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\begin{document}

\title{Hot and hungry: A mechanistic approach to the direct and indirect
effects of marine heatwaves on plankton communities}



\author[1]{Maria Grigoratou}%
\author[2]{Camila Serra-Pompei}%
\author[1]{Adam Kemberling}%
\author[1]{Andrew Pershing}%
\affil[1]{Gulf of Maine Research Institute}%
\affil[2]{Center for Climate Change Science, Massachusetts Institute of Technology}%


\vspace{-1em}



  
  \date{June 17, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Marine heatwaves, increasingly frequent, impact marine ecosystems and
services. Still, understanding how temperature affects observed
responses remains limited due to complex interactions among temperature,
abiotic and biotic factors, and community dynamics. Here we try to fill
this gap by exposing simulated plankton communities to seasonal
heatwaves of 4\selectlanguage{ngerman}°C with a trait- and size-structured model that accounts
for protists and the life cycle of copepods. Despite the short lifespans
and fast growth rates of plankton, results show that heatwaves affect
communities differently and for an extended period up to six years after
their appearance. Temperature affects species physiology and ecosystem
dynamics, directly and indirectly, shaping structure and biomass.
Species traits, interactions, and functional diversity under changing
temperatures emerge as pivotal. Our study advances mechanistic insights
into marine heatwave impacts, highlighting the complex connections
between temperature, species traits, and ecological interactions.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{Hot and hungry: A mechanistic approach to the direct and
indirect effects of marine heatwaves on plankton communities}

Maria Grigoratou, Camila Serra-Pompei, Adam Kemberling, Andrew J.
Pershing

\textbf{Maria Grigoratou} : Gulf of Maine Research Institute, Portland,
Maine, USA, Mercator Ocean International, Toulouse, France,
0000-0003-0484-1408, maria.grigoratou1@gmail.com

\textbf{Camila Serra- Pompei} : Center for Climate Change Science,
Massachusetts Institute of Technology, Boston, Massachusetts, USA,
0000-0003-2627-466X, camsp@mit.edu

\textbf{Adam Kemberling} : Gulf of Maine Research Institute, Portland,
Maine, USA, 0000-0003-0402-0829, akemberling@gmri.org

\textbf{Andrew J. Pershing:} Gulf of Maine Research Institute, Portland,
Maine, USA, Climate Central,

New Jersey, USA, 0000-0003-4432-0850, apershing@climatecentral.org

\textbf{Short running title of less than 45 characters including spaces}
: Modelling Plankton Responses to Marine Heatwaves

\textbf{10 keywords} : plankton, protists, copepods, marine, heatwave,
temperature, model, trait-based, size, biomass

\textbf{type of article} : Letter

\textbf{number of words in abstract:} 139

\textbf{number of words in text} (excluding abstract, acknowledgements,
references, table and figure legends): 4697

\textbf{number of figures:} 6

\textbf{number of references: 66}

\textbf{name and complete mailing address (including telephone and fax
numbers and e-mail address) of the person to whom correspondence should
be sent} : Maria Grigoratou, Mercator Ocean International, 2 Av. de
l'A\selectlanguage{ngerman}érodrome de Montaudran, 31400 Toulouse, maria.grigoratou1@gmail.com

\textbf{Authors contributions}

M.G and A.P. designed the study. C.S.P. provided the code of the NUM
model (Serra-Pompei et al., 2020), insights on the model behavior, and
feedback on the model development. A.K. provided the Sea Surface
Temperature data metanalysis, provided feedback, and developed the code
for Figures. M.G. developed the model, provided the data metanalysis for
the mixed layer depth, ran the simulations, and analyzed the model
output. A.P. provided feedback on model development and model output.
M.G. wrote the manuscript with the support of all authors.

\textbf{Data and code availability statement}

The code for the model and the figures and the model output are publicly
available and can be found online on
https://zenodo.org/doi/10.5281/zenodo.10822886 (Grigoratou,
Serra-Pompei, Kemberling, and Pershing, 2024).



\textbf{Abstract}

Marine heatwaves, increasingly frequent, impact marine ecosystems and
services. Still, understanding how temperature affects observed
responses remains limited due to complex interactions among temperature,
abiotic and biotic factors, and community dynamics. Here we try to fill
this gap by exposing simulated plankton communities to seasonal
heatwaves of 4°C with a trait- and size-structured model that accounts
for protists and the life cycle of copepods. Despite the short lifespans
and fast growth rates of plankton, results show that heatwaves affect
communities differently and for an extended period up to six years after
their appearance. Temperature affects species physiology and ecosystem
dynamics, directly and indirectly, shaping structure and biomass.
Species traits, interactions, and functional diversity under changing
temperatures emerge as pivotal. Our study advances mechanistic insights
into marine heatwave impacts, highlighting the complex connections
between temperature, species traits, and ecological interactions.



\textbf{Introduction}

Marine heatwaves, periods characterized by temperatures well above the
mean ranges for at least five days , are increasing in presence and
duration with various impacts on marine communities and ecosystem
services across spatial and temporal scales . Even if temperature has
been identified as the major environmental driver, our mechanistic
understanding of how temperature affects marine populations is still
incomplete, which limits our ability to forecast changes in marine
ecosystems.

Filling this knowledge gap is challenging, as temperature is strongly
linked with multiple biogeochemical processes, and each one of them is a
potential driver for changes at the individual level that can lead to
alterations in population, community, and ecosystem dynamics . For
example, temperature has a direct effect on an individual's enzymatic
kinetics resulting in changes in physiological rates, e.g., metabolism,
cell division, growth, ingestion, and respiration that can alter oxygen
and resource needs and impact species traits like size, mobility, and
reproduction . Temperature also affects organisms indirectly by altering
the environmental status of their habitat (e.g., stratification, oxygen
concentration, abundance, distribution, resources, and predators). Thus,
the fitness of an individual in its environment during a heatwave is
determined by the combination of temperature effects on an organismal
and environmental scale filtered through the organism's morphological,
behavioral, and life-history traits . Therefore, understanding and
identifying ecosystem drivers requires a perspective that encompasses
both individual-level traits and community dynamics.

Plankton regulates marine life and has been recognized as an Essential
Ocean and Climate Variable linked with various ecosystem services such
as climate stabilization, fisheries, water quality, or tourism . Hence,
it is crucial to understand how climate variability and human activities
affect plankton organisms and communities. Observations have shown that
the duration of community change depends on the nature of the heatwave
(e.g., seasonal appearance, temperature anomaly, duration), the
environmental and community properties; some ecosystems respond and
return to the pre-heatwave condition faster than others . For planktonic
metazoans, the main observed \emph{in-situ} pattern during and after a
heatwave is the alteration in community structure and composition,
either via indigenous or the appearance of invasive species that enter
the ecosystems through new warm water masses in an area .
The\emph{in-situ} observations reflect a mixed Eulerian perspective of
advection and ecosystem processes, which complicates pinpointing the
drivers of observed ecosystem changes before and after the heatwave. Are
the alterations of the observed ecosystem dynamics driven by the impact
of temperature on physiological processes (direct effects), the
resulting environmental changes (indirect effects), or both?

Laboratory and modeling studies, even if they may lack realism, can
scale down complexity and isolate drivers. Studies have revealed that
temperature triggers different responses in physiological processes and
rates of individuals . If these responses will be reflected on a
population or community level depends on how individuals react to their
entire environment, rather than just one environmental factor .
Therefore, it is important to design studies that focus on causation and
not only on the correlation between individual responses and
environmental drivers.

The present study investigates the direct and indirect effects of
temperature on plankton communities during seasonal heatwaves within a
mechanistic framework. Our study aims to answer three key questions:

What impact do seasonal heatwaves have on functional diversity, biomass,
and community structure during and after the heatwave?

What is the recovery time for a plankton community to regain its
pre-heatwave composition and characteristics, such as biomass size
distribution and functional diversity?

Which plankton community changes result from temperature itself versus
indirect effects from food web dynamics?

We examine those questions using the Nutrients-Unicellular-Multicellular
(NUM) model . NUM is a mechanistic size and trait-based model that
simulates community structures and predator-prey interactions for
protists (autotrophs, mixotrophs and heterotrophs) and the life cycle of
active and passive feeding copepods. We focus on the direct temperature
effects on individual rates and predator-prey interactions, without
considering species adaptation and any temperature effect on other
environmental factors like changes in the mixed layer depth and nutrient
concentration. For our experiment, we assume a Lagrangian view and track
a community as it experiences warming caused by a surface heat flux
anomaly. Using this model, we analyze how seasonal heatwaves impact
community biomass, diversity, and structure.

\textbf{Methods}

\emph{Nutrients-Unicellular-Multicellular (NUM) model}

Here we provide a short presentation of the NUM model and of the
modifications we made related to the temperature norm (see below and the
Supplementary Materials for more details). A detailed description of the
model and its governing equations can be found in Serra-Pompei et al.
(2020). NUM is a semi-chemostat size and trait-based plankton functional
type model that accounts for protists and copepod life cycles. The model
includes four abiotic factors: light, ambient temperature, mixed layer
depth, and nutrient concentration (nitrogen). The plankton populations
are homogeneously distributed in the upper mixed layer. Nitrogen enters
the system via the mixing rate between the upper and the deep layer and
leaves the system via sinking or particulate organic matter, but no
vertical migration (daily or seasonal) or other biological activity is
resolved in the deep layer. Nitrogen is channeled in the food web via
diffusive uptake by protists and predator-prey interactions. Finally,
the particulate matter generated by organisms is recycled, returning
nutrients to its dissolved form in the surface layer.

Each plankton group in the model represents a population of various
individuals with shared traits like size and foraging behavior. The
population growth rate depends on the uptake, encounter, ingestion,
assimilation, respiration, growth, and reproduction rates. Protists are
assumed to be spherical cells, distinguished by their size and
temperature norm (below and SM). As potential mixotrophs, protists
constantly move within the trait spectrum of autotrophy, mixotrophy, and
heterotrophy, depending on the available resources. Their uptake rates
follow a Holling type II response, and their biomass concentration is
the balance between energy gain and losses from predation and background
mortality (losses not caused by predation).

The life cycle of copepods is represented by 8 discrete life stages, 7
juveniles, and one adult. The juvenile stages invest all their energy
gain in somatic growth and the adult stage only in reproduction. Like
protists, the ingestion rate of copepods follows a Holling type II
functional response. All copepods are omnivorous and can prey on
protists or other copepods within their grazing kernel. Copepods are
distinguished by two traits: the maximum adult body length and foraging
mode -- active or passive. Active feeders have higher ingestion and
growth rates but face increased respiration costs and predation
mortality. In contrast, passive feeders have lower rates and predation
risks. Copepod losses arise from predation and background mortality,
with larger individuals facing additional predation from unspecified
larger predators (e.g., fish).

\emph{Temperature norm}

In the model, ambient temperature affects both protist and copepod
uptake, respiration, clearance, and ingestion rates. Serra-Pompei et al.
(2020) represent the temperature dependency as a Q\textsubscript{10}. In
the present study, we follow the approach and use an environmental trait
in the form of a temperature norm (Figure 1, and Supplementary
Materials). Groups can only grow within the temperature range of their
norms (Figure 1).

\emph{Model set up}

\emph{Environmental forcing}

For the environmental forcing, we used the Sea Surface Temperature and
Mixed Layer Depth (ECCO Consortium et al., 2021) daily mean of 10 years
(2000- 2010) of an offshore region of the Mid-Atlantic Bight, a
representative North Atlantic temperate ecosystem (Figures 1, SM1, and
Supplementary Materials).

We ran the model for 50 years to allow the community to reach a
steady-state condition (hereafter pre-heatwave conditions). Our focus is
solely on examining the temperature effects on plankton communities of a
specific water mass. Thus, we didn't change the mixed layer depth (MLD)
and nutrient input, acknowledging that this simplification reduces the
complexity typically found in natural ecosystems. For the marine
heatwave scenarios, we exposed the steady-state community to a 4 \selectlanguage{english}@C
temperature anomaly lasting for one season (three months) for either
winter (December- February), spring (March- May), summer (June- August),
or autumn (September- November). Observed heatwaves range in duration
from days to months, with no universally applicable average duration due
to variations influenced by factors like event intensity, geographic
location, and specific oceanographic conditions . For example, the
oceanic waters of the Northeastern United States Continental Shelf have
experienced long seasonal heatwaves up to 3 @\selectlanguage{english}C since 2012 . In this
context, we have opted to investigate the impact of an extended and
intense heatwave on plankton communities, portraying it as an extreme
scenario that may become increasingly common within ecosystems due to
ongoing climate change. After the heatwave event, we ran the model for
another 19 years with the pre-heatwave SST to examine the period needed
for the community to readjust to the pre-heatwave condition. To isolate
the processes responsible for the observed changes, we ran two
additional simulations. In the first, heatwaves solely affect protists'
rates, while in the second, only copepods are sensitive to the elevated
temperature. These experiments enabled us to examine whether changes in
communities are driven by direct temperature effects, indirect
temperature effects, or a combination of both.

\emph{Initial conditions and plankton groups}

We used the same initial conditions as in Serra-Pompei et al. (2020;
i.e., 1 \selectlanguage{greek}μ\selectlanguage{english}g N L\textsuperscript{-1} for the nitrogen and 5 \selectlanguage{greek}μ\selectlanguage{english}gC
L\textsuperscript{-1} for each plankton size class (protists and
copepods). We included 14 size classes of protists ranging from
10\textsuperscript{-7} \selectlanguage{greek}μ\selectlanguage{english}g C to 10\textsuperscript{-1} \selectlanguage{greek}μ\selectlanguage{english}g C mass per
cell. The size of adult copepods ranged from 0.2 \selectlanguage{greek}μ\selectlanguage{english}g C to 1000 \selectlanguage{greek}μ\selectlanguage{english}g C and
0.2 \selectlanguage{greek}μ\selectlanguage{english}g C to 5 \selectlanguage{greek}μ\selectlanguage{english}g C for active and passive copepod feeders, respectively.
The model had 8 temperature norms from 0 @\selectlanguage{english}C to 28 @\selectlanguage{english}C with a 4 @\selectlanguage{english}C
interval. Each temperature norm included 25 populations (14 protists,
eight active, and three passive copepod feeders). In total, the model
included 200 populations: 112 protists, 64 active and 24 passive
copepods. We also categorized the plankton biomass in size bins based on
protists and copepods' cell/body volume (six for protists and active
copepods, four for passive copepod feeders, Table SM1). We used the
Shannon Diversity Index to estimate the functional diversity of the
modelled plankton community (Supplementary Materials).

\textbf{Results}

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.

\emph{Modeled pre-heatwave conditions}

In the pre-heatwave conditions the Sea Surface Temperature (SST) ranges
from 13.5 @\selectlanguage{english}C (March 1) to 26.2 @\selectlanguage{english}C (August 4, Figure 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 14) to
93 m (February 23, Figure 1). Winter and spring have the deepest MLD,
followed by similar depths in autumn and summer (Figure 1).

The overall daily modeled biomass concentration of protists and copepods
declines from early winter (December) until the end of April (Figure 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 (Figure 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 (Figures 2, 3).
Overall, the plankton community is dominated by groups with temperature
optima of 20 @\selectlanguage{english}C and 24 @\selectlanguage{english}C (Figure 3). Both optima cover temperatures
from 10 to 30 @\selectlanguage{english}C and are within the daily (14 -- 30 @\selectlanguage{english}C) and annual (20
@\selectlanguage{english}C) temperature range. The temperature norms of dominant groups track
the annual mean temperature, not the Sea Surface Temperature seasonality
(Figure 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 .

\emph{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
(Figures. 3-6, SM4- SM6). Summer and autumn heatwaves (Figure 4, SM4)
cause the highest anomalies in terms of biomass concentration and
recovery times followed by spring and winter (Figures SM5-SM6). The
strongest copepod biomass decline occurs during summer heatwaves,
persisting for two years and eventually recovering to pre-heatwave
concentrations after six years (Figure 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
(Figure SM4). 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 (Figure SM5). 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 (Figure SM6). 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 (Figure 5, Supplementary Material
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 (Figure 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 (Figure 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 @\selectlanguage{english}C and 24 @\selectlanguage{english}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.

\emph{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 (Figure 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 (Figure 3). The model outputs suggest
that pinpointing a clear environmental driver becomes challenging as we
move from individuals to populations, functional groups, and
communities.

\textbf{Discussion}

Marine heatwaves are an increasing phenomenon with effects on plankton
organisms, food webs, biogeochemistry, and ecosystem services . Thus,
the development of reliable forecasting tools on heatwaves properties
(e.g., duration, intensity, depth) and ecosystem responses is crucial
for successful mitigation and adaptation actions for ocean
sustainability . Still, we lack a mechanistic understanding of how
temperature relates to the observed ecological alterations during and
after the heatwaves. This is mostly due to the strong connection of
temperature with various abiotic and biotic factors and the complex
temporal and spatial dynamics of marine communities.

In this study, we examine how the temperature anomaly of surface
seasonal heatwaves is affecting ecosystem dynamics in plankton
communities. We use a trait- and size-structured model that accounts for
protists and the life cycle of active and passive feeding copepods. We
highlight and discuss three key findings: Firstly, seasonal heatwaves
trigger contrasting, lasting effects on plankton communities (biomass,
size distribution, functional diversity), extending up to six years
post-heatwave onset. Secondly, it is difficult to separate temperature
as the key driver of the ecosystem changes we observe when we move from
individual processes to community dynamics. Lastly, temperature
anomalies can trigger functional groups differentially, with direct and
indirect effects varying across groups.

The model results show that the duration of community anomalies depends
on when the heatwave occurs. The system takes up to three years for the
winter and spring heatwaves and up to six years for the summer and
autumn heatwaves to reach the pre-heatwave state. The different mixed
layer depth of the seasons (shallow in summer/autumn, deeper in
winter/spring) could be a potential driver for this outcome, as it is
strongly related to the density of nutrients and plankton in the model
and the ocean . Though, since we kept the mixed layer depth fixed in our
experiments, we speculate that this outcome is driven by the temperature
differences among seasons caused by the heatwaves. The mean seasonal
temperature before the heatwaves varies between 15 @\selectlanguage{english}C and 16 @\selectlanguage{english}C for
winter and spring and 22 @\selectlanguage{english}C to 24 @\selectlanguage{english}C for autumn and summer, leading to a
temperature difference of up to 9 @\selectlanguage{english}C between seasons. The seasonal
heatwaves of 4 @\selectlanguage{english}C do not alter the mean annual temperature (20 @\selectlanguage{english}C).
Still, while winter and spring heatwaves maintain temperature
fluctuations within pre-heatwave seasonal ranges, summer and autumn
heatwaves lead to fluctuations exceeding the pre-heatwave ranges by 2 @\selectlanguage{english}C
(autumn) and 4 @\selectlanguage{english}C (summer). Thus, the model indicates that the
ecological disruption and recovery time are related to the temperature
anomaly compared to seasonal temperature fluctuation.

Our results show changes in biomass size bins, dominant groups, and
functional diversity index during and after heatwaves, differing across
protist and copepod functional groups. Starting with the temperature
environmental trait, the model includes functional groups of eight
temperature norms. For both protists and copepods, heatwaves lead to
changes in the relative biomass and order of the dominant groups during
and after the heatwave. Still, functional groups with temperature norms
of 20 @\selectlanguage{english}C and 24 @\selectlanguage{english}C dominate the plankton community before, during, and
after the heatwaves and between seasons.

The community size structure also reflects periodic variations caused by
marine heatwaves. However, no consistent pattern emerges across biomass
size bins for all heatwave scenarios, revealing the intricate synergy of
direct and indirect temperature effects. For years after the heatwaves,
the model shows changes in the order of dominant size groups,
highlighting that the effect of a seasonal heatwave on the community
properties can persist for a long period. However, the reposition of
some dominant size groups does not affect the core community size
structure. Our model output is supported by previous studies that show
that environmental factors beyond temperature likely contribute to size
structure variations we observe in nature . \emph{In-situ} observations
have shown that surface heatwaves alter the properties of plankton
communities like diversity and size distribution, strongly connected
with other environmental conditions such as the passive entrance of
species via water masses, stratification, and changes in nutrient
concentrations . Field observations show a shorter recovery period than
our model projects ranging from a few months to three years depending on
the duration of the heatwave . \emph{In-vitro} and mesocosm experiments
also indicate that warming can trigger alterations and different
recovery times on physiological rates, species density, and community
structure in the same direction as our model.

Our results are in a parallel direction with \emph{in-situ}
and\emph{in-vitro} observations but are not directly comparative as
model-observation disparities stem from differences in design,
environment representation, and ecological realism.
\emph{In-situ}observations are snapshots of an ecosystem shaped by many
physical, chemical, and biological processes, most of them recorded with
a limited temporal and spatial resolution. In comparison to the Eulerian
view of\emph{in-situ} observations, this study assumes a Lagrangian view
and allows us to focus on the theoretical community as moving through
time. Mesocosm and laboratory experiments also follow a Lagrangian
approach, but they run for shorter periods compared to our model
experiments (days to weeks). We also note that descriptive language in
most published studies (e.g., small vs big, warm vs cold species) lacks
quantitative data (e.g., body size, species temperature optima, and
physiological rates) necessary for direct model-observation comparisons.
Given plankton's adaptive plasticity and morphological variations
species can manifest as ''cold'' or ''warm'' depending on regional
context, contributing uncertainty to model-observations comparisons.

We propose two more drivers of this model-observational mismatch other
than the differences between our model design and\emph{in-situ/in-vitro}
marine heatwaves on the Lagrangian vs Eulerian approach and heatwave
properties (e.g., temperature anomaly and heatwave duration): (1) the
lack of a 3-dimensional dynamic environment in our model and (2) the
need for enhanced ecological and plankton diversity representation. In
marine ecosystems, surface heatwaves do not occur in isolation, as in
our modelling set-up. They are strongly connected with other abiotic
drivers of ecosystem dynamics (e.g., mixed layer depth, nutrient
cycling, salinity) that can alter nutrient resources, prey
concentrations, and community dynamics during the heatwave . These
environmental drivers can also mitigate or aggravate the signal of
temperature effect through time. Additionally, even if our model design
has complex ecosystem dynamics and higher functional diversity than most
ecosystem models (Petrick et al., 2022), it does not consider phenotypic
plasticity, evolution, or behavioral decisions like vertical migration
and changes in foraging and predation avoidance that can maximize
fitness on an individual level and resilience on a community level .
These physiological and behavioral responses might allow species
persistence that could dampen the impact of the heatwave and accelerate
recovery periods.

Our study highlights the essential role of functional diversity in
population dynamics. In the model, protists are the most diverse
community with plasticity on energy uptake and short life cycles. They
show dynamic responses to environmental conditions and experience more
changes in community composition compared to copepods. Passive copepod
feeders are more vulnerable than active feeders and have the longest
recovery time in terms of biomass concentration. This is probably due to
their trade-off disadvantage on resource competition combined with
predation losses from active feeders. Traditionally, research has
focused on prey density and properties, but studies have shown that the
modes of energy uptake and foraging also have a strong impact on
ecosystem dynamics, biogeography patterns, and biogeochemistry . For
example, studies have shown that mixotrophy evolved as a survival
strategy against prolonged periods of darkness and that some copepod
species can actively switch between passive and active feeding depending
on the environmental conditions (Ki\selectlanguage{ngerman}ørboe et al., 2018a). Closer
attention to the feeding mode and organismal behavioral decisions that
lead to trait optimization and fitness can help us to better understand
the community status in different environmental conditions and extreme
events. A gradual increase of functional diversity in the model could
provide us with a new level of mechanistic understanding of ecosystem
dynamics but probably increase the difficulty of distinguishing drivers.
It could also highlight suggestions on data needs for advancing the
state-of-the-art of forecasting tools and our confidence in trustworthy
projections crucial for policy advice and actions. Our model is a useful
tool for mechanistically exploring the effect of abiotic parameters in
ecosystems from individuals to community levels. We wish to see future
studies using and adjusting the model design to explore the resilience
of plankton communities under different environmental conditions.

\textbf{Conclusions}

As extreme events caused by climate change are increasing in frequency
and duration, it is important to develop a mechanistic understanding of
how ecosystems respond to temperature changes. Here we use a trait- and
size-structured model to study the effect of seasonal heatwaves on
plankton organisms. In the model, the plankton functional diversity is
represented by the traits of cell/body size, energy uptake (auto-, mixo-
and heterotrophy) for protists, and the life cycle of copepods with two
feeding modes (active, passive). The model showed that heatwave effects
on biomass, diversity, and community composition are present not only
during the heatwave but for up to six years after the temperature
perturbation. Autumn and summer heatwaves have the most profound
anomalies and longest-lasting effects, followed by winter and spring
heatwaves. Our results indicate that temperature can alter the dominance
of size groups, but temperature alone cannot lead to fundamental changes
in the community size structure and more environmental factors need to
be taken into consideration. In our study, we found a variety of
population and community alterations during the heatwave and different
recovery times to the pre-heatwave state. Two factors drive those
results: the heatwave temperature anomaly compared to the mean seasonal
temperature fluctuation and plankton functional diversity. Communities
have longer recovery times when experiencing seasonal heatwaves with
temperature anomalies outside the pre-heatwave seasonal temperature
fluctuation. Including functional diversity is crucial for exploring
ecosystem changes as protists, active, and passive copepod feeders have
dissimilar responses to the heatwaves, as well as recovery periods. Our
model provides a mechanistic framework with ecological realism, flexible
enough to scale up and down in complexity and test hypotheses for future
studies.

\textbf{Acknowledgements}

This work was supported by the National Science Foundation via the
``WARMEM'' project (OCE-1851866) to M.G, A.K and A.P. and by the Simons
Foundation (\#722859) to C.S.P. We would like to thank Kathy Mills for
her feedback on the study design and results and Gustav Delius for the
discussions on size-spectrum modelling.

\textbf{References}

\textbf{Figure Legends FIGURE 1:} A graphic summary of the model design,
with the environmental forcing (mixed layer depth and sea surface
temperature) and a graphic illustration of the temperature norm
environmental trait.

\textbf{FIGURE 2} : Absolute biomass concentrations (mg C m-3) expressed
in size bins for the pre-heatwave conditions for active and passive
copepod feeders and for protists: (a) daily biomass size bins (b)
seasonal total and mean biomass of the size bins. Dashed lines in
indicate the end of each season (winter, spring, summer, autumn).

\textbf{FIGURE 3:} Absolute seasonal biomass concentration of the five
dominant functional groups (in terms of their relative contribution to
total biomass) of (a.) active and (b.) passive copepod feeders and (c.)
protists for the winter (December- February), spring (March-May), summer
(June- August) and autumn (September- November) heatwave scenarios. Year
1: Heatwave. Years 2-7: years after the heatwaves.

\textbf{FIGURE 4:} Absolute Biomass concentration (mg C m-3) anomalies
during and after the summer seasonal heatwave (June-August) for the
biomass size bins of (a.) active and (b.) passive copepod feeders and
(c.) protists. Year 1 shows the seasonal biomass anomaly during the
heatwave (heatwave- pre heatwave biomass concentration). Years 2- 9 show
the seasonal biomass anomaly for 8 years after the seasonal heatwave
(after heatwave -- pre heatwave biomass concentration). HW on all
plankton groups: the heatwave directly affects the physiological rates
of all plankton groups. HW on copepods only: the heatwave directly
affects the physiological rates of copepods only. HW on protists only:
the heatwave directly affects the physiological rates of protists only.

\textbf{FIGURE 5} : Seasonal Shannon Diversity Index for (a.) active and
(b.) passive copepod feeders and (c.) protists for the winter (December-
February), spring (March- May), summer (June- August) and autumn
(September- November) heatwave scenarios. X-axis: years. Year 0:
pre-heatwave, Year 1: heatwave (in red) Years 2-5: after-heatwave. More
details about the Shannon Diversity Index can be found in the SM.

\textbf{FIGURE 6} : Biomass anomalies (heatwaves (HW) on protists or
copepods only -- heatwaves (HW) on both protists and copepods) during
all seasonal heatwaves and the seven seasons afterwards for (a.) active
and (b.) passive copepod feeders, and (c.) protists.\selectlanguage{english}
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