Discussion
We experimentally demonstrated that relative ecosystem size can mediate
the impact of resource flows on the function of
autotrophic-heterotrophic meta-ecosystems. Positive effects of resource
flow exchanges on meta-ecosystem total biomass were observed when the
larger patch was autotrophic, while the effects were negative when the
larger patch was heterotrophic. These findings were explained by the
coupling via resource flows between autotrophic and heterotrophic
patches increasing the local biomass density of autotrophic patches
while decreasing it in heterotrophic patches. Overall, our findings
suggest that resource flows between autotrophic and heterotrophic
ecosystems of different sizes can affect ecosystem functions at larger
scales and that the trophic balance of the larger ecosystem (net
autotrophic vs. heterotrophic) can determine the direction of the
meta-scale effect.
The negative impact of resource flows on heterotrophic ecosystem biomass
contrasts with previous results. We expected the carbon-enriched
resources from autotrophs to have a bottom-up positive effect on
heterotrophic protist biomass via a boost of the bacterial populations
they prey on (Gounand et al., 2017). We see at least two mutually
non-exclusive explanations for this counterintuitive result:
stoichiometric mismatch or oxygen limitation. A stoichiometric mismatch
would occur if imported resources dilute the limiting nutrients compared
to local resources (Pichon et al., 2023). This would mean that our
heterotrophic ecosystems were not carbon-limited, unlike in Gounand et
al. (2017). A difference with this previous experiment is the higher
diversity of our heterotrophic protist community (up to 10 protist
species compared to one or two), which could have caused more efficient
recycling (Delong & Gibert, 2019) and made the heterotrophic patch less
responsive to carbon-rich resources coming from the autotrophic patch in
the equally-dominated meta-ecosystems. Alternatively, resource flows
from autotrophic patches may have caused hypoxia through increased
bacterial growth. This might have negatively affected protist biomass in
small heterotrophic patches due to high relative carbon import and in
large ones due to pre-existing oxygen limitation from a low area-volume
ratio. Similar hypoxia from resource flows is widespread in nature, for
instance, when massive amounts of hippo faeces and urine enter confined
areas in streams (Dutton et al., 2018) or when fertilisers leach into
lakes or estuaries (e.g., Rabalais & Turner, 2019; Steffen et al.,
2012).
In contrast, the positive effect of resources coming from heterotrophic
ecosystems on the local production of autotrophic ecosystems has
consistently been observed in experiments (e.g., Gounand et al., 2017;
Harvey et al., 2016), as well as in empirical studies (Montagano et al.,
2019). This positive effect likely comes from relaxing the nutrient
limitation in autotroph species, which in our control settings might
just emerge from the differences in the stoichiometry of the abiotic
resources between ecosystem types resulting from carbon fixation and
direct use of inorganic nutrients in autotrophic ecosystems. In this
context, heterotrophic ecosystems export resources that are much richer
in nutrients relative to carbon, which should boost autotrophic
ecosystem production.
Our study suggests that resource flows between ecosystems of different
sizes can exacerbate the differences in production between
meta-ecosystems that were already present in their unconnected
counterparts. Autotrophic patches in our experiment sustained higher
biomass density than heterotrophic patches, leading to a decrease in
meta-ecosystem total biomass from autotrophic-dominated to
equally-dominated, and heterotrophic-dominated unconnected
meta-ecosystems (without resource flows connecting ecosystems). The
total biomass of a meta-ecosystem was, therefore, influenced by how much
of the size of the meta-ecosystem was allocated to the two types of
patches. Adding resource flows between patches allowed
autotrophic-dominated meta-ecosystems to become even more productive and
heterotrophic-dominated meta-ecosystems to become even less productive.
This suggests that disparities in function among ecosystems within a
landscape may arise not only from their intrinsic properties but also
from differences in their size, which influence resource flows and their
effects. Further, our findings suggest that ongoing changes to resource
flows connecting ecosystems around the world (e.g., Elser & Bennett,
2011; Peller & Altermatt, 2024; Smith et al., 2025) can significantly
impact ecosystem function across scales.
The results of this experiment also show that relative ecosystem
size influences the effects of resource flows and that it matters if the
heterotrophic or autotrophic patch is dominating in size, even when
resource flow quantities are equal and bi-directional. Unidirectional
resource flow effects on the recipient ecosystem have been shown in
field surveys and experiments to depend on the size of the ecosystem
they enter. For example, marine subsidies (e.g., seaweed detritus and
seabird fish scraps) increase secondary production the most in smaller
islands (Polis & Hurd, 1995, 1996), nitrogen brought by salmon gets
incorporated into plants and invertebrates the most in smaller river
watersheds (Hocking & Reimchen, 2009), and ocean seaweed provided to
the shores of islands increases lizards densities only on small islands
(Wright et al., 2020). Many ecosystems, however, are reciprocally
coupled, with resources flowing in both directions between ecosystems
(Gounand et al., 2020; Gounand, Little, et al., 2018). A recent protist
experiment manipulating the relative size of connected patches showed
that the connection through flows of resources could decrease the total
biomass of the meta-ecosystem (Giacomuzzo et al., 2024). While this work
explored the interaction between resource flows and ecosystem size, it
did not address the common case where the connected ecosystems differ in
type or trophic status. Our findings support the results of Giacomuzzo
et al., (2024), but significantly extend our knowledge by showing that
the trophic status of the ecosystem dominating the meta-ecosystem’s
size, can reverse the impact of resource flows on meta-ecosystem
function. Global change is altering the size of ecosystems, and our
findings suggest the potential for resource flows to mediate the effects
on ecosystem function.
An important factor to consider when interpreting these results in
relation to natural systems is the role of ecotones or the interfaces
between connected ecosystems. In our microcosm experiment, ecosystems
are relatively well-mixed and thus, resource flows can influence all
areas of the ecosystem. However, in many natural systems, the extent of
the ecotone, rather than the total size of the ecosystem, determines the
extent of coupling between ecosystems (Muehlbauer et al., 2014). For
instance, not all parts of a forest receive resource flows from an
adjacent river; rather, the sections at the interface (ecotone) are
predominantly involved (Harvey et al., 2023; Muehlbauer et al., 2014).
Consequently, it can be that in some landscapes the size of ecosystems
affected by resource exchanges is determined by the size of their
ecotones, while in others it is more affected by the spatial
structure/layout. Such finding is also consistent with continental-scale
observations that landscape diversity, that is, the diversity of
different ecosystems, per se can result in positive ecosystem function
effects (Mayor et al., 2025; Oehri et al., 2020), which has been
directly postulated through resource couplings and other cross-ecosystem
dynamics. In the context of our study, this suggests that the influence
of size may not be solely determined by the total area of autotrophic
and heterotrophic patches, but by the spatial extent of their ecotone,
where resource exchanges are most pronounced. Notably, ecotones are
recognized as relatively dynamic areas that naturally change in size
across time (Smith & Goetz, 2021). Therefore, our results can
potentially explain why resource flows have different effects at
different times (Anderson et al., 2008; Mulholland et al., 2006; Valett
et al., 2008).
In conclusion, our experiment provides experimental evidence that the
relative size of coupled autotrophic and heterotrophic ecosystems can
indirectly affect ecosystem function at local and meta-ecosystem scales.
Autotrophic and heterotrophic ecosystems are ubiquitously connected by
spatial flows of resources, yet these ecosystems commonly differ in
size—a feature that has generally been overlooked in studies of
spatial flows. Our findings underscore the importance of considering how
ecosystem size and type, as well as resource flow dynamics, interact to
drive ecosystem function across scales. By acknowledging the role of
ecosystem size and resource flows, we can better address the
complexities of ecosystem function in the context of ongoing global
change.