Discussion
Whilst we already knew from studies on particular subsets of communities
that non-trophic indirect effects must be important for understanding
community structure and dynamics this is thought to be the first truly
empirical study to demonstrate, for an entire community, how numerous
HOIs are acting at the same time. Here, we not only explored
community-wide effects but experimentally tested each of the interaction
modifications identified in situ in the field. By performing several
manipulations concomitantly under natural field conditions, we were able
to study the same interactions in different contexts and detect how
multiple non-trophic interactions can interfere with or modify a single
pairwise interaction. Thus, HOIs are not particular to certain sets of
species but rather an integral part of communities. The manipulations
revealed a hidden network of HOIs modifying the direct interactions, as
well as modifying each other, a level of complexity unexplored in
empirical studies and seldom mentioned in theoretical studies. Whilst
our study system focused on an insect community on a tropical shrub, a
hidden network of HOIs will occur in all ecological communities, and
therefore our results are of huge ecological relevance. The removal of
different groups indirectly affected the interactions between several
other pairs of groups with which the manipulated groups did not directly
interact. That indicated that the species are indirectly connected and
pairwise interactions are context-dependent. We acknowledge that the
three density effect links in the network may represent species
association and not true links (it would be difficult to differentiate
between the two), which would mean that the groups do not actually
affect one another directly and may be both affected by a third group.
However, we include these links, first, because it would be difficult to
clarify whether that is the case and, second, because the fact that a
node changes in the absence of other groups shows that they are somehow
connected, therefore there is potential for indirect interaction, albeit
via additional intermediate groups. Also, the HOIs are represented by
straight arrows in the network, but in reality, multiple steps may be
involved in their effect propagation pathways. What the arrow represents
is that the pairwise interaction is affected by the third group. This
level of detail on indirect non-trophic interactions, and in particular
for HOIs, for such a species-rich multi-trophic system, is truly
unsurpassed.
It seems almost impossible to determine how a species affects another
when we consider that all those non-trophic indirect effects may be
taking place at the same time and interfering with each other. Besides,
the links represented in the network may vary in magnitude through time,
or may even be transient . In the community studied, population
densities at a given time are influenced by the sum of several indirect
effects taking place at that time. If this is the case for natural
systems in general, no inference can be made on the magnitude or
direction of a given interaction in nature by studying it in isolation
such as in an experimental setting or in computational models. Thus,
depicting direct links between species in a network may be a
misrepresentation of species effects or roles at the community level.
The existence of this hidden network suggests that, in natural
conditions, it is not very likely that one species alone can determine
the persistence of any other, such as in competitive exclusion. The role
of competition in species coexistence has been widely demonstrated for
focal species , but rarely in species-rich communities . Here we show
that HOIs can hugely increase the context-dependency of pairwise
interactions, and by modifying interactions and offsetting or
complementing each other, can allow a flexible modulation of species
coexistence. Thus, the hidden network of HOIs very likely plays a
crucial role in diversity maintenance in multispecies communities.
It is imperative to devise methods to harmonize pairwise interaction
networks with the hidden network of HOIs. This would allow us to
recognise fundamental mechanisms involving non-trophic interaction
modulation that, for instance, allow the community as a whole to respond
to a specific manipulation such as the removal of a species. Advancing
our understanding of such mechanisms is likely to elucidate the
underlying causes of stability and persistence of ecological communities
and increase our ability to predict how they might respond to
perturbations. Computational simulations that account for HOIs are
helpful, but the results presented here suggest that empirical data will
be key to our understanding because of the numerous and often
unpredictable opportunities for indirect effects via a variety of
mechanisms and pathways.
Community ecology research rarely studies entire communities, in part
due to the logistical problems involved in studying multispecies
systems, but mostly due to the lack of tools to approach the complex
intricacies of ecological communities. The results gathered here are
unique, as the experimental exclusion of more than one group was
performed concomitantly in the field in a self-contained but diverse
system, and the densities of almost all groups of species were
monitored. The challenges of replicating this study in a larger or less
self-contained community are evident, but should not be a barrier to
further empirical investigation into the generality of the findings
presented here. We hope that this study will instigate new methodologies
for more holistic approaches to studying ecological communities in
general. The changes identified here could not be predicted from
analyses of pairwise networks. Unlike pairwise interactions, HOIs cannot
be predicted based on species functional traits or from previously
recorded interactions (e.g., plant pollination, predation, parasitism).
HOIs can be transient and involve effect propagation through several
intermediaries. Thus, through HOIs, species have global effects on the
community context. At the same time, these effects can vary in intensity
and direction depending on the community context (species composition
and abundances mainly) at each moment. This circular relationship
between the structure of the global system and the local interactions
among the components is typical of complex adaptive systems . Thus,
developing new methods of applying complexity theory to ecosystems could
be one way forward.