Multispecies models reveal that eDNA metabarcoding is more sensitive than backpack electrofishing for conducting fish surveys in freshwater streams

McColl-Gausden, Emily F.; Weeks, Andrew R.; Coleman, Rhys A.; Robinson, Katie L.; Song, Sue; Raadik, Tarmo A.; Tingley, Reid

doi:10.1111/mec.15644

Cited by 51 publications

(49 citation statements)

References 83 publications

(194 reference statements)

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“…The sensitivity, non-invasiveness, and cost-efficiency of environmental DNA (eDNA) based methods have been proven for diverse habitats and species making them powerful new tools for conservation biology and biodiversity assessments (Barnes and Turner, 2016;Deiner et al, 2017;Huerlimann et al, 2020). Regarding the detection of fish species, eDNA-based monitoring outperforms traditional methods such as electrofishing: for example, for the detection of the endangered European weather loach, Misgurnus fossilis (Sigsgaard et al, 2015), the assessment of fish communities in Australian streams (McColl-Gausden et al, 2020), and the distribution of brook trout, Salvelinus fontinalis in a US watershed (Evans et al, 2017). The manifold successes of eDNA-based species detection lead to a call for more standardization and better reporting practices (Goldberg et al, 2016;Minamoto et al, 2020;Thalinger et al, 2021a) and to an international effort for implementing the technology into routine species monitoring (Leese et al, 2016;Pilliod et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

The Effect of Activity, Energy Use, and Species Identity on Environmental DNA Shedding of Freshwater Fish

et al. 2021

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The quantitative measurement of environmental DNA (eDNA) from field-collected water samples is gaining importance for the monitoring of fish communities and populations. The interpretation of these signal strengths depends, among other factors, on the amount of target eDNA shed into the water. However, shedding rates are presumably associated with species-specific traits such as physiology and behavior. Although such differences between juvenile and adult fish have been previously detected, the general impact of movement and energy use in a resting state on eDNA release into the surrounding water remains hardly addressed. In an aquarium experiment, we compared eDNA shedding between seven fish species occurring in European freshwaters. The investigated salmonids, cyprinids, and sculpin exhibit distinct adaptions to microhabitats, diets, and either solitary or schooling behavior. The fish were housed in aquaria with constant water flow and their activity was measured by snapshots taken every 30 s. Water samples for eDNA analysis were taken every 3 h and energy use was determined in an intermittent flow respirometer. After controlling for the effect of fish mass, our results demonstrate a positive correlation between target eDNA quantities as measured with digital PCR, fish activity, and energy use, as well as species-specific differences. For cyprinids, the model based on data from individual fish was only partly transferable to groups, which showed lower activity and higher energy use. Our findings highlight the importance of fish physiology and behavior for the comparative interpretation of taxon-specific eDNA quantities. Species traits should therefore be incorporated into eDNA-based monitoring and conservation efforts.

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Section: Introductionmentioning

confidence: 99%

The Effect of Activity, Energy Use, and Species Identity on Environmental DNA Shedding of Freshwater Fish

et al. 2021

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“…The sensitivity, non-invasiveness and cost-efficiency of environmental DNA (eDNA) based methods has been proven for diverse habitats and species making them powerful new tools for conservation biology and biodiversity assessments (Barnes and Turner, 2016; Deiner et al, 2017; Huerlimann et al, 2020). Regarding the detection of fish species, eDNA-based monitoring outperforms traditional methods such as electrofishing: for example, for the detection of the endangered European weather loach, Misgurnus fossilis (Sigsgaard et al, 2015), the assessment of fish communities in Australian streams (McColl‐Gausden et al, 2020), and the distribution of brook trout, Salvelinus fontinalis in a US watershed (Evans et al, 2017). The manifold successes of eDNA-based species detection lead to a call for more standardization and better reporting practices (Goldberg et al, 2016; Minamoto et al, 2020; Thalinger et al, 2020a) and to an international effort for implementing the technology into routine species monitoring (Leese et al, 2016; Pilliod et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

The effect of activity, energy use, and species identity on environmental DNA shedding of freshwater fish

Thalinger

Rieder

Teuffenbach

et al. 2020

Preprint

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The quantitative measurement of eDNA form field-collected water samples is gaining importance for the monitoring of fish communities and populations. The interpretation of these signal strengths depends, among other factors, on the amount of target eDNA shed into the water. However, shedding rates are presumably associated with species-specific traits such as physiology and behavior. Although such differences between juvenile and adult fish have been previously detected, the general impact of movement and energy use in a resting state on eDNA release into the surrounding water remains hardly addressed. In an aquarium experiment, we compared eDNA shedding between seven fish species occurring in European freshwaters. The investigated salmonids, cyprinids and sculpin exhibit distinct adaptions to microhabitats, diets, and either solitary or schooling behavior. The fish were housed in aquaria with constant water flow and their activity was measured by snapshots taken every 30 s. Water samples for eDNA analysis were taken every 3 h and energy use was determined in an intermittent flow respirometer. After controlling for the effect of fish mass, our results demonstrate a positive correlation between target eDNA quantities as measured with digital PCR, fish activity and energy use, as well as species-specific differences. For cyprinids, the model based on data from individual fish was only partly transferable to groups, which exhibited lower activity and higher energy use. Our findings highlight the importance of fish physiology and behavior for the comparative interpretation of taxon-specific eDNA quantities. Species traits should therefore be incorporated into eDNA-based monitoring and conservation efforts.

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“…In previous studies of eDNA metabarcoding, multispecies site occupancy models have been applied by aggregating sequence reads into binary detection/non-detection data (Doi et al 2019, Bush et al 2020, McClenaghan et al 2020, McColl-Gausden et al 2020. In such an approach, sequence read counts are not explicitly modeled, making it difficult to adequately decompose the combined effects of throughput and relative frequency of species sequences on the probability of species detection.…”

Section: Discussionmentioning

confidence: 99%

“…The detection of species using eDNA may be more sensitive than that of traditional survey methods (Smart et al 2015, Yamamoto et al 2017, McColl-Gausden et al 2020).…”

Section: Introductionmentioning

confidence: 99%

“…To address these issues, we developed a novel extension of the multispecies site occupancy modeling framework (Dorazio & Royle 2005, Dorazio et al 2006. Multispecies site occupancy models account for the imperfect detection of species in a metacommunity and have recently been applied in eDNA metabarcoding (Doi et al 2019, Bush et al 2020, McClenaghan et al 2020, McColl-Gausden et al 2020. However, to apply these models to eDNA metabarcoding data, the original sequence read counts must be aggregated into binary detection and non-detection indicators.…”

Section: Introductionmentioning

confidence: 99%

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Multispecies site occupancy modeling and study design for spatially replicated environmental DNA metabarcoding

Fukaya

Kondo

Matsuzaki

et al. 2021

Preprint

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Environmental DNA (eDNA) metabarcoding has become widely applied to gauge biodiversity in a noninvasive and cost-efficient manner. The detection of species using eDNA metabarcoding is, however, imperfect owing to various factors that can cause false negatives in the inherent multi-stage workflow. Imperfect detection in the multi-stage workflow of eDNA metabarcoding also raises an issue of study design: namely, how available resources should be allocated among the different stages to optimize survey efficiency. Here, we propose a variant of the multispecies site occupancy model for eDNA metabarcoding studies where samples are collected at multiple sites within a region of interest. This model describes the variation in sequence reads, the unique output of the high-throughput sequencers, in terms of the hierarchical workflow of eDNA metabarcoding and interspecific heterogeneity, allowing the decomposition of the sources of variation in the detectability of species throughout the different stages of the workflow. We also introduced a Bayesian decision analysis framework to identify the study design that optimizes the efficiency of species detection with a limited budget. An application of the model to freshwater fish communities in the Lake Kasumigaura watershed, in Japan, highlighted a remarkable inhomogeneity in the detectability of species, indicating a potential risk of the biased detection of specific species. Species with lower site occupancy probabilities tended to be difficult to detect as they had lower capture probabilities and lower dominance of the sequences. The expected abundance of sequence reads was predicted to vary by up to 23.5 times between species. An analysis of the study design suggested that ensuring multiple within-site replications of the environmental samples is preferred in order to achieve better species detection efficiency, provided that a throughput of tens of thousands of sequence reads was secured. The proposed framework makes the application of eDNA metabarcoding more error-tolerant, allowing ecologists to monitor ecological communities more efficiently.

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Multispecies models reveal that eDNA metabarcoding is more sensitive than backpack electrofishing for conducting fish surveys in freshwater streams

Cited by 51 publications

References 83 publications

The Effect of Activity, Energy Use, and Species Identity on Environmental DNA Shedding of Freshwater Fish

The Effect of Activity, Energy Use, and Species Identity on Environmental DNA Shedding of Freshwater Fish

The effect of activity, energy use, and species identity on environmental DNA shedding of freshwater fish

Multispecies site occupancy modeling and study design for spatially replicated environmental DNA metabarcoding

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