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.