Introduction
The relationship between ecosystem productivity and biodiversity has
been examined well over 1,000 times since it was proposed
(Pianka 1966;
Odum
1969), with multiple conceptual frameworks and empirical tests. Yet
evidence of its direction is inconsistent among (e.g.,
(Mittelbach et al.2001) and even within (e.g.,
Adler et al. 2011)
studies: sometimes it takes on the expected hump shape, other times a
positive relationship, while in some cases a negative or non-existent
relationship (Mittelbachet al. 2001; Gillman
& Wright 2006; Pärtelet al. 2007). These inconsistencies have led to criticism and
intense debate (e.g.,
Fridley et al.2012; Tredennick et al. 2016) behind the mechanisms underpinning
these relationships (Abrams
1995) and methodological approaches
(Whittaker 2010). Focusing
on pinpointing the mechanisms that underlie diversity-productivity
relationships could address how different biodiversity patterns emerge,
identify significance of the patterns, and allow for predictive models.
A parallel goal in population ecology is understanding mechanisms that
yield variability in the performance of individual species along
gradients of environmental stress (i.e. productivity): the
‘stress-gradient hypothesis’
(Malkinson & Tielbörger
2010). Although the stress-gradient hypothesis tends to be tested at
geographic scales and for individual species, such as across a species’
range (Ziffer-Berger et
al. 2014), similar processes likely occur within landscapes. Despite
the similar goals of these two subfields, to our knowledge, methods from
population ecology have not been applied to the study of mechanisms
underlying diversity-productivity relationships in community ecology.
To understand how methods of testing the stress-gradient hypothesis
apply to diversity-productivity relationships, it is useful to see the
net biodiversity of communities as collections of populations across
environments. If a population can persist in an environment, it adds to
the richness of the community. ‘Persistence’ is defined as a
population’s ability to maintain itself via survival and reproduction,
i.e., per capita population growth rates (λ ) ≥ 1. In studies of
the stress-gradient hypothesis, fitness is commonly measured on
individuals that have been transplanted across the stress gradient. When
averaged across individuals, absolute fitness is equivalent to per
capita population growth
(Brady et al. 2019).
By employing methods that measure persistence, we can then identify (i)
where along the productivity gradient different species are expected to
persist and whether occupancy mirrors persistence, (ii) if different
species exhibit similar or dissimilar relationships with productivity,
and consequently, (iii) what biodiversity patterns emerge as we
aggregate species together in a given environment. For example,
biodiversity-productivity relationships might emerge if species differ
in how sensitive they are to conditions across the gradient, if the
magnitude of species interactions differs between environments, or if
species are increasingly lost in poor conditions due to an increased
effect of stochasticity within smaller population sizes
(Lande 1993; Shoemakeret al. 2020). In order to make these inferences, persistence of
all species under consideration must be tested together across the
extent of the same productivity gradient. As we will describe, adopting
this approach can help answer two outstanding questions about why
populations and communities are affected by environmental gradients and
address the implicit assumption that patterns in species occurrence and
biodiversity across gradients mirror persistence.
The first outstanding question is to what extent are species
interactions (e.g. competition, facilitation) versus environmental
filtering driving biodiversity-productivity relationships. Productivity
gradients may affect biodiversity patterns directly, due to abiotic
suitability (i.e., species’ fundamental niches), or indirectly, by
modifying the strength and direction of species interactions (i.e.,
species’ realized niches)
(Chase & Leibold
2009; Germain et al. 2018; Carscadden et al. 2020).
Theory suggests that as conditions improve, communities crowd causing
competition for limiting resources
(Harpole & Tilman 2007;
Craine & Dybzinski 2013), thus reducing opportunities for niche
partitioning and coexistence
(Harpole & Tilman 2007).
Yet the intensity of biotic interactions and consequences for diversity
across productivity gradients may not be so straightforward: competition
may vary linearly or nonlinearly or even transition to facilitative
interactions (a key prediction of the stress-gradient hypothesis) with
abiotic stress
(Bertness &
Callaway 1994; He et al. 2013; Louthan et al. 2021). To
disentangle direct effects of productivity on persistence from indirect
effects through biotic interactions, one could measure λ on
populations of different species transplanted across a productivity
gradient, removing neighbors (i.e., isolating the direct component) or
leaving biotic interactions intact. Comparing these λ elucidates
how biotic interactions change in magnitude and direction across the
productivity gradient. Although intuitive and straightforward, we
emphasize that applying this kind of manipulative approach has only been
proposed to test the stress-gradient hypothesis in the last half decade
(Louthan et al.2015; Jones & Gilbert 2016), and thus, empirical applications are
still uncommon, especially when scaling from single species to a
community context. Studies taking this approach would mutually benefit
both fields.
The second outstanding question is to what degree does species richness
reflect local conditions vs. conditions at larger scales via linkages
with dispersal. More specifically, a common goal in the stress-gradient
literature is to ask if range limits (i.e., the spatial extent of a
species’ distribution) reflect niche limits, as opposed to limited
dispersal (Hargreaveset al. 2014). By transplanting individuals into locations where
absent, thereby simulating dispersal, one can ask if species can
maintain populations, and thus if dispersal limitation decreases
diversity. This method can be easily extended to test dispersal’s other
effect: the maintenance of “sink” populations due to dispersal excess
that, in the absence of dispersal, would fail to persist
(Howe et al.1991; Pulliam 2000). Sinks may be common if there is high heterogeneity
in local conditions in space or time relative to the scale of dispersal
(Jorgensen & Fath 2008;
Zelnik et al. 2021). By measuring growth rates of transplanted
individuals along with species natural distributions, we can determine
how dispersal interacts with the biotic and abiotic environment to
result in biodiversity patterns
(Leibold & Chase 2017).
Compared to tests of the stress-gradient hypothesis, dispersal is less
often invoked as a mechanism affecting biodiversity-productivity
relationships (but see Pärtel
& Zobel 2007) despite being key to theories of biodiversity
maintenance (i.e., metacommunity theory)
(Leibold et al.2004; Leibold & Chase 2017).
In this study, we bridge from population to community ecology, testing
the interplay and strengths of local and regional processes that may
underlie the stress-gradient and biodiversity-productivity
relationships. To do so, we combined occupancy surveys, neighbor
manipulations, and fitness assays on transplanted individuals of four
annual plant species in a highly heterogeneous natural grassland that
spans harsh to productive serpentine habitat. We used these data to
test: (1) if species-level occupancy patterns align with persistence
under natural conditions, (2) the role of environmental filtering versus
biotic interactions in generating stress-gradient and
diversity-productivity relationships, and (3) the influence of dispersal
on diversity patterns. We predicted a poor alignment between occupancy
and persistence due to both dispersal of species beyond their niches and
transient populations caused by high spatiotemporal environmental
variability. Consistent with the stress-gradient hypothesis, we
predicted that competition would be most intense in high productivity
environments, weakening or even transitioning into facilitation in less
productive environments. Finally, paralleling metacommunity theory, we
hypothesized that dispersal would play a key role in structuring
diversity at the community level, while exploring if dispersal varies
across the productivity gradient and if dispersal excess vs. limitation
dominates. By integrating the stress-gradient hypothesis for populations
with diversity-productivity and metacommunity theory for communities, we
quantified both local and regional level processes structuring
biodiversity, thereby testing how well species occupancy mirrors
persistence and the mechanisms that may lead to mismatches.