Consequences of impediments to animal movements at different scales: A conceptual framework and review

2.1 Mechanism and scale are linked

Animal movements can be restricted at a range of spatial and temporal scales. Some movements are undertaken on a daily basis, some are undertaken once in a lifetime and some only occur once in several generations. Movements disrupted by habitat fragmentation on a daily basis are likely to affect a different mechanism than that affected by movement restrictions across multiple generations. For example, unwillingness or inability to routinely cross roads may restrict an animal's home range and influence their daily access to resources (Poessel et al., 2014), but may not impede once-in-a-lifetime dispersal events that facilitate gene flow. Both the temporal and spatial scales at which movement restrictions operate relate to the ecological mechanism affected, and ignoring this relationship could be costly for governments and conservation organizations in terms of conservation outcomes (Scott, Touloumis, Lehsten, Tzanopoulos, & Potts, 2014).

The consequences of small-scale movement restrictions are likely to occur over short time-scales, whereas the consequences of large-scale restrictions may only be evident after many generations. For example, habitat fragmentation can disrupt daily movements when home ranges encompass multiple patches. A gap between parts of a home range could quickly lead to poor condition of individuals if they continually expend extra energy navigating around it (Hinsley, 2000; Smith, Forbes, & Betts, 2013) or death if gap crossings are undertaken in the presence of predators (Eccard, Pusenius, Sundell, Halle, & Ylönen, 2008). Population sizes can respond quickly to changes to the health and survival of individuals (Desy & Batzli, 1989). In contrast, inbreeding depression is likely to be associated with long-term movement impediments, generally requires quite severe levels of habitat isolation and develops over multiple generations (Kenney, Allendorf, McDougal, & Smith, 2014).

2.2 Movement restrictions disrupt three key mechanisms

We consider three mechanisms through which impeded movements can have a direct, detrimental effect on animals: (1) limited resource access, (2) restricted demographic exchange, and (3) impeded gene flow (Figure 1). Habitat fragmentation can spatially segregate resources needed by an individual, reducing their ability to access them. Demographic exchange is restricted when individuals are not able to disperse to new localities or alternative populations to facilitate demographic processes and maintain sustainable demographic parameters within metapopulations or patchily distributed populations. Finally, impeded gene flow occurs when the movement and integration of genetic material from one spatially discrete population to another is restricted.

For any given species, each of these mechanisms operates over characteristic spatial and temporal scales (Jeltsch et al., 2013). However, the mechanisms are not mutually exclusive and can overlap in time and space. For example, if dispersal between two patches is prevented, an individual may also have trouble accessing sufficient resources if the occupied patch is depauperate. All three mechanisms do not need to be impeded for a species to go extinct (Harrisson et al., 2013). Individuals may be able to disperse successfully from a source population, but if they continually travel to a sink site harbouring insufficient resources, extinction may result (Dunning, Danielson, & Pulliam, 1992; Pulliam, 1988). While the absolute spatiotemporal scales most relevant to each mechanism will vary among taxa depending on their dispersal abilities, foraging range requirements and generation times, the relative scales applicable to each mechanism remain constant (Jackson & Fahrig, 2012; Thornton & Fletcher, 2014; Wiens, 1989). Below, we consider each mechanism in turn.

3.1 Literature search strategy and inclusion criteria

We searched the ISI Web of Science platform on 13 March 2015 using terms that are associated with movement, resources, demography or gene flow within fragmented landscapes. The search string was designed to deliver a broad and comprehensive list of articles particularly focused on the effects of habitat fragmentation on the mechanisms of interest. Specifically, a search of titles, abstracts and keywords was conducted using the following terms: topic = (“habitat fragmentation” OR “habitat configuration”) AND ((resource* OR food OR forag* OR feed OR “home range”) OR (dispersal OR migration OR immigration OR emigration OR demograph*) OR (“gene flow” OR genetic*) OR (movement*)). The search was limited to articles published from 1994 onwards. The search was then refined to exclude all document types except “article.”

The titles and abstracts of articles were examined to determine whether each warranted inclusion in the literature review. Four criteria were used for inclusion. First, the article must have reported findings from an empirical study in a peer-reviewed journal. Work of a purely theoretical nature, reviews and meta-analyses were excluded; computer simulations were included provided they employed or were tested against an empirical dataset. Second, the focal taxon must have been an animal. Studies on plants were excluded because resource access does not apply to plant movements. Third, the article must have investigated some aspect of habitat fragmentation per se, such as distance to neighbouring patch. Articles that only assessed the effects of habitat extent or patch size were excluded as these are more indicative of habitat loss. We excluded papers that only considered habitat loss because our focus was on structural separateness, not habitat amount. We recognize that measures such as patch isolation may be more appropriately treated as an effect of habitat amount (Fahrig, 2013); however, we have taken a more cautious approach as this suggestion has not yet been widely adopted. Finally, articles were only included if they explored a mechanism linking habitat fragmentation to a consequence for the focal taxon. Specifically, they must have investigated whether limited resource accessibility, restricted demographic exchange or impeded gene flow (as per our definitions above) led to the observed fragmentation effects. Thus, studies that only identified relationships between species abundance or distribution and patch or landscape metrics were excluded.

Due to the large number of results from the initial keyword search (n = 4,017), not all articles were subject to this filtering process. Rather, articles were assessed in a random order until we had a sample of 250 articles that met our inclusion criteria. The proportion of articles that examined each of the three mechanism categories did not vary by more than 1.8% between 200 and 250 articles. Thus, our results form a representative sample from our pool of articles.

3.2 Data collection and analysis

The 250 articles selected for inclusion (a list of the data sources is found in Appendix S1) were reviewed in full to extract: type of mechanism examined (limited resource access, restricted demographic exchange or impeded gene flow); geographic location of the study (tropics, subtropics as defined by Corlett (2013) and the temperate zone plus higher latitudes); and taxon examined (invertebrate, fish, amphibian, reptile, bird or mammal; see Table S1). Counts across categories may exceed 250 because some articles fell into multiple groupings. A chi-square goodness-of-fit test was used to assess whether research was evenly distributed across the three mechanisms. Fisher's exact tests were used to determine whether the relative proportions of observed mechanisms were different than expected across geographic zones and across taxa. Analyses were conducted using R version 3.2.0 (R Core Development Team, 2015).

5.1 Implications and limitations of the conceptual framework

It is crucial to distinguish among the three mechanisms in the conceptual framework when devising solutions that address population declines. In an ideal world, conservation managers would respond to all three mechanisms simultaneously by ensuring that there are sufficient resources within home ranges and individuals can disperse to distant habitat patches. However, there is usually little funding available and few feasible options, so solutions need to be targeted to the specific constraint acting on the population. Failing to consider multiple scales of movement restrictions potentially weakens conservation recommendations because each mechanism may require different conservation responses. Limited resource access could potentially be addressed by improving habitat quality to increase the carrying capacity of the habitat patch (Bonnot, Thompson, Millspaugh, & Jones-Farrand, 2013), but this would not assist if the threat to the local population occupying that patch was primarily caused by a lack of immigrating individuals. For example, habitat restoration in patches or the matrix would do little to restore gene flow between populations of arboreal mammals separated by a highway; a more effective solution may be to install rope bridges that facilitate safe passage (Goldingay, Rohweder, & Taylor, 2013). That solution, however, is of little use if cross-highway movements were adequately frequent to maintain genetic connectivity, but led to high mortality during normal within-home-range movements.

Solutions to different types of movement impediments are not mutually exclusive and could potentially address multiple interrupted mechanisms simultaneously. However, the scale of intervention could become a key determinant of how effectively the solution addresses each of the affected mechanisms (Gunton et al., 2014). For instance, adding corridors (linear strips of habitat) or stepping stones (small patches or isolated trees) to the matrix could help both long-range dispersal and multiple-patch use within a home range (Fischer & Lindenmayer, 2002; Saura, Bodin, & Fortin, 2014). A few, well-placed connections across a broad region may be enough to kick-start demographic or genetic rescue (Miquelle et al., 2015), but a greater number of connections within a more confined area may be needed if resource access is to be improved throughout multiple home ranges (Keeley, Beier, Keeley, & Fagan, 2017; Newmark, Mkongewa, & Sobek, 2010).

Several frameworks have previously been developed for conceptualizing the structural composition of landscapes (Fischer, Lindenmayer, & Fazey, 2004; Forman, 1995; McIntyre & Barrett, 1992; Watson, 2002; Wiens, Stenseth, Van Horne, & Ims, 1993). However, these frameworks were not extended to classify the mechanisms driving isolation effects on animal populations. Jeltsch et al. (2013) explored how different types of movements occurred over characteristic spatiotemporal scales and impacted ecosystems as a whole, such as through interspecific interactions and resource transportation. We take an alternative focus and instead consider how different proximate mechanisms are affected by scale.

Driscoll, Banks, Barton, Lindenmayer, and Smith (2013) outlined how the quality of the matrix in fragmented landscapes influences proximate processes. Specifically, they discussed how features of the matrix influence species’ persistence in the landscape through subsidizing resource availability, altering abiotic microclimates and facilitating movements. For instance, woodland-dependent species may more readily travel between woodland patches interspersed with a pine plantation matrix than one that is more structurally dissimilar to the woodland (Driscoll et al., 2013). Our frame of reference aligns with that of Driscoll et al. (2013); we consider the role of functional connectivity on movement, which is heavily dependent on matrix quality. Thus, both frameworks are complementary for conceptualizing the impacts of habitat fragmentation. In contrast to Driscoll et al. (2013), we explore one of the three core effects of the matrix: how the consequences of movement disruptions affect species. We also elucidate the relationships between the type of mechanism affected by fragmentation and the distance or time-scale over which movements are restricted.

Many mechanisms other than those linked directly to physical isolation are important in fragmented landscapes, such as edge effects (Porensky & Young, 2013; Ries, Fletcher, Battin, & Sisk, 2004; Zurita, Pe'er, Bellocq, & Hansbauer, 2012). Although we do not specifically include these in our framework, they are nonetheless relevant. One component of edge effects is the inability to source sufficient resources, such as sheltered protection from predators (Bennett et al., 2013). Habitat gaps between shelter sites and feeding locations could pose substantial risks. These mechanisms are incorporated into our framework when they are driven by increased isolation, such as when habitat gaps make movement risky. However, these impeded mechanisms could also result from reduced habitat quality, such as when abiotic changes along edge habitat lead to changes in flora (Ries et al., 2004). It is important to distinguish whether habitat fragmentation or related changes such as degradation are impacting species because the conservation solutions differ.

5.2 Distribution of research effort among mechanisms

The most frequently examined of the three mechanisms was impeded gene flow. It is unlikely that the heavy weighting towards genetic articles is an artefact of the keyword choices used for each mechanism because this imbalance was also evident in an informal scan of articles produced by a search of just “habitat fragmentation.” It is unsurprising that the total number of articles increased over time given increasing publication rates and that the number of impeded gene flow articles increased in recent years given the greater availability and affordability of genetic technology (Bolliger, Lander, & Balkenhol, 2014; Storfer, Murphy, Spear, Holderegger, & Waits, 2010). However, given that molecular methods, such as assignment tests and pedigree analyses, can be used to infer dispersal movements (Holderegger & Wagner, 2008; Manel, Gaggiotti, & Waples, 2005), it is surprising that the frequency of articles investigating restricted demographic exchange has not similarly spiked over the past decade. Additionally, it is important to note that an increase in the proportion of publications studying impeded gene flow does not necessarily reflect a corresponding increase in our understanding of the issue.

The key mechanisms we have identified in this study can be considered to form an overlapping, non-nested hierarchy across scales. Each successive mechanism works at progressively larger scales (Wiens, 1989). When habitat is fragmented, it takes time for the evidence of the negative effects to become apparent and the duration of this time-lag is dependent upon where the affected mechanism sits in the hierarchy (Metzger et al., 2009; Wiens, 1989). As the scale of fragmentation increases, impacts on mechanisms may accumulate. Systems that show signs of impeded gene flow may also be subject to impediments to demographic exchange and resource access. Thus, neglecting to take the impacts on these lower-level mechanisms into account could compromise conservation efforts. Additionally, impacts can have synergistic effects on ecological systems (Brown, Harborne, Paris, & Mumby, 2016; Zanette, Smith, van Oort, & Clinchy, 2003). It is currently unknown what interactive effects, if any, operate among the three mechanisms discussed here, but synergisms may partly explain why fragmentation effects are amplified at very low levels of habitat extent (Andrén, 1994; Radford, Bennett, & Cheers, 2005).

5.3 Geographic and taxonomic biases

The overall bias against limited resource access and restricted demographic exchange as a focus of research was disproportionately pronounced in particular taxa, notably reptiles, amphibians and fish. It is difficult to generalize across taxa, but reptiles and amphibians in particular contain a greater proportion of less-vagile species than birds, large mammals and flying insects (Allentoft & O'Brien, 2010; Mac Nally & Brown, 2001; Rivera-Ortíz, Aguilar, Arizmendi, Quesada, & Oyama, 2015). A considerable gap in knowledge about mechanisms operating at small-to-intermediate scales in generally less-mobile taxa could have important implications. For instance, landscape structure across small extents may have a greater impact on sedentary species than on nomadic species (Maron, Goulding, Ellis, & Mohd-Taib, 2012). It is important to gather a body of empirical data across a range of dispersal capabilities, range requirements, generation times and environments (notably aquatic versus terrestrial) both within and between taxa. Without this, it would not be appropriate to generalize findings.

As has been often identified in literature reviews (Bayard & Elphick, 2010; Lawler et al., 2006; Magle, Hunt, Vernon, & Crooks, 2012), the Southern Hemisphere and the tropical/subtropical regions were underrepresented in the literature we studied. However, the frequency that each mechanism was studied was consistent across geographic locations. The relative importance of different types of habitat fragmentation effects may vary between the northern temperate zones and lower latitudes. Many species undertake long-distance migrations to avoid harsh winters in the northern temperate region, while lower latitudes have a greater proportion of sedentary species (Chesser, 1998; Newton & Dale, 1996a, 1996b). Thus, there are important differences in dispersal ability, life history traits and population demography in species between these regions plus abiotic factors such as climate and productivity which may affect the relative influence of both habitat fragmentation and each of the three mechanisms on species’ responses (Betts et al., 2014; Newbold et al., 2013; Rivera-Ortíz et al., 2015). Therefore, geographic biases in research effort, especially when they occur in conjunction with a bias towards a particular mechanism, have the potential to hamper our ability to draw broad conclusions and develop appropriate conservation strategies accordingly.