1 Introduction

Amphibian invasions are a growing concern globally, with significant ecological consequences. These invasions can lead to declines in native species through mechanisms such as competition, predation, and disease transmission, ultimately disrupting local ecosystems and biodiversity (Falaschi et al., 2020). The introduction of invasive species often results in altered community structures and can exacerbate existing environmental challenges, such as habitat degradation and climate change (Gallardo et al., 2016).

Habitat fragmentation is increasingly recognized as a critical driver of amphibian invasions. Fragmentation results in the division of continuous habitats into smaller, isolated patches, which can facilitate the spread of invasive species by creating new niches and reducing the resilience of native populations (Cushman, 2006). The effects of fragmentation are particularly pronounced in amphibians due to their specific habitat requirements and limited dispersal abilities, making them vulnerable to changes in landscape connectivity (Zheng, 2023). Understanding the role of habitat fragmentation in facilitating invasions is essential for developing effective conservation strategies and mitigating the impacts of invasive species on native amphibian populations (Belasen et al., 2019).

This study attempts to identify key patterns and mechanisms by which fragmentation affects invasion dynamics, and to reveal the extent to which habitat fragmentation promotes amphibian invasion. By integrating existing literature, it is expected to provide insights that contribute to conservation efforts and guide future research directions for more effective management and conservation of amphibian biodiversity in fragmented landscapes.

2 Mechanisms of Habitat Fragmentation

2.1 Definition and causes of habitat fragmentation

Habitat fragmentation can occur through natural processes such as geological events, but it is predominantly driven by anthropogenic activities. Human-induced fragmentation is primarily due to land-use changes, which include urbanization, agriculture, and infrastructure development. These activities lead to the division of continuous habitats into smaller, isolated patches, significantly impacting biodiversity and ecosystem functions (Cushman, 2006).

Land-use change is a major driver of habitat fragmentation, often resulting from urban expansion, agricultural practices, and deforestation. Urbanization leads to the conversion of natural landscapes into urban areas, creating isolated habitat patches. Deforestation, particularly in tropical regions, is a significant cause of habitat fragmentation, reducing habitat availability for many species. Additionally, climate change exacerbates these effects by altering habitat conditions and further fragmenting ecosystems (Teixido et al., 2021; Becker et al., 2023).

2.2 Ecological consequences of fragmentation

Fragmentation creates edge effects, where the conditions at the boundary of habitat patches differ from the interior, often resulting in altered microclimates. These changes can affect temperature, humidity, and light levels, impacting species that are sensitive to such variations. Fragmentation also disrupts predator-prey dynamics by altering the availability and distribution of both predators and prey, potentially leading to imbalances in local ecosystems (May et al., 2019).

Habitat fragmentation is a leading cause of biodiversity loss, as it reduces habitat size and connectivity, making it difficult for species to maintain viable populations. However, fragmentation can also create opportunities for invasive species, which may thrive in disturbed environments and outcompete native species. This dual impact highlights the complexity of fragmentation’s ecological consequences, where it simultaneously threatens native biodiversity and facilitates invasions (Neely et al., 2024).

3 Amphibian Invasions: Patterns and Drivers

3.1 Common invasive amphibian species

Two prominent examples of widely distributed invasive amphibians are the American bullfrog (Lithobates catesbeianus) and the African clawed frog (Xenopus laevis). These species have been introduced to various regions outside their native ranges, often through human activities such as the pet trade and scientific research (Cushman, 2006). Their ability to thrive in diverse environments has facilitated their spread across multiple continents, impacting local ecosystems and native amphibian populations.

The invasive success of species like Lithobates catesbeianus and Xenopus laevis can be attributed to several key traits. These include high reproductive rates, broad dietary preferences, and adaptability to a wide range of environmental conditions (Belasen et al., 2019). Additionally, their ability to disperse over long distances and tolerate habitat fragmentation enhances their capacity to colonize new areas (Funk et al., 2005; Wright et al., 2020). These traits enable them to outcompete native species and establish stable populations in non-native habitats.

3.2 Key drivers of amphibian invasions

Human activities play a significant role in facilitating amphibian invasions. The pet trade and transportation networks are primary pathways for the introduction of invasive amphibians. These activities often result in the release or escape of non-native species into the wild, where they can establish invasive populations. The global movement of goods and people increases the likelihood of such introductions, making it a critical driver of amphibian invasions.

Climatic adaptability and reproductive strategies are crucial factors in the success of invasive amphibians. Species that can tolerate a wide range of climatic conditions are more likely to survive and reproduce in new environments. Additionally, amphibians with flexible reproductive strategies, such as prolonged breeding seasons and high fecundity, can rapidly increase their population size, enhancing their invasive potential (Teixido et al., 2021). These characteristics allow invasive amphibians to exploit new habitats and resources effectively, often at the expense of native species.

4 How Habitat Fragmentation Facilitates Amphibian Invasions

4.1 Creation of new habitats for invasive amphibians

Habitat fragmentation often results in the creation of isolated water bodies, which can serve as breeding sites for invasive amphibian species. These fragmented landscapes, particularly in agricultural and urban areas, provide new ecological niches that invasive species can exploit. For instance, studies have shown that amphibian assemblages are influenced by the presence of breeding pools in fragmented forest patches, which can increase the likelihood of colonization by invasive species.

Urbanization and habitat fragmentation lead to the development of artificial water bodies such as urban ponds, artificial wetlands, and drainage systems. These man-made habitats can support invasive amphibians by providing suitable breeding and foraging environments. The presence of such habitats in urban and agricultural regions has been linked to changes in amphibian assemblages, with some species thriving in these altered environments (Cushman, 2006).

4.2 Disruption of native communities

Fragmented habitats often result in reduced competition and predation pressure, which can facilitate the establishment of invasive amphibians. The isolation of habitat patches can lead to decreased species richness and altered community dynamics, making it easier for invasive species to establish themselves without facing significant biotic resistance from native species (Teixido et al., 2021).

Habitat fragmentation can disrupt trophic interactions within native communities, further facilitating amphibian invasions. The alteration of food webs and the loss of key species can create ecological opportunities for invasive species to exploit. For example, changes in predator-prey dynamics and the availability of resources in fragmented landscapes can lead to increased vulnerability of native amphibian populations to invasive species (Belasen et al., 2019).

4.3 Enhanced dispersal opportunities

Fragmented landscapes often consist of small habitat patches that can act as stepping stones, enhancing the dispersal opportunities for invasive amphibians. These patches can facilitate movement across the landscape, allowing invasive species to colonize new areas more effectively. The connectivity of these patches is crucial for maintaining population dynamics and enabling the spread of invasive species (Wright et al., 2020).

Human activities associated with habitat fragmentation, such as transportation and land development, can inadvertently assist in the dispersal of invasive amphibians. Roads and other infrastructure can serve as corridors for movement, while human-mediated transport can introduce invasive species to new areas. This human-assisted dispersal is a significant factor in the spread of invasive amphibians in fragmented landscapes (Funk et al., 2005).

5 Interactions Between Habitat Fragmentation and Other Environmental Stressors

5.1 Climate change and amphibian invasions

Climate change significantly impacts the distribution and habitat suitability for amphibians, often leading to shifts in their geographical ranges. For instance, studies have shown that climate change can cause a northward shift and reduction in suitable habitats for species like the giant spiny frog, which is indicative of broader trends affecting amphibians globally (Luo et al., 2021). Additionally, climate change scenarios predict that amphibians in China may lose a significant portion of their original ranges, with suitable habitats moving to higher altitudes and northern regions (Duan et al., 2016). These shifts can create new opportunities for invasive species to establish themselves in previously unsuitable areas, thereby facilitating invasions.

The interaction between habitat fragmentation and climate-driven range shifts can exacerbate the challenges faced by amphibians. Fragmented landscapes can hinder the ability of species to move to new suitable habitats, thus increasing the risk of local extinctions (Opdam and Wascher, 2004). For example, the mountain frog Quasipaa boulengeri is projected to experience significant habitat loss and fragmentation due to climate change, which could impede its ability to adapt to new environmental conditions (Yang et al., 2021). This interaction highlights the need for conservation strategies that enhance habitat connectivity to support range shifts in response to climate change.

5.2 Pollution and disease

Pollution in fragmented habitats can create conditions that favor invasive species. Fragmented landscapes often experience increased levels of pollutants, which can alter the ecological balance and provide a competitive advantage to invasive species that are more tolerant of such conditions (Rossetti et al., 2017). These pollutants can degrade habitat quality, making it more challenging for native species to survive and thrive, thereby facilitating invasions.

The presence of environmental stressors like pollution can also interact with diseases such as Batrachochytrium dendrobatidis (Bd), exacerbating their impact on amphibian populations. Fragmented habitats can increase the spread and severity of diseases by creating isolated populations that are more susceptible to outbreaks (Falaschi et al., 2020). The combination of pollution and disease can lead to significant declines in native amphibian populations, further opening niches for invasive species to exploit.

6 Case Analysis: The American Bullfrog (Lithobates catesbeianus) Invasion

6.1 Case background: spread and impact

The American bullfrog (Lithobates catesbeianus) is a highly invasive species that has spread across multiple continents, significantly impacting native amphibian populations. In Uruguay, the bullfrog was initially introduced for farming purposes in 1987, but has since established feral populations, particularly in areas like Rincón de Pando, Canelones, where they are displacing native amphibians and altering community structures (Laufer et al., 2008). In Mexico, the bullfrog's invasion poses a threat to 82 endemic frog species (Figure 1) due to its ability to adapt to new environmental conditions through niche shifts (López et al., 2017). In Europe, the bullfrog's potential distribution is expected to increase due to climate change, threatening native species within the Natura 2000 network (Johović et al., 2020). In South Korea, the bullfrog's spread is exacerbated by climate change, posing a significant threat to the critically endangered Suwon treefrog (Koo and Choe, 2021).

6.2 Role of habitat fragmentation in bullfrog invasion

Habitat fragmentation plays a crucial role in facilitating the spread of the American bullfrog. In the Colorado Front Range, landscape-level factors such as topographic complexity and wetland density are significant predictors of bullfrog occurrence, indicating that fragmented landscapes may facilitate their dispersal. In Uruguay, the bullfrog's presence in fragmented pond networks has led to reduced native anuran richness, with certain species like Pseudis minuta being more affected due to increased encounter rates with the invader (Laufer et al., 2023). The bullfrog's ability to thrive in fragmented habitats is further supported by its reproductive characteristics, such as reduced size at reproductive maturity, which enhances its colonization and spread (Urbina et al., 2020).

6.3 Lessons for management

Effective management of the American bullfrog invasion requires a multifaceted approach. In Uruguay, early-stage invasions present an opportunity for cost-effective management, with eradication being a plausible option if localized populations are targeted. The use of environmental DNA (eDNA) barcoding has proven to be a valuable tool for early detection of bullfrogs at low densities, surpassing traditional survey methods in sensitivity and reducing control costs (Dejean et al., 2012). In the Pacific Northwest, understanding the reproductive characteristics of bullfrogs can inform management actions, such as adjusting the definition of reproductively active adults to increase the target population for culling (Urbina et al., 2020). Additionally, prioritizing conservation areas based on vulnerability to bullfrog invasion, as demonstrated in Mexico, can help in allocating resources effectively to protect native species (López et al., 2017).

7 Conservation and Management Strategies

7.1 Habitat restoration approaches

Reconnecting fragmented landscapes is crucial for reducing the risks of amphibian invasions. Habitat fragmentation often leads to isolated populations, which can be more vulnerable to invasions by non-native species. By enhancing connectivity between habitats, such as through the conservation of ephemeral wetlands, the movement of native amphibians can be facilitated, thereby reducing the likelihood of invasive species establishing themselves (Allen et al., 2020). This approach not only aids in maintaining genetic diversity but also supports the resilience of native populations against invasive threats.

Strengthening the resilience of native species involves enhancing their ability to withstand environmental changes and competition from invasive species. This can be achieved by maintaining habitat quality and connectivity, which are essential for the survival and reproduction of native amphibians (Wright et al., 2020). Conservation efforts should focus on protecting core habitats and creating buffer zones that reduce the impact of invasive species. Additionally, promoting landscape heterogeneity through small-scale agriculture can support diverse amphibian communities and enhance their resilience (Brüning et al., 2018).

7.2 Invasive species control measures

Implementing early detection and rapid response strategies is vital for controlling invasive species. By monitoring amphibian populations and their habitats, conservationists can quickly identify and address new invasions before they become widespread. This proactive approach requires collaboration between researchers, land managers, and policymakers to ensure timely and effective interventions.

Control methods for invasive species include physical removal, biological control, and chemical treatments. Physical removal involves manually capturing and removing invasive species from critical habitats, while biological control uses natural predators or competitors to manage invasive populations (Scroggie et al., 2019). Chemical treatments, although effective, should be used cautiously to avoid harming native species and ecosystems (Hamer and Mcdonnell, 2008). A combination of these methods, tailored to specific contexts, can provide a comprehensive approach to managing invasive species.

7.3 Policy recommendations

Strengthening land-use planning is essential to limit habitat fragmentation and its associated risks. Policies should prioritize the conservation of large, contiguous habitats and the restoration of fragmented landscapes to maintain ecological connectivity (Teixido et al., 2021). Effective land-use planning can mitigate the impacts of urbanization and agriculture on amphibian habitats, thereby reducing the potential for invasions.

International cooperation is crucial for managing invasive species, as these challenges often transcend national borders. Collaborative efforts can facilitate the sharing of knowledge, resources, and strategies to address invasions more effectively (Marvier et al., 2004). By working together, countries can develop coordinated policies and actions that enhance the resilience of amphibian populations and their habitats on a global scale.

8 Research Gaps and Future Directions

8.1 Unresolved questions

Despite the recognition of habitat fragmentation as a significant driver of amphibian invasions, there remain substantial gaps in understanding the specific interactions between fragmentation and invasion dynamics. Current research often focuses on the immediate impacts of fragmentation, such as changes in species distribution and abundance, but lacks a comprehensive understanding of the long-term ecological consequences (Evans et al., 2017). Additionally, the role of habitat fragmentation in facilitating the spread of invasive species through altered ecological interactions, such as increased competition and predation, is not fully understood (Falaschi et al., 2020). There is a need for studies that explore how fragmentation influences the ecological niches of both native and invasive amphibian species, potentially altering competitive dynamics and facilitating invasions.

Most existing studies on habitat fragmentation and amphibian invasions are short-term, limiting our ability to predict long-term ecological outcomes. Long-term studies are crucial to understanding the cumulative effects of fragmentation on amphibian populations, including genetic diversity, disease susceptibility, and population connectivity (Belasen et al., 2019). Such studies would provide insights into the temporal dynamics of invasions and the potential for native species to adapt to fragmented landscapes over time.

8.2 Emerging research directions

The integration of advanced remote sensing technologies and ecological modeling presents a promising avenue for advancing our understanding of amphibian invasions in fragmented habitats. Remote sensing can provide detailed spatial data on habitat changes, allowing researchers to monitor fragmentation patterns and their impacts on amphibian distributions in real-time (Marvier et al., 2004; Barron et al., 2020). Coupling these data with ecological models can enhance predictions of invasion risks and inform management strategies aimed at mitigating the impacts of habitat fragmentation.

Genetic studies offer valuable insights into how invasive amphibians adapt to fragmented environments. Research has shown that habitat fragmentation can lead to genetic erosion, which may affect the adaptive potential of amphibian populations (Neely et al., 2004). Investigating the genetic mechanisms underlying adaptation to fragmented habitats can reveal how invasive species overcome environmental challenges and establish themselves in new areas. Such studies could also identify genetic markers associated with invasion success, providing targets for conservation efforts aimed at preserving native biodiversity.

Acknowledgments

The authors extend sincere thanks to two anonymous peer reviewers for their feedback on the manuscript.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Allen C., Gonzales R., and Parrott L., 2020, Modelling the contribution of ephemeral wetlands to landscape connectivity, Ecological Modelling, 419: 108944.

https://doi.org/10.1016/j.ecolmodel.2020.108944

Barron M., Liebhold A., Kean J., Richardson B., and Brockerhoff E., 2020, Habitat fragmentation and eradication of invading insect herbivores, Journal of Applied Ecology, 57(3): 590-598.

https://doi.org/10.1111/1365-2664.13554

Becker C., Greenspan S., Martins R., Lyra M., Prist P., Metzger J., Pedro V., Haddad C., Sage E., Woodhams D., and Savage A., 2023, Habitat split as a driver of disease in amphibians, Biological Reviews, 98(3): 727-746.

https://doi.org/10.1111/brv.12927

Belasen A., Bletz M., Leite D., Toledo L., and James T., 2019, Long-term habitat fragmentation is associated with reduced MHC IIB diversity and increased infections in amphibian hosts, Frontiers in Ecology and Evolution, 6: 236.

https://doi.org/10.3389/fevo.2018.00236

Brüning L., Krieger M., Meneses-Pelayo E., Eisenhauer N., Pinilla M., Reu B., and Ernst R., 2018, Land-use heterogeneity by small-scale agriculture promotes amphibian diversity in montane agroforestry systems of northeast Colombia, Agriculture, Ecosystems & Environment, 264: 15-23.

https://doi.org/10.1016/j.agee.2018.05.011

Cushman S., 2006, Effects of habitat loss and fragmentation on amphibians: a review and prospectus, Biological Conservation, 128: 231-240.

https://doi.org/10.1016/j.biocon.2005.09.031

Dejean T., Valentini A., Miquel C., Taberlet P., Bellemain E., and Miaud C., 2012, Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus, Journal of Applied Ecology, 49: 953-959.

https://doi.org/10.1111/j.1365-2664.2012.02171.x

Duan R., Kong X., Huang M., Varela S., and Ji X., 2016, The potential effects of climate change on amphibian distribution, range fragmentation and turnover in China, PeerJ, 4: e2185.

https://doi.org/10.7717/peerj.2185

Evans M., Banks S., Driscoll D., Hicks A., Melbourne B., and Davies K., 2017, Short- and long-term effects of habitat fragmentation differ but are predicted by response to the matrix, Ecology, 98(3): 807-819.

https://doi.org/10.1002/ecy.1704

Falaschi M., Melotto A., Manenti R., and Ficetola G., 2020, Invasive species and amphibian conservation, Herpetologica, 76: 216-227.

https://doi.org/10.1655/0018-0831-76.2.216

Funk C., Greene A., Corn P., and Allendorf F., 2005, High dispersal in a frog species suggests that it is vulnerable to habitat fragmentation, Biology Letters, 1: 13-16.

https://doi.org/10.1098/rsbl.2004.0270

Gallardo B., Clavero M., Sánchez M., and Vilà M., 2016, Global ecological impacts of invasive species in aquatic ecosystems, Global Change Biology, 22(1): 151-163.

https://doi.org/10.1111/gcb.13004

Hamer A., and McDonnell M., 2008, Amphibian ecology and conservation in the urbanising world: a review, Biological Conservation, 141: 2432-2449.

https://doi.org/10.1016/j.biocon.2008.07.020

Johović I., Gama M., Banha F., Tricarico E., and Anastácio P., 2020, A potential threat to amphibians in the European Natura 2000 network: forecasting the distribution of the American bullfrog Lithobates catesbeianus, Biological Conservation, 245: 108551.

https://doi.org/10.1016/j.biocon.2020.108551

Koo K., and Choe M., 2021, Distribution change of invasive American bullfrogs (Lithobates catesbeianus) by future climate threaten endangered Suweon treefrog (Hyla suweonensis) in South Korea, Animals, 11(10): 2865.

https://doi.org/10.3390/ani11102865

Laufer G., Canavero A., Núñez D., and Maneyro R., 2008, Bullfrog (Lithobates catesbeianus) invasion in Uruguay, Biological Invasions, 10: 1183-1189.

https://doi.org/10.1007/s10530-007-9178-x

Laufer G., Gobel N., Kacevas N., and Lado I., 2023, American bullfrog (Lithobates catesbeianus) distribution, impact on native amphibians and management priorities in San Carlos, Uruguay, Knowledge & Management of Aquatic Ecosystems, 424: 20.

https://doi.org/10.1051/kmae/2023016

López J., Estrada C., Méndez U., Rodríguez J., Goyenechea I., and Cerón J., 2017, Evidence of niche shift and invasion potential of Lithobates catesbeianus in the habitat of Mexican endemic frogs, PLOS ONE, 12(9): e0185086.

https://doi.org/10.1371/journal.pone.0185086

Luo Z., Wang X., Yang S., Cheng X., Liu Y., and Hu J., 2021, Combining the responses of habitat suitability and connectivity to climate change for an East Asian endemic frog, Frontiers in Zoology, 18(1): 14.

https://doi.org/10.1186/s12983-021-00398-w

Marvier M., Kareiva P., and Neubert M., 2004, Habitat destruction, fragmentation, and disturbance promote invasion by habitat generalists in a multispecies metapopulation, Risk Analysis, 24(4): 869-878.

https://doi.org/10.1111/j.0272-4332.2004.00485.x

May F., Rosenbaum B., Schurr F., and Chase J., 2019, The geometry of habitat fragmentation: effects of species distribution patterns on extinction risk due to habitat conversion, Ecology and Evolution, 9: 2775-2790.

https://doi.org/10.1002/ece3.4951

Neely W., Souza K., Martins R., Marshall V., Buttimer S., De Assis A., Medina D., Whetstone R., Lyra M., Ribeiro J., Greenspan S., Haddad C., Anjos L., and Becker C., 2024, Host-associated helminth diversity and microbiome composition contribute to anti-pathogen defences in tropical frogs impacted by forest fragmentation, Royal Society Open Science, 11(6): 240530.

https://doi.org/10.1098/rsos.240530

Opdam P., and Wascher D., 2004, Climate change meets habitat fragmentation: linking landscape and biogeographical scale levels in research and conservation, Biological Conservation, 117: 285-297.

https://doi.org/10.1016/j.biocon.2003.12.008

Rossetti M., Tscharntke T., Aguilar R., and Batáry P., 2017, Responses of insect herbivores and herbivory to habitat fragmentation: a hierarchical meta-analysis, Ecology Letters, 20(2): 264-272.

https://doi.org/10.1111/ele.12723

Scroggie M., Preece K., Nicholson E., McCarthy M., Parris K., and Heard G., 2019, Optimizing habitat management for amphibians: from simple models to complex decisions, Biological Conservation, 236: 60-69.

https://doi.org/10.1016/j.biocon.2019.05.022

Teixido A., Sehn H., Quintanilla L., Gonçalves S., Fernández-Arellano G., Dáttilo W., Izzo T., Layme V., and Moreira L., 2021, A meta-analysis of the effects of fragmentation on the megadiverse herpetofauna of Brazil, Biotropica, 53(3): 726-737.

https://doi.org/10.1111/btp.12955

Urbina J., Bredeweg E., Cousins C., Blaustein A., and Garcia T., 2020, Reproductive characteristics of American bullfrogs (Lithobates catesbeianus) in their invasive range of the Pacific Northwest, USA, Scientific Reports, 10(1): 16271.

https://doi.org/10.1038/s41598-020-73206-w

Wright A., Grant E., and Zipkin E., 2020, A hierarchical analysis of habitat area, connectivity, and quality on amphibian diversity across spatial scales, Landscape Ecology, 35: 529-544.

https://doi.org/10.1007/s10980-019-00963-z

Yang S., Wang X., and Hu J., 2021, Mountain frog species losing out to climate change around the Sichuan Basin, Science of the Total Environment, 806: 150605.

https://doi.org/10.1016/j.scitotenv.2021.150605

Zheng J., 2023, Impact of transportation infrastructure on amphibians, Theoretical and Natural Science, 6: 426-430.

https://doi.org/10.54254/2753-8818/6/20230313