Introduction
Ocean temperatures in the Northwest Atlantic have increased at a rate of 0.03 °C year
−1 over the past four decades and are warming faster than the global average of 0.01 °C year
−1 (
Wu et al. 2012;
Forsyth et al. 2015;
Pershing et al. 2015). Ocean temperatures in Canada are projected to continue increasing over the 21st century, and the waters around Nova Scotia are predicted to warm faster than the rest of the country under all emissions scenarios (
Greenan et al. 2018;
Lavoie et al. 2020). Warm water bottom temperature anomalies have also increased in offshore waters around Nova Scotia since the 1980s due, in part, to the influence of the Gulf Stream relative to the Labrador current (
Fisheries and Oceans Canada 2019).
The American lobster (
Homarus americanus H. Milne-Edwards, 1837) fishery is the most profitable commercial fishery in Atlantic Canada, valued at approximately $2 billion in 2021 (
Fisheries and Oceans Canada 2022) and takes place in warming nearshore and offshore areas. There are 41 discrete lobster fishing areas (LFAs) (
Lobster Council of Canada 2020) that are further sub-divided into a total of 47 unique zones (
Government of Canada 1985;
Serdynska and Coffen-Smout 2017). Within LFAs, lobster inhabit waters with a wide range of seasonal temperatures, from −1 to 26 °C (
Lawton and Lavalli 1995;
Quinn 2017); however, laboratory studies indicate a preferred temperature range between 12 and 18 °C for adults (
Crossin et al. 1998). Within this temperature range, lobster larvae display greater survival and faster growth (
MacKenzie 1988;
Annis et al. 2013;
Quinn 2017), whereas temperatures above 20 °C have been linked to higher physiological stress, disease, and mortality in both adults and larvae (
Pearce and Balcom 2005;
Glenn and Pugh 2006). Increases in temperature also correspond to an increase in metabolism for all poikilotherms, including lobster (
Jury and Watson 2000).
Early work tested the thermal limits of American lobster collected in the nearshore waters of eastern New Brunswick in the Gulf of St. Lawrence, Prince Edward Island, southwestern Nova Scotia, and Cape Breton Island (
McLeese 1956).
McLeese (1956) found that the upper thermal limit for American lobster could be increased by approximately 2.7 °C following a 3-week acclimation period at 5 °C versus 15 °C. This work was foundational in establishing a relationship between acclimation temperature and thermal tolerance in American lobster, but used a simple method to determine when lobsters were “dead”.
McLeese (1956) considered American lobster to be “dead” when they could detect no movement from any part on close examination. In more recent years with newer technology,
Camacho et al. (2006) demonstrated that temperature acclimation altered cardiac performance and critical thermal maximum in American lobster using an impedance converter connected to wires drilled through the carapace connected to the heart. Their findings supported earlier work of
McLeese (1956), and
Camacho et al. (2006) suggested that cold-acclimated lobster have a significant physiological advantage since they have a larger capacity for extending their upper thermal limit than warm-acclimated lobster and are living in conditions far below this limit.
In lobster, a beating heart is required to circulate haemolymph and deliver oxygen to the body. In vivo experimentation has demonstrated that lobster heartbeats can be detected using an impedance converter connected to wires inserted into the lobster carapaces (
Worden et al. 2006). For this invasive in vivo experiment, lobster had to be isolated and maintained for at least 48 h with the impedance converter prior to experimentation, to reduce the stress of the insertion of the wires through the carapace and into the heart (
Worden et al. 2006). Conversely, photoplethysmography (PPG) is a non-invasive technique that uses infrared (IR) light to measure changes in blood volume in real time (
Challoner and Ramsay 1974). This technique was originally developed to monitor the heart rates of children under anaesthesia and has also been tested in the Green crab (
Carcinus maenas) (
Depledge 1984). A variety of PPG devices have been used to infer heartbeats in other decapod crustaceans such as spiny lobsters (
Jasus edwardsii, Sagmariasus verreauxi, and
Panulirus ornatus) (
Oellermann et al. 2020), giant freshwater shrimp (
Macrobrachium rosenbergii) (
Ern et al. 2014), crayfish (
Astacus astacus) (
Fedotov et al. 2000), brown crabs (
Cancer pagurus) (
Maus et al. 2021), and Jonah crabs (
Cancer borealis) (
Kushinsky et al. 2019) in laboratory settings and in American lobster (
H. americanus) in the wild (
Gutzler and Watson 2022). The capacity to detect lobster heartbeats in vivo with non-invasive technology presents an exciting opportunity to investigate the effects of thermal acclimation on critical thermal maxima in real time.
While the work of
McLeese (1956) and
Camacho et al. (2006) were critical in establishing the relationship between thermal acclimation and thermal limits, they did not adequately address the potential effects of geographically separated lobster populations on thermal maxima. These populations may be adapted to local or regional temperatures (
Benestan et al. 2016) and consequently, have different thermal maxima. The present study used PPG to identify periods of thermal stress in real time as indicated by irregular cardiac activity to explore differences in euthanasia temperature between geographically separated American lobster populations from LFAs around Nova Scotia, Canada acclimated to either warm (15 °C) or cold (5 °C) water.
Discussion
The present study explored the relationship between acclimation temperature and LFA origin on euthanasia temperature for American lobsters harvested in the Canadian Maritimes. In agreement with previous studies (
McLeese 1956;
Camacho et al. 2006), the present paper demonstrated that lobster acclimated to warmer temperatures (15 °C) have a significantly higher thermal maximum (29.6 °C ± 0.11 (mean ± SE)) than lobsters acclimated to colder temperatures (5 °C; 25.7 °C ± 0.14 (mean ± SE)), regardless of the LFA of origin. All six LFAs used in the present study have significantly different mean annual bottom temperatures that do not directly correspond to increasing latitude (
Wang et al. 2018).
McLeese (1956) identified differences in life history strategies for lobster in the Gulf of St. Lawrence and southwestern New Brunswick that they attributed to differences in oceanographic conditions between those regions, yet, found no differences in thermal maxima between lobster from those regions. The present study corroborates these findings. While there were significant differences in weight of lobster between LFAs used in the present study, this did not have a significant effect on euthanasia temperature. Indeed, the only significant factor determining euthanasia temperature was acclimation temperature.
McLeese (1956) used acclimation temperatures of 5 and 15 °C on American lobster originating from different geographic regions to identify temperatures of 24–25.7 and 27.8–28.4 °C, respectively, that killed 50% of animals within 48 h.
Camacho et al. (2006) used acclimation temperatures of 4 and 20 °C on American lobster to identify changes in cardiac function at 25.4 and 30–30.3 °C, respectively. While
McLeese (1956) and
Camacho et al. (2006) used different endpoints and methods to assess thermal tolerance limits than the present study, they identified thermal tolerance limits that were remarkably close to the euthanasia temperatures presented here.
This research provides additional insight into the potential for thermal adaptation under climate change and impacts for considering lobster sensitively under climate change vulnerability assessments. Climate change and warming ocean waters pose many threats to poikilotherms, animals that are unable to metabolically self-regulate body temperature, like the American lobster. Lobsters in warmer waters tend to reach maturity at smaller sizes and younger ages, which may potentially reduce the overall fecundity and recruitment of the population (
Waller et al. 2017). An analysis of 30 years of survey data collected from southern New England and the Bay of Fundy found that, for every 1 °C increase in bottom temperature, lobster carapace size at maturity decreased by 2.8 mm (
Le Bris et al. 2017). Moreover, lobster are more susceptible to epizootic shell disease at temperatures above 10 °C and this condition can be fatal above 15 °C (
Stewart 1980). As well as reducing their survival, the signs of this disease can reduce catch value due to the presence of the characteristic corrosive brown-black lesions on lobster carapaces (
Glenn and Pugh 2006;
Castro et al. 2012). The prevalence of epizootic shell disease is strongly correlated with temperature and is, consequently, currently more of a concern in southern New England than in the Gulf of Maine and Scotian Shelf (
Shields 2019;
Mazur et al. 2020). As temperatures continue to warm in the Northwest Atlantic (
Wang et al. 2018), epizootic shell disease could potentially spread further north into Nova Scotia (
Maynard et al. 2016;
Groner et al. 2018;
Greenan et al. 2019). Consequently, further studies are warranted on the potential effects of epizootic shell disease on thermal tolerance,
i.e., do additional stressors such as shell disease affect thermal maximum?
Live lobster from Atlantic Canada is a high-value product (
Fisheries and Oceans Canada 2022) that is shipped around the globe using artificial cooling and oxygenation that comprises a substantial part of the international seafood market (
Fotedar and Evans 2011). Despite best practices to ensure lobster survival, many international lobster shipments arrive with some deceased lobster (Leo Muise, Executive Director—Nova Scotia Seafood Alliance pers. comm., 2020). The sale of dead lobster is illegal in Nova Scotia under the Fish Inspection Regulations and harvesters and lobster pound operators can face a substantial fine if they are caught in violation this (
Province of Nova Scotia 2017). These regulations are unique to Canada. For example, lobster harvesters in the United States are permitted to process and sell dead lobster, while Norway lobster (
Nephrops norvegicus) landed in Belgian harbors can be sold as lobster tails with the heads having been discarded in transit from the catch site (
Bekaert et al. 2015). The application of PPG as described in the present study could be used to monitor signs of stress (e.g., arrythmia) in American lobster prior to international shipment to potentially identify weak animals, ultimately reducing mortality rates during transportation.
In spite of the unique challenges that will be brought on by climate change within individual LFAs (
Brickman et al. 2021), acclimation temperature was the only significant predictor of euthanasia temperature in American lobster in the present study. This study demonstrates that adult American lobster living in the relatively cold waters surrounding Nova Scotia (
Wang et al. 2018) can acclimate to new temperatures as ocean temperatures continue to rise, up to a certain point. Additional studies on other American lobster life stages would be required to assess their acclimation and thermal tolerances. Using heart rate data loggers (
Gutzler and Watson 2022) for long-term deployment on lobster populations in the wild in Nova Scotia would provide additional valuable information on the effects of climate change on heart rate. Additionally, further research investigating the potential effects of thermal acclimation on survivability of soft-shelled lobster is warranted as global ocean temperatures continue to rise and adversely impact the lobster fishing industry.