Source-Sink Dynamics: a Neglected Problem for Landscape-Scale Biodiversity Conservation in the Tropics
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Ecologists have long recognised that populations can persist in poor-quality habitats with below-replacement population growth rates (‘sinks’) provided there is continual immigration from areas with positive intrinsic growth (‘sources’). Source-sink dynamics complicate the assessment of species-environment relationships, because species’ presence or density can be poorly correlated with underlying population productivity. Yet, applied conservation research often uses presence or abundance data to assess species responses to environmental change, particularly in the tropics where few long-term ecological studies are established. This approach assumes that abundance data reliably indicate habitat quality, but in sinks, this assumption can be violated. We review the recent literature and identify a regional bias in reporting of source-sink phenomena, with 71% of the 210 studies considered coming from temperate regions, particularly Eurasia and North America. Very few studies come from tropical and subtropical biomes, where human-driven biodiversity loss is occurring most rapidly, with over 80% not providing strong evidence in the form of demographic, dispersal or molecular data. Source-sink studies in tropical regions have predominantly investigated populations exposed to hunting/exploitation, with few examining land-use change. We review policy-relevant arenas where better treatment of source-sink dynamics is a priority: spatial conservation planning, assessments of land-sparing versus land-sharing, the conservation value of selectively logged forests, and species distribution modelling. Finally, we discuss ways to improve understanding of source-sink dynamics, particularly in tropical regions. Failure to detect source-sink patterns across the hyperdiverse tropics could limit the efficacy of conservation practice, leading us to underestimate the severity of human impacts on biodiversity.
KeywordsBiodiversity conservation Tropical ecology Source sink dynamics Spatial demography Land-use change Habitat quality Conservation planning Regional research biases
A large body of applied conservation research seeks to address three broad aims: estimating the impacts of anthropogenic change on native communities, identifying priority sites for protection, and determining management practices that can minimize biodiversity losses or maximise biodiversity recovery[1, 2].
At the landscape scale, these goals are often addressed by examining how population density (or presence/absence) varies in space and time, either across gradients of anthropogenic activity or between discrete habitat patches [3, 4]. Common to each of these approaches is an assumption that local population density is a reliable measure of underlying habitat-specific population growth, this being the ultimate determinant of long-term persistence . However, neither presence nor density necessarily indicate that a local population is self-sustaining. Intrinsic population growth rates may be below replacement within a given patch or habitat (a ‘sink’), but density may be sustained therein by emigration from surrounding ‘source’ areas that produce a surplus of dispersing individuals . This is a well-established concept in landscape ecology, addressed by a large body of research [7, 8, 9].
Despite this, source-sink dynamics remain seldom quantified in applied conservation research [9, 10]. Failure to identify sinks can lead to erroneous or perverse outcomes from conservation decision-making. For example, Wexford Slobs, Ireland, has the largest and most stable subpopulation of the threatened Greenland White-fronted Goose Anser albifrons flavirostris and thus has been identified as the critical location for protection . However, using 29-years of capture–mark–recapture, census and recruitment data to inform integrated population modelling, Weegman et al.  showed that Wexford Slobs are actually a sink, with persistence of the subpopulation only possible via high rates of immigration that exceeded emigration in each year. As another example, Gulo gulo wolverines in Norway are hunted in high-density areas where they are assumed to have large productive populations, but analysis of survival and emigration patterns instead reveals that these populations are maintained by compensatory immigration from Sweden, where wolverines are totally protected . Thus, continued hunting in sink areas in Norway may be causing a drain on the southern Scandinavian population as a whole. It remains unclear how often such source-sink patterns are being overlooked in conservation decision-making elsewhere.
A recent review of source-sink research  found only 73 studies that provide quantitative evidence for source-sink patterns in nature, from a sample of studies published between 2002 and 2013. The review also revealed evidence of a taxonomic bias towards mammals and birds in source-sink research, and the authors suggested that sources and sinks may be more commonplace in nature than studies suggest . Here, we perform a further review to examine whether there are regional biases in research on source-sink dynamics. Currently, human impacts on biodiversity are at their most severe in tropical regions, where land-use change and habitat degradation are pervasively re-shaping many of the most species-rich ecosystems worldwide . However, it is unclear whether conservation-orientated research in tropical regions is taking sufficient account of the potential for source-sink patterns to arise due to human-driven habitat change. Our review highlights a number of specific policy-relevant questions that are difficult to address without a better understanding of spatial demography. We also examine the factors that are likely to have limited the capacity for source-sink research to be conducted, particularly in tropical regions, and discuss ways to improve the integration of spatial demographics into landscape-scale conservation planning.
The Problem: Presence ≠ Persistence
All populations are exposed to some degree of spatial heterogeneity in biotic and/or abiotic conditions. This heterogeneity can drive spatial variation in vital demographic rates (births and deaths) and, consequently, intrinsic population growth rates (λ) across landscapes. Pulliam  first proposed that this spatial variation can lead to the emergence of ‘sink’ areas, where intrinsic growth rates are below replacement (λ < 1), but persistence is maintained by immigration from surrounding ‘source’ areas with higher intrinsic growth rates (λ > 1). Theoretical and empirical studies have shown that source-sink dynamics can emerge in equilibrium populations when there is temporal variability in environmental conditions , or when subordinate individuals are forced to occupy poor-quality habitats . Perhaps more importantly, sink habitats can emerge when environmental change causes declines in local habitat quality [15, 16, 17].
Source-sink systems have clear implications for conservation. In simple terms, spatial conservation planners generally seek to give priority to protecting source habitats, rather than sinks [18, 19], provided that sources are temporally consistent and can be identified with confidence [20, 21]. Populations exhibiting source-sink dynamics may be prone to local or even global extinction due to stochastic fluctuations [6, 22], making them particularly vulnerable to environmental change. Increases in the prevalence or severity of sinks can drive long-term population declines, as well as increased risk of stochastic extinction. In particular, source-sink populations may contribute to ‘extinction debts’ associated with environmental change, as source-sink populations can persist for many generations following change before extinction finally occurs [23, 24].
Perhaps the most neglected implication of source-sink dynamics for conservation concerns our approach to measuring the impacts of anthropogenic change on wild species. In source-sink systems, observed patterns of population density often deviate from underlying patterns of demographic productivity. If dispersal rates are high, density within sinks may differ little from density in sources . In some settings, sink density may even exceed that of sources, either due to competitive exclusion by dominant individuals  or the decoupling of settlement cues from underlying habitat quality (‘ecological traps’ [22, 25]). As such, studies that use presence or density indices to infer impacts of habitat change can provide misleading conclusions about conservation priorities in source-sink systems. The consequences of this could be severe; failure to recognize sink habitats could reduce the likelihood that effective conservation measures will be taken to protect a species, while at the same time increases in sink prevalence can greatly exacerbate extinction risk .
Despite this conservation significance, and the wealth of interest in source-sink dynamics among theoretical ecologists , the number of empirical studies directly demonstrating source-sink systems remains small. An important outstanding question is whether there are regional biases in research effort relating to source-sink dynamics. In particular, it is unclear whether source-sink research effort is spatially congruent with areas experiencing maximum environmental change and biodiversity loss (i.e. the tropics ). To answer this question, we conducted a further literature review to examine regional and taxonomic biases in research intensity.
Methods: Literature Review Protocol
We collected studies addressing the source-sink status of one or more wild terrestrial species, using a protocol following the guidelines outlined by Pullin & Stewart . We searched the online ISI Web of Science database for studies containing the following key words: ‘dispersal sink(s)’, ‘source habitat(s)’, ‘sink habitat(s)’, ‘source population(s)’ OR ‘sink population(s)’ OR ‘mortality sink(s)’ OR ‘source-sink’ (following 10). We refined the search to papers under the categories ‘ecology’, ‘plant science’ and ‘biodiversity conservation’, published between 2003 and 2016, yielding a total of 1195 papers. From these, we selected empirical studies of wild populations, excluding purely theoretical or laboratory-based experiments. We further excluded studies that did not explicitly consider source-sink dynamics or spatial demography, leaving 210 articles for further analysis (Appendix 1). We then classified each of these studies by climate zone (polar/boreal, temperate, subtropical, tropical), biogeographic realm (using realm classification of ), and study taxon (invertebrates, fish, herptiles [reptiles and amphibians], birds and mammals).
We further classified studies according to degree of quantitative evidence supporting the presence of source-sink dynamics in the study population. Source-sink dynamics are notoriously difficult to detect from field data , requiring quantification of habitat-specific population growth rates (λ) using accurate measures of demographic parameters (survival and productivity). However, mark-recapture studies often underestimate survival rates due to emigration outside of sampled areas [9, 31]. Dispersal is also an important component of source-sink dynamics, but is itself difficult to measure at population-relevant scales . Recently, further approaches to detecting source-sink dynamics have been developed using genetic signals, including patterns of asymmetric gene flow, immigration or linkage disequilibrium that are suggestive (but not necessarily confirmatory) of source-sink presence [33, 34]. We classified studies in relation to these three levels of evidence for source-sink dynamics: 1) measurement of habitat-specific demographic rates, 2) measurement of dispersal rates, and 3) genetic approaches. We considered studies that provide two or more of these classes to have ‘strong evidence’ for source-sink dynamics, and studies providing only one class to provide ‘weak evidence’. Some studies proposed source-sink dynamics on the basis of habitat-specific abundance or density patterns, but did not provide any of the three empirical forms of evidence—we classified these as ‘speculative’ source-sink cases.
Finally, we also classified studies according to type of anthropogenic stressor influencing the species in question. This allowed us to examine the extent to which source-sink research is directly addressing conservation-relevant issues, and explore regional variation in the types of anthropogenic impacts being explored from a source-sink perspective. We used the following categories: agricultural change (including intensification and expansion), fragmentation of natural habitat, logging (including selective and clear-felling), hunting/exploitation (including fishing, as well as accidental human-driven mortality, e.g. roadkill), species invasions and urbanization. A number of other stressors (including climate change and pollution) were lumped into a further category ‘other’. Studies that did not involve systems under the influence of anthropogenic stressors were classified separately. These studies were typically those aiming to elucidate spatial demographic mechanisms in wild populations under natural conditions.
Results: Regional Biases in Source-Sink Research
Overall, 63.3% of studies directly addressed cases where populations were impacted by anthropogenic stressors (i.e. were of direct conservation relevance). Studies conducted in tropical regions were more likely to address anthropogenic stressors (80.8% of studies) than studies in the subtropics (60.0% of studies), temperate regions (62.9% of studies) and boreal/polar regions (25% of studies).
Echoing the findings of Furrer & Pasinelli , we also found notable taxonomic biases in study effort, with a predominance of studies on mammals in all climate zones, and birds in particular in temperate zones (Fig. S1). Mammalian studies were particularly dominant in subtropical and tropical regions (37.9% and 46.7% of studies, respectively). There were notably few studies on fish, reptiles or amphibians in any climate zone (Fig. S1).
Discussion: What Drives Regional Research Biases?
Previous reviews have shown that source-sink dynamics receive relatively little empirical research attention overall in global terms [9, 10]. Our review demonstrates that this scant attention is compounded by a significant skew towards temperate regions in North America and Europe (Figs. 1 and 2). In boreal, tropical and subtropical climate zones, the detection of source-sink patterns has been extremely limited. Tropical and subtropical studies in particular are largely restricted to work in the Neotropics and Australasia (Fig. 2). Moreover, a strikingly high proportion of studies that report potential source-sink systems in the tropics are largely anecdotal, and do not provide rigorous empirical evidence in the form of quantitative analyses of demography, dispersal or molecular signals (Fig. 1; Appendix 1).
One possibility is that this paucity of published research stems from a genuine rarity of source-sink systems in nature, particularly in the tropics. The lack of published studies could then stem from publication bias, rather than lack of research effort, if source-sink studies that return negative results are less likely to get published. However, we contend that this explanation is unlikely. An absence of source-sink dynamics, if rigorously demonstrated, remains a scientifically interesting and important result; we, therefore, do not expect a significant publication bias against negative results in this case (although it cannot be ruled out). Rather, we contend that our review reflects a genuine pattern of regional disparity in research effort.
As stated previously, confirmation of source-sink dynamics in wild populations is extremely difficult, requiring detailed demographic data, dispersal measurements and/or molecular sampling , often over large geographic areas. Typically, long time series are also necessary to identify likely sources and sinks with any confidence (e.g. ), and to discount the possibility that apparent sinks are actually ‘pseudo-sinks’, where population growth rates are temporarily suppressed due to density-dependent competition, rather than underlying habitat quality . It seems likely that the difficulty and costliness of collecting the required data to detect a source-sink pattern is the primary reason for the paucity of research. Indeed, given that tropical regions have seen the fastest rates of land-use change and biodiversity loss worldwide over recent decades , it is perhaps reasonable to assume that human-driven sink habitats are increasingly emerging within the ranges of many species in tropical regions. Our review suggests that these impacts are currently largely going undetected. This could be contributing to a significant underestimation of biodiversity impacts from anthropogenic change.
It is notable that in the tropics, many studies reporting or speculating on the presence of source-sink dynamics addressed systems impacted by human hunting/exploitation (Fig. 3d), whilst studies of agricultural change were largely limited to temperate regions (Fig. 3b). This is surprising, given that agricultural intensification and expansion are occurring more rapidly in the tropics than anywhere else , and are among the most prominent drivers of biodiversity loss in those regions [28, 35, 36]. Much research has examined the biodiversity value of agricultural landscapes in the tropics, particularly low-intensity agroecosystems that often support surprisingly diverse communities [37, 38], and many studies have considered the potential for landscape-scale dispersal and ‘spill-over effects’ influence community composition in farmed areas [38 and refs therein]. However, our review suggests that relatively few studies have directly examined the spatial demography of populations inhabiting tropical agricultural landscapes, resulting in a paucity of studies reporting source-sink phenomena. Given the growing importance of tropical agricultural landscapes as reservoirs of biodiversity [39, 40], this may represent an important research gap.
What are the Conservation Implications of Failures to Detect Source-Sink Patterns?
Failure to identify source and sink habitats could limit the efficacy of conservation practice, as well as lead to overly optimistic assessments of species vulnerability and the magnitude of anthropogenic impacts on biodiversity . Below, we identify three particular areas of conservation research where the (non-)detection of source-sink patterns is particularly concerning. Given the severe deficiency of source-sink research in the tropics, where human-driven biodiversity losses are currently peaking , we focus primarily on the tropics in the following sections, although the issues discussed are broadly relevant in all biomes.
Issue 1: Spatial Conservation Planning
Conservation planners seek information on source-sink dynamics to identify areas of high importance for population persistence (sources), which can then be prioritized for protection. In the absence of detailed information on sources and sinks, decisions are more likely to be made using spatial patterns of density or incidence as proxies for importance. Often, these data are fed into spatial prioritization algorithms (e.g. [41, 42]) that seek to identify networks of sites that capture the full suite of biodiversity in a region. These algorithms incorporate a consideration of spatial connectivity between sites , but generally assume that species density within a site can be taken to indicate population persistence. Clearly, the long-term robustness of protected area networks could be limited if some or all of the prioritized sites for a given species actually represent sinks.
Issue 2: Conservation Value of Selectively Logged Forests
Selective logging is a major driver of habitat degradation in forests worldwide, and particularly in the tropics [35, 46]. However, evidence suggests that the impacts of logging on biodiversity can be surprisingly small, with high proportions of primary forest species being retained in logged landscapes [47, 48]. This has prompted calls from some conservationists to prioritize the protection of logged forests as a cost-effective conservation strategy . However, it is notable that a high proportion of studies examining the biodiversity impacts of logging have been conducted in areas adjacent to blocks of intact primary forest , and in most cases, impacts are assessed using relative measures of abundance, density or incidence [47, 48]. As such, inferences about the relative value of logged forests for biodiversity may fail to account for the possibility that logged areas represent sink habitats, where populations are maintained by immigration from surrounding intact forests. Studies examining intrinsic population growth rates within logged forest areas (e.g. ) should, therefore, be a high priority for conservationists to provide more robust inferences about the biodiversity value of these degraded forests .
Issue 3: Species Distribution Modelling
Correlative models linking species occurrence patterns to environmental variables are increasingly used in conservation biology for a range of purposes, including spatial planning, the identification of important habitats and sites, estimation of range limits, and the prediction of species responses to climate and habitat change . A wide range of statistical tools are available, each aimed at estimating the bioclimatic niche occupied by a given species. Popular platforms include MaxEnt  and other machine-learning algorithms (random forests, boosted regression trees), as well as statistical models such as GAMs . Much interest has been devoted to the refinement of modelling techniques, as well as the selection of environmental variables to use in modelling niche envelopes [51, 54], but less attention has been paid to whether models meaningfully inform us about spatial demography . Invariably, the species data that are fed into species distribution models (SDMs) involve measures of abundance or incidence [51, 55]. In doing so, these approaches again make the assumption that abundance is a reliable measure of local population viability. In source-sink systems, however, SDMs may overestimate the bioclimatic niche of a species by including areas of low suitability for population growth (sinks), and consequently produce unreliable predictions of current and future distributions . Furthermore, any such overestimation will be difficult to detect using standard diagnostic checks that are typically applied to assess model reliability (e.g. area under curve of receiver operating characteristic plots; ).
An important use of SDMs in conservation is to predict how species are likely to shift in space in response to climate change . Such predictions are increasingly used to inform conservation planning, with the aim of ensuring that protected area networks are ‘climate change ready’ by facilitating shifts from currently occupied ranges to areas where conditions may become suitable in the future. Clearly, such exercises rely on accurate model predictions of bioclimatic suitability, which may be compromised if models are naïvely applied to systems with undetected source-sink dynamics. Predictive models also make assumptions about the dispersal capacity of species, allowing estimation of the likelihood that new patches will be colonized by immigrants at range edges . Invariably, these assumptions are based on estimates of mean or maximum dispersal distance, derived from quantitative data where available . However, the likelihood of patch colonization might depend not only on the dispersal behaviour of individuals, but also on the source-sink status of occupied areas at the existing range edge. If habitats at range edges are sinks, the number of potential dispersers moving out into newly suitable areas may be severely reduced. To derive more realistic predictions of species responses to climate change, it may be necessary to model relationships between bioclimatic variables and local intrinsic population growth rates, allowing source-sink patterns to be accounted for within the SDM framework . However, the data requirements of such a model are likely to be prohibitive in most cases.
Moving Forwards: Redoubling Efforts to Detect Source-Sink Patterns in Tropical Landscapes
Incorporating spatial measures of demographic rates into conservation planning is a key challenge for landscape ecologists, particularly in mega-diverse tropical landscapes undergoing rapid anthropogenic change. Unfortunately, quantifying demographic rates is hugely data-hungry, and is unlikely to ever be achievable for large numbers of taxa or across large regions. As such, a satisfactory solution to the problem of unidentified sources and sinks is likely to be elusive, particularly in the tropics. Nevertheless, useful rules of thumb could be derived from detailed and rigorous studies of model taxa, allowing researchers to identify conditions in which source-sink patterns are most likely to emerge. More such studies are urgently needed, particularly within tropical environments, to provide an evidence base to better inform our understanding of spatial demography in tropical species that are threatened by current land-use change. The development of more sophisticated integrated population models, capable of bringing together data from multiple sources to estimate demographic rates, could increase our capacity to detect source-sink patterns in a wider range of systems [59, 60]. Improvements in the size, performance and cost-effectiveness of individual tracking technology might also aid considerably in the quantification of survival and dispersal patterns .
In some cases, conservation-relevant inferences about source-sink patterns can be made using other approaches. Some researchers, for example, have used the tools of macroecology to make predictions about long-term species persistence following environmental change. Pereira and Daily , for example, proposed a framework that combines species–area relationships with estimates of species affinity to primary habitats to derive predictions of extinction likelihood in response to environmental change. This approach, whilst falling short of providing direct estimates of source-sink patterns, can provide valuable inferences about the likelihood of species persistence in different landscape scenarios .
Other authors have taken a more simplistic approach, inferring likely source-sink patterns on the basis of changes in abundance with increasing distance from likely source habitats [64, 65]. For example, in cattle farming systems in the Colombian Andes, many bird and dung beetle species can persist in ‘wildlife-friendly’ low-intensity farmland, but their abundances decline rapidly with distance from contiguous forest edges [38, 64]. This suggests that low-intensity farmland may be a sink for these species, and that land-sparing may consequently be the optimal strategy for conservation, both for species richness and phylogenetic diversity [64, 66]. Although such approaches are again limited in their capacity to confirm source and sink habitats, they can provide important conservation-relevant insights with far lower data requirements than studies of habitat-specific spatial demography. Incorporating information on the spatial configuration of landscapes is, thus, vital in short-term research investigation of the impacts of land-use change and management on biodiversity.
Ultimately, however, genuine advances in our understanding of the impacts of environmental change will require redoubled efforts to measure the relationships between environmental variables and species’ birth, death and dispersal rates. Gathering such information typically requires intensive field-based research, using mark-recapture and/or telemetry approaches to estimate relevant survival and dispersal parameters. Only by quantifying spatial and temporal variation in these key parameters will we be able to identify the set of environmental characteristics that support positive population growth at landscape scales. Such detailed demographic information is essential if we are to fully understand how to optimise conservation actions for any given species.
This review highlights the current paucity of research into source-sink systems, particularly in tropical and subtropical regions. The tropics house the highest levels of biodiversity , and currently face the highest rates of habitat conversion and degradation , placing tropical regions at the epicentre of the biodiversity crisis. Researchers are struggling to document patterns of biodiversity loss in response to rapid rates of land-use change , and conservation decisions are continually being made on the basis of limited data . Much of current conservation practice is informed by patterns of species abundance or occurrence, but there are many circumstances in which these patterns can provide a misleading picture of the long-term suitability of habitats. Our review indicates that a significant increase in research effort is necessary, particularly in tropical regions, to measure how demographic rates and dispersal patterns are changing across landscapes in response to anthropogenic impacts.
We thank Dr. Heather Bird Jackson for inviting us to write this review.
Compliance with Ethical Standards
Conflict of Interest
Dr. James Gilroy and Dr. David Edwards have no conflicts of interest to declare.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
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