Physiological mechanisms linking cold acclimation and the poleward distribution limit of a range-extending marine fish

Abstract

Extensions of species’ geographical distributions, or range extensions, are among the primary ecological responses to climate change in the oceans. Considerable variation across the rates at which species’ ranges change with temperature hinders our ability to forecast range extensions based on climate data alone. To better manage the consequences of ongoing and future range extensions for global marine biodiversity, more information is needed on the biological mechanisms that link temperatures to range limits. This is especially important at understudied, low relative temperatures relevant to poleward range extensions, which appear to outpace warm range edge contractions four times over. Here, we capitalized on the ongoing range extension of a teleost predator, the Australasian snapper Chrysophrys auratus, to examine multiple measures of ecologically relevant physiological performance at the population’s poleward range extension front. Swim tunnel respirometry was used to determine how mid-range and poleward range edge winter acclimation temperatures affect metabolic rate, aerobic scope, swimming performance and efficiency and recovery from exercise. Relative to ‘optimal’ mid-range temperature acclimation, subsequent range edge minimum temperature acclimation resulted in absolute aerobic scope decreasing while factorial aerobic scope increased; efficiency of swimming increased while maximum sustainable swimming speed decreased; and recovery from exercise required a longer duration despite lower oxygen payback. Cold-acclimated swimming faster than 0.9 body lengths sec−1 required a greater proportion of aerobic scope despite decreased cost of transport. Reduced aerobic scope did not account for declines in recovery and lower maximum sustainable swimming speed. These results suggest that while performances decline at range edge minimum temperatures, cold-acclimated snapper are optimized for energy savings and range edge limitation may arise from suboptimal temperature exposure throughout the year rather than acute minimum temperature exposure. We propose incorporating performance data with in situ behaviour and environmental data in bioenergetic models to better understand how thermal tolerance determines range limits.

A cross‐scale framework to support a mechanistic understanding and modelling of marine climate‐driven species redistribution, from individuals to communities

“…Evans et al (2016) provides potential solutions to some of the barriers of using mechanistic models, including data availability. Perhaps we should not only design research tools or develop models based on data we already have (although this is inevitably needed), but instead identify the knowledge and data needed to understand processes that influence species range shifts (Evans et al 2013, Wolfe et al 2020. The models that could be developed from such an approach could then advise the collection of new data critical to continuing the improvement of understanding of the drivers behind species range shifts.…”

Contrasting patterns in the occurrence and biomass centers of gravity among fish and macroinvertebrates in a continental shelf ecosystem

“…Yet where species have some likelihood of occurring may not define where their most active centers of recruitment are located or where growth may be maximized (Galaiduk et al, 2017; Majoris et al, 2018). The poleward movement of species has generally been described as a thermal accommodation, and with warming conditions, generally more habitat within the thermal constraints of a species becomes available (Wolfe et al., 2020). However, other factors defining habitat may change with these warming trends and fail to provide food resources or competitive advantage for a particular species (Sánchez‐Hernández & Amundsen, 2018).…”

Effects of temperature on physiological performance and behavioral thermoregulation in an invasive fish, the round goby

“…Aerobic scope was, however, still diminished at temperatures at and below 10°C in the present study, indicating that these temperatures were unfavorable for the aerobic performance of round goby. This may restrict distribution at colder temperatures (Wolfe et al, 2020) and, in turn, limit secondary range-expansion into colder parts of newly invaded…”

“…Aerobic scope was, however, still diminished at temperatures at and below 10°C in the present study, indicating that these temperatures were unfavorable for the aerobic performance of round goby. This may restrict distribution at colder temperatures ( Wolfe et al, 2020 ) and, in turn, limit secondary range expansion into colder parts of newly invaded areas. Outside its native range, the round goby has presumably reached its northernmost boundary in the Great Lakes ( Kornis et al, 2012 ) and, similarly, has not established in the most north-eastern and coldest areas of the Baltic Sea ( Puntila et al, 2018 ).…”