Feedback loops between 3D vegetation structure and ecological functions of animals.

Ecosystems function in a series of feedback loops that can change or maintain vegetation structure. Vegetation structure influences the ecological niche space available to animals, shaping many aspects of behaviour and reproduction. In turn, animals perform ecological functions that shape vegetation structure. However, most studies concerning three-dimensional vegetation structure and animal ecology consider only a single direction of this relationship. Here, we review these separate lines of research and integrate them into a unified concept that describes a feedback mechanism. We also show how remote sensing and animal tracking technologies are now available at the global scale to describe feedback loops and their consequences for ecosystem functioning. An improved understanding of how animals interact with vegetation structure in feedback loops is needed to conserve ecosystems that face major disruptions in response to climate and land-use change.

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.

Are hippos Africa's most influential megaherbivore? A review of ecosystem engineering by the semi-aquatic common hippopotamus.

Megaherbivores perform vital ecosystem engineering roles, and have their last remaining stronghold in Africa. Of Africa's remaining megaherbivores, the common hippopotamus (Hippopotamus amphibius) has received the least scientific and conservation attention, despite how influential their ecosystem engineering activities appear to be. Given the potentially crucial ecosystem engineering influence of hippos, as well as mounting conservation concerns threatening their long-term persistence, a review of the evidence for hippos being ecosystem engineers, and the effects of their engineering, is both timely and necessary. In this review, we assess, (i) aspects of hippo biology that underlie their unique ecosystem engineering potential; (ii) evaluate hippo ecological impacts in terrestrial and aquatic environments; (iii) compare the ecosystem engineering influence of hippos to other extant African megaherbivores; (iv) evaluate factors most critical to hippo conservation and ecosystem engineering; and (v) highlight future research directions and challenges that may yield new insights into the ecological role of hippos, and of megaherbivores more broadly. We find that a variety of key life-history traits determine the hippo's unique influence, including their semi-aquatic lifestyle, large body size, specialised gut anatomy, muzzle structure, small and partially webbed feet, and highly gregarious nature. On land, hippos create grazing lawns that contain distinct plant communities and alter fire spatial extent, which shapes woody plant demographics and might assist in maintaining fire-sensitive riverine vegetation. In water, hippos deposit nutrient-rich dung, stimulating aquatic food chains and altering water chemistry and quality, impacting a host of different organisms. Hippo trampling and wallowing alters geomorphological processes, widening riverbanks, creating new river channels, and forming gullies along well-utilised hippo paths. Taken together, we propose that these myriad impacts combine to make hippos Africa's most influential megaherbivore, specifically because of the high diversity and intensity of their ecological impacts compared with other megaherbivores, and because of their unique capacity to transfer nutrients across ecosystem boundaries, enriching both terrestrial and aquatic ecosystems. Nonetheless, water pollution and extraction for agriculture and industry, erratic rainfall patterns and human-hippo conflict, threaten hippo ecosystem engineering and persistence. Therefore, we encourage greater consideration of the unique role of hippos as ecosystem engineers when considering the functional importance of megafauna in African ecosystems, and increased attention to declining hippo habitat and populations, which if unchecked could change the way in which many African ecosystems function.

Resistance of termite mounds to variation in long-term fire regimes across semi-arid African savannas.

Fire regimes are expected to change with climate change, resulting in a crucial need to understand the specific ways in which variable fire regimes impact important contributors to ecosystem functioning, such as mound-building termites. Termite mounds and fire are both important agents of savanna ecosystem heterogeneity and functioning, but there is little understanding of how they interact across savanna types. We used very high-resolution LiDAR remote sensing to measure the size and distribution of termite mounds across approximately 1300 ha of experimental burn plots in four South African savanna landscapes representing a wide range of fire treatments differing in seasonality and frequency of burning. In nutrient-poor granitic savannas, fire had no impact on termite mound size, densities and spatial distributions. In nutrient-rich basaltic savannas with high mammalian herbivore abundance and intermediate rainfall, very frequent fires caused a decrease in termite mound size, whereas in arid nutrient-rich basaltic savannas, fires that occurred at intermediate frequencies and in transitional seasons (i.e. late dry season and late wet season) decreased the degree of spatial overdispersal exhibited by mounds. Overall, our results suggest that termite mounds are resistant to variation in fire seasonality and frequency, likely indicating that ecosystem services provided by mound-building termites will be unaffected by changing fire regimes. However, consideration of changes to termite mound size and distribution could be necessary for land managers in specific savanna types, such as nutrient-rich soils with high mammalian herbivore abundance.

Species-level termite methane production rates.

Termites consume substantial amounts of plant material across tropical and subtropical ecosystems. During the process of lignocellulose digestion, the symbiotic methanogenesis within termites' guts produces the potent greenhouse gas methane (CH4 ). Termites contribute an estimated 1%-5% of global CH4 emissions, with these estimates derived from the product of termite biomass and termite CH4 production rate per unit of termite biomass. However, termite CH4 production rates vary significantly across species, genus, family, and feeding group, yet our understanding of this variation remains poor. Here, we reviewed papers published from 1975 to 2021 to create a single consistently derived list of species-level termite CH4 production rates. We searched the Google Scholar using two key words: termite and methane. We only included studies that had measured termite CH4 production rates using the incubation method. For each eligible study, we extracted and tabulated termite CH4 production rates and other relevant variables (e.g., feeding groups). We used µg CH4 g-1 (termite) h-1 as the standardized unit, and if other units were presented, we converted them into this standardized unit. Overall, these data include 134 termite species from 65 genera and 5 families. Termite CH4 production rates ranged from 0 to 25.26 µg CH4 g-1 (termite) h-1 , with an average rate of 3.74 (standard deviation = 4.08, n = 251). Reported CH4 production rates were largely concentrated in the family Termitidae. Across feeding groups, soil feeders tended to have higher CH4 production rates than wood feeders. However, published data represent fewer than 5% of described termite species, and therefore we hope that our study will initiate a community-wide effort to fill data gaps and advance our understanding of the role of termites in critical biogeochemical cycles and other ecosystem processes. The data set is in the public domain under a Creative Commons Zero (CC0) license waiver.

Limited increases in savanna carbon stocks over decades of fire suppression.

Savannas cover a fifth of the land surface and contribute a third of terrestrial net primary production, accounting for three-quarters of global area burned and more than half of global fire-driven carbon emissions1-3. Fire suppression and afforestation have been proposed as tools to increase carbon sequestration in these ecosystems2,4. A robust quantification of whole-ecosystem carbon storage in savannas is lacking however, especially under altered fire regimes. Here we provide one of the first direct estimates of whole-ecosystem carbon response to more than 60 years of fire exclusion in a mesic African savanna. We found that fire suppression increased whole-ecosystem carbon storage by only 35.4 ± 12% (mean ± standard error), even though tree cover increased by 78.9 ± 29.3%, corresponding to total gains of 23.0 ± 6.1 Mg C ha-1 at an average of about 0.35 ± 0.09 Mg C ha-1 year-1, more than an order of magnitude lower than previously assumed4. Frequently burned savannas had substantial belowground carbon, especially in biomass and deep soils. These belowground reservoirs are not fully considered in afforestation or fire-suppression schemes but may mean that the decadal sequestration potential of savannas is negligible, especially weighed against concomitant losses of biodiversity and function.

Mammalian herbivore movement into drought refugia has cascading effects on savanna insect communities.

Global climate change is predicted to increase the frequency of droughts, with major impacts on tropical savannas. It has been suggested that during drought, increased soil moisture and nutrients on termite mounds could benefit plants but it is unclear how such benefits could cascade to affect insect communities. Here, we describe the effects of drought on vegetation structure, the cascading implications for invertebrates and how termite mounds influence such effects. We compared how changes in grass biomass affected grasshopper and ant diversity on and off Macrotermes mounds before (2012) and during a drought (2016) at two locations that experienced large variation in drought severity (Skukuza and Pretoriuskop) in the Kruger National Park, South Africa. The 2013-2016 drought was not ubiquitous across the study site, with rainfall decreasing at Skukuza and being above average at Pretoriuskop. However, grass biomass declined at both locations. Grasshopper abundance decreased at droughted Skukuza both on and off mounds but decreased on mounds and increased off mounds at non-droughted Pretoriuskop. Ant abundance and species richness increased at Skukuza but remained the same on mounds and decreased off mounds at Pretoriuskop. Our results demonstrate the spatially extensive effects of drought. Despite above average rainfall in 2016 at Pretoriuskop, grass biomass decreased, likely due to an influx of large mammalian herbivores from drought-affected areas. This decrease in grass biomass cascaded to affect grasshoppers and ants, further illustrating the effects of drought on invertebrates in adjoining areas with higher rainfall. Our grasshopper results also suggest that increased drought in savannas will contribute to overall declines in insect abundance. Moreover, our recorded increase in ant abundance was primarily in the form of increases in dominant species, illustrating how drought-induced shifts in relative abundance will likely influence ecosystem structure and function. Our study highlights the phenomenon of spill-over drought effects and suggests rather than mitigating drought, termite mounds can instead become the focus for more intense grazing, with important consequences for insect communities.

Spatial heterogeneity facilitates carnivore coexistence.

Competitively dominant carnivore species can limit the population sizes and alter the behavior of inferior competitors. Established mechanisms that enable carnivore coexistence include spatial and temporal avoidance of dominant predator species by subordinates, and dietary niche separation. However, spatial heterogeneity across landscapes could provide inferior competitors with refuges in the form of areas with lower competitor density and/or locations that provide concealment from competitors. Here, we combine temporally overlapping telemetry data from dominant lions (Panthera leo) and subordinate African wild dogs (Lycaon pictus) with high-resolution remote sensing in an integrated step selection analysis to investigate how fine-scaled landscape heterogeneity might facilitate carnivore coexistence in South Africa's Hluhluwe-iMfolozi Park, where both predators occur at exceptionally high densities. We ask whether the primary lion-avoidance strategy of wild dogs is spatial avoidance of lions or areas frequented by lions, or if wild dogs selectively use landscape features to avoid detection by lions. Within this framework, we also test whether wild dogs rely on proactive or reactive responses to lion risk. In contrast to previous studies finding strong spatial avoidance of lions by wild dogs, we found that the primary wild dog lion-avoidance strategy was to select landscape features that aid in avoidance of lion detection. This habitat selection was routinely used by wild dogs, and especially when in areas and during times of high lion-encounter risk, suggesting a proactive response to lion risk. Our findings suggest that spatial landscape heterogeneity could represent an alternative mechanism for carnivore coexistence, especially as ever-shrinking carnivore ranges force inferior competitors into increased contact with dominant species.

Uncovering Ecological Patterns with Convolutional Neural Networks.

Using remotely sensed imagery to identify biophysical components across landscapes is an important avenue of investigation for ecologists studying ecosystem dynamics. With high-resolution remotely sensed imagery, algorithmic utilization of image context is crucial for accurate identification of biophysical components at large scales. In recent years, convolutional neural networks (CNNs) have become ubiquitous in image processing, and are rapidly becoming more common in ecology. Because the quantity of high-resolution remotely sensed imagery continues to rise, CNNs are increasingly essential tools for large-scale ecosystem analysis. We discuss here the conceptual advantages of CNNs, demonstrate how they can be used by ecologists through distinct examples of their application, and provide a walkthrough of how to use them for ecological applications.

No evidence of handling-induced mortality in Serengeti's African wild dog population.

The disappearance of an endangered African wild dog population from Serengeti National Park (SNP) led to international debate centered around one question: were researchers to blame? The "Burrows' hypothesis" postulated that stress induced by research-related immobilization and handling reactivated a latent rabies virus, eliminating the population. Insufficient data inhibited hypothesis testing, but since wild dogs persisted alongside SNP and have been studied since 2005, the hypothesis can be tested 25 years after its proposition. To be supported, wild dog immobilization interventions should have resulted in high mortality rates. However, 87.6% of 121 handled wild dogs (2006-2016) survived >12 months post-handling. Some argued that viral reactivation would necessitate long-term stress. Following immobilization, 67 animals were captured, transported, and held in a translocation enclosure. Despite the longer-term stress, 95.5% survived >12 months. Furthermore, the stable number of wild dog packs in the ecosystem over the past decade, and lack of recolonization of SNP, strongly oppose Burrows' hypothesis. Instead, factors such as heightened levels of interspecific competition are likely to have contributed to the wild dog disappearance and subsequent avoidance of the Serengeti plains. Handling and radio telemetry are invaluable when studying elusive endangered species, yielding information pertinent to their conservation and management, and had no effect on Serengeti wild dog survival.

Elephants limit aboveground carbon gains in African savannas.

Understanding the drivers of vegetation carbon dynamics is essential for climate change mitigation and effective policy formulation. However, most efforts focus on abiotic drivers of plant biomass change, with little consideration for functional roles performed by animals, particularly at landscape scales. We combined repeat airborne Light Detection and Ranging with measurements of elephant densities, abiotic factors, and exclusion experiments to determine the relative importance of drivers of change in aboveground woody vegetation carbon stocks in Kruger National Park, South Africa. Despite a growing elephant population, aboveground carbon density (ACD) increased across most of the landscape over the 6-year study period, but at fine scales, bull elephant density was the most important factor determining carbon stock change, with ACD losses recorded only where bull densities exceeded 0.5 bulls/km2 . Effects of bull elephants were, however, spatially restricted and landscape dependent, being especially pronounced along rivers, at mid-elevations, and on steeper slopes. In contrast, elephant herds and abiotic drivers had a comparatively small influence on the direction or magnitude of carbon stock change. Our findings demonstrate that animals can have a substantive influence on regional-scale carbon dynamics and warrant consideration in carbon cycling models and policy formulation aimed at carbon management and climate change mitigation.

Animals and the zoogeochemistry of the carbon cycle.

Predicting and managing the global carbon cycle requires scientific understanding of ecosystem processes that control carbon uptake and storage. It is generally assumed that carbon cycling is sufficiently characterized in terms of uptake and exchange between ecosystem plant and soil pools and the atmosphere. We show that animals also play an important role by mediating carbon exchange between ecosystems and the atmosphere, at times turning ecosystem carbon sources into sinks, or vice versa. Animals also move across landscapes, creating a dynamism that shapes landscape-scale variation in carbon exchange and storage. Predicting and measuring carbon cycling under such dynamism is an important scientific challenge. We explain how to link analyses of spatial ecosystem functioning, animal movement, and remote sensing of animal habitats with carbon dynamics across landscapes.

Woody encroachment slows decomposition and termite activity in an African savanna.

Woody encroachment can lead to a complete switch from open habitats to dense thickets, and has the potential to greatly alter the biodiversity and ecological functioning of grassy ecosystems across the globe. Plant litter decomposition is a critical ecosystem process fundamental to nutrient cycling and global carbon dynamics, yet little is known about how woody encroachment might alter this process. We compared grass decay rates of heavily encroached areas with adjacent nonencroached open areas in a semi-arid South African savanna using litterbags that allowed or excluded invertebrates. We also assessed the effect of woody encroachment on the activity of termites- dominant decomposer organisms in savanna systems. We found a significant reduction in decomposition rates within encroached areas, with litter taking twice as long to decay compared with open savanna areas. Moreover, invertebrates were more influential on grass decomposition in open areas and termite activity was substantially lower in encroached areas, particularly during the dry season when activity levels were reduced to almost zero. Our results suggest that woody encroachment created an unfavourable environment for invertebrates, and termites in particular, leading to decreased decomposition rates in these areas. We provide the first quantification of woody encroachment altering the functioning of African savanna ecosystems through the slowing of aboveground plant decomposition. Woody encroachment is intensifying across the globe, and our results suggest that substantial changes to the carbon balance and biodiversity of grassy biomes could occur.

Megafaunal effects on vegetation structure throughout a densely wooded African landscape.

Megafauna strongly affect vegetation structure and composition, often leading to management concern. However, the extent of their influence across large scales and varying ecosystems remains largely unknown. Using high resolution airborne Light Detection and Ranging (LiDAR), we investigated landscape-scale changes in vegetation height and three-dimensional (3D) structure across landscapes of varying elephant densities and presence over time, and in response to surface water distribution and terrain variability in the heavily managed thicket biome of the Addo Elephant National Park, South Africa. Elephants caused up to a fourfold reduction in vegetation height and altered the vertical profile, but increased vegetation height variability. Vegetation height also increased with elevation and distance from water, particularly in areas that elephants had long occupied at high densities. Slope had opposing effects on vegetation height, with height increasing with slope in areas long exposed to elephants, but decreasing where elephants had only recently been granted access. Our results suggest that elephants are the primary agents of vegetation change in this ecosystem, but that the strength of their effects varies across the landscape, enabling management to use water and terrain as mitigation tools. We further highlight the necessity of landscape-level experimental studies on megafaunal effects to untangle mechanisms and establish causality.

Riparian vegetation structure and the hunting behavior of adult estuarine crocodiles.

Riparian ecosystems are amongst the most biodiverse tropical habitats. They are important, and essential, ecological corridors, linking remnant forest fragments. In this study, we hypothesised that crocodile's actively select nocturnal resting locations based on increased macaque predation potential. We examined the importance of riparian vegetation structure in the maintenance of crocodile hunting behaviours. Using airborne Light Detection and Ranging (LiDAR) and GPS telemetry on animal movement, we identified the repeated use of nocturnal resting sites by adult estuarine crocodiles (Crocodylus porosus) throughout the fragmented Lower Kinabatangan Wildlife Sanctuary in Sabah, Malaysia. Crocodile resting locations were found to resemble, in terms of habitat characteristics, the sleeping sites of long-tailed macaque; positioned in an attempt to avoid predation by terrestrial predators. We found individual crocodiles were actively selecting overhanging vegetation and that the protrusion of trees from the tree line was key to site selection by crocodiles, as well as influencing both the presence and group size of sleeping macaques. Although these findings are correlational, they have broad management implications, with the suggestion that riparian corridor maintenance and quality can have implications beyond that of terrestrial fauna. We further place our findings in the context of the wider ecosystem and the maintenance of trophic interactions, and discuss how future habitat management has the potential to mitigate human-wildlife conflict.

Canopy structure drives orangutan habitat selection in disturbed Bornean forests.

The conservation of charismatic and functionally important large species is becoming increasingly difficult. Anthropogenic pressures continue to squeeze available habitat and force animals into degraded and disturbed areas. Ensuring the long-term survival of these species requires a well-developed understanding of how animals use these new landscapes to inform conservation and habitat restoration efforts. We combined 3 y of highly detailed visual observations of Bornean orangutans with high-resolution airborne remote sensing (Light Detection and Ranging) to understand orangutan movement in disturbed and fragmented forests of Malaysian Borneo. Structural attributes of the upper forest canopy were the dominant determinant of orangutan movement among all age and sex classes, with orangutans more likely to move in directions of increased canopy closure, tall trees, and uniform height, as well as avoiding canopy gaps and moving toward emergent crowns. In contrast, canopy vertical complexity (canopy layering and shape) did not affect movement. Our results suggest that although orangutans do make use of disturbed forest, they select certain canopy attributes within these forests, indicating that not all disturbed or degraded forest is of equal value for the long-term sustainability of orangutan populations. Although the value of disturbed habitats needs to be recognized in conservation plans for wide-ranging, large-bodied species, minimal ecological requirements within these habitats also need to be understood and considered if long-term population viability is to be realized.

Limited spatial response to direct predation risk by African herbivores following predator reintroduction.

Predators affect ecosystems not only through direct mortality of prey, but also through risk effects on prey behavior, which can exert strong influences on ecosystem function and prey fitness. However, how functionally different prey species respond to predation risk and how prey strategies vary across ecosystems and in response to predator reintroduction are poorly understood. We investigated the spatial distributions of six African herbivores varying in foraging strategy and body size in response to environmental factors and direct predation risk by recently reintroduced lions in the thicket biome of the Addo Elephant National Park, South Africa, using camera trap surveys, GPS telemetry, kill site locations and Light Detection and Ranging. Spatial distributions of all species, apart from buffalo, were driven primarily by environmental factors, with limited responses to direct predation risk. Responses to predation risk were instead indirect, with species distributions driven by environmental factors, and diel patterns being particularly pronounced. Grazers were more responsive to the measured variables than browsers, with more observations in open areas. Terrain ruggedness was a stronger predictor of browser distributions than was vegetation density. Buffalo was the only species to respond to predator encounter risk, avoiding areas with higher lion utilization. Buffalo therefore behaved in similar ways to when lions were absent from the study area. Our results suggest that direct predation risk effects are relatively weak when predator densities are low and the time since reintroduction is short and emphasize the need for robust, long-term monitoring of predator reintroductions to place such events in the broader context of predation risk effects.

Seasonal variation in the relative dominance of herbivore guilds in an African savanna.

African savannas are highly seasonal with a diverse array of both mammalian and invertebrate herbivores, yet herbivory studies have focused almost exclusively on mammals. We conducted a 2-yr exclosure experiment in South Africa's Kruger National Park to measure the relative impact of these two groups of herbivores on grass removal at both highly productive patches (termite mounds) and in the less productive savanna matrix. Invertebrate and mammalian herbivory was greater on termite mounds, but the relative importance of each group changed over time. Mammalian offtake was higher than invertebrates in the dry season, but can be eclipsed by invertebrates during the wet season when this group is more active. Our results demonstrate that invertebrates play a substantial role in savanna herbivory and should not be disregarded in attempts to understand the impacts of herbivory on ecosystems.

Effects of Vegetation Structure on the Location of Lion Kill Sites in African Thicket.

Predator-prey relationships are integral to ecosystem stability and functioning. These relationships are, however, difficult to maintain in protected areas where large predators are increasingly being reintroduced and confined. Where predators make kills has a profound influence on their role in ecosystems, but the relative importance of environmental variables in determining kill sites, and how these might vary across ecosystems is poorly known. We investigated kill sites for lions in South Africa's thicket biome, testing the importance of vegetation structure for kill site locations compared to other environmental variables. Kill sites were located over four years using GPS telemetry and compared to non-kill sites that had been occupied by lions, as well as to random sites within lion ranges. Measurements of 3D vegetation structure obtained from Light Detection and Ranging (LiDAR) were used to calculate the visible area (viewshed) around each site and, along with wind and moonlight data, used to compare kill sites between lion sexes, prey species and prey sexes. Viewshed area was the most important predictor of kill sites (sites in dense vegetation were twice as likely to be kill sites compared to open areas), followed by wind speed and, less so, moonlight. Kill sites for different prey species varied with vegetation structure, and male prey were killed when wind speeds were higher compared to female prey of the same species. Our results demonstrate that vegetation structure is an important component of predator-prey interactions, with varying effects across ecosystems. Such differences require consideration in terms of the ecological roles performed by predators, and in predator and prey conservation.