Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks

Donoso, Isabel; Sorensen, Marjorie C.; Blendinger, Pedro G.; Kissling, W. Daniel; Neuschulz, Eike Lena; Mueller, Thomas; Schleuning, Matthias

doi:10.1038/s41467-020-15438-y

Cited by 51 publications

(61 citation statements)

References 74 publications

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“…This finding is also consistent with a recent simulation study showing that defaunation, i.e. the size-structured extinction of avian seed dispersers, leads to a rapid decay in seed-dispersal distances across a range of tropical seed-dispersal networks (Donoso et al 2020).…”

Section: Discussionsupporting

confidence: 92%

Community‐wide seed dispersal distances peak at low levels of specialisation in size‐structured networks

Sorensen

Donoso

Neuschulz

et al. 2020

Oikos

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Network approaches provide insight into the complex web of interspecific interactions that structure ecological communities. However, because data on the functional outcomes of ecological networks are very rarely available, the effect of network structure on ecosystem functions, such as seed dispersal, is largely unknown. Here, we develop a new approach that is able to link interaction networks to a trait‐based seed–dispersal model to estimate community‐wide seed dispersal distances. We simulated networks, using a niche model based on size‐matching between plants and birds, that varied in the degree of niche partitioning, i.e. the overlap in interaction partners between coexisting species. We found that community‐wide dispersal distances were longest when networks had low degrees of niche partitioning. We further found that dispersal distances of plant species with small fruits peaked in models without niche partitioning, whereas dispersal distances of medium and large‐fruited plants peaked at low degrees of niche partitioning. Our simulations demonstrate that the degree of niche partitioning between species is an important determinant of the ecological functions derived from ecological networks and that simulation approaches can provide new insights into the relationship between the structural and functional components of ecological networks.

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Section: Discussionsupporting

confidence: 92%

Community‐wide seed dispersal distances peak at low levels of specialisation in size‐structured networks

Sorensen

Donoso

Neuschulz

et al. 2020

Oikos

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“…The loss of species from a community is often uneven across traits or ecological strategies. For example, losses are often biased towards large-bodied species (Santini et al 2017) leading to the decline or loss of long-distance seed dispersal as well as altering the quantity of seeds dispersed (McConkey et al 2012, Donoso et al 2020.…”

Section: Validity Of the Analysesmentioning

confidence: 99%

“…Human‐induced alteration of composition of animal communities, such as changes in the number of individuals or species has been shown to impact seed dispersal patterns (Fontúrbel et al 2015). In particular, LDD has been significantly reduced by defaunation or species loss (Donoso et al 2020). Previous work has demonstrated that the loss of megafauna (i.e.…”

Section: Introductionmentioning

confidence: 99%

Human‐induced reduction in mammalian movements impacts seed dispersal in the tropics

et al. 2021

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Seed dispersal is a key process affecting the structure, composition and spatial dynamics of plant populations. Numerous plant species in the tropics rely upon animals to disperse their seeds. Humans have altered mammalian movements, which will likely affect seed dispersal distances (SDD). Altered SDD may have a range of consequences for plant communities including reduced seedling recruitment and plant biomass, seed trait homogenization, altered gene flow and a reduced capacity to respond to environmental changes. Therefore, modelling the consequences of altered animal behaviour on ecosystem processes is important for predicting how ecosystems will respond to human impacts. While previous research has focused on the link between animal species extirpation and SDD, it remains unclear how changes in mammalian movement will impact SDD. Here we implemented a mechanistic modelling approach to examine how mammalian movement reductions impact SDD in the tropics. We combined allometric theory with a mechanistic seed dispersal model to estimate SDD via the movement of 37 large frugivorous mammals (> 10 kg) in the tropics under different levels of human footprint, a global proxy of direct and indirect human disturbances. Our results suggest that assemblage-level SDD reductions are estimated to be up to 80% across the tropics in response to human disturbance. This is particularly the case in areas with high human impact such as agricultural landscapes and suburban areas. The region with the largest reductions in SDD was the Asia-Pacific with average reductions of 25%, followed by Central-South America (16%) and then Africa (15%). Our study provides insights into how human-induced changes in movement behaviour of large mammals could translate into altered ecosystem functioning.

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“…Similarly, lateral nutrient movement by terrestrial mammals has been estimated to have reduced by >90% following the downsizing of mammals over the last 10,000 years (Doughty, Roman, et al, 2016; Hempson et al., 2017) while global microbe dispersal in faeces has decreased seven‐fold, possibly increasing independent microbial evolution through an ‘island biogeography effect’, which is believed to increase the emergence of infectious diseases (Doughty et al., 2020). Likewise, significant reductions in seed dispersal have been shown following changes to populations of large frugivorous bird species (Donoso et al., 2020; Jordano et al., 2007; Wotton & Kelly, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…At present, dispersal models that assess biological dispersal of seeds, nutrients and microbes across a broad suite of taxa often use generalised mass‐based scaling parameters for gut passage time (e.g. Donoso et al., 2020; Doughty et al., 2020; Doughty, Roman, et al, 2016; Hempson et al., 2017; Pires et al, 2018; Sorensen et al., 2020; Viana et al., 2013; Wolf et al., 2013; Yoshikawa et al., 2019). The reasoning behind the choice of allometric scaling is based on theoretical grounds as gut capacity scales linearly to body mass (BM 1.00 ) and dry matter intake to the metabolic rate (BM 0.75 ; Demment & Van Soest, 1985).…”

Section: Introductionmentioning

confidence: 99%

Improved estimation of gut passage time considerably affects trait‐based dispersal models

et al. 2021

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Animals are important vectors for transporting seeds, nutrients and microbes across landscapes. However, models that quantify the magnitude of these ecosystem services across a broad range of taxa often rely on generalised mass‐based scaling parameters for gut passage time. This relationship is weak and fundamentally breaks down when considering individual species, indicating that current models may incorrectly attribute or estimate the magnitude of dispersal. We collated a large dataset of gut passage time for endothermic animals measured using undigested markers (n = 391 species). For each species, we compiled trait data, including body mass, morphology, gut physiology, diet and phylogeny. We then compared the ability of five statistical models (constant, generalised least squares, phylogenetic generalised least squares, general linear model and random forest) to estimate the time of first marker appearance (transit time; TT) and mean marker retention time (MRT) for particle and solute markers in mammals and birds separately. For mammals, we found that the inclusion of additional traits appreciably reduced the median root‐mean squared error across all markers in a leave‐one‐out cross validation. For birds, however, additional traits did not significantly improve our ability to predict gut passage time across markers. This may have occurred due to the smaller number of bird species included in our analysis or the absence of important explanatory factors such as differences in gastrointestinal morphology. Using the MRTparticle random forest model from this study, we updated two trait‐based dispersal models for seed and nutrient movement by mammals. The magnitude of dispersal in our updated predictions ranged from 66% to 176% of the original model formulation for different scenarios, highlighting the importance of gut passage time for dispersal models. Furthermore, the contribution by individual or groups of species was found sizeably altered in our updated models. Future modelling studies of dispersal by mammals, for which empirical estimates of gut passage time are absent, will benefit from predicting gut passage time using statistical models that incorporate traits including animal morphology, diet and gut physiology. A free Plain Language Summary can be found within the Supporting Information of this article.

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Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks

Cited by 51 publications

References 74 publications

Community‐wide seed dispersal distances peak at low levels of specialisation in size‐structured networks

Community‐wide seed dispersal distances peak at low levels of specialisation in size‐structured networks

Human‐induced reduction in mammalian movements impacts seed dispersal in the tropics

Improved estimation of gut passage time considerably affects trait‐based dispersal models

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