We used a trait- and size-structure model to examine (1) if and how a temperature anomaly of a seasonal heatwave can affect plankton communities, (2) how long it takes for the plankton communities to return to their pre-heatwave state in terms of seasonal patterns of the biomass size-bin concertation, diversity and dominant functional groups, and (3) if and how the individual responses of different trophic levels (protists and metazoans) can mitigate potential disturbances of temperature in ecosystem dynamics.
Modeled pre-heatwave conditions
In the pre-heatwave conditions the Sea Surface Temperature (SST) ranges from 13.5 ˚C (March 1st) to 26.2 ˚C (August 4th, Fig. 1) with winter exhibiting the lowest mean SST, followed by spring, autumn, and summer (Fig 1). The Mixed Layer Depth (MLD) varies from 28 m (September 14th) to 93 m (February 23rd, Fig. 1). Winter and spring have the deepest MLD, followed by similar depths in autumn and summer (Fig. 1).
The overall daily modeled biomass concentration of protists and copepods declines from early winter (December) until the end of April (Fig. 2). Copepod biomass gradually increases from May to its peak in autumn (September/October). The biomass concentration of protists has a strong variation in summer and autumn. Still, overall, it shows an increasing trend from summer to mid-autumn with three biomass peaks in summer (August), early autumn (September) and early winter (December). Autumn holds the highest mean biomass concentration for protists and copepods, followed by summer, winter, and spring (Fig. 2).
Protists constitute the most diverse community, followed by active and passive copepod feeders. Depending on the season, ten functional groups contribute 70 % to 86 % of the total protist biomass, while five functional groups represent 82 % to 100% of the total copepod biomass. Protists' highest diversity is not only due to their big pool of initial groups in the model set-up (112 groups) but mostly due to their short life cycle (asexual, one life stage), their opportunistic ability to grow with different resources (nitrogen, prey, mixotrophy) at any time, and the dynamic losses (grazing, background mortality). In contrast, copepods have longer life cycles (sexual, eight life stages), and their growth relies only on one energy source (prey availability). These trait disparities account for variations in population coexistence, biomass distribution among groups, and temperature norms (Figs. 2, 3). Overall, the plankton community is dominated by groups with temperature optima of 20 ˚C and 24 ˚C (Fig. 3). Both optima cover temperatures from 10 to 30 ˚C and are within the daily (14 – 30 ˚C) and annual (20 ˚C) temperature range. The temperature norms of dominant groups track the annual mean temperature, not the Sea Surface Temperature seasonality (Fig. 3), as life cycles, growth rates, and population dynamics introduce delays between abiotic and biotic seasonalities, allowing populations to persist even when some environmental conditions fall outside their optimal growth range (e.g., Holmes-Hackerd et al. 2023).
Biomass, functional diversity and community composition during seasonal heatwaves
In our modelling study, we observed that heatwaves induce changes in community biomass, diversity, and dominant functional groups of plankton (Figs. 3-6, SI4- SI6). Summer and autumn heatwaves (Fig. 4, SI4) cause the highest anomalies in terms of biomass concentration and recovery times followed by spring and winter (Figs. SI5-SI6). The strongest copepod biomass decline occurs during summer heatwaves, persisting for two years and eventually recovering to pre-heatwave concentrations after six years (Fig. 4). Protists also experience strong biomass declines during and after the summer heatwaves with a stronger periodic signal than in copepods. The biomass anomalies for the autumn heatwave (September- November) are similar to the summer heatwave (Fig. SI4). The only exception is that the biomass of active feeders increases when the autumn heatwave occurs. The winter heatwave (Dec-Feb) positively impacts plankton biomass, particularly for active and passive feeders, while total protist biomass declines for the remainder of the year (Fig. SI5). The biomass anomalies are less profound a year after the winter heatwave and the biomass returns to pre-heatwave conditions after three years. The spring heatwave (Mar-May) exhibits similar biomass anomaly patterns to the winter heatwave (Fig. SI6). The total biomass of both active and passive copepod feeders increases, while the total protist biomass stays the same despite the fluctuations in the size bins.
Looking at the Shannon Diversity Index (Fig. 5, Supplementary Information section: “Shannon Index”), heatwaves also affect plankton functional diversity with the anomaly signal being extended into subsequent seasons. For both protists and copepods, functional diversity stays the same or increases during winter, spring, and summer heatwaves, while it decreases during the autumn heatwave. The autumn heatwave causes the strongest anomaly, followed by summer, winter, and spring. After the heatwave, the time-traveling anomaly signals show that heatwaves affect plankton functional groups differently.
Examining community composition, heatwaves alter the order of dominant groups based on their relative contribution to the total biomass at the time (Fig. 3). These changes persist for up to six years before returning to pre-heatwave conditions. Like biomass and diversity, the alterations in dominant groups are more profound for the summer and autumn heatwaves (Fig. 5). All four heatwave scenarios cause more changes in protists than in copepods. We speculate that this is due to protists shorter live-cycles, higher community diversity, and stronger ecosystem dynamics (resource competition, predation). Still, two temperature norms (20 ˚C and 24 ˚C) dominate the community before, during, and after all heatwaves. Our findings indicate that despite temperature impacts on individuals’ physiology, populations and communities remain resilient during seasonal heatwaves. Smaller-size groups may benefit, but larger groups also show increased biomass, suggesting the influence of resource competition and predator-prey dynamics alongside temperature.
Direct versus indirect effects of temperature on community properties
Complex ecosystem dynamics pose challenges in determining whether the primary driver of plankton community changes is the temperature on organismal physiology (direct effects), predator-prey dynamics (indirect effects), or both. We conducted two sets of simulations to separate the direct and indirect effects of temperature; one where we exposed solely protists on the heatwave and one only on copepods. Looking at the biomass size bins, both copepods and protists show a variety of biomass anomalies depending on the temperature simulations (Fig. 6). For copepods, functional diversity exhibits similar anomaly patterns between the initial heatwave simulations (which consider heatwave impacts on both protists and copepods' physiology) and simulations where the heatwave solely affects copepods' physiological rates while protists show more diverse anomaly patterns (Fig. 3). The model outputs suggest that pinpointing a clear environmental driver becomes challenging as we move from individuals to populations, functional groups, and communities.