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Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities

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Abstract
Horizon scans have emerged as a valuable tool to anticipate the incoming invasive alien species (IAS) by judging species on their potential impacts. However, little research has been conducted on quantifying actual impacts and assessing causes of species-specific vulnerabilities to particular IAS due to persistent methodological challenges. The underlying interspecific mechanisms driving species-specific vulnerabilities therefore remain poorly understood, even though they can substantially improve the accuracy of risk assessments. Given that interspecific interactions underlying ecological impacts of IAS are often shaped by phenological synchrony, we tested the hypothesis that temporal mismatches in breeding phenology between native species and IAS can mitigate their ecological impacts. Focusing on the invasive American bullfrog (Lithobates catesbeianus), we combined an environmental DNA (eDNA) quantitative barcoding and metabarcoding survey in Belgium with a global meta-analysis, and integrated citizen-science data on breeding phenology. We examined whether the presence of native amphibian species was negatively related to the presence or abundance of invasive bullfrogs and whether this relationship was affected by their phenological mismatches. The field study revealed a significant negative effect of increasing bullfrog eDNA concentrations on native amphibian species richness and community structure. These observations were shaped by species-specific vulnerabilities to invasive bullfrogs, with late spring- and summer-breeding species being strongly affected, while winter-breeding species remained unaffected. This trend was confirmed by the global meta-analysis. A significant negative relationship was observed between phenological mismatch and the impact of bullfrogs. Specifically, native amphibian species with breeding phenology differing by 6 weeks or less from invasive bullfrogs were more likely to be absent in the presence of bullfrogs than species whose phenology differed by more than 6 weeks with that of bullfrogs. Taken together, we present a novel method based on the combination of aqueous eDNA quantitative barcoding and metabarcoding to quantify the ecological impacts of biological invaders at the community level. We show that phenological mismatches between native and invasive species can be a strong predictor of invasion impact regardless of ecological or methodological context. Therefore, we advocate for the integration of temporal alignment between native and IAS's phenologies into invasion impact frameworks.
Keywords
American bullfrog (Lithobates catesbeianus), alien invasive species, citizen‐science, environmental DNA (eDNA) metabarcoding, global meta‐analysis, interspecific interactions, invasion management, timing of breeding, BULLFROGS RANA-CATESBEIANA, AMERICAN BULLFROGS, ALIEN, MANAGEMENT, FRAMEWORK, BIODIVERSITY, RESPONSES, DYNAMICS, ISLAND, ERROR

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MLA
Everts, Teun, et al. “Phenological Mismatches Mitigate the Ecological Impact of a Biological Invader on Amphibian Communities.” ECOLOGICAL APPLICATIONS, vol. 34, no. 6, 2024, doi:10.1002/eap.3017.
APA
Everts, T., Van Driessche, C., Neyrinck, S., Haegeman, A., Ruttink, T., Jacquemyn, H., & Brys, R. (2024). Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities. ECOLOGICAL APPLICATIONS, 34(6). https://doi.org/10.1002/eap.3017
Chicago author-date
Everts, Teun, Charlotte Van Driessche, Sabrina Neyrinck, Annelies Haegeman, Tom Ruttink, Hans Jacquemyn, and Rein Brys. 2024. “Phenological Mismatches Mitigate the Ecological Impact of a Biological Invader on Amphibian Communities.” ECOLOGICAL APPLICATIONS 34 (6). https://doi.org/10.1002/eap.3017.
Chicago author-date (all authors)
Everts, Teun, Charlotte Van Driessche, Sabrina Neyrinck, Annelies Haegeman, Tom Ruttink, Hans Jacquemyn, and Rein Brys. 2024. “Phenological Mismatches Mitigate the Ecological Impact of a Biological Invader on Amphibian Communities.” ECOLOGICAL APPLICATIONS 34 (6). doi:10.1002/eap.3017.
Vancouver
1.
Everts T, Van Driessche C, Neyrinck S, Haegeman A, Ruttink T, Jacquemyn H, et al. Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities. ECOLOGICAL APPLICATIONS. 2024;34(6).
IEEE
[1]
T. Everts et al., “Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities,” ECOLOGICAL APPLICATIONS, vol. 34, no. 6, 2024.
@article{01JD4C4DBMT18TPYX48HGXFCC4,
  abstract     = {{Horizon scans have emerged as a valuable tool to anticipate the incoming invasive alien species (IAS) by judging species on their potential impacts. However, little research has been conducted on quantifying actual impacts and assessing causes of species-specific vulnerabilities to particular IAS due to persistent methodological challenges. The underlying interspecific mechanisms driving species-specific vulnerabilities therefore remain poorly understood, even though they can substantially improve the accuracy of risk assessments. Given that interspecific interactions underlying ecological impacts of IAS are often shaped by phenological synchrony, we tested the hypothesis that temporal mismatches in breeding phenology between native species and IAS can mitigate their ecological impacts. Focusing on the invasive American bullfrog (Lithobates catesbeianus), we combined an environmental DNA (eDNA) quantitative barcoding and metabarcoding survey in Belgium with a global meta-analysis, and integrated citizen-science data on breeding phenology. We examined whether the presence of native amphibian species was negatively related to the presence or abundance of invasive bullfrogs and whether this relationship was affected by their phenological mismatches. The field study revealed a significant negative effect of increasing bullfrog eDNA concentrations on native amphibian species richness and community structure. These observations were shaped by species-specific vulnerabilities to invasive bullfrogs, with late spring- and summer-breeding species being strongly affected, while winter-breeding species remained unaffected. This trend was confirmed by the global meta-analysis. A significant negative relationship was observed between phenological mismatch and the impact of bullfrogs. Specifically, native amphibian species with breeding phenology differing by 6 weeks or less from invasive bullfrogs were more likely to be absent in the presence of bullfrogs than species whose phenology differed by more than 6 weeks with that of bullfrogs. Taken together, we present a novel method based on the combination of aqueous eDNA quantitative barcoding and metabarcoding to quantify the ecological impacts of biological invaders at the community level. We show that phenological mismatches between native and invasive species can be a strong predictor of invasion impact regardless of ecological or methodological context. Therefore, we advocate for the integration of temporal alignment between native and IAS's phenologies into invasion impact frameworks.}},
  articleno    = {{e3017}},
  author       = {{Everts, Teun and Van Driessche, Charlotte and Neyrinck, Sabrina and Haegeman, Annelies and Ruttink, Tom and Jacquemyn, Hans and Brys, Rein}},
  issn         = {{1051-0761}},
  journal      = {{ECOLOGICAL APPLICATIONS}},
  keywords     = {{American bullfrog (Lithobates catesbeianus),alien invasive species,citizen‐science,environmental DNA (eDNA) metabarcoding,global meta‐analysis,interspecific interactions,invasion management,timing of breeding,BULLFROGS RANA-CATESBEIANA,AMERICAN BULLFROGS,ALIEN,MANAGEMENT,FRAMEWORK,BIODIVERSITY,RESPONSES,DYNAMICS,ISLAND,ERROR}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{19}},
  title        = {{Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities}},
  url          = {{http://doi.org/10.1002/eap.3017}},
  volume       = {{34}},
  year         = {{2024}},
}

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