Consequences of Lemur Loss for Above-Ground Carbon Stocks in a Malagasy Rainforest
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Anthropogenic disturbances have resulted in declines of seed-dispersing primate frugivores in tropical forests. Previous work has suggested that loss of seed dispersal by large frugivores may have a negative impact on ecosystem carbon storage by reducing tree biomass. However, we know little about the potential impacts of losing frugivores in Madagascar’s diverse rainforest ecosystem. Understanding the effects of frugivore extinction on carbon loss is relevant in Madagascar, where threatened lemur taxa are the only dispersers of many large-seeded plant species. Using a dataset of tree species composition and traits from the southeastern rainforests of Ranomafana National Park, we examined whether seed size and lemur-dependent dispersal are positively associated with above-ground tree biomass. We then simulated different scenarios of population declines of large-seeded trees (>10 mm seed length) dependent on lemur-mediated seed dispersal, to examine potential directional changes in carbon storage capacity of Malagasy forests under lemur loss. Lemur-dispersed tree species, which have large seeds, had higher above-ground biomass than other species. Our simulations showed that the loss of large frugivorous primates in Madagascar may decrease the forest’s potential to store carbon. These results demonstrate the importance of primate conservation for maintaining functioning ecosystems and forest carbon stocks in one of the world’s hottest hotspots of biodiversity.
KeywordsAbove-ground biomass Conservation Extinction Primate Seed dispersal Tropical forest
Anthropogenic disturbances have resulted in significant declines and/or loss of vertebrate species worldwide (Dirzo et al. 2014; Johnson et al. 2017; Malhi et al. 2016). In addition to the direct impact of species loss on biodiversity, there is increasing concern that this pattern of biodiversity loss may also result in negative, cascading impacts at the ecosystem level (Dirzo et al. 2014; Galetti and Dirzo 2013). Because vertebrates perform important ecological roles, understanding functional consequences of vertebrate declines is important for understanding long-term impacts of environmental change. A pervasive pattern in the tropics has been the loss of large-bodied frugivores, including primates, which are important seed dispersers for many large-seeded plant species. Loss of large frugivores could favor fast-growing pioneer trees, which tend to rely on wind or small birds for dispersal (Foster and Janson 1985), and that hold less biomass than larger, mature-forest species. Loss of vertebrates could thus reduce a forest’s potential for above-ground carbon storage, by altering the trait composition of plant communities. While recent studies in the Neotropics and Africa have suggested that vertebrate loss is likely to reduce above-ground biomass through changes in plant communities, generalizations may not hold across tropical regions (Bello et al. 2015; Osuri et al. 2016; Peres et al. 2016). Impacts of vertebrate declines on above-ground carbon storage are not evident in Asia, for example, where there is an abundance and diversity of large, wind-dispersed tree species (Harrison et al. 2013; Osuri et al. 2016).
In Madagascar’s tropical ecosystems, frugivorous lemurs constitute a large portion of the frugivore biomass and are the primary seed dispersal agents for many large-seeded plant species (see review in Razafindratsima 2014). With a majority of lemur species threatened with extinction (Schwitzer et al. 2014), there are increasing concerns about the negative consequences of lemur loss on forest composition, regeneration, and dynamics (Federman et al. 2016; Ganzhorn et al. 1999; Razafindratsima and Dunham 2015). For instance, a recent study reports a fourfold lower recruitment probability for a population of an abundant, long-lived canopy tree species in the absence of lemur frugivores (Razafindratsima and Dunham 2015). However, we know relatively little about the potential impacts of losing lemurs at the ecosystem level, including whether their loss might affect carbon storage in Malagasy forests.
Madagascar’s tropical forests represent an important reservoir of terrestrial carbon. For instance, a recent study in Madagascar’s northern humid forests estimates a mean above-ground carbon density of 99.5 metric ton (Mg) C/ha with estimates ranging as high as 257.4 Mg C/ha (Asner et al. 2012). Unfortunately, the potential of Malagasy forests to store carbon is threatened by not only incessant deforestation, fragmentation, and logging (Allnutt et al. 2013; Ganzhorn et al. 2001; Harper et al. 2007), but also by the potential disruptions of frugivore-mediated seed dispersal. The potential impact of losing Madagascar’s largest frugivores on above-ground carbon storage is unknown but understanding potential patterns is important for maintaining ecosystem services and the long-term conservation of these unique ecosystems.
Loss of seed dispersal service from Madagascar’s biodiverse forests may be especially critical because Madagascar is already poor in terms of frugivore richness (Fleming et al. 1987), which is highly threatened by increasing anthropogenic pressures (Dewar and Richard 2012; Ganzhorn et al. 2001). Large-bodied lemurs may play a disproportionate role as seed dispersal agents in Madagascar because 1) many Malagasy tree species have traits adapted for seed dispersal by frugivores, and 2) large-bodied lemurs (>1 kg) are often the only seed dispersers for tree species with the largest seeds (Bollen et al. 2004; Martinez and Razafindratsima 2014; Razafindratsima 2014; Razafindratsima and Martinez 2012; Razafindratsima and Razafimahatratra 2010). Unfortunately, ca. 94% of lemur species (N = 101) are currently under high risk of extinction (Schwitzer et al. 2014), from fragmentation, hunting, and climate change (Barrett and Ratsimbazafy 2009; Borgerson et al. 2016; Dunham et al. 2008, 2011; Ratsimbazafy et al. 2012; Schwitzer et al. 2014), with the larger species at greater risk (Fritz et al. 2009).
Here, we examine the potential impacts of losing Madagascar’s threatened large-bodied frugivores (diurnal lemurs) on above-ground biomass in a diverse rainforest ecosystem. The impacts of losing large frugivores are expected to be greatest in systems that are structured by compatibility in size between plants and animals (“size matching”; Donoso et al. 2017). Thus, we first examined whether plant traits, including seed size and lemur-dependent dispersal, were positively associated with above-ground tree biomass. Then, we examined potential directional changes in carbon storage capacity of Malagasy forests under lemur loss by simulating different scenarios of population declines of large-seeded lemur-dispersed trees. Our dataset includes trait measurements of 7233 individuals of 275 tree species and the species composition of eight 1-ha plots scattered throughout the rainforest of Ranomafana National Park, in southeastern Madagascar. Our simulations estimate forest compositional change after lemur loss and were run under different scenarios in which lemur-dispersed tree individuals were removed at an increasing percentage and replaced by randomly drawing individual trees from the remaining pool.
Ranomafana National Park (RNP), located in southeastern Madagascar (47°18′–47°37′E, 21°02′– 21°25′S), comprises an area of 41,600 ha of evergreen rainforest and is home to more than 330 species of trees and large shrubs (Razafindratsima and Dunham 2015). The assemblage of known seed dispersers of the diverse plant species in RNP (Dew and Wright 1998; Rakotomanana et al. 2003; Razafindratsima 2014; Razafindratsima and Dunham 2015; Razafindratsima et al. 2014) consists of three large-bodied diurnal lemur species (mean body mass ca. 2.00–3.50 kg; one classified as Critically Endangered and two Vulnerable), two small-bodied lemur species (mean body mass ca. 0.04–0.5 kg on average; one classified as Vulnerable and one as Data Deficient), three bat species (mean body mass ca. 0.05-0.36 kg on average; two classified as Vulnerable and one as Near Threatened) and six bird species (mean body mass ca. 0.01–0.20 kg on average, all classified as Least Concern) (body mass measurements: Razafindratsima et al. 2018b, c; threat status: IUCN 2017). The interior forests of RNP are estimated to have a mean above-ground biomass of 243 Mg/ha (Razafindratsima et al. 2018a).
The dataset on the tree community used in this study was from surveys within eight 1-ha plots scattered throughout RNP (cf. map in Electronic Supplementary Material [ESM] Fig. S1). We obtained data on six plots through the online database of the Tropical Ecology Assessment and Monitoring Network (http://www.teamnetwork.org/, dataset identifier: TEAM-DataPackage-20170908090439_2451). We considered only the latest survey, conducted in 2016–2017, from this multiple-year monitoring dataset and removed any dead individuals. With the help of local research technicians trained in florisitic identification, O. H. Razafindratsima conducted vegetation surveys in two additional 1-ha plots in 2015–2016. In each plot, all trees of >10 cm diameter at breast height (DBH) in each plot were identified. For accuracy and consistency in nomenclature, we checked and standardized all species names and families in accordance with the currently accepted taxonomies in the Taxonomic Name Resolution Service v4.0 (http://tnrs.iplantcollaborative.org/). We excluded nonwoody vegetation (such as tree ferns), lianas, and unknown tree species. In total, our dataset comprised 7233 individuals of 275 tree species, 127 genera, and 57 families in all 8 plots.
We compiled data on seed dispersal mode, seed length, and wood density for each tree species in our vegetation plots. Following previous studies of seed dispersal in this system, we categorized species as primarily dispersed by birds, lemurs, or both groups of frugivores (“mixed” dispersal mode), and dispersed by abiotic means (such as by explosion and wind) (Razafindratsima et al. 2018a). We gathered data on seed dispersal mode of each species from our own observations of frugivory interactions, from the long-term knowledge of the local fauna and flora by local field technicians in RNP, and from the literature (Dew and Wright 1998; Overdorff 1993; Rakotomanana et al. 2003; Razafindratsima and Dunham 2016; Razafindratsima et al. 2014, 2017, 2018a; White et al. 1995). We selected length to represent seed size, although seed diameter may also be a limiting trait for seed ingestion in some frugivores (Galetti et al. 2013; Levey 1987), because seed length and diameter are strongly correlated in our system such that species long seeds are also wide (ESM Fig. S2), and to ensure more robust comparison with other studies, which use this metric as their seed size index (Osuri et al. 2016). We obtained data on seed length (measurement along the longest axis of the seed) through our own measurements in the field and in herbaria, and from literature (Dew and Wright 1998; Overdorff and Strait 1998; Razafindratsima et al. 2017, 2018a). We assigned mean genus-length level for species without known seed length (this included genera that are not in this study’s dataset but occur in RNP), given that seed length at the species and genus levels are often positively correlated (Osuri et al. 2016). We obtained data on wood density (g/cm3) from the literature (Razafindratsima et al. 2017, 2018a), from the Global Wood Density Database (Chave et al. 2009; Zanne et al. 2009), and from our own field measurements of oven-dried wood mass over green volume of tree cores, following the procedures in these published measurements. For species with unavailable wood density values, we assigned the mean genus and family levels following previous studies (Bello et al. 2015; Lewis et al. 2009; Osuri et al. 2016; Slik et al. 2013). Genus-level means of wood density provide useful approximation values for the species values because wood density has been found to be conservative at the genus level (Chave et al. 2006). We used these estimates of trait values at the genus and family levels only in the simulations, but not for assessing allometric relationships. ESM Fig. S3 presents the distributions of trait data across the different dispersal modes.
Relationship Between Seed Size and Biomass-Related Traits
We examined the relationships between each biomass-related traits (DBH and wood density) and seed length, by performing Generalized Linear Models in R v. 3.4.1 (R Core Team, Vienna), using the “Gaussian” family. Only the variable wood density was normally distributed, even when we log-transformed the data. The performances of the GLMs are presented in ESM Fig. S4.
Carbon Storage Estimations
We combined the eight plots into one large community; our dataset for simulation of carbon changes included only species with data on all four traits (seed length, dispersal mode, DBH, and wood density), for a total of 4226 individuals. To simulate changes in the tree community, we ran two hypothetical scenarios: 1) Directed, in which large-seeded (>10 mm length) tree species that are primarily dispersed by lemurs were removed and then replaced, and 2) Random, in which tree removal was independent of seed size and dispersal mode. In the directed scenario, species with mixed dispersal mode (i.e., dispersed by both birds and lemurs) were not treated as primarily lemur-dispersed because birds may be able to compensate for the loss of lemur frugivores and disperse the seeds of these species. As a conservative measure, we used a cutoff of 10 mm seed size for our trees already characterized as primarily lemur-dispersed because these larger seeds are less likely to have compensatory dispersal by other frugivores in the system. In each scenario, we removed/replaced an increasing percentage of individual trees (25%, 50%, 75%, and 100%) and ran the simulations 1000 times for each percentage category. Each simulation had two steps: 1) Removal of individual trees from the community, and 2) Random draw of individual trees from the remaining community to replace the lost individuals and construct a new final community. The number of individuals removed in Directed and Random scenarios was the same. We calculated the community-level carbon storage by summing up the carbon stored in each individual tree in the initial community and in each final simulated community. Carbon change is reported as the percentage of change (increase or decrease) from the initial carbon to the final carbon. For each simulation run, we also calculated community-stand wood density and volume (which is the second part of the foregoing biomass equation). We examined whether the estimated carbon changes under the Directed scenario were related to overall changes in community-level volume and/or wood densities by performing Pearson correlation tests. Simulations and calculations were run using basic functions implemented in R.
The datasets analyzed during the current study are available from the corresponding author on reasonable request.
Data collection efforts adhered to the legal requirements of Madagascar (Wilmé et al. 2016), where the research was conducted. This research did not involve animal handling. The authors declare no conflict of interest.
Large frugivorous vertebrates, including primates, are experiencing high rates of population decline across the tropics as a result of human activities (Dirzo et al. 2014; Fritz et al. 2009; Malhi et al. 2016). In systems in which large dense trees tend to rely on large frugivores to disperse their seeds, frugivore loss could have negative consequences for above-ground carbon storage (Bello et al. 2015; Galetti and Dirzo 2013; Kurten 2013; Nuñez-Iturri and Howe 2007; Terborgh et al. 2008). Our data and simulations from Madagascar’s southeastern rainforest suggests that if lemur extinctions result in population declines of trees that specialize on lemurs for dispersal, reduction of above-ground tree biomass is a likely outcome. The simulated replacement of large-seeded, lemur-dispersed tree species decreased estimated above-ground biomass by an average of about 5% under the 50% directed scenario (half of the individuals of large-seeded lemur-dispersed trees lost from communities and replaced with individuals of other species), and by an average of about 9% under the 100% replacement scenario. These results are similar in scale to studies simulating removal and replacement of large-seeded trees in other tropical forests, where a large majority of trees are dispersed by vertebrates (Osuri et al. 2016). These results highlight the potential for lost ecosystem services as Madagascar’s larger-bodied (>1 kg) lemur populations continue to edge towards extinction. Our results support the suggestion that maintaining populations of large frugivores should be included as part of the agenda for conservation programs aimed at reducing emissions and maintaining long-term carbon stocks in tropical forests, such as the REDD+ program (Peres et al. 2016).
To assess potential impacts of losing large frugivores on above-ground carbon storage, we applied models used in previous studies of Africa, Asia, and the Neotropics to allow a comparison with Madagascar (Bello et al. 2015; Osuri et al. 2016). Our results suggest consequences of large frugivore loss similar to that found for Neotropical, African, and Indian rainforests, where endozoochory is also the main mode of seed dispersal, but not in Malaysia, Australia, or Indonesia, where seed dispersal by wind is common among large tree species (Bello et al. 2015; Osuri et al. 2016; Peres et al. 2016). Across the tropics, it appears that downsizing in ecological networks (i.e., when larger species are lost) is likely to have the greatest impacts when interactions are structured by size matching (Donoso et al. 2017), such as when large trees are dependent on large frugivores for dispersal and recruitment. In Madagascar, understanding the impacts of defaunation is especially important given the high levels of extinction risk facing large-bodied lemurs on the island (Schwitzer et al. 2014).
Our current study and previous work using such simulations rely on the assumption that disperser loss will negatively impact tree fitness. In Madagascar, frugivorous lemurs have been shown to positively influence 3-year sapling recruitment (Razafindratsima and Dunham 2015). However, because of the difficulty in studying population dynamics of long-lived organisms such as trees, empirical data are limited on impacts of frugivores on adult tree populations. Our simulations may overestimate impacts of frugivore loss on above-ground biomass if later stages of tree recruitment ultimately drive population sizes of adult trees. We also know little about how other organisms may compensate for the loss of large lemurs in this system. Because of this uncertainty, we feel it is inappropriate to make specific quantitative predictions of carbon loss after lemur extinction. Regardless, our results suggest that the decline of lemur-dispersed trees could reduce the forest’s ability to store above-ground carbon.
Loss of seed dispersal services by the lemur frugivores could have important effects on plant community composition if loss of dispersal services impacts demographic rates. While several studies have suggested negative demographic and genetic effects of losing large frugivores on large-seeded tree species (Carvalho et al. 2016; Laughlin 2014; Razafindratsima and Dunham 2015; Wotton and Kelly 2011), some studies have suggested that plants with lower partner diversity may depend less on mutualistic interactions (Fricke et al. 2017). In addition, the loss of large seed dispersers may be compensated through secondary seed dispersal (Culot et al. 2017; Jansen et al. 2012). In Madagascar, large-seeded tree species have specialized mutualisms with large frugivorous primates; but some authors have suggested that secondary dispersal of these tree species could be performed by ground-dwelling rodents (Dausmann et al. 2008; Ganzhorn et al. 1999; Goodman and Sterling 1996; Razafindratsima 2014). However, even though native rodents have been observed to remove seeds on the ground in Malagasy systems (Dausmann et al. 2008; Goodman and Sterling 1996), there are no known scatter-hoarding rodents and currently no evidence of secondary dispersal by larder-hoarding rodents (Razafindratsima 2017). To resolve this, more studies are needed to understand the importance of seed dispersal for the recruitment of large-seeded plants across systems.
In recent decades, a looming threat to Madagascar’s biodiverse tropical forests has become apparent as Malagasy flora face increased threat of losing critical seed dispersers (Razafindratsima 2014). Lemurs play important ecological role in plant communities as seed dispersers because many Malagasy plant species are dispersed by lemurs (Birkinshaw 1999; Bollen et al. 2004, 2005; Razafindratsima 2014). Unfortunately, large-bodied lemurs are facing especially high risk of extinction through the combined effects of hunting, habitat destruction and even climate change (Barrett and Ratsimbazafy 2009; Borgerson et al. 2016; Dewar and Richard 2012; Dunham et al. 2008, 2011; Schwitzer et al. 2014). Our findings highlight the fragility of Malagasy tropical forests and the urgent need to develop more efficient ways to protect Malagasy primates for maintaining forest integrity and ecosystem services in one of the world’s hottest hotspots of biodiversity.
We thank numerous field research technicians for their valuable help in data collection and species identification. Part of the data used in this publication were provided by the Tropical Ecology Assessment and Monitoring (TEAM) Network, a collaboration between Conservation International, the Missouri Botanical Garden, the Smithsonian Institution, and the Wildlife Conservation Society, and partially funded by these institutions, the Gordon and Betty Moore Foundation, and other donors. We also thank Yamato Tsuji and two anonymous reviewers for their insightful comments that improved an earlier version of this manuscript.
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