Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore

Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.     

Low species turnover of upland Amazonian birds in the absence of physical barriers

Aim

One of the oldest and most powerful ways for ecologists to explain distinct biological communities is to invoke underlying environmental differences. But in hyper-diverse systems, which often display high species richness and low species abundance, these sorts of community comparisons are especially challenging. The classic view for Amazonian birds posits that riverine barriers and habitat specialization determine local and regional community composition. We test the tacit, complementary assumption that similar bird communities should therefore permeate uniform habitat between major rivers, regardless of distance.

Location

Upland (terra firme) rainforests of central Amazonia.

Methods

We conducted intensive whole-community surveys of birds in three pairs of 100-ha plots, separated by 40–60 km. We then used dissimilarity indices, cluster analysis, and ordination to characterize differences among the six avian communities.

Results

In all, we detected 244 forest-dependent birds, with an average of 190 species (78%) per plot. Species turnover was negligible, no unique indicator species were found among plot pairs, and all documented species were already known from a complete inventory at one of the three sites.

Main Conclusions

Our study corroborates the classic biogeographical pattern and suggests that turnover contributes little to regional avian diversity within upland forests. Using a grain size of 100 ha, this implies that upland birds perceive the environment as uniform, at least over distances of ~60 km. Therefore, to maximize both local species richness and population persistence, our findings support the conservation of very large tracts of upland rainforest. Our analyses also revealed that the avifauna at Reserva Ducke, encroached by urban sprawl from the city of Manaus, shows the hallmarks of a disturbed community, with fewer vulnerable insectivores. This defaunation signals that even an enormous preserve (10 × 10 km) in lowland Amazonia is not insulated from anthropogenic degradation within the surrounding landscape.     

Seed dispersal networks in tropical forest fragments: Area effects,remnant species,and interaction diversity

Seed dispersal interactions involve key ecological processes in tropical forests that help to maintain ecosystem functioning. Yet this functionality may be threatened by increasing habitat loss, defaunation, and fragmentation. However, generalist species, and their interactions, can benefit from the habitat change caused by human disturbance while more specialized interactions mostly disappear. Therefore, changes in the structure of the local, within fragment, networks can be expected. Here we investigated how the structure of seed dispersal networks changes along a gradient of increasing habitat fragmentation. We analyzed 16 bird seed dispersal assemblages from forest fragments of a biodiversity-rich ecosystem. We found significant species–, interaction–, and network–area relationships, yet the later was determined by the number of species remaining in each community. The number of frugivorous bird and plant species, their interactions, and the number of links per species decreases as area is lost in the fragmented landscape. In contrast, network nestedness has a negative relationship with fragment area, suggesting an increasing generalization of the network structure in the gradient of fragmentation. Network specialization was not significantly affected by area, indicating that some network properties may be invariant to disturbance. Still, the local extinction of partner species, paralleled by a loss of interactions and specialist–specialist bird–plant seed dispersal associations, suggests the functional homogenization of the system as area is lost. Our study provides empirical evidence for network–area relationships driven by the presence/absence of remnant species and the interactions they perform.     

Carnivores (Mammalia: Carnivora) in South China: a status review with notes on the commercial trade

• 1 Evidence from the literature, interviews, market surveys, general rapid field surveys and camera trapping was reviewed to infer the regional status of 33 recorded carnivores in South China (Guangxi, Guangdong, Hainan, Hong Kong and Macau).
• 2 The carnivore fauna in South China is among the most depleted for any continental area in the world.
• 3 The tiger Panthera tigris, leopard Panthera pardus, grey wolf Canis lupus and binturong Arctictis binturong are probably extirpated.
• 4 The dhole Cuon alpinus, Asiatic golden cat Catopuma temmincki and clouded leopard Neofelis nebulosa are at great risk of regional extirpation, as are the more ecologically adaptable red fox Vulpes vulpes, raccoon dog Nyctereutes procyonoides, Asian badger Meles leucurus, Eurasian otter Lutra lutra, Oriental small‐clawed otter Aonyx cinereus and large Indian civet Viverra zibetha.
• 5 Though more widely reported, the Asiatic black bear Ursus thibetanus, yellow‐throated marten Martes flavigula, hog badger Arctonyx collaris and Siberian weasel Mustela sibirica are at regional risk.
• 6 The status of the Burmese ferret‐badger Melogale personata, stripe‐backed weasel Mustela strigidorsa, smooth‐coated otter Lutrogale perspicillata, large‐spotted civet Viverra megaspila and Owston's palm civet Chrotogale owstoni is uncertain due to inadequate information.
• 7 Five carnivore species – the Chinese ferret‐badger Melogale moschata, masked palm civet Paguma larvata, yellow‐bellied weasel Mustela kathiah, small Indian civet Viverricula indica and leopard cat Prionailurus bengalensis– are relatively secure (though not common) in the region, along with the Asian palm civet Paradoxurus hermaphroditus and the Javan mongoose Herpestes javanicus in some areas, while the spotted linsang Prionodon pardicolor and crab‐eating mongoose Herpestes urva may have been under‐reported.
• 8 The main threats have been habitat destruction and unsustainable exploitation. Only in Hong Kong, where enforcement of protection legislation has been stronger, are the surviving carnivore species easily encountered.
• 9 Improved enforcement and monitoring are essential to retaining the remainder of South China's carnivores. Support could be boosted by conservation education and better research.

     

Game Vertebrate Densities in Hunted and Nonhunted Forest Sites in Manu National Park,Peru

Manu National Park of southern Peru is one of the most renowned protected areas in the world, yet large-bodied vertebrate surveys conducted to date have been restricted to Cocha Cashu Biological Station, a research station covering <0.06 percent of the 1.7 Mha park. Manu Park is occupied by >460 settled Matsigenka Amerindians, 300–400 isolated Matsigenka, and several, little-known groups of isolated hunter–gatherers, yet the impact of these native Amazonians on game vertebrate populations within the park remains poorly understood. On the basis of 1495 km of standardized line-transect censuses, we present density and biomass estimates for 23 mammal, bird, and reptile species for seven lowland and upland forest sites in Manu Park, including Cocha Cashu. We compare these estimates between hunted and nonhunted sites within Manu Park, and with other Neotropical forest sites. Manu Park safeguards some of the most species-rich and highest biomass assemblages of arboreal and terrestrial mammals ever recorded in Neotropical forests, most likely because of its direct Andean influence and high levels of soil fertility. Relative to Barro Colorado Island, seed predators and arboreal folivores in Manu are rare, and generalist frugivores specializing on mature fruit pulp are abundant. The impact of such a qualitative shift in the vertebrate community on the dynamics of plant regeneration, and therefore, on our understanding of tropical plant ecology, must be profound. Despite a number of external threats, Manu Park continues to serve as a baseline against which other Neotropical forests can be gauged. Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp .     

Consequences of defaunation for a tropical tree community

Hunting affects a considerably greater area of the tropical forest biome than deforestation and logging combined. Often even large remote protected areas are depleted of a substantial proportion of their vertebrate fauna. However, understanding of the long‐term ecological consequences of defaunation in tropical forests remains poor. Using tree census data from a large‐scale plot monitored over a 15‐year period since the approximate onset of intense hunting, we provide a comprehensive assessment of the immediate consequences of defaunation for a tropical tree community. Our data strongly suggest that over‐hunting has engendered pervasive changes in tree population spatial structure and dynamics, leading to a consistent decline in local tree diversity over time. However, we do not find any support for suggestions that over‐hunting reduces above‐ground biomass or biomass accumulation rate in this forest. To maintain critical ecosystem processes in tropical forests increased efforts are required to protect and restore wildlife populations.     

Size-Related Differential Seed Predation in a Heavily Defaunated Neotropical Rain Forest

Hunting and habitat loss represent an increasingly common anthropogenic impact. Available evidence suggests that defaunation is typically differential: medium/large mammals are most affected while small rodents are less affected, or even favored. In heavily impacted areas, such as Los Tuxtlas, the residual mammalian fauna is dominated by small rodents. We tested the expectation that if small rodents will preferentially attack small-seeded species, large-seeded species may escape predation in the absence of medium/large seed predators and that this may affect germination and, possibly, recruitment. Experiments with caged rodents ( Heteromys desmarestianus ) under laboratory conditions showed a preference for smaller seeds. A field experiment involving seeds of contrasting size showed that small, unprotected seeds experienced a predation risk 30-times larger than protected seeds, while the effect of protection was not significant for large seeds. These patterns of predation led to significant differences in germination: protected small-seeded species had a fourfold greater germination than unprotected small-seeded species, while germination was not significantly different between exposed and protected large seeds. The observed contrasts in germination suggest that under heavy defaunation, small-seeded species are likely to be penalized by the overabundance of small rodents, while large-seeded species escape predation. Our results are consistent with the observation of dense seedling carpets dominated by large-seeded species in the understory of Los Tuxtlas. We speculate that the patterns we uncovered may explain, at least partly, the impoverished diversity of the understory vegetation that characterizes heavily defaunated understories and that this has the potential to affect forest regeneration.     

Down‐sizing of dung beetle assemblages over the last 53 000 years is consistent with a dominant effect of megafauna losses

The ongoing down‐sizing of the global mammal communities is assumed to have subsequent effects on mutualistic species communities. Dung beetles co‐evolved with large‐sized animals since millennia and depend on the megafauna feces of an appropriate size. Mammal community down‐sizing as a result of past and ongoing megafauna losses is therefore likely to result in a down‐sizing of dung beetle communities. However, empirical evidence for this co‐down‐sizing is lacking especially on larger spatial scales and over extended periods of time. Here, we show a significant down‐sizing of European dung beetle assemblages over the last ~53 000 years by relating Quaternary fossil records with trait information on body size of beetles. This significant down‐sizing of dung beetle communities was thereby not linear, but characterized by a weak decrease until the early Holocene but a strong acceleration in the recent pre‐history, from 6–7000 years BP onwards. This acceleration of down‐sizing coincides with the completion of the Quaternary megafauna extinction and the start of major shifts in human agricultural land‐use. In contrast, assemblage mean body size of non‐coprophagous scarabids as well as ground beetles – two groups of beetles with no or weak relations to megafauna – was observed to increase towards the present with an acceleration of body size increase coinciding with the onset of late‐glacial warming (14 200 years BP). In summary, the observed late‐Quaternary down‐sizing of European dung beetle communities is consistent with an effect of pre‐historic megafauna losses, and not with the coincident general warming. Ongoing down‐sizing of mammal communities is therefore likely to result in further down‐sizing of dung beetle assemblages, with potential effects on their important role for nutrient cycling and secondary seed dispersal in natural and extensive agro‐ecosystems. Future nature management initiatives could halt or even reverse this functional diversity loss via effective protection or restoration of megafauna communities.     

Defaunation impacts on seed survival and its effect on the biomass of future tropical forests

Large animal species, which provide important ecological functions such as dispersal of seeds or top–down control of seed predators, are very vulnerable in fragmented forests, being unable to survive in small fragments, and facing increasing hunting pressure. The loss of large animals affects two main ecological processes crucial for the tree reproductive cycle: seed dispersal of large seeds (e.g. provided by tapirs) and control of seed predator population (e.g. provided by large cats). The changes in both processes are expected to increase seed mortality since seeds are not dispersed away from conspecifics (causing increased pre‐dispersal mortality due to negative density dependent effects) and/or face increased predation after a dispersal event (post‐dispersal mortality). Although an extensive body of empirical knowledge exists on seed predation, the link between seed loss and adult tree community composition and structure is not well established, as well as the temporal scale seed changes affect adults. Using an individual‐based forest model (FORMIND), we evaluate the long‐term consequences of increased pre and post‐dispersal seed mortality on the future forest biomass retention of a Brazilian northeastern Atlantic forest. Our results show that forest biomass is significantly affected after 80–93% pre‐dispersal loss of large seeds, or post‐dispersal predation densities of 20–25 predators per parent tree. Large‐seeded tree species are at increased risk of local extinction causing up to 26.2% loss of forest biomass when both pre and post‐dispersal processes are combined. However, these changes can last up to 100 years after the occurrence of defaunation. In summary we conclude that large animal loss has the potential to reduce future forest biomass and tree species‐richness by impacting seed survival, and should be considered in the planning of biodiversity friendly landscapes as well as in calculations of the global carbon budget.     

The key role of the largest extant Neotropical frugivore (Tapirus terrestris) in promoting admixture of plant genotypes across the landscape

The historical and contemporary loss of large‐bodied frugivores has disrupted many plant‐disperser mutualisms, with potentially profound consequences for plants. Although several aspects of seed dispersal by megafrugivores have already been examined, the role of these species in promoting seed‐mediated gene flow has remained unexplored. We evaluated the role of the Amazonian tapir (Tapirus terrestris), the largest Neotropical frugivore, in shaping plant genetic structure through seed‐mediated gene flow. We used microsatellites to analyze the genetic patterns of Syagrus romanzoffiana seedlings recruited in tapir latrines and around conspecific adult palms, the two sites where seeds and seedlings are most frequently found in this species. While the genetic diversity of seedlings was rather similar in both sites, the kinship structure was substantially weaker in latrines. Most seedlings recruited around adult palms were half‐ or full‐sibs originating from those adults. In contrast, seedlings recruited in latrines came from several (>5, on average) contributing mothers other than the nearest adult (95%) and were mostly non‐sibs (72%). Kinship patterns indicated that tapir‐mediated dispersal promotes the admixture of genotypes across space. Also, our results suggested that genetic diversity and the number of contributing mothers in latrines increase with the number of fruiting adults visited by tapirs before defecating and with the accumulation of feces over time. We provide evidence of the relevance of tapirs in mobilizing maternal progenies (and genotypes) across the landscape and recruiting clusters of unrelated seedlings. This study suggests a key role for plant–megafrugivore interactions in seed‐mediated gene flow and emphasizes the importance of preserving such mutualisms.