoid depression (= maximum distance between the center of the eye (E) to the anteriormost tip of the hyoid bar (D)), peak lower-jaw rotation (= maximum posteroventral rotation of the lower-jaw, measured as the angle formed by line segments AB (= jaw-joint) to BC), and peak cranial rotation (= maximum posterodorsal rotation of the neurocranium, measured by the angle formed by line segments AG (= dorsal tip of the pectoral-fin base) to GF (= anterior tip of the dorsal-fin base)).
Figure 2. Diagram of the pike killifish, Belonesox belizanus (top), lionfish, Pterois volitans (middle), and Mayan cichlid, Cichlasoma urophthalmus (bottom) showing the homologous hotspots used to measure peak gape (= maximum distance measured from the anteriormost tip of the premaxilla (A) to the anteriormost tip of the dentary (C)), peak hyoid depression (= maximum distance between the center of the eye (E) to the anteriormost tip of the hyoid bar (D)), peak lower-jaw rotation (= maximum posteroventral rotation of the lower-jaw, measured as the angle formed by line segments AB (= jaw-joint) to BC), and peak cranial rotation (= maximum posterodorsal rotation of the neurocranium, measured by the angle formed by line segments AG (= dorsal tip of the pectoral-fin base) to GF (= anterior tip of the dorsal-fin base)).
Biology 05 00046 g002
Figure 3. Select frames of representative films of two lionfish showing the sequence of kinematic events during prey capture in lionfish, Pterois volitans, at 20 °C, and 30 °C. Note that all species of invasive fishes successfully captured prey in both temperatures.
Figure 3. Select frames of representative films of two lionfish showing the sequence of kinematic events during prey capture in lionfish, Pterois volitans, at 20 °C, and 30 °C. Note that all species of invasive fishes successfully captured prey in both temperatures.
Biology 05 00046 g003
Figure 4. Scatterplot showing the relationship between each of the four kinematic-velocity variables and feeding temperature 20 °C, 25 °C, and 30 °C. Results of the regression analysis that quantified the effect of temperature on each of the kinematic events are presented in Table 1.
Figure 4. Scatterplot showing the relationship between each of the four kinematic-velocity variables and feeding temperature 20 °C, 25 °C, and 30 °C. Results of the regression analysis that quantified the effect of temperature on each of the kinematic events are presented in Table 1.
Biology 05 00046 g004
Figure 5. Mean Q10 values for kinematic-velocity in each of the three invasive-fish species. Note that except for the mean Q10 values for lower-jaw rotation in the Mayan cichlid and lionfish, all Q10 values of kinematic velocity were significantly less than the expected Q10 value of 2.0 for fish feeding at 20 °C and 30 °C. Error bars indicate standard error of the mean.
Figure 5. Mean Q10 values for kinematic-velocity in each of the three invasive-fish species. Note that except for the mean Q10 values for lower-jaw rotation in the Mayan cichlid and lionfish, all Q10 values of kinematic velocity were significantly less than the expected Q10 value of 2.0 for fish feeding at 20 °C and 30 °C. Error bars indicate standard error of the mean.
Biology 05 00046 g005
Table 1. Results of the regression analysis examining the effects of temperature on the kinematic velocities of maximum gape, hyoid depression, cranial rotation and lower-jaw rotation.
Table 1. Results of the regression analysis examining the effects of temperature on the kinematic velocities of maximum gape, hyoid depression, cranial rotation and lower-jaw rotation.
KinematicsSpeciesabr2p
GapeP0.2450.03430.07340.163
L1.797−0.03570.08590.130
M1.821−0.03760.08930.122
HyoidP0.393−1.14 × 10−34.53 × 10−40.914
DepressionL0.738−0.01620.08530.131
M0.980−0.02670.2270.010
CranialP11.385−0.2430.04190.296
RotationL8.808−0.1079.38 × 10−30.624
M−1.8170.3680.1010.099
Lower-JawP13.365−0.1790.02860.390
RotationL−3.5680.6100.2330.009
M8.0890.06643.61 × 10−30.761
Coefficients defining the regression equation, y = a + bx are shown. y = velocity to reach maximum Gape, Hyoid Depression, Cranial Rotation, and Lower-Jaw Rotation. a = intercept; b = slope. R2 = Coefficient of Determination. p = probability associated with the null hypothesis that the slope of each regression is significantly different from zero. P = Pike killifish, Belonesox belizanus; L = Lionfish, Pterois volitans; M = Mayan cichlid, Cichlasoma urophthalmus.
Table 2. Results of the Paired t-Tests comparing the difference between mean Q10s of each of the kinematic velocity variables and the expected value of 2.0.
Table 2. Results of the Paired t-Tests comparing the difference between mean Q10s of each of the kinematic velocity variables and the expected value of 2.0.
KinematicsSpeciesMean Q10t-StatisticDfp
GapeP0.973−7.617430.005
L0.922−6.444830.008
M1.046−4.385930.022
HyoidP1.047−30.027338.113 × 10−5
L0.559−67.103637.239 × 10−6
M0.876−9.861730.002
CranialP1.049−6.827530.006
RotationL1.054−9.724730.002
M1.033−19.076933.145 × 10−4
Lower-JawP1.004−6.971930.006
RotationL1.294−2.810630.063
M1.444−1.661730.195
Relevant statistics are shown for P = Pike killifish, Belonesox belizanus; L = Lionfish, Pterois volitans; M = Mayan cichlid, Cichlasoma urophthalmus. Note that except for the Q10 of the velocity of lower-jaw rotation in Mayan cichlid and lionfish, all Q10 values of kinematic velocities are statistically less than the expected value of 2.0.
Biology EISSN 2079-7737 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top