Mass disappearance of intertidal mussels after an unusual winter cold snap in eastern Canada

Abstract

On temperate marine rocky shores, mussels often form dense intertidal stands that extend across the substrate at various spatial scales. As these stands offer food and shelter for many small species, they are important for the preservation of coastal biodiversity (Arribas et al., 2014; Lafferty & Suchanek, 2016). In the last few decades, the abundance of intertidal mussels has declined considerably on some shores because of anthropogenic factors, which is concerning due to the wider ecological implications (Fields & Silbiger, 2022; Sorte et al., 2017). Particularly marked declines have occurred from extreme weather events caused by the ongoing climate change, as weather conditions affect intertidal species during low tides. A dramatic example occurred recently on the NE Pacific coast. In the summer of 2021, a strong heatwave broke historical records of maximum air temperature, causing mass mortality of mussels in rocky intertidal habitats, which experienced temperatures higher than 50°C at low tide under direct sunlight (Raymond et al., 2022; White et al., 2023).

Although average temperatures are increasing globally, severe cold stress in winter can take place regionally. For example, the winter temperature gradient between the Arctic and middle latitudes is weakening because Arctic winter temperatures are rising faster. This phenomenon can lead to polar air being transported to middle latitudes in winter, resulting in cold air outbreaks in Eurasia and North America (Cohen et al., 2021; You et al., 2021). In eastern Canada, unusually cold weather occurred in early February 2023 (Environment Canada, 2023). Annual surveys from 2014 to 2017 showed that mussels (Mytilus edulis and M. trossulus) were common at mid-to-high intertidal elevations in wave-exposed rocky habitats in southeastern Nova Scotia (Scrosati et al., 2022; Figures 1 and 2). However, shortly after the 2023 cold snap, a mass disappearance of these mussels took place. To document this loss, in April 2023 we measured mussel percent cover at mid-to-high elevations along the same transects surveyed from 2014 to 2017 at Duck Reef (44.4913, −63.5270), Western Head (43.9896, −64.6607), and West Point (43.6533, −65.1309), surveying 30 quadrats (20 cm × 20 cm) at each location. We then used the 2014–2017 data on mussel cover as a reference. To describe the 2023 cold snap, we obtained hourly values of air temperature between 1 December and 15 April for the last 10 years (Environment Canada, 2023). We included data up to 15 April because in 2023 we measured mussel cover at the first location (Western Head) on 16 April (we surveyed Duck Reef on 21 April and West Point on 22 April). We used temperature data for the last 10 years because the earliest data on mussel cover were collected in 2014 (Scrosati et al., 2022). These locations span a linear distance of 160 km. For this coastal range, the only coastal weather station with air temperature data measured since at least 2014 is Western Head Station (43.9900, −64.6642), located a few hundred meters from the shore. We avoided weather stations further inland because thermal variation often differs from nearshore environments. As air temperature affects intertidal organisms during low tides, we determined for the February 2023 cold snap (Figure 1) the times when tide height became higher and lower than the elevation of the surveyed intertidal transects. At Western Head, this elevation was 1.5 m above chart datum, which in Canada is the lowest normal tide (Scrosati et al., 2022); the maximum tidal amplitude at this location is ~2.4 m. We obtained the tide height data for Liverpool Bay (44.0500, −64.7167; Tide and Current Predictor, 2023), which is the tide station closest to Western Head.

Our surveys done before 2023 showed that mussels were always present on the shore forming patches of various sizes (Figures 1 and 2). Between 2014 and 2017, quadrats with low mussel cover were always found (denoting the patchy distribution of mussels), but cover values between 7% and 88% were also common. Although mussel cover was not quantified between 2018 and 2023, periodic observations of the same transects until June 2021 at West Point, October 2022 at Western Head, and January 2023 at Duck Reef always found mussel patches with those characteristics. In April 2023, however, just one or a few scattered juvenile mussels were found in a small proportion of the quadrats along these permanent transects (Figures 1 and 2). These interannual differences were supported by Kruskal–Wallis analyses of variance (H₄ = 41.3 for Duck Reef, H₄ = 65.7 for Western Head, and H₄ = 103.0 for West Point; p < 0.001). The loss of mussels in 2023 was exceptionally high at Western Head (Figures 1 and 2), where only four of the 30 surveyed quadrats showed any mussel presence, but simply because one or two small juveniles were present, amounting to less than 1% cover. At Western Head, the areas previously occupied by mussel patches were largely only covered in April 2023 by byssal threads (Figure 2), indicating the recent occurrence of mussels that were lost. Visual surveys at the same intertidal elevation but outside these transects found a few patches composed mostly of open valves of dead mussels still attached to the substrate with byssal threads (Figure 2). Those valves were intact and showed no boreholes. Observations done at Western Head in August 2023 still revealed the virtual absence of mussels along these permanent transects at the mid-to-high intertidal zone (mussel patches were only found at the low intertidal zone).

Between 3 and 4 February 2023, air temperature on this coast dropped below −20°C for the first time in the last 10 years, reaching −23.2°C at 03:00 on 4 February (Figure 1). These extreme values spanned several hours while tide height was lower than the mid-to-high elevation where mussel patches used to occur (Figure 1). Importantly, this February cold snap occurred after mild winter conditions in December and January relative to the previous 9 years (Figure 1).

We will now evaluate possible explanations for the mass disappearance of mussels. In the studied habitats, dogwhelks (Nucella lapillus) are almost the only predators of mussels (Scrosati et al., 2022). Dogwhelks drill a borehole on a mussel's shell to eat a mussel (Sherker et al., 2017), but none of the open mussel valves found in April 2023 had boreholes, suggesting that predators did not cause this massive loss. In fact, dogwhelks are inactive between November and April (Etter, 1989). Another factor to consider is ice scour. In Nova Scotia, winter ice scour can physically disturb intertidal habitats, but only on northern shores, as no significant ice forms in wave-exposed habitats on southern shores and spring drift ice from northern shores has not reached southern locations in recent years (Canadian Ice Service, 2023; Scrosati et al., 2022). Also, mass loss of mussels could only occur after extreme ice scour (Petzold et al., 2014), but the fucoid algae that coexisted with mussels at our locations before 2023 were as abundant in April 2023 as in previous years. This analysis also excludes extreme wave action as a possible driver of the observed mussel loss, as the fucoid algae found in April 2023 did not show any unusual signs of damage. Based on our findings of a few open valves of dead mussels still attached to the mid-to-high intertidal substrate in April 2023, wave action may have simply removed the valves of mussels after they died.

The February 2023 cold snap then emerges as the most likely driver of the mass disappearance of mussels. While temperate intertidal invertebrates possess adaptations to limit deaths in winter (Loomis, 1995), extreme low temperatures can be lethal even when brief (Clarke, 2017). Lethal temperatures for Mytilus edulis from Atlantic Canada range between −13 and −20°C (Bourget, 1982). Thus, our air temperature data suggest that lethal cold stress may have occurred at low tide between 3 and 4 February 2023. Mussels disappeared even in areas covered by fucoid algae, which is noteworthy because fucoid canopies moderate understory temperatures during winter low tides (Scrosati & Ellrich, 2018). Interestingly, this severe cold snap was also followed by mass bleaching in red turf algae (Chondrus crispus and Corallina officinalis) at lower intertidal elevations (Scrosati & Cameron, 2023), which was not seen in a survey done in January 2023. Finally, it is worth noting that, before the February cold snap, the 2022–2023 winter had been mild in Nova Scotia compared with previous years (Figure 1), which may have weakened the winter acclimation of intertidal organisms (Kennedy et al., 2020).

While the 2021 NE Pacific heat wave has been attributed to climate change (Philip et al., 2022), an equivalent conclusion for the 2023 NW Atlantic cold snap is currently unavailable, although it would not be surprising given that cold spells in eastern North America are favored by climate change (You et al., 2021). Whether mussels can regain historical abundances in the studied habitats (see also the declines reported for New England, south of Nova Scotia; Sorte et al., 2017) depends, among other factors, on future cold spells and heatwaves. As the frequency of extreme weather events will likely increase with climate change (IPCC, 2023; Studd et al., 2021), the ecology of these coastal ecosystems may experience significant changes in the future.

The authors declare no conflicts of interest.