Abstract
Any attempt to describe the spatial ecology of sharks and rays should consider the drivers responsible for movement. Research has shown fluctuations in the environment (abiotic factors) can trigger movement and changes in behaviour and habitat use for many elasmobranch species. Most studies to date have selectively focused on a small number of abiotic factors (i.e. temperature, salinity); however, other factors such as dissolved oxygen, tide, photoperiod, barometric pressure and pH have also been documented to act as drivers of movement in shark and ray species. Although usually examined individually, abiotic factors rarely act in isolation and often differ in their level of influence between species, sex, ontogenetic stage, season and geographic location. This paper reviews the role of abiotic factors as a driver of movement and changes in behaviour and habitat use in elasmobranchs. In the context of a changing climate, insight into how sharks and rays may respond to fluctuating environmental conditions projected under future scenarios is required.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Sharks and rays are predators within the marine environment and many species are thought to play an important role in coastal and oceanic ecosystems worldwide (Bascompte et al. 2005; Ferretti et al. 2008; Heithaus et al. 2008). Several studies have suggested that the removal of large predators from marine systems can lead to drastic and lasting effects in the form of trophic cascades and/or the collapse of marine communities (Dulvy et al. 2000; Shepherd and Myers 2005; Polovina et al. 2009). To date, most studies examining predator removal from marine systems have focused on the effects of overfishing (Stevens et al. 2000; Baum and Worm 2009; Polovina et al. 2009). However, other drivers exist that may affect the distribution and abundance of sharks and rays within marine ecosystems and, by association, the broader marine community. Abiotic factors are easily measured and may form some of the main drivers for behavioural patterns within marine ecosystems. Biotic factors such as prey density and availability (Heithaus 2001; Heithaus et al. 2002; Torres et al. 2006; Goetze and Fullwood 2013), and predator avoidance (Heupel and Hueter 2002; Collins et al. 2007; Heithaus et al. 2009) have also been shown to play a role in the spatial ecology of elasmobranchs. These studies illustrate that a range of drivers influence shark and ray populations and the ecosystems where they occur.
Recent studies have shown that abiotic factors may be significant drivers of movement among sharks and rays. Both acute (e.g. severe weather events; Heupel et al. 2003; Matich and Heithaus 2012) and chronic (e.g. seasonal temperature change; Hopkins and Cech 2003; Heupel 2007; Carlisle and Starr 2009) changes have been linked to movement. For example, Matich and Heithaus (2012) found that juvenile bull sharks, Carcharhinus leucas, either permanently left an estuarine system or died during an extreme “cold snap.” In Tomales Bay, California, the bat ray, Myliobatis californica, leopard shark, Triakis semifasciata, and brown smooth-hound shark, Mustelis henlei, were observed to emigrate from the bay in response to a seasonal decrease in water temperature (Hopkins and Cech 2003). In addition to temperature, abiotic factors such as salinity (Collins et al. 2008; Heupel and Simpfendorfer 2008; Ubeda et al. 2009; Simpfendorfer et al. 2011), dissolved oxygen (Parsons and Hoffmayer 2005; Heithaus et al. 2009; Craig et al. 2010; Espinoza et al. 2011), tide (Medved and Marshall 1983; Ackerman et al. 2000; Knip et al. 2011a; Campbell et al. 2012), photoperiod (Grubbs et al. 2005; Heupel 2007; Kneebone et al. 2012; Nosal et al. 2014), barometric pressure (Heupel et al. 2003; Udyawer et al. 2013) and pH (Ortega et al. 2009) have all been reported to play a role in the location and movement of sharks and rays.
Understanding how species respond to changes in their environment is increasingly important given reports of growing human-mediated environmental effects on marine systems. Sharks and rays currently face an array of anthropogenic threats, especially in coastal ecosystems (Knip et al. 2010; Dulvy et al. 2014). For example, chemical pollutants and pesticides found in river run-off have been shown to have a negative impact on both ecosystem health and productivity (Fabricius 2005; Hutchings et al. 2005; Schaffelke et al. 2005). Most notably, Gelsleichter et al. (2005) documented a possible link between exposure to organochloride contaminants found in Florida estuaries and reproductive health in the bonnethead shark, Sphyrna tiburo. Intense coastal development such as dredging, construction and deforestation has also been linked to wide-scale habitat alteration and destruction (Edgar et al. 2000; Lotze et al. 2006). Perhaps unsurprisingly, recent studies have reported changes in abundance and distribution of several elasmobranch species associated with human-altered habitats (Jennings et al. 2008; Jirik and Lowe 2012; Werry et al. 2012; Curtis et al. 2013). It is important to note, however, that the effects of utilising modified habitats for sharks and rays are not necessarily negative. Research into use of restored estuarine habitat by round stingrays, Urobatis halleri, suggested that female rays may have benefited from the significantly higher mean water temperatures found in restored estuarine basins than in adjacent natural areas (Jirik and Lowe 2012). Collectively, these studies highlight how human-mediated environmental changes have the potential to alter local environmental conditions, affecting the health and spatial ecology of sharks and rays, both positively and negatively.
Compounding anthropogenic changes in coastal systems is the fact that key inshore habitats for many species are often characterised by fluctuating environmental conditions such as high freshwater run-off/low salinity events (Mann 2000; Devlin and Schaffelke 2009), tropical storms (Conner et al. 1989) and large and/or rapid changes in temperature (Mann 2000). With the global population expected to reach an estimated 9 billion by 2050 (Cohen 2003, 2005), and with future climate change scenarios predicting substantial changes in a range of environmental parameters (Emanuel 2005; Webster et al. 2005; Hoegh-Guldberg et al. 2007; Rahmstorf 2007), most of these environmental changes are expected to be exacerbated.
In light of current and projected environmental changes on marine systems, and given the important role predators such as sharks and rays play in the trophic dynamics of coastal and oceanic ecosystems globally, it is vital to understand the drivers behind movement. As movement plays a critical role in defining the use and importance of key habitats for sharks and rays, resolving whether abiotic factors drive movement will provide essential information on spatial ecology and provide data valuable to the successful management of these species and habitats. This review paper outlines and discusses: (1) abiotic factors linked to movement of sharks and rays; (2) complexities associated with determining environmental drivers of movement; and (3) the role of environmental change on spatial ecology.
Abiotic factors linked to movement of sharks and rays
Abiotic factors may influence movement either indirectly (e.g. altering patterns of abundance and distribution of principal prey species) or directly. Given that the energetic demands of key metabolic and physiological processes (e.g. digestion, osmoregulation) for sharks and rays are known to fluctuate in response to changes in abiotic factors such as temperature and salinity (Bernal et al. 2012), the primary way in which abiotic factors are thought to influence elasmobranch movement is directly, via their effect on physiology. Specifically, movement may occur in response to a physiological limit being reached or to a physiological preference, where individuals move to maintain abiotic factors at levels that provide them with some form of advantage.
As mobile marine predators, most sharks and rays have the ability to leave an area should local environmental conditions change sufficiently that the energetic costs of maintaining key metabolic and physiological processes become too demanding. Individuals that leave, however, risk the inability to find new suitable habitat and an increased chance of predation, while those that stay must exist in a stressed state or, at worst, suffer death. Whether or not individuals that leave return to their original habitat or relocate permanently often depends on the length and severity of environmental fluctuations. The following section outlines abiotic factors currently linked to movement of sharks and rays.
Temperature
Temperature is well-known to have an effect on the physiology of ectotherms (Fry 1971; Crawshaw 1977; Bernal et al. 2012). The rate of important metabolic and physiological functions such as digestion, somatic growth, and reproduction is determined by the core body temperature of fish which, in turn, is directly controlled by the temperature in their surrounding environment. This is in contrast to endothermic species that are able to regulate their internal body temperature and help maintain metabolic rates using specialized circulatory mechanisms that retain heat (Anderson and Goldman 2001; Dickson and Graham 2004; Donley et al. 2007). Most sharks and rays are ectothermic with the only exceptions found within the family Lamnidae, comprising just five species (Bernal et al. 2012). Given the role that ambient temperature plays in influencing key metabolic and physiological processes for ectotherms, it is perhaps unsurprising that many sharks and rays are sensitive to changes in temperature.
Temperature-related mortality events (i.e. “cold kills”) have been documented for some sharks and rays in response to extreme drops in temperature (Snelson and Bradley 1978; Poulakis et al. 2011; Matich and Heithaus 2012). In contrast, laboratory-held Atlantic stingrays, Dasyatis sabina, acclimated to temperatures at or lower than those experienced in their natural habitat (Fangue and Bennett 2003). The authors suggested that by being able to adapt to temperatures lower than those present in their natural habitat rays were able to exploit a wider range of resources than competitors and/or use thermal gradients as a refuge from predators. While sharks and rays that choose to remain within their home range area when temperatures fluctuate must either adapt to the new conditions or suffer death, many species respond through movement.
Temperature-mediated seasonal (Dunbrack and Zielinski 2003; Hopkins and Cech 2003; Heupel 2007; Vaudo and Heithaus 2009) and diel (Carey and Scharold 1990; Economakis and Lobel 1998; Matern et al. 2000; Sims et al. 2006) movements are well-documented in the literature. For example, juvenile blacktip sharks, Carcharhinus limbatus, in nearshore waters of the Gulf of Mexico used decreases in water temperature as a cue to leave their summer nursery area—a seasonal exodus to avoid lethal winter temperatures (Heupel 2007). In addition to movement in response to seasonal temperature change, many species are thought to use movement to actively seek out preferred temperatures throughout the day. Common thresher sharks, Alopias vulpinus, displayed diel patterns in depth distribution and activity indicating a nocturnal preference for the warmer mixed layer after daytime activity in deeper, cooler water (Cartamil et al. 2010). Collectively, studies documenting temperature-mediated seasonal and diel movements indicate that temperature often works on shark and ray populations at a variety of temporal scales.
Movement to locate a spatially variable preferred temperature range (i.e. behavioural thermoregulation) may be important to foraging (Carey and Scharold 1990; Matern et al. 2000; Sims et al. 2006; Thums et al. 2013) and reproductive (Economakis and Lobel 1998; Hoisington and Lowe 2005; Hight and Lowe 2007; Jirik and Lowe 2012; Speed et al. 2012) strategies among sharks and rays. Thermoregulatory behaviour may confer biological advantages to the individual that offset movement costs. Benefits often include energy savings that could be allocated to growth or other biological functions (e.g. reproduction).
The use of behavioural thermoregulation as a foraging strategy may be the reason why deep dives by blue sharks, Prionace glauca, were punctuated by frequent short periods at the surface (Carey and Scharold 1990). Since muscle warms more quickly than it cools, blue sharks were thought to re-warm quickly at the surface between dives, allowing them to extend their foraging time below the thermocline. Similarly, a recent study investigating movement of whale sharks, Rhincodon typus, off the coast of Western Australia found post-dive surface duration to be negatively correlated with the minimum temperature of dives, thought to be a thermoregulatory strategy where sharks re-warm at the surface after foraging in cooler, deep waters (Thums et al. 2013). Movement into cooler water after feeding has been suggested to decrease the rate of gastric evacuation and increase assimilation efficiency for several species (Matern et al. 2000; Sims et al. 2006; Di Santo and Bennett 2011). A 10 °C decrease in water temperature, for example, resulted in a 30 % increase in overall food absorption in Atlantic stingrays (Di Santo and Bennett 2011). By adopting a “hunt warm, rest cool” strategy male dogfish, Scyliorhinus canicula, were thought to lower their daily energetic costs by just over 4 % (Sims et al. 2006). Increases in assimilation efficiency and extended foraging times are examples of how sharks and rays use temperature-mediated movement to conserve energy and improve individual foraging success.
In contrast, movement of female sharks and rays into warm, shallow water is thought to provide reproductive benefits (Economakis and Lobel 1998; Hoisington and Lowe 2005; Hight and Lowe 2007; Jirik and Lowe 2012; Nosal et al. 2013, 2014). Female leopard sharks off the coast of California actively sought out the warmest part of an embayment as temperatures fluctuated throughout the day (Hight and Lowe 2007). The authors estimated that elevated core body temperatures could increase metabolic rates by up to 17 % and augment physiological functions, possibly increasing the rate of embryonic development and decreasing gestation period. By shortening the gestation period, female sharks would have more time to replenish energy reserves following parturition before the onset of winter and the next reproductive cycle (Wallman and Bennett 2006; Jirik and Lowe 2012). Jirik and Lowe (2012) suggested that preferential use of warm, restored estuarine habitat by female round stingrays during gestation may increase the size of offspring at birth, presumably enhancing the survival rates of newborn rays. Alternatively, as females of some shark species are thought to reach sexual maturity at a size greater than their male conspecifics, it has been suggested that aggregations of female sharks in warm waters may increase somatic growth rates, allowing them to reach reproductive maturity more quickly (Economakis and Lobel 1998; Robbins 2007). Whether due to a physiological limitation or as a thermoregulatory strategy in response to physiological preferences, it is clear that temperature is an important driver of movement and space use.
Salinity
Salinity is also well-known to have a strong influence on physiology (Pang et al. 1977; Bernal et al. 2012). Although some species are euryhaline and able to exploit a wide range of salinities (Thorson 1972, 1974; Montoya and Thorson 1982; Hazon et al. 2003), the vast majority of sharks and rays are strictly stenohaline and occupy a narrow salinity range (Froeschke et al. 2010; Martin et al. 2012). Regardless of individual salinity tolerances, however, optimal habitat requirements for sharks and rays must be balanced against the energetic costs of osmoregulation, resulting in species-specific responses to changes in salinity.
Salinity has been reported to influence both distribution (Simpfendorfer et al. 2005; Collins et al. 2008; Ubeda et al. 2009; Knip et al. 2011b; Francis 2013) and local abundance (Hopkins and Cech 2003; Carlisle and Starr 2009; Poulakis et al. 2011) of sharks and rays. For example, juvenile pigeye sharks, Carcharhinus amboinensis, in a tropical nearshore environment shifted their home range areas during extreme wet season flooding events to avoid freshwater inflow and decreased salinity (Knip et al. 2011b). Similarly, cownose rays, Rhinoptera bonasus, monitored in a southwest Florida estuary occurred farther upriver during periods of decreasing flow and increasing salinity (Collins et al. 2008). Given that most sharks and rays are stenohaline, movement in response to salinity change may simply be a means to avoid physiological stress and possible mortality when salinity levels fall outside of individual tolerances. It is important to note that, as a driver of movement, salinity most likely has a greater influence on nearshore species than species that occur further from shore as sharks and rays utilising inshore habitats are more frequently exposed to freshwater runoff and associated salinity fluctuations.
Similar to behavioural thermoregulation, some species have been shown to use movement to actively seek out spatially variable preferred salinity ranges, a type of behavioural osmoregulation thought to confer a biological advantage (Collins et al. 2008; Heupel and Simpfendorfer 2008; Froeschke et al. 2010; Simpfendorfer et al. 2011). Juvenile bull sharks within a Florida estuary selected habitat based on salinity, avoiding areas of low salinity and moving to remain within a preferred salinity range (Simpfendorfer et al. 2005; Heupel and Simpfendorfer 2008). Selection for a preferred salinity range may minimize the energetic costs associated with osmoregulation, energy that presumably could be allocated to growth or other physiological processes (Simpfendorfer et al. 2005; Heupel and Simpfendorfer 2008; Froeschke et al. 2010).
In addition to reducing the energetic costs of osmoregulation, movement to remain within a specific salinity range may also be a means of predator avoidance for some species (Poulakis et al. 2011; Simpfendorfer et al. 2011). Simpfendorfer et al. (2011) found that young smalltooth sawfish, Pristis pectinata, demonstrated an affinity for different salinities than those of most marine predators. Within this estuarine system large bull sharks used salinities ranging from 7 to 20 psu (dimensionless “units” of the Practical Salinity Scale) while juvenile sawfish occupied salinities from 18 to 24 psu. By moving to remain within a different salinity range than that used by bull sharks, young sawfish presumably lowered their risk of predation and increased survival. Whether as a means to reduce the energetic costs associated with osmoregulation, or to avoid predation, it is apparent that salinity plays a role in moderating distribution and movement patterns of some sharks and rays.
Dissolved oxygen
Although comparatively fewer studies have focused on the role of dissolved oxygen in spatial ecology, this abiotic factor has been shown to influence both distribution (Grubbs and Musick 2007; Carlisle and Starr 2009; Espinoza et al. 2011; Knip et al. 2011b; Drymon et al. 2013) and abundance (Parsons and Hoffmayer 2005; Heithaus et al. 2009) of several shark and ray species. Heithaus et al. (2009) found dissolved oxygen concentrations to be the best predictor of bull shark abundance within a Florida estuary. The authors suggested that, over small spatial and temporal scales movement was driven largely by the effort of individuals to remain within optimal dissolved oxygen conditions. Similarly, habitat use and movement of the gray smooth-hound shark, Mustelus californicus, in a newly restored estuary in southern California, indicated individuals avoided the warmest inner basin during the day due to spatial differences in dissolved oxygen levels (Espinoza et al. 2011). These studies indicate that fluctuations in dissolved oxygen levels may be a significant driver of movement for some species. It is important to note, however, that as a driver of movement, dissolved oxygen most likely has a greater influence on those species utilising comparatively lower oxygen habitats.
In contrast to studies documenting movement in response to changes in dissolved oxygen concentrations, several studies have shown that some species display a degree of tolerance to fluctuations in dissolved oxygen levels. Epaulette sharks, Hemiscyllium ocellatum, provide perhaps the best example of hypoxia tolerance in elasmobranchs (Wise et al. 1998; Routley et al. 2002; Nilsson and Renshaw 2004; Speers-Roesch et al. 2012). A study by Wise et al. (1998) found epaulette sharks to be tolerant to both mild hypoxia (20 % of normoxia) and to cyclic exposure to extreme hypoxia (5 % of normoxia). As a resident on shallow reef platforms characterised by large tidal fluctuations, epaulette sharks are exposed to progressively longer and more severe hypoxic conditions as tides become lower, a natural preconditioning regimen that elicits an enhanced physiological response to hypoxia, allowing it to better exploit its niche environment (Routley et al. 2002; Nilsson and Renshaw 2004).
Laboratory studies on the bonnethead shark (Parsons and Carlson 1998; Carlson and Parsons 2001, 2003) and blacknose shark, Carcharhinus acronotus (Carlson and Parsons 2001), determined that these species were able to tolerate at least moderate hypoxic conditions. The authors speculated that behavioural (i.e. increase in swimming activity, mouth gape) and associated physiological (i.e. increase in oxygen uptake) mechanisms employed by these two species may allow them to exploit warm shallow environments (where dissolved oxygen levels can be variable) more effectively than other species (Parsons and Carlson 1998; Carlson and Parsons 2001). Similarly, the observed ability of the scalloped hammerhead shark, Sphyrna lewini (Jorgensen et al. 2009), and cownose ray (Craig et al. 2010) to penetrate hypoxic environments may mean these species have access to prey not accessible to other predators. Therefore, dissolved oxygen levels may play an important role in the spatial ecology of some sharks and rays, with individuals driven by a need to remain within optimal dissolved oxygen conditions or as a means to exploit habitats and/or resources inaccessible to others and hence reduce competition.
Tide
Tidally-influenced movement has been observed for both sharks (Medved and Marshall 1983; Ackerman et al. 2000; Wetherbee and Rechisky 2000; Carlisle and Starr 2010) and rays (Smith and Merriner 1985; Whitty et al. 2009; Campbell et al. 2012). In separate studies examining movement patterns of juvenile sandbar sharks, Carcharhinus plumbeus, off the east coast of the United States, young sharks were observed to move predominantly in the direction of tidal current flow (Medved and Marshall 1983; Wetherbee and Rechisky 2000). Tidally-driven movement patterns are thought to be related to foraging tactics (Smith and Merriner 1985; Ackerman et al. 2000; Campos et al. 2009; Carlisle and Starr 2010), energy conservation strategies (Ackerman et al. 2000; Ortega et al. 2009; Whitty et al. 2009; Campbell et al. 2012), and predator avoidance (Wetherbee et al. 2007; Knip et al. 2011a; Guttridge et al. 2012). For example, species typically found in nearshore waters such as the leopard shark (Ackerman et al. 2000; Carlisle and Starr 2009, 2010), brown smooth-hound shark (Campos et al. 2009) and cownose ray (Smith and Merriner 1985) move into shallow water on incoming tides, presumably to forage. Movement with the tide allows individuals to maximise their foraging area by utilising regions only available at high tide (Smith and Merriner 1985; Gilliam and Sullivan 1993; Ackerman et al. 2000; Carlisle and Starr 2010) as well as providing access to comparatively rich prey resources found only in intertidal areas (Carlisle and Starr 2009).
Movement with the tide may also serve to minimize energy expenditure for some sharks (Ackerman et al. 2000; Ortega et al. 2009; Conrath and Musick 2010) and rays (Whitty et al. 2009; Campbell et al. 2012). Conrath and Musick (2010) found that 53.6 % of the net movements of juvenile sandbar sharks were with the tide. Due to strong tidal currents within the area the authors speculated that it was energetically costly for young sharks to swim against tidal currents. Energy conservation was also suggested to explain why 98 % of young-of-the-year (0+) freshwater sawfish, Pristis microdon, moved in the direction of the tide (Whitty et al. 2009). In addition, Ackerman et al. (2000) estimated that tidally-assisted swimming could potentially conserve up to 6 % of total energy expenditure for leopard sharks, suggesting that energy savings acquired by young sharks and rays through tidally-directed movement may be considerable.
Movement with the tide may also be a means for juvenile sharks and rays to avoid larger predators (Wetherbee et al. 2007; Guttridge et al. 2012). Movement patterns of juvenile lemon sharks, Negaprion brevirostris, on a Brazilian atoll revealed the smallest individuals were most strongly influenced by tides, restricting their movements to the shallowest tide pools at low tide (Wetherbee et al. 2007). Similarly, Knip et al. (2011a) concluded that changes in water depth associated with the tide had the strongest influence on the youngest individuals within a population of pigeye sharks. It is important to note that depth is associated with tide and both authors speculated that, as small individuals are likely to be the most vulnerable to predation, tidally-based movement may be a mechanism to avoid predators by remaining in shallow water. These studies indicate that tide may be an important environmental driver of movement among sharks and rays, as a refuging strategy, a foraging tactic, or as a means to conserve energy.
Photoperiod and light
Few studies have identified photoperiod as a potential driver of movement for sharks and rays (Grubbs et al. 2005; Heupel 2007; Kneebone et al. 2012; Nosal et al. 2014). However, long-term movements of juvenile sandbar sharks indicated that winter migration from a summer nursery area was highly correlated with decreasing day length (Grubbs et al. 2005). As an abiotic driver of movement, photoperiod is perhaps more important for species found in temperate regions that are subject to greater differences in seasonal day length. It is also important to note that photoperiod on a seasonal scale is probably an indicator for correlated temperature changes. For example, Grubbs et al. (2005) speculated that the return of juvenile sandbar sharks to nursery areas in the spring was triggered by both photoperiod and temperature with day length a signal to begin northward migrations and temperature the primary driver stimulating movement into the nursery. Similarly, emigration of juvenile sand tiger sharks, Carcharias taurus, from a Massachusetts estuary was correlated to both day length and water temperature (Kneebone et al. 2012). Although both factors may be influential, the authors speculated that photoperiod was a stronger, more consistent cue driving movement.
In addition to day length, light intensity has been suggested to drive movement for some species (Nelson et al. 1997; Cartamil et al. 2003; Andrews et al. 2009; Whitty et al. 2009). Andrews et al. (2009) suggested that changes in light intensity during crepuscular periods may initiate nocturnal foraging behaviour in sixgill sharks, Hexanchus griseus. Similarly, diel patterns of movement observed in the Hawaiian stingray, Dasyatis lata, were thought to be more influenced by light intensity than temperature or tidal stage (Cartamil et al. 2003). Finally, Nelson et al. (1997) revealed crepuscular vertical migrations of the megamouth shark, Megachasma pelagios, closely tracked specific isolumes. The authors concluded that depth selection was related to light level. As potential drivers of movement, both photoperiod and light intensity have been shown to play a key role in the spatial ecology of several elasmobranch species, but remain relatively understudied to date.
Other factors
Two other abiotic factors have been identified as drivers of movement among sharks and rays, but neither has been examined in detail. The first of these is barometric pressure. Changes in barometric pressure associated with tropical storms can trigger movement in sharks (Heupel et al. 2003; Udyawer et al. 2013). Heupel et al. (2003) found that juvenile blacktip sharks left a nursery area in response to a decrease in barometric pressure associated with a tropical storm. Findings by Udyawer et al. (2013), however, indicate movement in response to extreme storm events may be species-specific. Five species of coastal shark (Carcharhinus limbatus, C. tilstoni, C. melanopterus, C. sorrah, and C. amboinensis) responded differently to changes in barometric pressure before, during and after a severe tropical storm. A short-term flight response was observed in all monitored species except the blacktip reef shark (C. melanopterus) which did not depart or change location. The authors speculated that blacktip reef sharks are perhaps more tolerant to the adverse conditions associated with tropical storms or that the benefits gained by individuals who remain in their preferred habitat outweigh the benefits of departing.
The second rarely examined environmental driver of movement for elasmobranch species is pH (Ortega et al. 2009). Juvenile bull sharks within a Florida river were tracked before and after an influx of freshwater revealing two distinct movement patterns. Movement and location of individuals were either primarily nocturnal and correlated with salinity, temperature and dissolved oxygen, or diurnal in nature and correlated with temperature, dissolved oxygen, turbidity and pH (Ortega et al. 2009). Although under-represented in the literature, changes in barometric pressure and pH may play a role in influencing movement and their role should be explored further.
Complexities associated with determining environmental drivers of movement
Although there are multiple studies linking shark and ray movement with abiotic factors, these studies often present unique problems. For example, links between movement and environment are inherently correlative and do not provide conclusive evidence that abiotic factors and not some other driver (e.g. predator avoidance, prey distribution/availability) are behind such movement. In addition, if abiotic factors are shown to be responsible for movement, it often remains unclear whether species are actively seeking specific conditions or merely reacting to them. Finally, abiotic factors rarely occur in isolation, making it difficult to determine which factor is of highest importance or whether synergistic interactions between different factors are occurring. The influence of other factors confounds interpretation of abiotic cues for movement including biological and physiological processes and geographic variability. Here we discuss some of the complexities associated with determining environmental drivers of movement for elasmobranchs.
Biotic factors
Several biotic factors have been shown to trigger movement and changes in behaviour among sharks and rays. In particular, prey density and availability (Heithaus et al. 2002; Shepard et al. 2006; Torres et al. 2006; Jaine et al. 2012) and predator avoidance (Heupel and Hueter 2002; Collins et al. 2007; Heithaus et al. 2009) are thought to influence movement patterns and habitat choice for many species. Movements of several planktivorous sharks and rays, for example, have been linked to tidally-concentrated plankton aggregations (Sims and Quayle 1998; Shepard et al. 2006; Priede and Miller 2009; Jaine et al. 2012). Similarly, spatial patterns in abundance for the gray smooth-hound shark (Espinoza et al. 2011), tiger shark (Heithaus 2001) and sixgill shark (Andrews et al. 2010) were shown to be influenced by both water temperature and prey availability, most likely due to these species following a seasonal shift in prey resources. As biotic factors may work alongside and/or mask the effects of abiotic factors, it is often a challenge to decipher the exact effects of abiotic factors on movement.
Variation between seasons
Seasonal variability in abiotic factors may complicate resolution of important drivers of movement for sharks and rays. For example, Campbell et al. (2012) observed that while movement of the freshwater whipray, Himantura dalyensis, was dominated by the diel cycle during the wet season, whipray movement patterns during the dry season were related to the tidal/lunar cycle. The authors concluded that the observed shift from tidal/lunar to diel periodicity in movement was related to the seasonal suppression of tidal flow during the wet season. Similarly, seasonal differences in diving patterns were observed for the blue shark where individuals made frequent diurnal excursions to depth resting at the surface between dives during winter, but did not show this pattern in summer (Carey and Scharold 1990). The authors speculated that seasonal changes in the type or availability of prey, or sexual activity associated with the onset of mating season, may be responsible for the observed change in swimming behaviour. Since conditions often vary between seasons, it is important that studies include long-term monitoring of individuals when possible to encompass seasonal differences.
Variation between sexes
Sexual segregation is a common characteristic of shark and ray populations (Klimley 1987; Sims 2005; Robbins 2007; Wearmouth and Sims 2008; Mucientes et al. 2009) so it is perhaps unsurprising that research has also shown variability in response to abiotic factors between sexes. Male Atlantic stingrays, for example, exhibited little change in preferred temperature while females showed thermal preferences based on feeding and reproductive state (Wallman and Bennett 2006). The authors concluded that female selection for a preferred temperature range may be due to higher energetic demands to maintain a larger body size, the reproductive cost of yolking eggs, or to meet nutritional demands of pups during gestation. Sexual segregation was also observed in round stingrays monitored in a restored Californian estuary (Jirik and Lowe 2012). Preferential use of warmer, shallow waters of the restored basin by female stingrays was thought to provide some reproductive benefit. Given that energetic demands vary due to sex-specific costs in reproduction, it may not be uncommon for environmental drivers of movement to differ between sexes, making consideration of sex-based differences important to data interpretation.
Variation between size classes
Ontogenetic shifts in movement, behaviour and habitat use have been widely documented (Gruber et al. 1988; Papastamatiou et al. 2009; Andrews et al. 2010; Heupel et al. 2010) and several studies have shown environmental drivers of movement to vary between size classes (Wetherbee et al. 2007; Heupel and Simpfendorfer 2008; Whitty et al. 2009; Knip et al. 2011a). For example, bull sharks in the Caloosahatchee River, Florida, partitioned habitat among size classes, with the youngest, smallest individuals typically found upriver while older, larger juveniles occurred farther downstream in adjacent embayments (Simpfendorfer et al. 2005; Heupel and Simpfendorfer 2008). As the youngest individuals displayed an affinity for salinities between 7 and 20 psu, and given that the Caloosahatchee River was the only place within the system where salinities <20 psu regularly occurred, the authors speculated that salinity was an important factor in the observed size-based partitioning, possibly as a means to reduce intraspecific predation.
Similarly, studies on movement patterns of juvenile pigeye sharks (Knip et al. 2011a), freshwater sawfish (Whitty et al. 2009) and lemon sharks (Wetherbee et al. 2007) all reported movement by the youngest, smallest individuals into the shallowest habitat with the tides. This behaviour is thought to be a refuging strategy from larger predators. Ontogenetic differences in habitat requirements among sharks and rays may translate into different abiotic drivers of movement between size classes and highlights the need to include a range of age groups within a given sampling pool before population level conclusions are drawn.
Variation between and within geographic locations
To further complicate identification of triggers for movement, environmental drivers may differ between and within regions for a given species. For example, the primary abiotic factor influencing the distribution of bull sharks in the Caloosahatchee River was salinity (Simpfendorfer et al. 2005; Heupel and Simpfendorfer 2008), whereas in the Florida Everglades dissolved oxygen was reported to be the greatest predictor of bull shark abundance (Heithaus et al. 2009). Heithaus et al. (2009) speculated that differences in primary environmental drivers of movement between regions may be due to site-specific differences in the physical structure and hydrological dynamics of the two estuaries. Specifically, the Caloosahatchee River estuary is affected by acute low salinity/high freshwater run-off events while the Everglades estuary is not, resulting in salinity having a lower influence in this region. Similarly, residency and movement patterns of cownose rays in a southwest Florida estuary indicated no relationship between ray activity and tidal stage (Collins et al. 2007), contrasting with previous results from Chesapeake Bay (Smith and Merriner 1985, 1987). Collins et al. (2007) speculated that site-specific differences in foraging profitability may explain the differing drivers of movement observed between these two regions.
Abiotic factors triggering movement and changes in behaviour may also differ over smaller spatial scales. Carlisle and Starr (2010) reported that distribution and movement of leopard sharks within an estuarine system on the coast of California were strongly influenced by the tides, but that the pattern of movement depended on what section of the site sharks were using. In the main channel sharks were observed to move with the tide, maximising their foraging area over a more dispersed prey field, while in the adjacent Elkhorn Slough National Estuarine Research Reserve sharks swam against tidal currents, most likely in an effort to remain close to intertidal mudflats where prey resources were abundant. Similarly, Rechisky and Wetherbee (2003) examined the short-term movements of young sandbar sharks within a nursery ground in Delaware Bay and found movement patterns of sharks to differ between sections of the same bay. On the shallow shelf of western Delaware Bay shark movements were tidally-based while movements on the deeper eastern side of the bay were independent from tidal currents. Studies on spatial ecology of elasmobranchs must consider differences in species response to environmental drivers over both broad and small spatial scales and ensure that all habitat types are represented within a sample to provide sufficient resolution of species behaviour.
The role of environmental change on spatial ecology
A wide range of abiotic factors are expected to fluctuate within the next century as a result of climate change. Current estimates by the Intergovernmental Panel on Climate Change (IPCC) predict a 1–6 °C rise in average sea surface temperature (SST) by 2100 (IPCC 2007). In addition, projected increases in both the frequency and intensity of tropical storms and associated high rainfall events (Emanuel 2005; Webster et al. 2005) will most likely result in acute fluctuations in barometric pressure and salinity levels. Atmospheric carbon dioxide levels are expected to exceed 500 parts per million by the end of this century, dramatically altering the pH of oceans due to ocean acidification (Hoegh-Guldberg et al. 2007). Given that many of the abiotic factors predicted to fluctuate under future climate change scenarios have been shown to trigger movement and changes in behaviour and habitat use of sharks and rays, it is important to consider their responses to future changes in their environment.
A recent integrated risk assessment looking at the vulnerability of sharks and rays on Australia’s Great Barrier Reef (GBR) to climate change found that vulnerability was driven by case-specific interactions of multiple factors (e.g. water temperature, ocean acidification) and species attributes (e.g. habitat specificity, mobility) (Chin et al. 2010). Based on this, the authors concluded that freshwater/estuarine and reef associated sharks and rays are particularly vulnerable to climate change impacts since key habitats for these species are affected by an array of anthropogenic and environmental impacts, thus reducing the overall resilience of these species. Although there is an argument to be made that changing conditions may benefit species by making some habitats available that previously were not, movement to alternative locations may not be possible or desirable for many species. For freshwater/estuarine and reef associated sharks and rays, the risks of moving to find new, suitable habitat (e.g. increased chance of predation, inability to find new suitable habitat) must be weighed against the energetic costs of remaining in an altered environment. Individuals that choose to remain in these habitats may exist in a stressed state, forced to allocate energy to physiological processes such as osmoregulation that could be put towards growth and/or reproduction, resulting in a loss to overall fitness or, at worst, mortality. Furthermore, although laboratory studies have demonstrated that some elasmobranch species are able to acclimate to higher than average temperatures, adaptation to extreme environmental fluctuations remains poorly studied.
Temperature and salinity are the two abiotic factors predicted to have the greatest effects on sharks and rays under current climate change projections (Chin et al. 2010). Given that many species have been shown to behaviourally regulate these two factors, fluctuations in either may cause alteration of movement, changing the way species interact with and utilise habitat, or departure from affected areas should conditions become intolerable. If adverse conditions persist they could induce permanent range contractions or shifts as individuals attempt to locate and/or remain in suitable habitat (Last et al. 2011; Hazen et al. 2013). Range contractions could negatively affect populations by making them more susceptible to localised depletion (i.e. fishing impacts) or mortality due to site-specific degradation and loss of habitat. Range shifts have already been observed for many temperate marine fishes (Holbrook et al. 1997; Perry et al. 2005; Munday et al. 2007) and some sharks (Last et al. 2011; Hazen et al. 2013) in response to higher than average ocean temperatures. Hazen et al. (2012) predicted substantial northward displacement of a range of predators under current climate change scenarios, with an up to 35 % change in core habitat for some species. The authors concluded that the shark guild showed the greatest risk of pelagic habitat loss. Ultimately, selection of preferred environmental conditions via movement may dictate the distribution of not just individuals, but populations and could significantly alter entire ecosystems and their associated marine communities.
Conclusion and future work
This review has shown that many shark and ray species actively select for or exploit specific environmental conditions, often forgoing their home range areas to access a spatially variable resource. Movement to seek out and/or remain within preferred environmental conditions highlights the important role abiotic factors play in the spatial ecology of many marine predators. However, abiotic factors rarely act in isolation and behavioural responses may differ between species, sex, ontogenetic stage, season and geographic location. Movement of sharks and rays is most likely driven by a suite of factors—both abiotic and biotic—with habitat selection by individuals representing a compromise between the need to optimize metabolic/physiological function and maintain access to valuable resources (e.g. food, shelter from predators). Recent studies looking at aggregation behaviour in female leopard sharks, for example, have shown drivers of movement to be complex and influenced by preferred environmental conditions (i.e. low wave intensity, warm water temperatures) as well as proximity to key foraging grounds (Nosal et al. 2013, 2014). Future research should consider both abiotic and biotic factors and their potential roles in shaping movement behaviour.
Resolution of the specific role abiotic factors play in shark and ray movement, behaviour and habitat use may be improved through long-term monitoring studies examining movement at multiple scales and through laboratory research. A long-term acoustic monitoring study on the ray community in Shark Bay, Western Australia, found that previously observed differences in seasonal abundance of rays was most likely due to seasonal changes in habitat use rather than large-scale migrations as was previously thought (Vaudo and Heithaus 2009, 2012). The authors were able to compare movement patterns of tracked individuals to abundance data and speculated that observed decreases in ray density during winter may be due to more time spent in deep water habitats rather than emigration from the bay. Laboratory studies can help clarify response to abiotic factors by separating out and testing individual factors while controlling for others. For example, results from controlled experiments that display species actively seeking out a preferred temperature range (Casterlin and Reynolds 1979; Wallman and Bennett 2006) or improving digestive efficiency through post-feeding thermotaxis (Di Santo and Bennett 2011) serve to provide support for behavioural thermoregulation.
Past studies on elasmobranch response to environmental change have focused primarily on coastal species and are heavily biased to sharks. Reasons for this are multifold, but typically include economic constraints, the highly variable nature of coastal systems and ease-of-access to nearshore shark species. As such, the current body of literature concerning the effects of abiotic factors on movement, behaviour and habitat use of elasmobranchs is not necessarily reflective of all species traits or habitat types. Information on response to abiotic factors for sharks resident on coral reefs, for example, remains relatively unknown despite their identification as some of the species most at risk from climate change effects (Heupel and Simpfendorfer 2014). Future studies examining the role of environmental drivers on elasmobranch spatial ecology should include species from a broad range of habitats to gain a better understanding of the importance of these variables across this diverse family.
References
Ackerman JT, Kondratieff MC, Matern SA, Cech JJJ (2000) Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata, in Tomales Bay, California. Environ Biol Fishes 58(1):33–43
Anderson SD, Goldman KJ (2001) Temperature measurements from salmon sharks, Lamna ditropis, in Alaskan waters. Copeia 3:794–796
Andrews KS, Williams GD, Farrer D, Tolimieri N, Harvey CJ, Bargmann G, Levin PS (2009) Diel activity patterns of sixgill sharks, Hexanchus griseus: the ups and downs of an apex predator. Anim Behav 78:525–536
Andrews KS, Williams GD, Levin PS (2010) Seasonal and ontogenetic changes in movement patterns of sixgill sharks. PLoS One 5(9):e12549
Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci USA 102(15):5443–5447
Baum JK, Worm B (2009) Cascading top–down effects of changing oceanic predator abundances. J Anim Ecol 78(4):699–714
Bernal D, Carlson JK, Goldman KJ, Lowe CG (2012) Energetics, metabolism, and endothermy in sharks and rays. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives, 2nd edn. CRC Press, Boca Raton, pp 211–237
Campbell HA, Hewitt M, Watts ME, Peverell S, Franklin CE (2012) Short- and long-term movement patterns in the freshwater whipray (Himantura dalyensis) determined by the signal processing of passive acoustic telemetry data. Mar Freshw Res 63(4):341–350
Campos BR, Fish MA, Jones G, Riley RW, Allen PJ, Klimley PA, Cech JJ Jr, Kelly JT (2009) Movements of brown smoothhounds, Mustelus henlei, in Tomales Bay, California. Environ Biol Fishes 85(1):3–13
Carey FG, Scharold JV (1990) Movements of blue sharks (Prionace glauca) in depth and course. Mar Biol 106:329–342
Carlisle AB, Starr RM (2009) Habitat use, residency, and seasonal distribution of female leopard sharks Triakis semifasciata in Elkhorn Slough, California. Mar Ecol Prog Ser 380:213–228
Carlisle AB, Starr RM (2010) Tidal movements of female leopard sharks (Triakis semifasciata) in Elkhorn Slough, California. Environ Biol Fishes 89(1):31–45
Carlson JK, Parsons GR (2001) The effects of hypoxia on three sympatric shark species: physiological and behavioral responses. Environ Biol Fishes 61(4):427–433
Carlson JK, Parsons GR (2003) Respiratory and hematological responses of the bonnethead shark, Sphyrna tiburo, to acute changes in dissolved oxygen. J Exp Mar Bio Ecol 294:15–26
Cartamil DP, Vaudo JJ, Lowe CG, Wetherbee BM, Holland KN (2003) Diel movement patterns of the Hawaiian stingray, Dasyatis lata: implications for ecological interactions between sympatric elasmobranch species. Mar Biol 142(5):841–847
Cartamil D, Wegner NC, Aalbers S, Sepulveda CA, Baquero A, Graham JB (2010) Diel movement patterns and habitat preferences of the common thresher shark (Alopias vulpinus) in the Southern California Bight. Mar Freshw Res 61:596–604
Casterlin ME, Reynolds WW (1979) Shark thermoregulation. Comp Biochem Physiol A Physiol 64(3):451–453
Chin A, Kyne PM, Walker TI, McAuley RB (2010) An integrated risk assessment for climate change: analysing the vulnerability of sharks and rays on Australia’s Great Barrier Reef. Glob Chang Biol 16(7):1936–1953
Cohen JE (2003) Human population: the next half century. Science 302(5648):1172–1175
Cohen JE (2005) Human population grows up. Sci Am 293:48–55
Collins AB, Heupel MR, Motta PJ (2007) Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. J Fish Biol 71(4):1159–1178
Collins AB, Heupel MR, Simpfendorfer CA (2008) Spatial distribution and long-term movement patterns of cownose rays Rhinoptera bonasus within an estuarine river. Estuaries Coast 31(6):1174–1183
Conner WH, Day JW, Baumann RH, Randall JM (1989) Influence of hurricanes on coastal ecosystems along the northern Gulf of Mexico. Wetl Ecol Manag 1(1):45–56
Conrath CL, Musick JA (2010) Residency, space use and movement patterns of juvenile sandbar sharks (Carcharhinus plumbeus) within a Virginia summer nursery area. Mar Freshw Res 61:223–235
Craig J, Gillikin P, Magelnicki M, May L (2010) Habitat use of cownose rays (Rhinoptera bonasus) in a highly productive, hypoxic continental shelf ecosystem. Fish Oceanogr 19(4):301–317
Crawshaw LI (1977) Physiological and behavioral reactions of fishes to temperature change. J Fish Board Can 34(5):730–734
Curtis TH, Parkyn DC, Burgess GH (2013) Use of human-altered habitats by bull sharks in a Florida nursery area. Mar Coast Fish 5(1):28–38
Devlin M, Schaffelke B (2009) Spatial extent of riverine flood plumes and exposure of marine ecosystems in the Tully coastal region, Great Barrier Reef. Mar Freshw Res 60(11):1109–1122
Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78:195–207
Dickson KA, Graham JB (2004) Evolution and consequences of endothermy in fishes. Physiol Biochem Zool 77(6):998–1018
Donley JM, Shadwick RE, Sepulveda CA, Syme DA (2007) Thermal dependence of contractile properties of the aerobic locomotor muscle in the leopard shark and shortfin mako shark. J Exp Biol 210(7):1194–1203
Drymon JM, Carassou L, Powers SP, Grace M, Dindo J, Dzwonkowski B (2013) Multiscale analysis of factors that affect the distribution of sharks throughout the northern Gulf of Mexico. Fish Bull 111(4):370–380
Dulvy NK, Metcalfe JD, Glanville J, Pawson MG, Reynolds JD (2000) Fishery stability, local extinctions, and shifts in community structure in skates. Conserv Biol 14(1):283–293
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LN, Fordham SV, Francis MP (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590
Dunbrack R, Zielinski R (2003) Seasonal and diurnal activity of sixgill sharks (Hexanchus griseus) on a shallow water reef in the Strait of Georgia, British Columbia. Can J Zool 81(6):1107–1111
Economakis A, Lobel P (1998) Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fishes 51(2):129–139
Edgar GJ, Barrett NS, Graddon DJ, Last PR (2000) The conservation significance of estuaries: a classification of Tasmanian estuaries using ecological, physical and demographic attributes as a case study. Biol Conserv 92(3):383–397
Emanuel K (2005) Increasing destructiveness of tropical cyclones over the past 30 years. Nature 436(7051):686–688
Espinoza M, Farrugia TJ, Lowe CG (2011) Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary. J Exp Mar Bio Ecol 401:63–74
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50(2):125–146
Fangue NA, Bennett WA (2003) Thermal tolerance responses of laboratory-acclimated and seasonally acclimatized Atlantic stingray, Dasyatis sabina. Copeia 2:315–325
Ferretti F, Myers RA, Serena F, Lotze HK (2008) Loss of large predatory sharks from the Mediterranean Sea. Conserv Biol 22(4):952–964
Francis MP (2013) Temporal and spatial patterns of habitat use by juveniles of a small coastal shark (Mustelus lenticulatus) in an estuarine nursery. PLoS One 8(2):e57021
Froeschke J, Stunz GW, Wildhaber ML (2010) Environmental influences on the occurrence of coastal sharks in estuarine waters. Mar Ecol Prog Ser 407:279–292
Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish physiology: environmental relations and behavior. Academic Press, New York, pp 1–98
Gelsleichter J, Manire CA, Szabo NJ, Cortes E, Carlson J, Lombardi-Carlson L (2005) Organochlorine concentrations in bonnethead sharks (Sphyrna tiburo) from four Florida estuaries. Arch Environ Contam Toxicol 48(4):474–483
Gilliam D, Sullivan KM (1993) Diet and feeding habits of the southern stingray Dasyatis Americana in the central Bahamas. Bull Mar Sci 52(3):1007–1013
Goetze JS, Fullwood LAF (2013) Fiji’s largest marine reserve benefits reef sharks. Coral Reefs 32:121–125
Grubbs RD, Musick J (2007) Spatial delineation of summer nursery areas for juvenile sandbar sharks in Chesapeake Bay, Virginia. In: McCandless CT, Kohler NE, Jr. HLP (eds) Shark nursery grounds of the Gulf of Mexico and east coast waters of the United States, vol 50. Am Fish Soc Symp, Bethesda, MD, pp 87–108
Grubbs RD, Musick JA, Conrath CL, Romine JG (2005) Long-term movements, migration, and temporal delineation of a summer nursery for juvenile sandbar sharks in the Chesapeake Bay region. In: McCandless CT, Kohler NE, Jr. HLP (eds) Shark nursery grounds of the Gulf of Mexico and east coast waters of the United States, vol 50. Am Fish Soc Symp, Bethesda, MD, pp 63–86
Gruber SH, Nelson DR, Morrissey JF (1988) Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bull Mar Sci 43(1):61–76
Guttridge TL, Gruber SH, Franks BR, Kessel ST, Gledhill KS, Uphill J, Krause J, Sims DW (2012) Deep danger: intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Mar Ecol Prog Ser 445:279–291
Hazen EL, Jorgensen S, Rykaczewski RR, Bograd SJ, Foley DG, Jonsen ID, Shaffer SA, Dunne JP, Costa DP, Crowder LB (2013) Predicted habitat shifts of Pacific top predators in a changing climate. Nat Clim Chang 3:234–238
Hazon N, Wells A, Pillans RD, Good JP, Gary Anderson W, Franklin CE (2003) Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity. Comp Biochem Physiol B: Biochem Mol Biol 136(4):685–700
Heithaus MR (2001) The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environ Biol Fishes 61:25–36
Heithaus MR, Dill LM, Marshall GJ, Buhleier B (2002) Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Mar Biol 140:237–248
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23(4):202–210
Heithaus MR, Delius BK, Wirsing AJ, Dunphy-Daly MM (2009) Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnol Oceanogr 54(2):472–482
Heupel MR (2007) Exiting Terra Ceia Bay: examination of cues stimulating migration from a summer nursery area. In: McCandless CT, Kohler NE Jr, HLP (eds) Shark nursery grounds of the Gulf of Mexico and east coast waters of the United States, vol 50. Am Fish Soc Symp, Bethesda, MD, pp 265–280
Heupel MR, Hueter RE (2002) Importance of prey density in relation to the movement patterns of juvenile blacktip sharks (Carcharhinus limbatus) within a coastal nursery area. Mar Freshw Res 53(2):543–550
Heupel MR, Simpfendorfer CA (2008) Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquat Biol 1:277–289
Heupel M, Simpfendorfer C (2014) Importance of environmental and biological drivers in the presence and space use of a reef-associated shark. Mar Ecol Prog Ser 496:47–57
Heupel MR, Simpfendorfer CA, Hueter RE (2003) Running before the storm: blacktip sharks respond to falling barometric pressure associated with Tropical Storm Gabrielle. J Fish Biol 63:1357–1363
Heupel MR, Simpfendorfer CA, Fitzpatrick R (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS One 5(3):5
Hight BV, Lowe CG (2007) Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioral thermoregulation? J Exp Mar Bio Ecol 352(1):114–128
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318(5857):1737–1742
Hoisington G, Lowe CG (2005) Abundance and distribution of the round stingray, Urobatis halleri, near a heated effluent outfall. Mar Environ Res 60(4):437–453
Holbrook SJ, Schmitt RJ, Stephens JS (1997) Changes in an assemblage of temperate reef fishes associated with a climate shift. Ecol Appl 7(4):1299–1310
Hopkins TE, Cech JJ (2003) The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California. Environ Biol Fishes 66(3):279–291
Hutchings P, Haynes D, Goudkamp K, McCook L (2005) Catchment to Reef: water quality issues in the Great Barrier Reef Region—an overview of papers. Mar Pollut Bull 51(1–4):3–8
IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jaine FRA, Couturier LIE, Weeks S, Townsend KA, Bennett MB, Fiora K, Richardson AJ (2012) When giants turn up: sighting trends, environmental influences and habitat use of the manta ray Manta alfredi at a coral reef. PLoS One 7(10):e46170
Jennings DE, Gruber SH, Franks BR, Kessel ST, Robertson AL (2008) Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas. Environ Biol Fish 83(4):369–377
Jirik KE, Lowe CG (2012) An elasmobranch maternity ward: female round stingrays Urobatis halleri use warm, restored estuarine habitat during gestation. J Fish Biol 80(5):1227–1245
Jorgensen SJ, Klimley AP, Muhlia-Melo AF (2009) Scalloped hammerhead shark Sphyrna lewini, utilizes deep-water, hypoxic zone in the Gulf of California. J Fish Biol 74(7):1682–1687
Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fishes 18(1):27–40
Kneebone J, Chisholm J, Skomal GB (2012) Seasonal residency, habitat use, and site fidelity of juvenile sand tiger sharks Carcharias taurus in a Massachusetts estuary. Mar Ecol Prog Ser 471:165–181
Knip DM, Heupel MR, Simpfendorfer CA (2010) Sharks in nearshore environments: models, importance, and consequences. Mar Ecol Prog Ser 402:1–11
Knip DM, Heupel MR, Simpfendorfer CA, Tobin AJ, Moloney J (2011a) Ontogenetic shifts in movement and habitat use of juvenile pigeye sharks Carcharhinus amboinensis in a tropical nearshore region. Mar Ecol Prog Ser 425:233–246
Knip DM, Heupel MR, Simpfendorfer CA, Tobin AJ, Moloney J (2011b) Wet-season effects on the distribution of juvenile pigeye sharks, Carcharhinus amboinensis, in tropical nearshore waters. Mar Freshw Res 62(6):658–667
Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeogr 20(1):58–72
Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312(5781):1806–1809
Mann KH (2000) Ecology of coastal waters: with implications for management, 2nd edn. Blackwell Science, Malden
Martin CS, Vaz S, Ellis JR, Lauria V, Coppin F, Carpentier A (2012) Modelled distributions of ten demersal elasmobranchs of the eastern English Channel in relation to the environment. J Exp Mar Bio Ecol 418:91–103
Matern SA, Cech JJ Jr, Hopkins TE (2000) Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioural thermoregulation? Environ Biol Fishes 58:173–182
Matich P, Heithaus MR (2012) Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas. Mar Ecol Prog Ser 447:165–178
Medved RJ, Marshall JA (1983) Short-term movements of young sandbar sharks, Carcharhinus plumbeus (Pisces, Carcharhinidae). Bull Mar Sci 33(1):87–93
Montoya RV, Thorson TB (1982) The bull shark (Carcharhinus leucas) and largetooth sawfish (Pristis perotteti) in Lake Bayano, a tropical man-made impoundment in Panama. Environ Biol Fishes 7(4):341–347
Mucientes GR, Queiroz N, Sousa LL, Tarroso P, Sims DW (2009) Sexual segregation of pelagic sharks and the potential threat from fisheries. Biol Lett 5(2):156–159
Munday PL, Jones GP, Sheaves M, Williams AJ, Goby G (2007) Vulnerability of fishes on the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds) Climate change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia, pp 357–391
Nelson DR, McKibben JN, Strong WR, Lowe CG, Sisneros JA, Schroeder DM, Lavenberg RJ (1997) An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertical migrator. Environ Biol Fishes 49(4):389–399
Nilsson GE, Renshaw GMC (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207(18):3131–3139
Nosal A, Cartamil D, Long J, Luhrmann M, Wegner N, Graham J (2013) Demography and movement patterns of leopard sharks (Triakis semifasciata) aggregating near the head of a submarine canyon along the open coast of southern California, USA. Environ Biol Fish 96(7):865–878
Nosal A, Caillat A, Kisfaludy E, Royer M, Wegner N (2014) Aggregation behavior and seasonal philopatry in male and female leopard sharks Triakis semifasciata along the open coast of southern California, USA. Mar Ecol Prog Ser 499:157–175
Ortega LA, Heupel MR, Van Beynen P, Motta PJ (2009) Movement patterns and water quality preferences of juvenile bull sharks (Carcharhinus leucas) in a Florida estuary. Environ Biol Fishes 84(4):361–373
Pang PKT, Griffith RW, Atz JW (1977) Osmoregulation in elasmobranchs. Am Zool 17(2):365–377
Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90(4):996–1008
Parsons GR, Carlson JK (1998) Physiological and behavioral responses to hypoxia in the bonnethead shark, Sphyrna tiburo: routine swimming and respiratory regulation. Fish Physiol Biochem 19:189–196
Parsons GR, Hoffmayer ER (2005) Seasonal changes in the distribution and relative abundance of the Atlantic sharpnose shark Rhizoprionodon terraenovae in the North Central Gulf of Mexico. Copeia 4:914–920
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915
Polovina JJ, Abecassis M, Howell EA, Woodworth P (2009) Increases in the relative abundance of mid-trophic level fishes concurrent with declines in apex predators in the subtropical North Pacific, 1996–2006. Fish Bull 107(4):523–531
Poulakis GR, Stevens PW, Timmers AA, Wiley TR, Simpfendorfer CA (2011) Abiotic affinities and spatiotemporal distribution of the endangered smalltooth sawfish, Pristis pectinata, in a south-western Florida nursery. Mar Freshw Res 62(10):1165–1177
Priede IG, Miller PI (2009) A basking shark (Cetorhinus maximus) tracked by satellite together with simultaneous remote sensing II: new analysis reveals orientation to a thermal front. Fish Res 95(2–3):370–372
Rahmstorf S (2007) A semi-empirical approach to projecting future sea-level rise. Science 315(5810):368–370
Rechisky EL, Wetherbee BM (2003) Short-term movements of juvenile and neonate sandbar sharks, Carcharhinus plumbeus, on their nursery grounds in Delaware Bay. Environ Biol Fishes 68(2):113–128
Robbins RL (2007) Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia. J Fish Biol 70(5):1350–1364
Routley MH, Nilsson GE, Renshaw GMC (2002) Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comp Biochem Physiol A: Mol Integr Physiol 131(2):313–321
Schaffelke B, Mellors J, Duke NC (2005) Water quality in the Great Barrier Reef region: responses of mangrove, seagrass and macroalgal communities. Mar Pollut Bull 51(1–4):279–296
Shepard ELC, Ahmed MZ, Southall EJ, Witt MJ, Metcalfe JD, Sims DW (2006) Diel and tidal rhythms in diving behaviour of pelagic sharks identified by signal processing of archival tagging data. Mar Ecol Prog Ser 328:205–213
Shepherd TD, Myers RA (2005) Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico. Ecol Lett 8(10):1095–1104
Simpfendorfer CA, Freitas GG, Wiley TR, Heupel MR (2005) Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28(1):78–85
Simpfendorfer CA, Yeiser BG, Wiley TR, Poulakis GR, Stevens PW, Heupel MR (2011) Environmental influences on the spatial ecology of juvenile smalltooth sawfish (Pristis pectinata): results from acoustic monitoring. PLoS One 6(2):1–12
Sims DW (2005) Differences in habitat selection and reproductive strategies of male and female sharks. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, New York, pp 127–147
Sims DW, Quayle VA (1998) Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature 393(6684):460–464
Sims DW, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, Hutchinson N, Budd GC, Righton D, Metcalfe J, Nash JP, Morritt D (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. J Anim Ecol 75(1):176–190
Smith JW, Merriner JV (1985) Food habits and feeding behavior of the cownose ray, Rhinoptera bonasus, in lower Chesapeake Bay. Estuaries 8(3):305–310
Smith JW, Merriner JV (1987) Age and growth, movements and distribution of the cownose ray, Rhinoptera bonasus, Chesapeake Bay. Estuaries 10(2):153–164
Snelson FF, Bradley WK (1978) Mortality of fishes due to cold on the east coast of Florida, January. Fla Sci 41(1):1–12
Speed CW, Meekan MG, Field IC, McMahon CR, Bradshaw CJA (2012) Heat-seeking sharks: support for behavioural thermoregulation in reef sharks. Mar Ecol Prog Ser 463:231–244
Speers-Roesch B, Brauner CJ, Farrell AP, Hickey AJ, Renshaw GM, Wang YS, Richards JG (2012) Hypoxia tolerance in elasmobranchs. II. Cardiovascular function and tissue metabolic responses during progressive and relative hypoxia exposures. J Exp Biol 215(1):103–114
Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57(3):476–494
Thorson TB (1972) The status of the bull shark, Carcharhinus leucas, in the Amazon River. Copeia 3:601–605
Thorson TB (1974) Occurence of the sawfish, Pristis perotteti, in the Amazon River, with notes on P. pectinatus. Copeia 2:560–564
Thums M, Meekan M, Stevens J, Wilson S, Polovina J (2013) Evidence for behavioural thermoregulation by the world’s largest fish. J R Soc Interface 10(78):20120477
Torres LG, Heithaus MR, Delius B (2006) Influence of teleost abundance on the distribution and abundance of sharks in Florida Bay, USA. Hydrobiologia 569(1):449–455
Ubeda AJ, Simpfendorfer CA, Heupel MR (2009) Movements of bonnetheads, Sphyrna tiburo, as a response to salinity change in a Florida estuary. Environ Biol Fishes 84:293–303
Udyawer V, Chin A, Knip D, Simpfendorfer CA, Heupel MR (2013) Variable response of coastal sharks to severe tropical storms: environmental cues and changes in space use. Mar Ecol Prog Ser 480:171–183
Vaudo JJ, Heithaus MR (2009) Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia. Mar Biol 156(12):2579–2590
Vaudo JJ, Heithaus MR (2012) Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system. Mar Freshw Res 63:1077–1084
Wallman HL, Bennett WA (2006) Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina (Lesueur). Environ Biol Fishes 75:259–267
Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. In: Sims DW (ed) Advances in marine biology, vol 54. Elsevier Academic Press, San Diego, pp 107–170
Webster PJ, Holland GJ, Curry JA, Chang HR (2005) Changes in tropical cyclone number, duration, and intensity in a warming environment. Science 309(5742):1844–1846
Werry JM, Lee SY, Lemckert CJ, Otway NM (2012) Natural or artificial? Habitat-use by the bull shark, Carcharhinus leucas. Plos One 7(11):e49796
Wetherbee BM, Rechisky EL (2000) Movement patterns of juvenile sandbar sharks on their nursery grounds in Delaware Bay. In: Eiler JH, Alcorn DJ, Neuman MR (eds) Biotelemetry 15: proceedings of the 15th international symposium on biotelemetry. International Society on Biotelemetry, Wagenigen, pp 91–98
Wetherbee BM, Gruber SH, Rosa RS (2007) Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes. Mar Ecol Prog Ser 343:283–293
Whitty JM, Morgan DL, Peverell SC, Thorburn DC, Beatty SJ (2009) Ontogenetic depth partitioning by juvenile freshwater sawfish (Pristis microdon: Pristidae) in a riverine environment. Mar Freshw Res 60(4):306–316
Wise G, Mulvey JM, Renshaw GMC (1998) Hypoxia tolerance in the epaulette shark (Hemiscyllium ocellatum). J Exp Zool 281(1):1–5
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schlaff, A.M., Heupel, M.R. & Simpfendorfer, C.A. Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review. Rev Fish Biol Fisheries 24, 1089–1103 (2014). https://doi.org/10.1007/s11160-014-9364-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-014-9364-8