Impacts of large herbivores on terrestrial ecosystems.

Large herbivores play unique ecological roles and are disproportionately imperiled by human activity. As many wild populations dwindle towards extinction, and as interest grows in restoring lost biodiversity, research on large herbivores and their ecological impacts has intensified. Yet, results are often conflicting or contingent on local conditions, and new findings have challenged conventional wisdom, making it hard to discern general principles. Here, we review what is known about the ecosystem impacts of large herbivores globally, identify key uncertainties, and suggest priorities to guide research. Many findings are generalizable across ecosystems: large herbivores consistently exert top-down control of plant demography, species composition, and biomass, thereby suppressing fires and the abundance of smaller animals. Other general patterns do not have clearly defined impacts: large herbivores respond to predation risk but the strength of trophic cascades is variable; large herbivores move vast quantities of seeds and nutrients but with poorly understood effects on vegetation and biogeochemistry. Questions of the greatest relevance for conservation and management are among the least certain, including effects on carbon storage and other ecosystem functions and the ability to predict outcomes of extinctions and reintroductions. A unifying theme is the role of body size in regulating ecological impact. Small herbivores cannot fully substitute for large ones, and large-herbivore species are not functionally redundant - losing any, especially the largest, will alter net impact, helping to explain why livestock are poor surrogates for wild species. We advocate leveraging a broad spectrum of techniques to mechanistically explain how large-herbivore traits and environmental context interactively govern the ecological impacts of these animals.

Rapid population growth and high management costs have created a narrow window for control of introduced hippos in Colombia.

The introduction of hippos into the wild in Colombia has been marked by their rapid population growth and widespread dispersal on the landscape, high financial costs of management, and conflicting social perspectives on their management and fate. Here we use population projection models to investigate the effectiveness and cost of management options under consideration for controlling introduced hippos. We estimate there are 91 hippos in the middle Magdalena River basin, Colombia, and the hippo population is growing at an estimated rate of 9.6% per year. At this rate, there will be 230 hippos by 2032 and over 1,000 by 2050. Applying the population control methods currently under consideration will cost at least 1-2 million USD to sufficiently decrease hippo population growth to achieve long-term removal, and depending on the management strategy selected, there may still be hippos on the landscape for 50-100 years. Delaying management actions for a single decade will increase minimum costs by a factor of 2.5, and some methods may become infeasible. Our approach illustrates the trade-offs inherent between cost and effort in managing introduced species, as well as the importance of acting quickly, especially when dealing with species with rapid population growth rates and potential for significant ecological and social impacts.

The meta-gut: community coalescence of animal gut and environmental microbiomes.

All animals carry specialized microbiomes, and their gut microbiota are continuously released into the environment through excretion of waste. Here we propose the meta-gut as a novel conceptual framework that addresses the ability of the gut microbiome released from an animal to function outside the host and alter biogeochemical processes mediated by microbes. We demonstrate this dynamic in the hippopotamus (hippo) and the pools they inhabit. We used natural field gradients and experimental approaches to examine fecal and pool water microbial communities and aquatic biogeochemistry across a range of hippo inputs. Sequencing using 16S RNA methods revealed community coalescence between hippo gut microbiomes and the active microbial communities in hippo pools that received high inputs of hippo feces. The shared microbiome between the hippo gut and the waters into which they excrete constitutes a meta-gut system that could influence the biogeochemistry of recipient ecosystems and provide a reservoir of gut microbiomes that could influence other hosts. We propose that meta-gut dynamics may also occur where other animal species congregate in high densities, particularly in aquatic environments.

Hippopotamus are distinct from domestic livestock in their resource subsidies to and effects on aquatic ecosystems.

In many regions of the world, populations of large wildlife have been displaced by livestock, and this may change the functioning of aquatic ecosystems owing to significant differences in the quantity and quality of their dung. We developed a model for estimating loading rates of organic matter (dung) by cattle for comparison with estimated rates for hippopotamus in the Mara River, Kenya. We then conducted a replicated mesocosm experiment to measure ecosystem effects of nutrient and carbon inputs associated with dung from livestock (cattle) versus large wildlife (hippopotamus). Our loading model shows that per capita dung input by cattle is lower than for hippos, but total dung inputs by cattle constitute a significant portion of loading from large herbivores owing to the large numbers of cattle on the landscape. Cattle dung transfers higher amounts of limiting nutrients, major ions and dissolved organic carbon to aquatic ecosystems relative to hippo dung, and gross primary production and microbial biomass were higher in cattle dung treatments than in hippo dung treatments. Our results demonstrate that different forms of animal dung may influence aquatic ecosystems in fundamentally different ways when introduced into aquatic ecosystems as a terrestrially derived resource subsidy.

Hippos (Hippopotamus amphibius): The animal silicon pump.

While the importance of grasslands in terrestrial silicon (Si) cycling and fluxes to rivers is established, the influence of large grazers has not been considered. Here, we show that hippopotamuses are key actors in the savannah biogeochemical Si cycle. Through a detailed analysis of Si concentrations and stable isotope compositions in multiple ecosystem compartments of a savannah-river continuum, we constrain the processes influencing the Si flux. Hippos transport 0.4 metric tons of Si day-1 by foraging grass on land and directly egesting in the water. As such, they bypass complex retention processes in secondary soil Si pools. By balancing internal processes of dissolution and precipitation in the river sediment, we calculate that hippos affect up to 76% of the total Si flux. This can have a large impact on downstream lake ecosystems, where Si availability directly affects primary production in the diatom-dominated phytoplankton communities.

A 2000-year sediment record reveals rapidly changing sedimentation and land use since the 1960s in the Upper Mara-Serengeti Ecosystem.

The Mara River basin is a trans-boundary basin of international importance. It forms the headwaters of the Nile River and serves as the primary dry season water source for an estimated 1.1 million rural people and the largest remaining overland migration of 1.4 million wildebeest in the Serengeti-Mara Ecosystem. Changes throughout the basin are impacting the quantity and quality of the Mara River, yet the historical context of environmental conditions in the basin is not well known. We collected sediment cores throughout the wetland at the mouth of the Mara River, and we used isotopic dating methods and a suite of analyses to examine historical patterns of sediment quantity and source, mercury contamination, and carbon and nutrient loading. Our results show that ecological conditions in the Mara River basin were fairly stable over paleoecological time scales (2000-1000 years before present), but there has been a period of rapid change in the basin over the last 250 years, particularly since the 1960s. A shift in the source and quantity of sediments in the river began in the late 1700s and became much more pronounced in the 1950s and 1960s, coincident with increasing mercury concentrations. The quantity of sediment from the Upper Mara increased, particularly since 1960, but the proportion of total sediment from this region decreased as the Talek and Middle Mara portions of the basin began producing more sediment. The decadal oscillation in sediment accumulation was congruent with known periods of extreme precipitation events. Carbon and nitrogen loading also increased since the 1960s, and the shift in the isotopic ratio of nitrogen provides evidence for increased anthropogenic loading. Altogether, these data likely reflect patterns of change also experienced in other basins throughout East Africa.

Context dependency of animal resource subsidies.

The transport of resource subsidies by animals has been documented across a range of species and ecosystems. Although many of these studies have shown that animal resource subsidies can have significant effects on nutrient cycling, ecosystem productivity, and food-web structure, there is a great deal of variability in the occurrence and strength of these effects. Here we propose a conceptual framework for understanding the context dependency of animal resource subsidies, and for developing and testing predictions about the effects of animal subsidies over space and time. We propose a general framework, in which abiotic characteristics and animal vector characteristics from the donor ecosystem interact to determine the quantity, quality, timing, and duration (QQTD) of an animal input. The animal input is translated through the lens of recipient ecosystem characteristics, which include both abiotic and consumer characteristics, to yield the QQTD of the subsidy. The translated subsidy influences recipient ecosystem dynamics through effects on both trophic structure and ecosystem function, which may both influence the recipient ecosystem's response to further inputs and feed back to influence the donor ecosystem. We present a review of research on animal resource subsidies across ecosystem boundaries, placed within the context of this framework, and we discuss how the QQTD of resource subsidies can influence trophic structure and ecosystem function in recipient ecosystems. We explore the importance of understanding context dependency of animal resource subsidies in increasingly altered ecosystems, in which the characteristics of both animal vectors and donor and recipient ecosystems may be changing rapidly. Finally, we make recommendations for future research on animal resource subsidies, and resource subsidies in general, that will increase our understanding and predictive capacity about their ecosystem effects.

Organic matter and nutrient inputs from large wildlife influence ecosystem function in the Mara River, Africa.

Animals can be important vectors for the movement of resources across ecosystem boundaries. Animals add resources to ecosystems primarily through egestion, excretion, and carcasses, and the stoichiometry and bioavailability of these inputs likely interact with characteristics of the recipient ecosystem to determine their effects on ecosystem function. We studied the influence of hippopotamus excretion/egestion and wildebeest carcasses, and their interactions with discharge, in the Mara River, Kenya. We measured nutrient dissolution and decomposition rates of wildlife inputs, the influence of inputs on nutrient concentrations and nutrient limitation in the river and the influence of inputs on biofilm growth and function in both experimental streams and along a gradient of inputs in the river. We found that hippopotamus excretion/egestion increases ammonium and coarse particulate organic matter in the river, and wildebeest carcasses increase ammonium, soluble reactive phosphorus, and total phosphorus. Concentrations of dissolved carbon and nutrients in the water column increased along a gradient of wildlife inputs and during low discharge, although concentrations of particulate carbon decreased during low discharge due to deposition on the river bottom. Autotrophs were nitrogen limited and heterotrophs were carbon limited and nitrogen and phosphorus colimited upstream of animal inputs but there was no nutrient limitation downstream of inputs. In experimental streams, hippo and wildebeest inputs together increased biofilm gross primary production (GPP) and respiration (R). These results differed in the river, where low concentrations of hippo inputs increased gross primary production (GPP) and respiration (R) of biofilms, but high concentrations of hippo inputs in conjunction with wildebeest inputs decreased GPP. Our research shows that inputs from large wildlife alleviate nutrient limitation and stimulate ecosystem metabolism in the Mara River and that the extent to which these inputs subsidize the ecosystem is mediated by the quantity and quality of inputs and discharge of the river ecosystem. Thus, animal inputs provide an important ecological subsidy to this river, and animal inputs were likely important in many other rivers prior to the widespread extirpation of large wildlife.

Organic matter loading by hippopotami causes subsidy overload resulting in downstream hypoxia and fish kills.

Organic matter and nutrient loading into aquatic ecosystems affects ecosystem structure and function and can result in eutrophication and hypoxia. Hypoxia is often attributed to anthropogenic pollution and is not common in unpolluted rivers. Here we show that organic matter loading from hippopotami causes the repeated occurrence of hypoxia in the Mara River, East Africa. We documented 49 high flow events over 3 years that caused dissolved oxygen decreases, including 13 events resulting in hypoxia, and 9 fish kills over 5 years. Evidence from experiments and modeling demonstrates a strong mechanistic link between the flushing of hippo pools and decreased dissolved oxygen in the river. This phenomenon may have been more widespread throughout Africa before hippopotamus populations were severely reduced. Frequent hypoxia may be a natural part of tropical river ecosystem function, particularly in rivers impacted by large wildlife.

The influence of a semi-arid sub-catchment on suspended sediments in the Mara River, Kenya.

The Mara River Basin in East Africa is a trans-boundary basin of international significance experiencing excessive levels of sediment loads. Sediment levels in this river are extremely high (turbidities as high as 6,000 NTU) and appear to be increasing over time. Large wildlife populations, unregulated livestock grazing, and agricultural land conversion are all potential factors increasing sediment loads in the semi-arid portion of the basin. The basin is well-known for its annual wildebeest (Connochaetes taurinus) migration of approximately 1.3 million individuals, but it also has a growing population of hippopotami (Hippopotamus amphibius), which reside within the river and may contribute to the flux of suspended sediments. We used in situ pressure transducers and turbidity sensors to quantify the sediment flux at two sites for the Mara River and investigate the origin of riverine suspended sediment. We found that the combined Middle Mara-Talek catchment, a relatively flat but semi-arid region with large populations of wildlife and domestic cattle, is responsible for 2/3 of the sediment flux. The sediment yield from the combined Middle Mara-Talek catchment is approximately the same as the headwaters, despite receiving less rainfall. There was high monthly variability in suspended sediment fluxes. Although hippopotamus pools are not a major source of suspended sediments under baseflow, they do contribute to short-term variability in suspended sediments. This research identified sources of suspended sediments in the Mara River and important regions of the catchment to target for conservation, and suggests hippopotami may influence riverine sediment dynamics.

Annual mass drownings of the Serengeti wildebeest migration influence nutrient cycling and storage in the Mara River.

The annual migration of ∼1.2 million wildebeest (Connochaetes taurinus) through the Serengeti Mara Ecosystem is the largest remaining overland migration in the world. One of the most iconic portions of their migration is crossing of the Mara River, during which thousands drown annually. These mass drownings have been noted, but their frequency, size, and impact on aquatic ecosystems have not been quantified. Here, we estimate the frequency and size of mass drownings in the Mara River and model the fate of carcass nutrients through the river ecosystem. Mass drownings (>100 individuals) occurred in at least 13 of the past 15 y; on average, 6,250 carcasses and 1,100 tons of biomass enter the river each year. Half of a wildebeest carcass dry mass is bone, which takes 7 y to decompose, thus acting as a long-term source of nutrients to the Mara River. Carcass soft tissue decomposes in 2-10 wk, and these nutrients are mineralized by consumers, assimilated by biofilms, transported downstream, or moved back into the terrestrial ecosystem by scavengers. These inputs comprise 34-50% of the assimilated diet of fish when carcasses are present and 7-24% via biofilm on bones after soft tissue decomposition. Our results show a terrestrial animal migration can have large impacts on a river ecosystem, which may influence nutrient cycling and river food webs at decadal time scales. Similar mass drownings may have played an important role in rivers throughout the world when large migratory herds were more common features of the landscape.