Range-extending coral reef fishes trade-off growth for maintenance of body condition in cooler waters
Graphical abstract
Introduction
Anthropogenic climate change is forcing species to either locally adapt or relocate to more suitable habitats. This relocation can be a change in altitude (Dirnbӧck et al., 2011), a change in water depth (Perry et al., 2005), or a change in latitude (Booth et al., 2011, Feary et al., 2014). In the case of marine species, water temperature increases due to ocean warming may exceed their optimal thermal ranges (Burrows et al., 2011, Doney et al., 2012), forcing them to move to environments with more appropriate water temperatures. These range shifts involve a ‘leading’, or expanding edge, which is usually the coolest area of a species’ range, and/or a ‘trailing’, or contracting edge, which is generally the warmest area (Donelson et al., 2019). Currently, 75% of marine range expansions occur in a poleward direction, towards cooler waters at higher latitudes (Sorte et al., 2010). Often these range extensions are facilitated by the strengthening of ocean currents such as the East Australian Current (Booth et al., 2007) and can be altered by changes in freshwater flow related to rainfall and droughts (Booth et al., 2011, Johnson et al., 2011). The range extension of tropical fish into temperate communities is known as tropicalization, a phenomenon being observed increasingly around the world, including in Japan (Nakamura et al., 2013), Mexico (Heck et al., 2015), and Australia (Vergés et al., 2014).
Transition areas, or the regions where the leading edge of tropical range-extending species overlaps with existing temperate communities, are often more biodiverse as they are composed of complex species assemblages from different origins that are adapted to a variety of habitats (Horta e Costa et al., 2014). Within these temperate transition zones, species distributions are mainly determined by water temperature. Presently, more warm-water species are advancing into cool waters as opposed to cold-water species retreating from warm waters (Hawkins et al., 2009). As tropical fish extend their ranges into temperate ecosystems, novel species assemblages and changes in trophic food webs may arise in these transition zones (Perry et al., 2005). Consequences of such range extensions include food scarcity (Ramos et al., 2014), interactions with novel predators (Siepielski and Beaulieu, 2017), effects on extant species (Vergés et al., 2016), and competition for resources (Comte et al., 2017). Consequences could also be physiological in nature, such as changes in feeding performance and growth (Amara et al., 2007, Bolger and Connolly, 1989). Several in situ proxies exist to test how range-extending species adjust to suboptimal conditions in their new ranges. For example, bite rate is indicative of food intake. Similarly, activity levels are indicative of energy expenditure. Somatic growth rate gives a quantitative value of how much of any excess energy (i.e. not needed for basic maintenance) has been allocated to growth. Body condition (i.e. energy reserves) can be correlated to individual fitness (Irons et al., 2007) and survival of an organism (Bolger and Connolly, 1989, Lambert and Dutil, 1997, Schulte-Hostedde et al., 2001). Survival, growth, and reproduction are usually higher in fish with better condition (Brosset et al., 2016, Lloret et al., 2014, Millar and Hickling, 1990), linking body condition with future population success (Jakob et al., 1996, Van Beveren et al., 2014).
Temperature plays a crucial role in the physiology and therefore ecological success of range-extending species (Angilletta et al., 2002, Pörtner and Farrell, 2008). At the trailing edges of temperate species ranges, increasing water temperatures have been shown to increase the growth rate of marine ectotherms, until maximum thermal tolerances are reached (Pörtner, 2002). In contrast, at the leading edges of range extensions, low temperatures have been shown to decrease the growth rate of tropical fishes by decreasing metabolism (Enders et al., 2006, Green and Fisher, 2004, Pörtner et al., 2001) which can lead to decreased swimming ability and activity levels due to energy redistribution to other, more critical physiological processes (Batty and Blaxter, 1992, Lyon et al., 2008). Energy allocation theories, such as the Dynamic Energy Budget (DEB), state that energy is stored in reserves and then divided among physiological processes, such as basic maintenance (body condition), development, reproduction, and growth (Lika and Kooijman, 2003, Monaco et al., 2014), with maintenance taking precedence (Heino & Kaitala, 1999, Jokela and Mutikainen, 1995, Kooijman, 2001). In situations where organisms are unable to maximise all of their life-history traits simultaneously, trade-offs may occur among physiological processes (Brosset et al., 2016, Stearns, 1992), especially in environments with limited resources (Stearns, 1989).
Here we test how invading tropical and native temperate fish species perform physiologically in co-inhabited shallow-water assemblages along their Australian leading and trailing edges, respectively. The southeast coast of Australia is a ‘hotspot’ for ocean warming, with water temperatures increasing at a rate more than triple the global average (Hobday and Pecl, 2014, Ridgway, 2007). Our study was performed along 730 km or 6° latitude of coastline, providing a natural temperature gradient for testing the performance of tropical and temperate species. We hypothesize that tropical species may trade-off growth rate for maintenance and exhibit decreased growth rate along their leading edge in cool, higher-latitude communities while temperate species increase growth rate along their trailing edge in warm, lower-latitude communities. We show that tropical fishes make this growth–maintenance trade-off in favour of body condition maintenance in cool waters, resulting in decreased growth rates in temperate ecosystems.
Section snippets
Fish collection
To assess how latitude-associated temperature differences affect fish performance, three distinct regions were studied, with both tropical and temperate fishes sampled from two sub-tropical (North and Middle) and one temperate (South) region. Regions were grouped according to mean sea surface winter temperatures (Table S1) and flow regime of the East Australian Current, both of which affect local recruitment of tropical fishes (NOAA, 2019). Fishes were collected along the southeast coast of
Body condition
Temperate species showed no difference in the three proxies of their body condition as a function of latitude (i.e. water temperature) (two-way ANOVAs: Fulton’s condition index p = 0.504; tissue protein content p = 0.057), with the exception of tissue C:N ratio in one species (region × species interaction p = 0.004), which was higher in the Middle compared to the South for A. strigatus (Fig. 2, Fig. S1, Tables S3a, S4a). Likewise, tropical species showed no differences in any condition proxy as
Growth–maintenance trade-off in tropical species
We show that tropical fishes that are invading temperate ecosystems face a trade-off between maintenance of body condition and growth (Table S5). As these fishes extend their ranges into higher latitudes, the cooler waters typically decrease their metabolism (Enders et al., 2006). We found that this was associated with lower activity levels, including reduced bite rates, which would lead to decreased food intake and consequently reduced energy allocation to hierarchically less-important
Conclusions
In summary, tropical fishes maintained their body condition in temperate environments despite declines in activity and feeding performance due to cooler waters. These fishes appear to face a trade-off between growth rate and body condition, favouring condition due to its hierarchical importance for fitness. Temperate fishes predominantly did not exhibit differences in body condition and showed similar performance across latitudes. With seawater temperatures set to further increase under climate
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Funding for this project was provided by an Australian Research Council Discovery Project (DP170101722) awarded to IN, BMG, and DJB, a grant from the Environment Institute (The University of Adelaide) awarded to IN, a LIEF grant (LE120100054) awarded to BMG, and a Beacon of Enlightenment Scholarship awarded to KMK by The University of Adelaide. All animal research complied with The University of Adelaide’s Animal Ethics guidelines (approval S-2017-002) as well as the University of Technology
References (84)
- et al.
The evolution of thermal physiology in ectotherms
J. Therm. Biol
(2002) - et al.
Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current
Estuarine Coastal Shelf Sci.
(2007) - et al.
Growth-temperature relation for young-of-the-year ruffe
J. Great Lakes Res.
(1993) - et al.
Low temperature as a limiting factor for introduction and distribution of Indo-Pacific damselfishes in the eastern United States
J. Therm. Biol
(2008) - et al.
Temperature influences swimming speed, growth and larval duration in coral reef fish larvae
J. Exp. Mar. Biol. Ecol.
(2004) - et al.
Climate change cascades: shifts in oceanography, species' ranges and subtidal marine community dynamics in eastern Tasmania
J. Exp. Mar. Biol. Ecol.
(2011) - et al.
Life history implications of allocation to growth versus reproduction in dynamic energy budgets
(2003) - et al.
Towards a dynamically balanced eddy-resolving ocean reanalysis: BRAN3
Ocean Model.
(2013) - et al.
The effects of temperature on metabolic interaction between digestion and locomotion in juveniles of three cyprinid fish (Carassius auratus, Cyprinus carpio and Spinibarbus sinensis)
Comp. Biochem. Physiol. A: Mol. Integr. Physiol.
(2011) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals
Comp. Biochem. Physiol. A: Mol. Integr. Physiol.
(2002)