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Article history: The effect of biodiversity on ecosystem functioning is one of the major questions of ecology. However,
Received 18 August 2016 the role of phytoplankton functional diversity in ecosystem productivity and stability under fluctuating
Received in revised form 18 June 2017 (i.e. non-equilibrium) environments remains largely unknown. Here we use a marine ecosystem model
Accepted 19 June 2017
to study the effect of phytoplankton functional diversity on both ecosystem productivity and its stability
Available online 29 August 2017
for seasonally variable nutrient supply and temperature. Functional diversity ranges from low to high
along these two environmental axes independently. Changes in diversity are obtained by varying the
Keywords:
range of uptake strategies and thermal preferences of the species present in the community. Species can
Shannon entropy
Plankton foodwebs
range from resource gleaners to opportunists, and from cold to warm thermal preferences. The phyto-
Species-traits plankton communities self-assemble as a result of species selection by resource competition (nutrients)
Ecological selection and environmental filtering (temperature). Both processes lead to species asynchrony but their effect
Ecosystem modelling on productivity and stability differ. We find that the diversity of temperature niches has a strong and
direct positive effect on productivity and stability due to species complementarity, while the diversity of
uptake strategies has a weak and indirect positive effect due to sampling probability. These results show
that more functionally diverse phytoplankton communities lead to higher and more stable ecosystem
productivity but the positive effect of biodiversity on ecosystem functioning depends critically on the
type of environmental gradient.
© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
http://dx.doi.org/10.1016/j.ecolmodel.2017.06.020
0304-3800/© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.
0/).
S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196 185
1.2 1.2
0.8 0.8
0.4 0.4
0 0
0 0.4 0.8 1.2 1.6 2 2.4 0.05 0.15 0.55 2.15
DIN (mmolN m−3) Nopt (mmolN m−3)
Fig. 2. Optimal niches of nutrient concentration (Nopt ; mmol N m−3 ) from gleaners to opportunists as a function of dissolved inorganic nitrogen DIN, and optimal niches of
temperature (Topt ; ◦ C) from colder to warmer preference as a function of sea surface temperature SST for the highest functional diversity phytoplankton community. (a)
The resource uptake [d−1 ] curves of the four uptake strategies result from a trade-off between uptake affinity and maximum growth rate ( · max = constant): slow-growing
gleaners are superior competitors at low nutrient concentration because they have a higher nutrient affinity, while fast-growing opportunists are superior competitors at
high nutrient concentration because they have a higher maximum growth rate. Thus each max corresponds to a different Nopt . (b) The competitive fitness d−1 of the uptake
strategies depends on the nutrient concentration (e.g. when DIN = 0.05 mmol N m−3 the fastest uptake corresponds to nutrient gleaners; when DIN = 2.15 mmol N m−3 the
fastest uptake corresponds to nutrient opportunists). (c) The fitness factor [n.d.] (i.e. competitive fitness normalized by its maximum value) reveals more clearly the nutrient
niches as a function of the resource uptake strategy. (d) The fitness factor [n.d.] of the thermal niches depends on the ocean temperature. A total of four optimal uptake
strategies (c) and four optimal temperature preferences (d) lead to a combination of 4 × 4 =16 ecological niches (Nopt , Topt ), each of them filled by one of the 16 phytoplankton
species present in the community.
curves to intersect (Sommer, 1986; Grover, 1997). For this growth- all become perfectly redundant (Thebault and Loreau, 2005). For
affinity or “gleaner-opportunist” trade-off (Grover, 1997; Litchman the highest diversity there is only one possible set of phytoplankton
et al., 2015), the optimal nutrient concentration of each species species that can fill all the 16 (Nopt , Topt ) niches, one per species (see
corresponds to their half-saturation constant for nutrient uptake, Table S1 in Supplementary Material). At the other extreme, how-
unless all species have exactly the same uptake strategy because ever there are 16 possible combinations of phytoplankton species
then the very concept of Nopt vanishes. Therefore, max alone deter- for the lowest functional diversity, each corresponding to one of the
mines the nutrient uptake curve and thus the Nopt (see Fig. 2). A 16 (Nopt , Topt ) ecological niches to where all the species in the com-
gleaner-opportunist trade-off has been suggested to explain the munity can functionally converge (see Table S2 in Supplementary
observed succession of phytoplankton species in natural commu- Material). Since we change functional diversity in 8 incremental
nities (Sommer, 1981; Smayda and Reynolds, 2001), and has been steps along each environmental axis independently (see Fig. 1), this
confirmed in the laboratory using chemostat competition experi- led to a total of: 8 × 8 ×16 = 1024 individual simulations that were
ments where the gleaner wins under steady-state nutrient supply performed to cover the whole range of community combinations
and the opportunist wins under pulsed nutrient supply (Sommer, (see Figs. S3 and S4).
1984, 1985, 1986; Cermeno et al., 2011). When placed together, a The interplay of competition and filtering leads to asynchrony
continuum of these resource uptake strategies leads to different by confining species to their particular nutrient and thermal niches.
nutrient niches from low to high concentration through resource However, nutrient optima differ from temperature optima in which
competition (see Fig. 2c). Similarly, a continuum of thermal optima they only appear when different nutrient uptake strategies are
leads to different temperature niches under environmental filtering present together in the same phytoplankton community; other-
(see Fig. 2d). wise when just one uptake strategy is present, there are no Nopt
Decreasing the level of functional diversity of the phytoplankton niches as such. That means that when all species are ecologically
community means increasing the similarity of the species until they equivalent in their uptake strategy, resource competition is neu-
S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196 187
Table 1
Ecosystem model state-variables.
tral. Under these conditions any one single uptake strategy can
freely occupy the whole range of nutrient concentrations. This is
because the species fundamental niche (Hutchinson, 1957) for nutri-
ents is given by their resource uptake curves, which are open-ended
to the right (i.e. high nutrient concentrations are not harmful for
growth; see Fig. 2a). Therefore all species share and could poten-
tially grow over the whole range of nutrient concentration that
is above its basal requirements. Only when species with different
uptake strategies are placed together, will the species be pushed
to their particular optima of nutrient concentration where they are
the best competitors, that is, to their realized niche (Hutchinson,
1957). However, it is worth mentioning that solar radiation is also
a growth-limiting resource, although here assumed to be affect-
ing equally all species. Therefore, there is an implicit potential
resource-ratio differentiation among species. Thermal optima, on
the other hand, are intrinsic properties that do not depend on the
other species Topt . The thermal fundamental niche of species is
given by their Topt ± a tolerance range above or below which the
species cannot grow. This leads to distinct closed-ended negative-
skew Gaussian bell curves, regardless of who else is present in
the community. Higher diversity of temperature preferences may
narrow the thermal realized niches of each species but will at
the same time increase the coverage of the temperature gradient
by the whole phytoplankton community. When only one thermal Fig. 3. Seasonal environmental forcing of photosynthetically active radiation (top
panel), ocean temperature (middle-top panel), turbulent diffusivity (middle-bottom
preference is present in the community, large segments of the
panel), and seasonal variability of community-level primary production (bottom-
temperature gradient will be devoid of any phytoplankton species panel) for the highest functional diversity phytoplankton community. The vertical
(Isbell et al., 2017). This distinction between shared (open-ended) axis represent depth [m]. The white continuous line gives the depth of the mixing
fundamental niches for nutrients and distinct (closed-ended) fun- layer. The winter turbulent mixing brings nutrients to the ocean surface that are
damental niches for temperature (Wisheu, 1998) is important to taken up by the phytoplankton community during the spring bloom when solar
radiation is increasing and the mixing layer depth is decreasing (Behrenfeld and
understand their effect on ecosystem functioning.
Boss, 2014). Production decreases over summer due to nutrient exhaustion after
vertical sinking of senescent phytoplankton cells as detritus. The secondary autumn
3. Methods bloom in production results from the deepening of the mixing layer that brings
nutrients to the surface when solar radiation is decreasing but still high enough to
sustain production.
3.1. MIT ecological selection model (MITesm)
Table 3
Ecosystem model parameters.
all phytoplankton species with killing-the-winner (KTW) preda- the optimal irrandiance for growth, after which phytoplankton
tion strategy (see Eq. (25), where parameter ˛ >1 implies active populations suffer photoinhibition. Solar irradiance is subjected
prey-switching). The generic carnivore zooplankton feeds upon the to vertical exponential attenuation due to water absortion and
herbivore zooplankton and upon itself acting as a closure term phytoplankton self-shading (Eq. (23)). Light harvesting capabilities
(see Eq. (26)) (Vallina et al., 2014b). The model mass currency is are common to all phytoplankton species and phytoplankton self-
nitrogen and it resolves four types of abiotic compounds: nitrates shading is also assumed to affect equally all species. Thus there
(NO3 ), ammonium (NH4 ), dissolved organic nitrogen (DON) and is no differential fitness along the solar radiation environmental
particulate organic nitrogen (PON) (Eqs. (3)–(6); respectively). The gradient. The coupled biophysical model was run for 4 years until
model assumes Monod kinetics for the uptake of dissolved inor- reaching a repeated seasonal cycle of the population dynamics. The
ganic nitrogen (DIN = NO3 + NH4 ) and therefore uptake and growth input data used as environmental variables for the model (i.e. solar
are assumed to be coupled (Eqs. (14) and (15)). There is only one irradiance, sea temperature, turbulence) were numerically gener-
nutrient uptake affinity (j = maxP
/KPj ) for each species j which ated to simulate a seasonal forcing characteristic of subtropical
j
applies for both nitrate and ammonium. However, ammonium is regions. The model is written in Matlab/Octave computer program-
assumed to be taken up preferentially over nitrate (Eqs. (15) and ming language.
(14)) (Vallina and Le Quéré, 2008). Temperature preferences (Fig. 3)
follow negative-skew gaussian bell curves (Eq. (17)) where Topt 3.2. Species-trait variability
defines the optimal temperature for growth and T the temper-
ature tolerance range (Eq. (22)). Solar radiation limitation follows a Functional diversity refers to phytoplankton species-trait
positive-skew non-gaussian bell curve (Eq. (16)) where Iopt defines variability along two environmental gradients independently: dis-
S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196 189
solved nutrient concentration and ocean temperature. Regarding h =− f(x, y) lnf(x, y)dx dy of the bivariate gaussian probability
the uptake strategy, there is a transition from resource gleaners density function f(x,y) that was fitted to the observed species distri-
to resource opportunists. The diversity in nutrient uptake strate- bution of each annually-averaged phytoplankton community (see
gies results from a “gleaner-opportunist” trade-off that provides Fig. 6). The gaussian approximation is fairly accurate and leads to
each phytoplankton species with a particular nutrient niche: slow- a good agreement between the observed and predicted biomass
growing nutrient gleaners are superior competitors at low nutrient of each phytoplankton species (see Fig. S1). The effective richness
concentration because they have a higher nutrient affinity, while was computed as the exponential of the Shannon (i.e. discrete)
fast-growing nutrient opportunists are superior competitors at entropy (Shannon, 1948) H =− pj lnpj , where pj is the proportion
high nutrient concentration because they have a higher maximum of species j in each annually-averaged phytoplankton community.
growth rate (Litchman et al., 2015). This growth-affinity trade- The discrete (Shannon) entropy gives a measure of the richness
off ( · max = constant) implies that the species-trait maximum and evenness of species in each phytoplankton community, while
growth (max ) alone is enough to define the nutrient uptake curve the continuous (differential) entropy gives a measure of the rela-
(see Fig. 2a) and thus the optimal nutrient concentration (Nopt ) of tive spread of the species’ functional traits. The realized functional
any given uptake strategy (see Fig. 2d). The diversity in tempera- diversity (continuous entropy) and the effective richness (discrete
ture preferences results from different temperature optima (Topt ) entropy) display the same seasonality for the highest diversity sim-
with a tolerance range (see Fig. 2c). ulation (not shown). However, for the lowest diversity simulation
There are four Nopt and four Topt (see Fig. 2) which leads although the effective richness is maximum (16 species), the func-
to 4 × 4 =16 species, each with a particular nutrient-temperature tional diversity is minimum (zero) because all the phytoplankton
optimal niche when they are ecologically different. We decrease species are ecologically equivalent and therefore there is no spread
functional diversity in 8 steps along each axis (nutrient and tem- in the species’ traits; which also implies that there is no seasonal
perature) independently until making all species converge to the pattern in either measure of diversity.
same max and Topt , which leads to 8 × 8 =64 functional diversity
levels (see Fig. 1) for each final nutrient-temperature niche where 4. Results
all species become perfectly redundant (full niche overlapping).
Therefore the variability of niches (16) and functional diversities The model simulates the seasonal dynamics of open ocean
(64) leads to a total of 16 × 64 = 1024 individual simulations. For mid latitudes using a 1D (depth-resolved) setup (see Fig. 3). Solar
each simulation we compute the functional diversity (potential radiation increases from winter (December through February) to
and realized) of the annually-averaged phytoplankton community, summer (June through August), which leads to an increase of sea
the effective richness, the annually averaged community-level pro- surface temperature, stratification and shallowing of the mixing
duction (mmol C m−3 d−1 ) and its temporal stability (i.e. inverse of layer depth, and a decrease of turbulent diffusion. The combination
the coefficient of variation) (see Figs. S3 and S4 in Supplemen- of solar radiation, ocean temperature and vertical mixing controls
tary Material). The potential functional diversity
was measured the seasonal dynamics of community-level primary production,
as the euclidean distance d = ( (xj − x̄)2 + (yj − ȳ)2 )/2 of which we show for the marine phytoplankton community with
the species-traits, where x = Nopt (in log scale) and y = Topt (in lin- highest functional diversity (see Fig. 3 – bottom panel). The annual
ear scale) (see Fig. 1). Note that Nopt is directly related to max peak of strongest turbulent diffusion during late winter brings
and equal to the half-saturation constant for nutrient uptake KP . nutrients to the surface and disrupt predator–prey coupling, fuel-
The realized functional diversity was measured as the exponen- ing the phytoplankton spring (March through May) bloom when
tial of the differential (i.e. continuous) entropy (Shannon, 1948) solar radiation starts to rise (Sverdrup, 1953; Behrenfeld and Boss,
2014). The shallow mixing layer and weaker turbulent diffusion
Fig. 4. Seasonal community-level primary production (mmol C m−3 d−1 ) after grouping the species according to their thermal preference (given by their temperature optima)
and uptake strategy (given by their maximum growth rate). The upper panels show the segregation of thermal niches that result solely from changes in ecological fitness due
to environmental filtering (i.e. for a given thermal niche, all uptake strategies are present in the community). The lower panels show the segregation of nutrient niches that
result solely from changes in ecological fitness due to resource competition (i.e. for a given uptake strategy, all thermal niches are present in the community). Environmental
filtering leads to species asynchrony by confining the species to the thermal range where they can grow (and are filtered out elsewhere). Resource competition leads to
species asynchrony by confining the species to the nutrient concentration range where they are superior competitors (and are competitive excluded elsewhere).
190 S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196
Fig. 5. Phytoplankton annual community-level primary production (mmol C m−3 d−1 ), its temporal stability seasonal cycle (inverse of the coefficient of variation normalized
by its maximum value; n.d.), and the ratio of temporal variability (CV) at the population-level over the community-level (n.d.) as a function of the diversity in thermal
preferences (horizontal axis) and the diversity in nutrient uptake strategies (vertical axis). This figure gives the median values resulting from the 1024 simulations that
were performed (see Figs. S3 and S4). Increasing the diversity of thermal preferences of the phytoplankton community (horizontal axis) leads to a strong increase in the
community-level production, its temporal stability, and to the stabilization of aggregate community-level production respect to population-level production. Increasing the
diversity of uptake strategies of the phytoplankton community (vertical axis) leads to a weaker increase in the community-level production, its temporal stability, and to a
weaker stabilization of aggregate community-level production respect to population-level production.
during summer leads to a minima in phytoplankton production nity, while the exponential of the Shannon (i.e. discrete) entropy
because nutrients are scarce due to vertical sinking of detritus gives a measure of its effective richness (see Fig. 6).
particles outside the euphotic layer before they can be fully rem- The impact of functional diversity on ecosystem production
ineralized. A weaker secondary peak in phytoplankton production and stability therefore depends on the type of functional diversity
happens during autumn (September through November) when a we are evaluating: uptake strategy versus temperature preference.
seasonal breaking of the strong summer thermocline by turbulent Higher functional diversity of temperature optima leads to a higher
diffusion brings nutrients back to the surface when solar radiation and more stable community-level production than lower diversity
is still high enough to sustain primary production before winter of temperature optima (see Fig. 5). This happens for all the com-
comes and light limitation becomes too severe for phytoplankton to binations of the lowest functional diversity of temperature optima
grow. Although community-level primary production for the high- (see Figs. S3 and S4 in Supplementary Material). On the other hand,
est functional diversity displays a smooth seasonal variability, the varying the diversity of nutrient uptake strategies has a weaker
individual population dynamics varies considerably as each species effect on both production and stability (see Fig. 5). When the lowest
occupies a particular (Nopt , Topt ) niche (see Fig. S2 in Supplementary diversity of resource uptake strategies corresponds to a community
Material). with all species following an opportunist strategy, the community-
By grouping the species according to either their thermal optima level production and its stability is almost indistinguishable from
or uptake strategy we can isolate the segregation of niches that that of a community with all resource uptake strategies present
occur both along a temporal gradient of temperature (thermal (i.e. from gleaner to opportunists) (see Figs. S3 and S4 in Supple-
niches) and along a temporal gradient of resource concentra- mentary Material). Therefore even though the presence of several
tion (nutrient niches) (see Fig. 4). Species asynchrony along the uptake strategies should theoretically lead to a higher and more
temperature and nutrient gradients are the result of the inter- stable total community-level production through temporal selec-
species competitive interactions and ecological fitness. The change tion and dominance of the most efficient strategy, in practice this
in species fitness along the temperature gradient is due to environ- positive influence of a higher diversity of uptake strategies is small.
mental filtering of the different thermal preferences. The change This contrasts with the strong positive influence that a higher diver-
in species fitness along the nutrient gradient is due to the resource sity of temperature optima has on the community-level production
competitive ability of the different uptake strategies. Yet, resource and its temporal stability.
competition also occurs among species with different temperature Increasing the potential diversity of thermal and/or uptake
optima if their thermal niches overlap, although this does not alter strategies preferences of the phytoplankton community leads to
their intrinsic Topt . However, it can alter the width of their response a linear increase of the realized functional diversity while the
curve through niche contraction and therefore their location along effective richness remains rather constant and close to its max-
the temperature gradient. Both fundamental niche differences and imum value (see Fig. 6). Higher diversity of thermal preferences
resource competition thus act simultaneously when species differ has a “direct” positive effect on ecosystem functioning on a sea-
in their nutrient uptake strategy and thermal optimum. For the sonal basis because it leads to niche complementarity of the species,
highest functional diversity simulation, each local (depth, time) which allows covering the whole temporal gradient in tempera-
phytoplankton community contains a subset of the total integrated ture. Otherwise some seasons of the year would be void of any
species richness over time due to local selection and dominance of phytoplankton species, leading to suboptimal use of the nutrients
the most efficient strategies. The annually-averaged phytoplank- and higher volatility of community-level production. This direct
ton community contains all the species that were locally successful positive effect leads to a strong increase in the median value of pri-
at some point through the year, and their observed distribution mary production and its stability with Topt diversity, and also to a
can be approximated by a gaussian probability density function similar increase of both the minimum and maximum values of the
pdf(Nopt , Topt ) (see Section 3). The exponential of the differential distribution (see Fig. 7). Covering the temporal gradient of nutri-
(i.e. continuous) entropy of the probability density function gives a ent concentration, on the other hand, does not require a diversity
measure of the realized functional diversity of the annual commu- of uptake strategies because any strategy can do so. Yet, a higher
diversity of uptake strategies still has a positive “indirect” influence
S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196 191
Fig. 6. Functional diversity (exponential of the differential entropy of the continuous probability density function pdf(Nopt , Topt ), normalized by its maximum value; n.d.) and
effective species richness (exponential of the Shannon diversity index; # species) for the annually-averaged phytoplankton community as a function of the diversity in thermal
preferences (left panels) and the diversity in nutrient uptake strategies (right panels). This figure gives the distribution of values resulting from the 1024 simulations that
were performed. The red dots correspond to the median value of the distribution. The gray shaded area spans from the minimum to the maximum value of the distribution.
Increasing the diversity of thermal and/or uptake strategies preferences of the phytoplankton community leads to a strong increase in the median, minimum and maximum
value of the functional diversity while the effective richness remains constant and close its maximum value. (For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article.)
on ecosystem functioning through a sampling probability effect: but fails to survive even in the absence of neighbours; competi-
the more uptake strategies are potentially available, the higher the tive exclusion occurs when a species arrives and can persist in the
chance of sampling a faster-growing opportunist strategy (Tilman absence of neighbours but not in their presence (Kraft et al., 2015).
et al., 1997). This indirect positive effect leads to a strong increase The interplay of competition- and filtering-driven fitness leads to
in the minimum value of production and its stability with Nopt the ecological selection of species, a concept that refers to changes
diversity, but to a weak increase of the median values of the dis- in dominance and species composition due to survival selection
tribution, and has no effect whatsoever on the maximum values of on ecological time-scales driven by differences in species traits
the distribution (see Fig. 7). (Loreau and Hector, 2001; Litchman et al., 2015). The rate of com-
petitive exclusion is slower for species with similar fitness (Kraft
et al., 2015), which has significant implications for the coexistence
5. Discussion
of phytoplankton species in the ocean (Barton et al., 2010).
Phytoplankton species have been described to fill distinct
Community assembly theory suggest that the two main pro-
ecological niches of temperature-, light-, and nutrient-optima
cesses that determine the distribution of species are ecological
(Johnson et al., 2006; Irwin et al., 2015) leading to niche parti-
fitness by resource competition ability and environmental filter-
tioning along environmental gradients, which has been modelled
ing (Cornwell et al., 2006; Kraft et al., 2015). Priority effects such
mechanistically (Follows et al., 2007). Our simulations also show
as species invasion order are suggested to be of minor importance
that a diversity of uptake strategies leads to species segregation
for phytoplankton (i.e. being the first species to invade does not
along the resource concentration gradient, while a diversity of
guarantee ecological success) (Robinson and Edgemon, 1988). Inva-
thermal preferences leads to species segregation along the temper-
sion rate can, however, alter species composition due to transient
ature gradient (Fig. 4). The best adapted species to each particular
dynamics sustained by oceanic dispersal (Robinson and Edgemon,
environment or ecological niche tend to dominate the community
1988; Clayton et al., 2013; Levy et al., 2014). Environmental filter-
(Fig. S2 in Supplementary Material). Therefore, temporal selection
ing refers to the abiotic factors that prevent the survival of species
and dominance of ecologically superior phytoplankton species is
in a particular environment in the absence of biotic interactions,
expected to affect the average production and stability of a com-
while competitive exclusion refers to the biotic interactions that
munity of primary producers over a seasonal cycle that generates
prevent the survival of species in a particular environment. Envi-
contrasting environmental conditions. More diverse communities
ronmental filtering occurs when a species arrives at a focal site
192 S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196
Fig. 7. Phytoplankton annual average community-level primary production (mmol C m−3 d−1 ) and its temporal stability (inverse of the coefficient of variation normalized
by its maximum value; n.d.) as a function of the diversity in thermal preferences (left panels) and the diversity in nutrient uptake strategies (right panels). This figure gives
the distribution of values resulting from the 1024 simulations that were performed (see Figs. S3 and S4 in Supplementary Material). The red dots correspond to the median
value of the distribution. The gray shaded area spans from the minimum to the maximum value of the distribution. Increasing the diversity of thermal preferences of the
phytoplankton community leads to a strong increase in the median, minimum and maximum value of the community-level production and its temporal stability over a
seasonal cycle. Increasing the diversity of uptake strategies of the phytoplankton community leads to a strong increase of only the minimum value of the community-level
production and its temporal stability over a seasonal cycle, to a weak increase of the median value, and has no effect on the maximum values of the distribution. (For
interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
from a functional point of view should theoretically be more capa- (Loreau, 2010; Dutkiewicz et al., 2009). Functional compensation
ble of coping and taking advantage of this environmental variability is in turn the basis for the suggested insurance that biodiver-
than less diverse communities (Yachi and Loreau, 1999). More sity provides to ecosystem functioning (Yachi and Loreau, 1999).
functional roles, however, may help sustain ecosystem processes When species respond asynchronously, the average community-
under variable environmental conditions in the long run at the level production over a seasonal cycle should be expected to be
expenses of decreasing ecosystem performance locally (Ulanowicz higher (enhancement effect) and less variable (buffering effect)
et al., 2009). This has been suggested in the context of information than when species respond synchronously (Yachi and Loreau,
theory (IF) as a competitive balance between “effective perfor- 1999). The enhancement effect of biodiversity results from tran-
mance” and unutilized “reserve capacity” of any complex system sient selection and dominance of the most productive species,
based on flow networks, such as ecosystem foodwebs (Zorach and while the buffering effect results from compensatory dynamics
Ulanowicz, 2003). Basically, higher diversity is regarded as a way to (Loreau, 2010). Furthermore, having a high functionally diverse
store potential ecosystem functioning by paying the price of losing community has been suggested to lead to lower variability (high
ecosystem performance locally. This view has led to the suggestion stability) of community-level production, while leading to higher
that ecosystems have a domain termed “window of vitality” that variability (low stability) of the individual populations (Loreau,
delimit a region of network complexity for which the ecosystem 2010). Our results do show that phytoplankton functional diversity
functions in the most sustainable way by optimizing this balance increases the ratio of population- over community-level tempo-
between opposite forces (Zorach and Ulanowicz, 2003; Ulanowicz ral variability of primary production (see Fig. 5). This reconciles
et al., 2009). early theoretical works that suggested that diversity should lead to
Differences in species fundamental niches may lead to dif- ecosystem instability (Hutchinson, 1961; May, 1974; Tilman, 1982)
ferences in realized temporal niches because the species will with observations in the field that suggest otherwise (Tilman et al.,
thus respond asynchronously to changes in the environmental 2006).
conditions (Loreau, 2010). This temporal asynchrony in species Are functionally-rich ecosystems more capable of both buffer-
environmental responses is the basis for functional compensa- ing environmental variability (increase stability) and enhancing
tion among competing species and explains their co-existence ecosystem functioning (increase production) than functional-poor
under non-equilibrium (e.g. seasonal) environmental conditions ecosystems? Our results suggest they do, yet the strength of the
S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196 193
relationship between diversity and ecosystem functioning may tional diversity can also affect ecosystem functioning at shorter
depend critically on the type of niche and functional diversity we time-scales closer to the generation times of planktonic organ-
are evaluating. Functional diversity along a climatic gradient such isms being subject to high-frequency perturbations (Smith et al.,
as temperature, for which species have distinct niches subject to 2016). Our numerical experimental design is relatively specific;
environmental filtering, does lead to higher community-level pro- it evaluates the effect of phytoplankton diversity on ecosystem
duction and temporal stability. A community composed by species functioning along only two environmental gradients: nutrient con-
that differ in their thermal optima will display functional compen- centration and ocean temperature. Real ecosystems have, however,
sation through time by which there is always at least one species many environmental axes and therefore the niche space can be
that finds the current environmental conditions optimal for growth, huge and possibly n-dimensional. Phytoplankton species can com-
while the rest of species grow sub-optimally due to environmental pete for several essential nutrients (C, N, P, etc.); be subject to
filtering. Thus, the community as a whole will be able to use the environmental filtering by solar radiation, pH, or some other cli-
resources over a seasonal cycle more efficiently than a diversity- matic metric; may have different strategies for intracellular storage
poor community composed of species that only survive during a of nutrients; may have different defense strategies; etc. However,
short temporal window (only winter or only summer). Therefore, exploring high-dimensional niche spaces is probably beyond the
ecological selection of complementary species mediated by envi- means of simple numerical simulations. Exploring extensively our
ronmental filtering along a thermal gradient has a strong positive 2-dimensional niche space already required over one thousand
effect on ecosystem productivity and stability. simulations. Higher food web trophic levels will add another level
On the other hand, functional diversity along a resource gradi- of complexity. Yet our results may be generalized to many different
ent such as nutrients for which species have shared niches, lead to environmental gradients. The key aspect of our study is: either the
a weaker positive effect of diversity on community-level primary fundamental niche (i.e. in the absence of species interactions) along
productivity and stability. A phytoplankton community composed a given environmental gradient is “closed-ended” or it is “open-
of species that differ in their nutrient uptake strategy will also dis- ended”. The diversity of closed fundamental niches has a stronger
play functional compensation through time because there is always effect on ecosystem functioning than the diversity of open funda-
at least one dominant species that finds the current environmental mental niches. This conclusion should hold for any environmental
conditions optimal for growth, at the expense of other species not gradient that falls into any of these two categories.
being at their optimal nutrient concentration. Thus, although one
would expect that in theory a community composed of species that 7. Conclusion
cover the whole range of uptake strategies should lead to a higher
productivity over a seasonal cycle by optimizing resource uptake, Functional diversity positively affects average community-level
our results suggest that the enhancement is small. As long as an production and its temporal stability over a seasonal cycle. This
opportunist strategy is present in the phytoplankton community, effect can be either strong when there is a diversity of temper-
the diversity of uptake strategies does not have a significant impact. ature preferences, or weak when there is a diversity of uptake
Thus, ecological selection mediated by resource competition abil- strategies. Temperature niches are closed-ended due to environ-
ity along a gradient of nutrient concentration has a weak positive mental filtering, while nutrient niches only become closed by
effect on ecosystem productivity and stability. resource competition. Thus, having a diversity of thermal prefer-
An additional distinction between nutrient and temperature ences allows a larger coverage of the range of temperature values.
niches is the presence of a feedback between nutrients and phyto- On the other hand, having a diversity of uptake strategies is not
plankton dynamics. That is, nutrient concentrations are consumed necessary to cover the whole range of nutrient concentration. The
and therefore affected by phytoplankton dynamics while ambient concept of thermal niche and nutrient niche are therefore quite
temperature is mostly unaffected by phytoplankton biomass (but different and care should be taken when making generic state-
see (Manizza, 2006)). This feedback combined with detritus sinking ments about the role of biodiversity on ecosystem functioning
has a tendency to favour gleaner species during summer. The onset through species functional compensation and asynchrony of their
of the spring bloom is, however, independent of this feedback since responses to the environmental conditions. Both environmental
it is controlled by vertical supply from turbulent diffusion. Thus, the filtering and resource competition can lead to functional compen-
nutrient concentration in the euphotic layer fluctuates seasonally sation and asynchrony of individual populations. However, the
as a consequence of the following processes: (i) nutrient supply diversity of environmental filtering niches (e.g. thermal optima)
(independent of biomass dynamics); (ii) primary production and affects community-level production and stability in a much larger
vertical export by sinking particles (which depends on biomass degree than the diversity of resource competition niches (e.g. nutri-
dynamics). This makes the dynamics of phytoplankton relatively ent optima).
more complex along the nutrient axis than along the tempera-
ture axis. However, this increased dynamical complexity does not Authors’ contributions
translate to a larger role of the diversity in uptake strategies for
ecosystem functioning. Thus, we can safely conclude that nutri- S.M.V.: designed the initial study. Conducted model simulations.
ent feedback has a minor role in the observed difference between Wrote first draft of the manuscript. P.C.: provided feedback on the
temperature and nutrient niches for primary production. study design. Contributed to data analysis and interpretation of
results. S.D.: provided feedback on the study design. Contributed to
data analysis and interpretation of results. M.L.: provided critically
6. Limitations and generality important intellectual content. Contributed to the interpretation of
results. J.M.M.: provided critically important intellectual content.
Our study measures the effect of phytoplankton functional Contributed to the interpretation of results. All authors discussed
diversity on ecosystem-level productivity and stability at seasonal the results, reviewed the manuscript, and contributed to its subse-
time-scales, which provides large although low-frequency envi- quent revisions.
ronmental variability. The focus was placed on community-level
primary production and its stability because phytoplankton is at Conflict of interest
the base of the trophic foodweb. Marine ecosystems are generally
at seasonal steady-state (i.e. annual mass balance). However, func- The authors declare no competing financial interests.
194 S.M. Vallina et al. / Ecological Modelling 361 (2017) 184–196
We thank Jim P. Grover and one anonymous reviewer for FPj = FPNO3 + FPNH4 (7)
j j
their constructive review. This work was funded by national
research grants CGL2013-41256-P (MARES) and CTM2014-54926- FPNO3 = max (QPNO3 QPSST Q PAR )Pj (8)
j P j j j
R (SUAVE) from the Spanish government. S.M.V. and P.C. are
supported by «Ramon y Cajal» (RyC) contracts from the Spanish FPNH4 = max (QPNH4 QPSST Q PAR )Pj (9)
j P j j j
government. S.D. was supported by NSF (grant 1434007) from the
United States government. M.L. and J.M.M. are supported by the
FPNO3 = FPNO3 (10)
French Laboratory of Excellence project «TULIP» (ANR-10-LABX-41; j
j
ANR-11-IDEX-0002-02). M.L. was also supported by the BIOSTASES
Advanced Grant, funded by the European Research Council under
FPNH4 = FPNH4 (11)
the European Union’s Horizon 2020 research and innovation pro- j
j
gramme (grant agreement No 666971) and J.M.M. by the Region
Midi- Pyrenees project (CNRS 121090).
FP = FPj (12)
j
Appendix A. Ecosystem model equations
QPDIN = QPNO3 + QPNH4 ≤ 1 (13)
A.1 Ecosystem model equations j j j
∂Pj NH4
= FPj − EPj − GPj − MPj + ∇ z (∇ z Pj ) (1) QPNH4 = (14)
∂t j KPDIN + NH4
j
∂Zj
= FZj − EZj − GZj − MZj + ∇ z (∇ z Zj ) (2) NO3
∂t QPNO3 = (1 − QPNH4 ) (15)
j KPDIN + NO3 j
j
∂NO3
= −FP
NO3
∂t I I
Q PAR = exp 1− ≤1 (16)
+ε(P→NO3 ) EP Iopt Iopt
+˝(P→NO3 ) MP
1
pdf (x) = √ exp(−x2 /2) (18)
(3) 2
+˝(Z→NO3 ) MZ
1
+ı(PON→NO3 ) MPON cdf (z) = (1.0 + erf (z)) (19)
2
+ı(DON→NO3 ) MDON
(exp(z) − exp(−z))
erf (z) ≈ tanh(z) = (20)
+ı(NH4 →NO3 ) MNH4 (exp(z) + exp(−z))
√
x
+∇ z (∇ z NO3 ) T
z= log(2) √ (21)
2
∂NH4 NH4
= −FP − MNH4 T − Topt
∂t x= (22)
T
+ε(P→NH4 ) EP + ε(Z→NH4 ) EZ ⎛ ⎞
(4)
z
+˝(P→NH4 ) MP + ˝(Z→NH4 ) MZ
I = I0 exp ⎝− (kw + kp Pj )dz ⎠ (23)
+ı(PON→NH4 ) MPON + ı(DON→NH4 ) MDON 0
j
+∇ z (∇ z NH4 )
A.3 Zooplankton production (preyi , predatorj )
∂DON
= −MDON
∂t QZj = QZPi + QZZi = QZtot ≤ 1 (24)
j j j
+ε(P→DON) EP + ε(Z→DON) EZ i i
+˝(P→DON) MP + ˝(Z→DON) MZ
(5) ij Pi˛
QZPi = QZtot (25)
j ( k
kj Pk˛ + ϕ Z˛)
k kj k
j
+ı(PON→DON) MPON
ϕij Zi˛
+∇ z (∇ z DON) QZZi = QZtot (26)
j ( k
kj Pk˛ + ϕ Z˛)
k kj k
j
∂PON ˇ
= −MPON ( kj Pk + ϕ Z )
∂t k k kj k
QZtot = (27)
j ˇ ˇ
+ε(P→PON) EP + ε(Z→PON) EZ KZ + ( P +
k kj k
ϕ Z )
k kj k
(6) j
+˝(P→PON) MP + ˝(Z→PON) MZ
GPi = (max
Z Zj )QZPi (28)
j j
+∇ z (∇ z PON) + ω∇ z PON j
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