Table 1. Number of published articles on the impact of habitat degradation of tropical montane forests TMF in three major regions per unit area of forest. Figure 3.
Map of the number of articles published from to on the impacts of habitat degradation on tropical montane biodiversity in different countries. The diameter of the circles is directly proportional to the number of published articles. Country names represent the highest number of articles published in the region. At the ecological level, most research focused on community ecology, followed by research on ecosystem functioning, species interactions, population ecology and population genetics Figure 2B.
Most articles studied the effects of deforestation, followed by land-use change, fragmentation and edge effects Figure 2C. Plants were the most studied taxon, followed by arthropods and birds Figure 2D. There were articles focused on community ecology, with most articles from Latin America and the fewest from Southeast Asia.
The best studied taxa were vascular plants followed by insects and birds Table 2. Most studies used species richness and species composition beta diversity to measure the impacts of environmental change, with only a few measuring functional diversity Figure 4A. Table 2. Number of articles on the impact of habitat degradation of tropical montane forests at various ecological levels distributed across regions, impact types and taxonomic groups.
Figure 4. A Number of published articles on the impacts of habitat degradation on tropical montane biodiversity using different community response metrics. The proportion of articles showing the community responses to deforestation and habitat disturbance measured using B species richness; and C species composition. The numbers in parentheses refer to the number of articles for each type of response. Of 69 articles on ecosystem services, most were from North America largely from Mexico; Table 2.
Ecosystem services were broadly classified as water regulation including erosion control and purification, maintenance of soil fertility, carbon storage and sequestration, and nutrient cycling.
Each category was well-represented, with a slight bias toward articles exploring hydrological impacts and soil fertility Figure 5A. Figure 5. Number of articles published on the impacts of habitat degradation on tropical montane biodiversity studying different types of A ecosystem services, and B species interactions.
The impacts measured were almost equally represented, with edge effects slightly more studied than deforestation, land conversion or fragmentation Table 2. Studies on predation often lacked identification of the predators, due to the rarity of documenting such events. Population ecology i. Survival rates and fitness-related traits e. To assess the conservation statuses of species in the population studies, we omitted two articles that measured demographic parameters but with a greater focus on community level responses Hitimana et al.
Figure 6. Number of population ecology articles published on the impacts of habitat degradation on tropical montane biodiversity that: A measured different demographic parameters, and B studied species listed in the various categories of the IUCN Red List.
Only 12 articles described genetic studies Table 2. The earliest study from explored the impacts of habitat degradation logging on the genetics of an endemic species of oak in China Zheng et al. Other genetic studies were published from to , with six from Latin America, four from Africa and one from Asia Table 2.
Most explored the impacts of habitat degradation on a single focal species, but two drew comparisons between two species Winkler et al. Most articles examined the impact of fragmentation or edge effects on genetic diversity or gene flow, while a few studied the effects of deforestation or land-use change Table 2.
A myriad of habitat degradation effects on biodiversity and ecosystem services in TMFs were reported Figure 7. Equivocal or inverse responses in species richness may be due to sampling in habitats with intermediate levels of degradation, which often show higher species richness than pristine environments e.
The main cause cited was higher resource availability e. Changes in species composition across a disturbance gradient were often reported, with resilient species more likely to be generalists e. Figure 7. Schematic of the major effects of habitat degradation on tropical montane forest across levels of organization.
The degradation of TMF can be detrimental to some species interactions such as predator-prey e. Increased predation of seedlings was observed in deforested areas due to a lack of concealment from predators Anthelme et al. Habitat degradation also interfered with mutualistic relationships between plant and soil microbes. For example, plant growth showed a positive response to soil filtrate from TMF due to the presence of beneficial soil microbes, but was negatively affected by soil filtrate from pastures Pizano et al.
Parasitic infections generally intensified with increased habitat disturbance. Amphibian chytrid fungus Batrachochytrium dendrobatidis was most prevalent in agroforests Murrieta-Galindo et al. There were a small number of TMF articles that have investigated how populations respond to habitat degradation. From these studies, habitat fragmentation was shown to reduce the population size of birds and foxes Husemann et al.
For example, the effective of population sizes of the mountain white-eye Zosterops poliogaster in East Africa were higher in larger and interconnected forest patches Husemann et al. Habitat fragmentation can also decrease fecundity in plants Somanathan and Borges, ; Franceschinelli et al.
Fragmentation also resulted in reduced plant survival which could be attributed to higher desiccation and seedling predation Alvarez-Aquino et al. Trees in isolated patches were also found to be to have altered plant sex ratios apart from natural populations due to a lack of pollinator visits to female trees Somanathan and Borges, While genetic studies conducted in TMFs were rare, most revealed that populations in isolated forests had lower genetic diversity due to inbreeding and reduced gene flow Cascante-Marin et al.
For example, a lack of genetic variation in epiphytic bromeliad Guzmania monostachia populations in Costa Rican forest patches was attributed primarily to anthropogenic barriers to gene flow but could also be influenced by life history traits such as its selective breeding system and limited seed dispersal ability Cascante-Marin et al.
Habitat degradation in TMFs has been shown to disrupt several hydrological processes like affecting water conduction in soils, with reduced hydraulic conductivity in secondary forests and plantations Marin-Castro et al. In turn, this likely contributed to increased surface runoff in cultivated land Lorup and Hansen, ; Munoz-Villers and McDonnell, ; Suescun et al. With increasing surface water runoff, streamflow in degraded landscapes can be higher following rainfall Munoz-Villers et al.
Water storage was also lower in agricultural areas Guardiola-Claramonte et al. Land conversion in TMFs can lead to declines in mean carbon densities due to biomass loss De Jong et al. Impacts of land conversion on soil organic carbon SOC are less conclusive; most studies reported lower SOC in cultivated land relative to montane forest e.
Such conflicting results may be attributed to variation in soil properties, age since disturbance, the type of cultivated land, and altitude Twongyirwe et al. Habitat degradation in TMF can lead to marked changes in N storage and conversion rates. Total dissolved nitrogen was higher in plantations than in TMF catchments, probably due to more leaching Jacobs et al. Additionally, the rate of N decay from leaf litter in plantations, or in streams within pastures, was slower compared to natural TMFs Encalada et al.
Land use change alters the properties of montane soils, such as decreasing soil moisture Schrumpf et al. Soil microbial biomass generally declines as land disturbance intensifies Campos et al.
Macroinvertebrate diversity in soils is lower in deforested sites Yankelevich et al. Our method of gauging research effort per country, by aggregating the number of studies stemming from the country of interest, is likely biased by the extent of TMFs available. Estimating the number of studies per area unit of TMF in each country will provide better resolution. Another caveat to note is that community responses were tabulated without accounting for the intensity of disturbance, beyond broad classifications of habitat types.
Also, our classifications did not consider spatial differences among studies, and the impacts of habitat degradation at a site, country or regional scale will vary. Last, our assessment of articles covering ecosystem services mainly focused on those that provided supporting and regulation services, with less emphasis on provisioning and cultural services Alcamo and Bennett, A separate systematic review on the impacts of habitat degradation on the ecosystem services provided by TMFs is recommended by using additional search terms e.
Average annual deforestation rates from to for montane forests in Southeast Asia ranged from 0. While roads are essential for economic development, they are a major threat to biodiversity Laurance et al. In Peninsular Malaysia, the construction of the second East-West highway, completed in , has led to rampant deforestation in the Lojing Highlands despite regulations that restrict logging above 1, m Singh, Much of the cleared land has been converted to agricultural farms Omar and Hamzah, Alarmingly, nearly half of montane primary forest loss in Indonesia has occurred within protected areas Margono et al.
To tackle illegal logging, Malaysian and Indonesian governments have implemented schemes that award certification to producers that promote sustainable logging practices e. However, such initiatives have not stopped deforestation of protected areas Peh et al. Imposing sanctions on non-compliant timber producers, and stricter assessments to gain certifications are needed to secure the remaining TMFs in Asia Chitra and Cetera, Research in African TMFs was also poorly represented globally, yet much of Africa's TMF is threatened from overexploitation through illegal logging and poaching, and habitat loss via land conversion to agriculture and charcoal burning Cronin et al.
Although there are designated protected areas in Africa, their coverage is inadequate and many protected sites are poorly managed Cronin et al. Further, the heavy reliance of fertilizers in farms increases nutrient loads in streams that lead to a deterioration in water quality and eutrophication Jacobs et al. Political unrest in countries such as Sudan also affect the state of natural resources, such as those in the Imatong Mountains and surrounds which are part of the Eastern Afro-montane ecosystem—considered to be one of Africa's biodiversity hot spots Uma, Two decades of civil war have decimated large swathes of forest, particularly on Mount Dongotomea, with two-thirds of the forest lost since Gorsevski, ; African Wildlife Foundation, A lack of livelihoods for returning refugees and strong dependence on natural resources has led to increased poaching for bushmeat, illegal logging and fires set deliberately for shifting agriculture Gorsevski, ; African Wildlife Foundation, Articles describing research conducted in Mexico comprised a third of all relevant papers in this mapping exercise.
Deforestation rates in the highlands of Mexico have also intensified sharply Cayuela et al. In the Chiapas highlands, the annual rate increased from 1.
More recent estimates of TMF deforestation rates are lacking in Mexican TMF, and considering that the last reported deforestation rates were rising nearly two decades ago, an updated estimate is crucial to assess the current extent of forest loss and re-valuate its impact to montane biota.
These included changes in species distribution and population sizes, germination and seedling development, community structure, food webs and nutrient availability. For example, the altitudinal distribution of several dung beetle species was higher in deforested areas where it was hotter and drier than in intact landscapes Larsen, Harsher microclimates in altered habitats negatively affected germination rates, seedling development and recruitment, which in turn hampered recolonization rates Werner and Gradstein, ; Anthelme et al.
Epiphyte species richness declined due to warmer and drier microclimates in disturbed forests Barthlott et al. Clearly, the most urgent research priority with regards the impacts of habitat degradation on TMF is to understand its effects on population genetics Figure 8. Aside from there being so few genetic studies of species occurring in this forest type, the preservation of genetic diversity is fundamental in maintaining viable populations that have adaptive potential. We suggest applying next-generation sequencing NGS in future genetic research, as inferences from NGS are drawn genome-wide Angeloni et al.
This is unlike the studies identified via our systematic map, where traditional methods like Sanger sequencing or microsatellites targeted only a few genes. Figure 8. Research priorities for conserving the world's tropical montane forest ecosystems, indicated in order of importance. A logical group for thorough evaluation of their genetic structure are threatened or endemic species, many of which are likely to exist as small populations that are vulnerable to the effects of genetic drift.
The findings from the limited number of studies conducted in TMF have shown expected results: 1 habitat fragmentation can impede gene flow and lead to a loss of genetic variation, and 2 , improving fragment connectivity can help reserve this trend. Where possible, drawing inferences on gene flow and genetic diversity from multiple species within an ecosystem is ideal, as species responses to fragmentation can differ in concert with variation in species traits.
For instance, a study of montane forest birds in Kenya revealed tighter genetic clustering among sedentary species compared to more mobile species Callens et al. Further, generalist species are often more robust to the impacts of habitat fragmentation Janecka et al. Not yet documented in our mapping exercise are studies that examine the role played by habitat degradation and likely interactions with climate change on introgression in TMF biota.
Introgression is the hybridization of closely related species accompanied by repeated back-crossing of the hybrid with a parent species Anderson, It is pervasive in natural populations and can accelerate the loss in genetic diversity Harrison and Larson, A study in the Ethiopian highlands found that the wild gene pool for Coffea arabica had admixed with cultivars grown in close proximity to natural populations Aerts et al.
If so, montane endemics may experience genetic swamping i. Research that investigates the impacts of habitat fragmentation and edge effects on montane biota should also be prioritized, as the results will have profound implications for sustainable land-use planning e.
Although fragmentation is well-known for reducing gene flow, it has far-reaching consequences at all ecological levels, including ecosystem services. In general, fragmentation has a negative impact on communities; resulting in a decline in species richness e. However, some studies have highlighted that certain spatial characteristics such as fragment area and isolation have no effect on abundance, density or diversity Muriel and Kattan, ; Ulrich et al.
While the extent of degradation may lead to conflicting results, deeper examination of species functional traits, which are indicators of habitat use, reveal that some groups within a community are more affected than others. For instance, two avian studies independently concluded that understory insectivores and canopy frugivores were more sensitive to fragmentation than other functional groups Kattan et al.
Thus, within-community differences should be accounted for in future fragmentation research in TMF. Our current understanding of the long-term effects of fragmentation is also limited by the scarcity of relevant historical data. In the short term, diversity may not be adversely affected by fragmentation and may even increase Rey-Benayas et al. Elucidating the environmental factors driving colonization and extinction patterns will allow better comprehension of community dynamics in a fragmented landscape.
Both are hierarchical models, but the dynamic model accounts for changes in occupancy over time by including sub-models of colonization and persistence that affect the previous occurrence state. Crucially, DCM models do not assume perfect detection among species, which can lead to misconstrued interpretations of occupancy dynamics.
A key recommendation from our mapping exercise is that effects of fragmentation should be examined at multiple spatial scales, as scaling dependencies in fragmented landscapes are vital for conservation planning Cushman and McGarigal, While broad spatial effects have been documented to affect biotic responses Chiavacci et al. For example, research on golden-cheek warblers, Setophaga chrysoparia , showed that landscape composition best predicted species density, but vegetation characteristics was the best predictor of nesting success Reidy et al.
Region-wise, research in Asian TMF is under-represented at all ecological levels, impact type and taxa Figure 8. The future discovery of new species is particularly likely in Southeast Asia, given the regions' unique biogeographical history Holloway and Hall, In the last 5 years, several new species were discovered in TMFs in Southeast Asia, including amphibians and reptiles from Vietnam Grismer et al.
In these regions, attaining baseline ecological data such as a country-by-country species inventory represents a crucial first step in efficient data-sharing, and accumulation of large databases that facilitate multidisciplinary ecological research. Although we encourage further research of poorly studied taxa, available data for better represented groups such as vascular plants and birds are already useful for comparative studies, and to gain perspective on the overall response of the biome to habitat degradation Figure 8.
Comparisons between the responses of endotherms and ectotherms will be of interest, as the latter are more likely to be adversely affected by degradation due to their sensitivity to microclimatic change and generally lower dispersal abilities. Greater attention should be given to how functional diversity, which characterizes the range of ecological roles played by species in a community, may be affected by anthropogenic change in TMFs Petchey and Gaston, Species richness estimates and related indices assume all species perform the same roles, but high species richness does not necessarily beget high functional diversity Stuart-Smith et al.
For example, while bird species richness and density in medium-sized fragments were higher than larger fragments in Mexican TMFs, larger fragments had a distinct functional composition, with a greater proportion of understory insectivore species and canopy frugivores Rueda-Hernandez et al. Furthermore, functional diversity may be a better predictor of ecosystem function than species richness or abundance indices Gagic et al.
Applying an ecological network is a useful approach to test the effects of degradation on species interactions at the community-level.
An ecological network is a collection of nodes represented by species that are joined by links that either represent antagonistic or mutualistic interactions Pascual and Dunne, The resilience of ecological networks can be compared along a disturbance gradient Harvey et al. In one study, seed-dispersal networks of birds in the montane forest interior and edge were compared, revealing that functional and interaction diversity were higher at forest edges Saavedra et al.
Such conflicting responses to habitat degradation may relate to different levels of disturbance in these networks i. As montane species are highly sensitive to disturbance Long, ; Brooks et al. The lack of population studies of TMF species in Southeast Asia is troubling given that the number of montane species threatened with extinction in this region may be underestimated Brooks et al. Indeed, some NE species may be included in national threatened species lists, however, evaluation against IUCN Red List criteria is crucial for formulating policy and prioritizing management of threatened species at multiple scales e.
Disappointingly, only a few articles investigated the effects of habitat fragmentation or edge effects on ecosystem services in tropical montane environments Table 2. Factors such as fragment size and isolation can influence ecosystem services; for example, regulation of crop pests is more effective next to a forest, but crop production is greatest at intermediate distances from a forest Mitchell et al. Careful consideration of the ecosystem services affected by fragmentation is crucial, as trade-offs between different services can be expected.
For instance, in a study of montane heathlands, decreasing fragment size reduced biodiversity and recreational value, but increased carbon storage and timber value Cordingley et al. The framework provided by Mitchell et al. Our systematic map has shown that habitat degradation in TMFs has had discernible impacts on biodiversity and ecosystem services.
While the impacts of this degradation are fairly well-studied at the community level, and adequate data may be available for meta-analysis, the impacts on genetic diversity and gene flow are less well-understood. Thus, population genetic studies should be prioritized for endemic species that are extinction-prone.
We used the distribution of occupancy estimates from Deramakot FR as our reference assemblage. We selected Deramakot FR as the reference because it is the least degraded site and is not subject to hunting pressure. We used Monte Carlo sampling to construct the probability distribution of D.
To do this we sampled random values from the posterior distributions of species-specific occupancy probabilities for all five sites for each species pair and used these values to calculate D where N k,r and N k,f are the occupancy of species k in the reference and focal assemblage, respectively.
We repeated this procedure 30, times to generate a distribution of D values. We scaled all covariates before analysis, with covariates scaled independently between the hunted and degraded sites, respectively. Numbers further from 0 indicate a stronger effect of the associated covariate. A positive effect size indicates that occupancy probability increases as the associated covariate increases.
Further information on research design is available in the Nature Research Reporting Summary linked to this article. The data used in this study are not publicly archived because it contain information on the locations of Red Listed as well as hunted and traded species. However, all data in support of the findings of this study are available from the corresponding author by reasonable request. Butchart, S. Global biodiversity: indicators of recent declines.
Science , — Bradshaw, C. Tropical turmoil: a biodiversity tragedy in progress. Article Google Scholar. Achard, F. The impact of hunting on tropical mammal and bird populations.
Dirzo, R. Defaunation in the Anthropocene. Redford, K. The empty forest. BioScience 42 , — Tilker, A. Saving the saola from extinction.
Science , Galetti, M. Ecological and evolutionary consequences of living in a defaunated world. Functional extinction of birds drives rapid evolutionary changes in seed size. Nasi, R. Empty forests, empty stomachs? Bushmeat and livelihoods in the Congo and Amazon Basins. Forestry Rev. Young, H.
Patterns, causes, and consequences of anthropocene defaunation. Margono, B. Primary forest cover loss in Indonesia over — Change 4 , Imai, N. Effects of selective logging on tree species diversity and composition of Bornean tropical rain forests at different spatial scales. Plant Ecol.
Hansen, M. High-resolution global maps of 21st-century forest cover change. Yue, S. Oil palm plantations fail to support mammal diversity. Alroy, J. Effects of habitat disturbance on tropical forest biodiversity. Natl Acad. USA , — Brooks, T. Habitat loss and extinction in the hotspots of biodiversity. Cleary, D. Bird species and traits associated with logged and unlogged forest in Borneo. Meijaard, E. Brodie, J. Differential responses of large mammals to logging and edge effects.
Burivalova, Z. Thresholds of logging intensity to maintain tropical forest biodiversity. Bennett, E. Hunting of wildlife in tropical forests - implications for biodiversity and forest peoples. Environment Department working papers; no. Biodiversity Series. The World Bank, Washington, D. Google Scholar.
Ripple, W. Open Sci. Cardillo, M. Multiple causes of high extinction risk in large mammal species. Bogoni, J. Landscape features lead to shifts in communities of medium-to large-bodied mammals in subtropical Atlantic Forest.
Cullen, L. Oryx 35 , — Di Bitetti, M. Differential responses to hunting in two sympatric species of brocket deer Mazama americana and M. Biotropica 40 , — Flesher, K. Protecting wildlife in a heavily hunted biodiversity hotspot: a case study from the Atlantic Forest of Bahia, Brazil. Tropical Conserv. Brashares, J. Economic and geographic drivers of wildlife consumption in rural Africa.
Sodhi, N. Southeast Asian biodiversity: an impending disaster. Trends Ecol. Evolution 19 , — De Bruyn, M. Borneo and Indochina are major evolutionary hotspots for Southeast Asian biodiversity. Phillipps, Q. John Beaufoy, Oxford, England, Princeton University Press, Baltzer, M. Towards a vision for biodiversity conservation in the forests of the lower Mekong ecoregion complex: summary of the biological assessment for the Ecoregion Biodiversity Conservation Program in the forests of the lower Mekong ecoregion complex WWF International, WWF Indochina, Van Dung, V.
A new species of living bovid from Vietnam. Nature , Tuoc, D. Introduction of a new large mammal species in Viet Nam. Surridge, A. Striped rabbits in southeast Asia. Averianov, A. Zoological Institute, St. Petersburg, Russia, Gaveau, D.
Four decades of forest persistence, clearance and logging on Borneo. PLoS One , 9, e Bennet, E. L Columbia University Press, Gray, T. The wildlife snaring crisis: an insidious and pervasive threat to biodiversity in Southeast Asia.
Hearn, A. The first estimates of marbled cat Pardofelis marmorata population density from Bornean primary and selectively logged forest. PLoS One 11 , e Responses of two sympatric species of peccaries Tayassu pecari and Pecari tajacu to hunting in Calakmul, Mexico. Ong, R. Sollmann, R. Diversity Distrib. Brozovic, R. Effects of forest degradation on the moonrat Echinosorex gymnura in Sabah, Malaysian Borneo.
Meyfroidt, P. Forest transition in Vietnam and its environmental impacts. Change Biol. Wilkinson, N. Report on effects of five years of snare removal patrols on snaring in the Thua Thien Hue - Quang Nam Saola Landscape: an analysis of data collected by Forest Guard patrols. Giacomini, H. An index for defaunation. Dorazio, R. Estimating size and composition of biological communities by modeling the occurrence of species.
Caro, T. On the use of surrogate species in conservation biology. Sinclair, A. Mammal population regulation, keystone processes and ecosystem dynamics. B: Biol. Clark, C. Logging concessions can extend the conservation estate for Central African tropical forests. Structurally complex habitats provide a wide range of ecosystem functions to the environment including food and refuge provision for other species, trapping sediment, modifying light and hydrodynamic conditions, providing resilience to the system.
When the habitats are lost this functions are lost with them [5] [4]. For example, the replacement of macroalgal canopies by turfs affects sediment dynamics on rocky coasts, where fronds prevents accumulation of sediments while turfs tend to trap sediments even on exposed coasts.
Habitat loss has been generally associated to drastic declines in overall abundance and diversity of marine organisms. For example, in the Wadden Sea, the destruction of biogenic habitats has caused the regional extinction of at least 26 species during the past years [6]. Similarly, the loss of seagrass meadows results in a reduction in the number of species and abundance of fishes. Generally, the environmental changes associated with the destruction of natural habitats promote the arrival and colonization of opportunistic species that can benefit from conditions in disturbed condition.
One example is the expansion of opportunistic green ephemeral algae or turf forming algae following the destruction of removal of canopy forming species, such as kelp. Other species that can favor from disturbed habitats condition are alien species. Once alien species are established they can contribute further to reduce local diversity by interacting with native species.
Some anthropogenic activities responsible for habitat destruction include the construction of coastal protection, land reclamation, aggregate sand and gravel extraction, recreation and developments including ports, harbours and industries. Additionally, the growing number of tourists presents a significant threat to many coastal habitats in Europe, which can disturb by trampling or direct harvesting.
In offshore waters, exploration and development of oil and gas activities threaten marine habitats, mainly with discharges of oil and other pollutants. Physical damage to marine habitats can result from fishing activities such as bottom trawling. Deep-water trawlers use heavy rock-hopping equipment, which has been reported to cause long-term to seabed habitats such as cold-water coral reefs in Norwegian, Scottish and Irish waters.
But while this research has confirmed that habitat destruction deeply influences the way species interact, until now we have lacked a full understanding of the effects of habitat loss on community stability. Similarly, we have not known to what extent community responses change depending on the nature of habitat loss. For our study, we looked into these issues of community stability and response using a mathematical representation of an ecological system.
This model simulates interactions and changes in species populations through time in a range of different landscapes — from pristine continuous habitats to highly fragmented habitats. These are based on what areas subjected to habitat loss look like in the real world. Our results suggest that habitat loss affects community stability, through changes in ecological interactions, by altering the abundance and spatial distribution of species through time.
And, as noted above, we also found that these ecological interactions change well before species extinctions. Limited animal movement between remaining habitats translates into negative changes in things like eating patterns, which in turn affects the way population sizes change through time and across space.
We also found that the specific way in which habitat is destroyed is a key determinant of the community responses to habitat loss.
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