DISCUSSION
Combining long-term multitrophic datasets and an energetic food web
approach, we explore the temporal relationship between diversity and
energy flux, and how human pressures drive such relationships. First, we
found evidence of a decline of at least 72% in the number of
top-carnivore species over 17 years, suggesting a clear process of
trophic downgrading (Estes et al. 2011). Second, the abundance of all
trophic guilds declined over time, indicating that the Río Uruguay is
consistently becoming defaunated, a similar pattern observed in other
rivers worldwide (Olden et al. 2008; Comte et al. 2021; Romero et al.
2021; Oliveira et al. 2015). Third, there were declines in energy flux
at the whole-network level and a clear mismatch in the distribution of
flux between trophic guilds. Fourth, species richness and energy flux in
all trophic guilds were positively associated. Fifth after accounting
for key drivers of diversity and ecosystem functioning, we found direct
and indirect negative effects of human footprint on species richness and
energy flux and such negative effects have intensified over time. These
results suggest long-term reductions in the diversity and functioning of
fish food webs, which is largely driven by increasing human pressures.
Our analysis revealed reductions in energy flux at the whole-network
level over time, suggesting a loss of multitrophic functionality. There
was a reduction in the amount of energy flux in all fish trophic
compartments in the last year (2021) compared to the first year (2005)
of the study (Fig. S7). In addition, the distribution of energy flux
between trophic compartments has changed over time, driven by reductions
in energy flow to the upper compartments (i.e., top- and
meso-carnivores). Consequently, the energy flux was retained at the
bottom of the food web. For instance, our analysis reveals a retention
of at last 75% of the energy flux in the omnivore compartment over
time. The reduction in the species richness and energy flux of
top-carnivores further reinforces a process of trophic downgrading and
simultaneously highlights a loss of functioning of the fish food web
(i.e., decreasing carnivory). The high concentration of energy flux to
the omnivorous species highlights their central role in food webs as
they support the energetic needs of species from higher trophic levels
(top- and meso-carnivores).
We show remarkedly consistent positive relationships between species
richness and energy flux. This indicates that the increase in diversity
causes the energy flux to intensify through the food webs. For all
trophic compartments, the energy flux peaks occurred when diversity
reached their highest values. These results underline the important role
of diversity in driving the functioning of fish food webs, as also
observed for insects (Barnes et al. 2014) and nematodes (Wan et al.
2022). The close association between diversity and energy flux also
implies that a species loss might impact the ability of fish trophic
guilds to capture and process resources, reducing the functioning of the
entire food web (Thompson et al. 2012).
We show negative effects of human footprint on species richness of
top-carnivore and mesocarnivore. The human footprint has also negatively
affected (directly or indirectly) the energy flux of top-carnivores,
mesocarnivores, omnivores and detritivores. These findings suggest that
human pressure may be the major driver of the observed temporal decline
in both diversity and ecosystem functionalities over time, and this
applies to both lower (direct) and upper (indirect) trophic
compartments. Perhaps more importantly, we have shown an increase in the
human footprint over time (Fig. S6). Moreover, the negative effects of
the human footprint on diversity and energy flux remain remarkedly
consistent even after accounting for multiple ecosystem factors. We also
demonstrate that time mediated the negative effects of the human
footprint on diversity and energy flux. This indicates that the human
footprint increased over time, and as a result its deleterious effects
on diversity and energy flux intensified. Our results expand on those of
experimental studies (e.g., Barnes et al. 2014; Polazzo et al. 2022),
suggesting that in real-world ecosystems, increasing human pressures
impair the functioning of food webs and that human impacts intensify
over time as their influence on natural ecosystems increases (Tilman et
al. 2014).
As we showed, human footprint reduced energy flux of top- and
meso-carnivore compartments through direct and diversity-mediated
indirect pathways. This suggests that human pressure has potentially
stronger impacts on diversity and energy flux of upper trophic
compartments (Strong & Frank 2010). In fact, due to lower population
sizes, carnivores are more sensitive to human pressure intensification
(Estes et al. 2003; Moi & Teixeira de Mello, 2022) and losses of
carnivore species occur in human-dominated environments (Myers & Worm
2003). In addition, carnivores have a high degree of resource
specialization, which makes them more sensitive to resource depletion
(Duffy 2002). For instance, resource subsidies that fuel top-carnivore
fish originate within the fish community (Fig. 1). This makes carnivores
dependent on the productivity of the fish community itself, and as the
biomass of the lower trophic guilds reduces the energy flux to
carnivores will be greatly impaired. These findings indicate that
carnivory function should be more likely to decline as human influence
on natural ecosystems increases over time. The reduction in diversity
and energy flux in carnivores can have two profound implications for
natural ecosystems: (i) making food webs shorter and more vulnerable to
disturbance (Neutel et al. 2007); (ii) carnivores determine food webs
architecture through top-down control and their collapse can trigger
imbalances in the food web functioning (Ripple et al. 2014).
The Río Uruguay covers regions of intensive agricultural crops, cities
and industries (Soutullo et al. 2020). These multiple human-induced
pressures jointly can reduce diversity and riverine functioning (Moi et
al. 2022). Human pressure decreases availability of resources that fuel
trophic guilds, reducing food web complexities (Rooney et al. 2006), and
also impacts food web functioning. For example, in the Río Uruguay,
human activities have promoted the invasion of the golden mussel
(Limnoperna fortunei ), which is one of the most harmful invasive
species in Neotropical rivers (González-Bergonzoni et al. 2020).
Experimental studies have shown that this mollusk became a predominant
food resource for about one third of the fish species and subsidized
>10% of total fish community biomass in the Río Uruguay
(González-Bergonzoni et al. 2020). Consequently, this disrupts the
trophic niche of many fish species (González-Bergonzoni et al. 2020),
impacting the riverine functioning.
Our analysis revealed positive effects of precipitation on the species
richness and energy flux of detritivores and top-carnivore fishes. The
richness and productivity of most detritivore and top-carnivore fishes
enhance after periods with large flood pulses, probably due to the
increased recruitment of juveniles (Oliveira et al. 2015), but also
because of bottom-up trophic cascades. Indeed, during periods of high
precipitation, the biomass production of detritivores increases due to
greater support of allochthonous detritus (González-Bergonzoni et al.
2019), which leads to a greater energetic support of the top-carnivores
fish species. Supporting this prediction, we found higher energy
transference from detritivores to top-carnivorous fishes with increasing
precipitation (Fig. S9 and Table S5). Considering that precipitation
relates to energy flux both at the bottom and the top of fish food webs,
it is likely that the predicted changes in precipitation regimes through
longer drought periods followed by intense precipitation events (IPCC
2022) will alter the multitrophic functioning in riverine systems.
Future studies could address whether periods of intense precipitation
will be able to counteract the negative effects of droughts on
multitrophic functioning.