Multiple Measures of Thermal Performance of Early Stage Eastern Rock Lobster in a Fast-Warming Ocean Region

Vol. 624: 1–11, 2019 MARINE ECOLOGY PROGRESS SERIES Published August 15 https://doi.org/10.3354/meps13054 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Multiple measures of thermal performance of early stage eastern rock lobster in a fast-warming ocean region Samantha Twiname1,*, Quinn P. Fitzgibbon1, Alistair J. Hobday2, Chris G. Carter1, Gretta T. Pecl1 1Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart, TAS 7001, Australia 2CSIRO Oceans and Atmosphere, Castray Esplanade, Hobart, TAS 7001, Australia ABSTRACT: To date, many studies trying to understand species’ climate-driven changes in distribution, or ‘range shifts’, have each focused on a single potential mechanism. While a single performance measure may give some insight, it may not be enough to ac - curately predict outcomes. Here, we used multiple measures of performance to explore potential mechanisms behind species range shifts. We examined the thermal pattern for multiple measures of performance, including measures of aerobic metabolism and multiple as pects of escape speed, using the final larval stage (puerulus) of eastern rock lobster Sagmariasus verreauxi as a model species. We found that aerobic scope and escape speed had different thermal per- Single thermal performance measures for eastern rock lob- formances and optimal temperatures. The optimal ster Sagmariasus verreauxi may not accurately predict whole temperature for aerobic scope was 27.5°C, while the animal performance under future ocean warming. pseudo-optimal temperature for maximum escape Photo: Peter Mathew speed was 23.2°C. This discrepancy in thermal performance indicators illustrates that one measure of performance may not be sufficient to accurately pre- 1. INTRODUCTION dict whole-animal performance under future warming. Using multiple measures of performance and ap - propriate modelling techniques may lead to a more Ocean warming is affecting marine species world- accurate prediction of future range shifts, in cluding wide (Pecl et al. 2017). One of the most prevalent the timing and extent of climate-driven species effects are changes to species’ geographical distribu- redistribution. tions (Sunday et al. 2012, Poloczanska et al. 2013). While these ‘range shifts’ occur in many marine sys- KEY WORDS: Aerobic scope · Climate change · tems, we do not yet have a clear understanding of the Crustacean larvae · Escape speed · Puerulus · Respi- mechanisms driving the high variation in rate and ratory metabolism · Sagmariasus verreauxi magnitude of the changes within (Last et al. 2011, Sunday et al. 2015) and between regions (Poloczan- © The authors 2019. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 624: 1–11, 2019 ska et al. 2013). Part of the explanation may lie in the thermal preference or performance in juvenile barra- complex physiology of marine species and how each mundi (Norin et al. 2014). aspect of their physiology reacts to changes in their To gain a more robust understanding of the effects thermal environments. of climate change on marine communities, we need to Many marine species are ectothermic, meaning incorporate measures of species’ interactions, such as that their internal physiology is highly dependent on competition or predation performance, along with ambient temperature which, in turn, strongly in - this individual physiological performance data (Evans fluences a species’ function and behaviour (Pörtner & et al. 2015). Another potential constraint, or conversely, Knust 2007, Pörtner & Farrell 2008, Doney et al. 2012). facilitator, to species’ range change under ocean warm- To understand the effect of temperature on many ing are inter-specific interactions. Changes to a spe- physiological and biological processes, thermal per- cies’ individual physiology under climate change are formance curves can be constructed. Thermal per- also likely to influence its interactions with other spe- formance curves allow visualisation of the effects of cies, by modifying or eliminating current interactions temperature on bodily rates such as meta bolism, or creating new ones (Pitt et al. 2010, Kordas et al. growth and reproduction (Eme & Bennett 2009, Dell 2011, Pinsky et al. 2013). For example, predation plays et al. 2014, Donelson et al. 2014). With in creasing a critical role in the structuring and functioning of ocean temperatures, bodily rates are likely to change marine communities, as predator−prey interactions due to heightened metabolic performance, with con- provide a link for transfer of energy, nutrients and sequent effects on species performance and behav- materials from basal species to apex predators (Paine iour. While single thermal performance curves may 1974, Dell et al. 2014). Predator−prey interactions are provide some insight to how a particular body function affected by temperature through effects on active may change under ocean warming, it may be of lim- body velocity in ectotherms (Grigaltchik et al. 2012, ited use as a predictor of whole-animal performance. Dell et al. 2014). As attack and escape performance Aerobic scope, a proxy for the amount of energy are key factors in the outcome of predator−prey inter- available for non-essential body processes, is a key actions, the effect of ocean warming on ectotherm mo- component of organismal energy budgets and is bility and locomotion may have far-reaching effects dependent on ambient temperature experienced by on marine community structure (Cairns et al. 2008, ecto therms (Watson et al. 2014). The oxygen and Dell et al. 2014, Öhlund et al. 2015). capacity-limited thermal tolerance hypothesis pro- The south east coast of Australia has been identified poses that there is a limited thermal range for in- as an ocean warming hotspot, where rates of warming dividual ectotherm species in which performance, are up to 4 times the global average (Hobday & Pecl measured as aerobic scope, is maximised (Pörtner & 2014, Pecl et al. 2014). In recent years, Australia has Knust 2007). This optimisation, and subsequent de - seen many changes in the distribution and abundance cline in performance at temperatures outside of this of local species as well as new species not previously optimal range, is hypothesised to be due to the mis- recorded in the region, from pelagic fish to sedentary match between oxygen demand and supply (Pörtner invertebrates (Pitt et al. 2010, Last et al. 2011, Robin- & Knust 2007). This measure of organismal perform- son et al. 2015). One such species suspected of under- ance has been proposed as a way to predict future going a range shift into the area is the eastern rock changes in population characteristics under climate lobster S. verreauxi (H. Milne Edwards, 1851), a large change (Pörtner & Farrell 2008). While aerobic scope species of spiny lobster found along the east coast of is a valuable measure of performance, there has been Australia between southern Queensland and northern an increase in the number of studies that suggest that Tasmania, as well as New Zealand. There is evidence aerobic scope is an incomplete measure of whole- that S. verreauxi is becoming more common further organism performance (Norin et al. 2014, Fitzgibbon south along the Tasmanian east coast (Robinson et al. et al. 2017, Jutfelt et al. 2018). Different organismal 2015), although isolated individuals have been re- processes have different responses to increases in ported over many decades. This potential range shift ambient temperatures, such as the difference between has implications for both fisheries and ecological growth rate optimums and aerobic scope in juvenile management. While not currently a targeted fisheries eastern rock lobster Sagmariasus verreauxi (Fitzgib- species in Tasmania due to low abundance, continued bon et al. 2017) and different thermal optima for ocean warming and in creased S. verreauxi recruit- feeding and growth performance in juvenile barra- ment may facilitate a new lobster fishery or compete mundi Lates calcarifer (Katersky & Carter 2007). with the more valuable existing southern rock lobster Moreover, aerobic scope is not useful for predicting Jasus edwardsii fishery in the region. Twiname et al.: Thermal performance of early stage lobster 3 Spiny lobsters have among the longest and most from phyllosoma to puerulus stage larvae, animals complex larval life cycles of any marine invertebrate, were transferred to individual cylindrical vessels lasting for up to 2 yr in some species, with this stage (300 ml) suspended in a 68 l polypropylene sump. being important for dispersal and possible range Each sump held 9 vessels, each with a single pueru- extension (Phillips et al. 2006). These early life stages lus within, with each temperature treatment con- may also be more susceptible to effects of climate ducted in separate sumps. Each vessel had a 5 mm change and ocean warming than their juvenile and oyster mesh shelter for the pueruli, a mesh bottom adult counterparts (Pörtner & Farrell 2008, Storch et and received water circulated from the sump. The al. 2011, Fitzgibbon et al. 2014b). The puerulus stage sumps were supplied with flow-through filtered sea- of the spiny lobster life cycle is a critical transitional water from a larger temperature-controlled sump at a stage from pelagic larvae to recruitment into the rate of 50 l h−1 (0.74 exchanges h−1). An air stone was juvenile population. It is a nektonic, non-feeding used to increase mixing and aeration within each stage that actively swims to settle onto suitable habi- sump, which was maintained above 100% dissolved tat substrate in coastal regions (Fitzgibbon et al. oxygen saturation. Upon placement of pueruli into 2014a). Like many larvae settling into new communi- this holding system, they were held for a period of ties, puerulus must survive the ‘wall of mouths’ in 7−9 d at 21°C before any experimental treatments their new environment (Emery 1973, Hamner et al. were applied.

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