Introduction
In light of global change and biodiversity loss, it is a key challenge
to advance our understanding about ecosystem resilience and its
relationship with diversity. Resilience is defined as the capacity of
ecosystems to absorb changes in the environment without exhibiting large
changes in ecosystem state (Holling 1973). Biodiversity among and within
species may increase ecosystem resilience (Hughes & Stachowicz 2004;
Isbell et al. 2015), when species (or genotypes) perform similar
functions but respond differently to environmental change (Leary &
Petchey 2009). Hence, a key aspect of diversity is variation in
functional traits, i.e. the traits that determine how organisms respond
to environmental change and affect ecosystem processes (Naeem & Wright
2003; Suding et al. 2008). Corresponding research has primarily
focused on ecosystems with single equilibria (Yachi & Loreau 1999;
Loreau & Mazancourt 2013), but was recently extended to ecosystems with
alternative stable states (Dakos et al. 2019; Chaparro-Pedrazaet al. 2021). When such ecosystems experience a change in
environmental conditions, higher biodiversity may prevent or delay the
shift to an alternative ecosystem state (Figure 1; Chaparro-Pedrazaet al. 2021). Resilience is particularly crucial in these systems
because shifts to alternative states often occur abruptly, are difficult
to reverse, and can entail high costs when the ecosystem transitions to
a state that is undesired for ecological and/or economic reasons
(Scheffer et al. 1993; Foley et al. 2003; Diaz &
Rosenberg 2008).
Ecosystems with alternative stable states are characterized by
displaying two or more different states at identical external conditions
(Fig. 1a). As an environmental driver increases gradually, the ecosystem
shifts abruptly to an alternative state once a threshold, the tipping
point, is passed, but recovers to its original state only at lower
threshold conditions (Fig. 1a; Scheffer et al. 2001). Between
these two threshold values, the state of the ecosystem depends on its
history, a phenomenon termed hysteresis. A key mechanism behind
hysteresis is positive feedback between organisms and their environment
(Kéfi et al. 2016). For example, in shallow lakes submerged
plants and phytoplankton can interact via mutual inhibition (a positive
feedback), where macrophytes inhibit phytoplankton by consuming
nutrients, while phytoplankton inhibit macrophytes by reducing water
clarity (Kéfi et al. 2016). At intermediate nutrient
concentrations, shallow lakes can thus be in a clear state dominated by
submerged plants or in a turbid state dominated by phytoplankton,
depending on which of these two functional groups dominated in the past
(Scheffer et al. 1993).
Effects of diversity on the resilience of systems with alternative
stable states were addressed conceptually (Dakos et al. 2019) and
investigated with mathematical models of predator-prey systems
(Ceulemans et al. 2019; Chaparro-Pedraza 2021; Wojcik et
al. 2021) and shallow lakes (Chaparro-Pedraza et al. 2021). Two
of these studies are particularly relevant here because they analyzed
how trait change influences the position of tipping points along an
environmental gradient (Chaparro-Pedraza 2021; Chaparro-Pedraza et
al. 2021). Using three model systems (a population model, a
predator-prey model, and a model of a shallow lake ecosystem), the
authors report that trait change shifted the transition to an
alternative state to a higher level of environmental stress
(Chaparro-Pedraza 2021; Chaparro-Pedraza et al. 2021). In the
shallow lake model system the shifts from a clear to turbid state and
back from turbid to clear both occurred at higher nutrient loading when
macrophytes varied in shade tolerance (Chaparro-Pedraza et al.2021). In this example, diversity was manipulated in one functional
group. Yet, multiple functional groups may simultaneously be present,
and the effect of diversity on ecosystem resilience may be different if
more than one functional group varied in traits.
Studies on systems without alternative stable states have shown that
simultaneous changes of diversity in multiple functional groups may lead
to complex relationships between diversity and ecosystem processes
(Thébault & Loreau 2003; Ceulemans et al. 2021). Specifically,
diversity of one functional group can enhance (Eisenhauer et al.2012; Zhao et al. 2019), dampen (Bruno et al. 2008), or
reverse (Thébault & Loreau 2003) the diversity effects of another
functional group. These previous studies focused on trophic and
facilitative interactions. It is unclear, however, how simultaneous
versus independent changes of diversity play out when functional groups
interact via mutual inhibition, an interaction that is characteristic of
many ecosystems with alternative stable states (Kéfi et al. 2016;
Bush et al. 2017).
Here we investigate how trait diversity in one, two, or three functional
groups influences the resilience of ecosystems that have alternative
stable states. We used a mathematical model developed by Bush et
al. (2017) which describes abrupt oxic-anoxic regime shifts of aquatic
ecosystems in response to changes in oxygen diffusivity. In this system,
regime shifts are mediated by mutual inhibition of cyanobacteria and two
types of sulfur bacteria (sulfate-reducing bacteria and phototrophic
sulfur bacteria). The already published model (Bush et al. 2017)
assumes no trait variation within each of the three functional groups,
which is equivalent to there being only one strain in each functional
group. We extended this model to include trait variation among multiple
strains within each of the three groups of bacteria, and tested if the
effect of diversity on resilience depends on (i) the amount of trait
variation, and (ii) the combination of functional groups that contain
variation. Increased resilience can be considered beneficial when it
concerns the desired ecosystem state (oxic), but detrimental when it
concerns the undesired state (anoxic). To describe our findings, we use
the visualization framework illustrated in Figure 1 and terminology
explained in Box 1.
We focused on a model that is simple enough to give generally applicable
insights about the biodiversity-resilience relationship, but that is of
sufficient complexity and realism to provide testable hypotheses for
experiments and suggest novel approaches in ecosystem management.
Moreover, by using a model of a specific ecosystem type, we may detect
mechanisms that might be overlooked with simpler and more abstract
models. We show that diversity can both enhance and reduce resilience
depending on which and how many functional groups vary in traits, which
illustrates the importance of considering multiple groups and their
complex interactions.