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Received: 23 January 2019 Accepted: 20 May 2019

DOI: 10.1111/jfb.14053

BRIEF COMMUNICATION FISH

Environmental DNA metabarcoding as an effective and rapid


tool for fish monitoring in canals

Allan D. McDevitt1* | Naiara Guimarães Sales1* | Samuel S. Browett1 |


Abbie O. Sparnenn1 | Stefano Mariani1 | Owen S. Wangensteen2 | Ilaria Coscia1* |
Chiara Benvenuto1*

1
Ecosystems and Environment Research
Centre, School of Environment and Life Abstract
Sciences, University of Salford, Salford, UK We focus on a case study along an English canal comparing environmental DNA
2
Norwegian College of Fishery Science,
(eDNA) metabarcoding with two types of electrofishing techniques (wade-and-reach
University of Tromsø, Tromsø, Norway
and boom-boat). In addition to corroborating data obtained by electrofishing, eDNA
Correspondence
provided a wider snapshot of fish assemblages. Given the semi-lotic nature of canals,
Allan D. McDevitt, Ecosystems and
Environment Research Centre, School of we encourage the use of eDNA as a fast and cost-effective tool to detect and moni-
Environment and Life Sciences, University of
tor whole fish communities.
Salford, Salford M5 4WT, UK.
Email: a.mcdevitt@salford.ac.uk
KEYWORDS
Funding information canals, eDNA, electrofishing, fish survey
Financial support was provided by The
People's Postcode Lottery and the University
of Salford.

Biodiversity in England, UK, depends on diverse habitats that are cur- thereby leading to an insufficient representation of the community
rently protected as sites of special scientific interest (SSSI). Among (Evans & Lamberti, 2017). Furthermore, the limited access to spe-
these designated areas, there are several canal systems, which are cialised equipment (such as electrofishing gear) and funding can make
monitored for habitat quality and the occurrence of certain indicator traditional surveys expensive and restrictive (Shaw et al., 2016).
species (Mainstone et al., 2018). Long-term and routine monitoring of Environmental DNA (eDNA) metabarcoding has emerged as an
canal systems is critically important, as these can be key in the assess- innovative and effective biodiversity monitoring tool that enables the
ment of invasive, migratory and endangered species, as well as rapid classification of multiple taxa without the assistance of a taxono-
safeguarding against the spread of diseases through the early detec- mist or local fishing knowledge (Taberlet et al., 2012). A cost-effective,
tion of pathogens. However, despite there being over 3000 km of fast and non-invasive eDNA protocol could prove extremely useful to
canals in the UK, little has been done to assess their entire biodiver- provide a constantly updated and broad monitoring of the aquatic bio-

sity (Natural England, 2011). diversity of canals and its changes through time. The present study
Traditionally, teleost populations have been monitored through focuses on the detection capability of eDNA metabarcoding com-

live capture and subsequent morphological identification of specimens pared with two different types of electrofishing for the detection of

(Hill et al., 2005). Such practices are intrusive, can compromise the fish species along a stretch of the Huddersfield Narrow Canal in the

health of targeted species and induce stress (Goldberg et al., 2016). UK (Figure 1a). This canal is a designated SSSI and has very limited

The selectivity of equipment used during traditional surveying prac- data available in terms of fish assemblage and biodiversity.
Three stretches of the canal were chosen for a Canal and River
tices can also lead to inaccuracies when monitoring freshwater eco-
Trust (www.canalrivertrust.org.uk) commissioned fish survey between
systems because specialised equipment can exclude the sampling of
December 2017 and January 2018. Electrofishing surveys were con-
specific species (due to size, microhabitat use, and low abundances),
ducted using two methods: backpack electrofishing with water levels
*These authors contributed equally to this work. lowered and surveyors wading through the canal bed between locks

J Fish Biol. 2019;1–4. wileyonlinelibrary.com/journal/jfb © 2019 The Fisheries Society of the British Isles 1
2
FISH MCDEVITT ET AL.

(a) (b)
eDNA Electrofishing

Phoxinus phoxinus
Locks 15-16
Anguilla anguilla

Esox lucius
Number of reads
<10
Cous gobio
<10–100
Wade-and-reach
<100–1000
Gymnocephalus cernua
Locks 14-15
Barbatula barbatula 1000–10000

Squalius cephalus

Boom-boat Thymallus thymallus >10000

Cyprinus carpio

Abramis brama Number of individuals

Salmo salar <10


10–50
Perca fluvialis
>250
Gobio gobio

Gasterosteus aculeatus

Rulus rulus
Locks 11-12
Salmo trua

250m 11-12 15-16 14-15 11-12 15-16 14-15


Locks Locks

F I G U R E 1 (a) Aerial photograph of the study area showing sampling locations for electrofishing (wade-and-reach and boom-boat) and eDNA
between locks 11–16 of the Huddersfield narrow canal. (b) A bubble graph showing presence–absence and categorical values of the number of
reads retained (after bioinformatic filtering) for eDNA (water and sediment combined) and the number of individuals caught for electrofishing for
16 fish species. Fish illustrations are not shown to scale

11–12 and 15–16 (Figure 1a) and a boom boat with water levels macroremains. Amplification of a fragment of the mitochondrial 12S
maintained between locks 14–15 (Figure 1a). Three sweeps were rRNA gene was conducted using the MiFish 12S primer set (Miya
undertaken at each stretch and fish were identified to species level et al., 2015) and library preparation were conducted according to the
(Supporting Information Methods in File S1). One to 16 h prior to protocol described in Sales et al. (2018). A total of 29 samples (includ-
these surveys being conducted (and before water levels were ing collection blanks and laboratory negative controls) were
lowered), water temperature and pH were measured, and water sequenced in a single multiplexed Illumina MiSeq (www.illuima.com)
(5 × 2 l) and sediment (3 × c. 10 g) samples were taken from each of run along with samples from a non-related project (Supporting Infor-
the three stretches of the canal. We chose to test both water and sed- mation Methods in File S1).
iment for eDNA detection as taxonomic composition can vary Water temperature ranged from 4.6 to 5.2 C and pH from 6.13 to
depending on the substrate analysed due to the habitat preferences 6.68. A total of nine species were identified with the two electrofish-
and life histories of different species (Koziol et al., 2019). Water sam- ing methods. With the boom boat, pike Esox lucius (L. 1758), roach
ples were filtered (250–400 ml) within 3 h of sampling in a Rutilus rutilus (L. 1758), chub Squalius cephalus (L. 1758) and carp
decontaminated laboratory using Sterivex 0.45 μM filters (Merck; Cyprinus carpio (L. 1758) were captured between locks 14–15. Using

www.merckmillipore.com) that were then kept at −20 C; sediment the other electrofishing method (wade-and-reach) between locks
samples were stored in 100% ethanol at room temperature. To avoid 11–12 and 15–16, perch Perca fluviatilis (L. 1758), gudgeon Gobio
cross contamination between samples, appropriate decontamination gobio (L. 1758), bream Abramis brama (L. 1758), ruffe Gymnocephalus
measures–precautions were taken: gloves were worn at all times, cernuus (L. 1758) and bullhead Cottus gobio (L. 1758) were captured in
equipment and surfaces were treated with bleach (10%) and three addition to the previous four species. Only R. rutilus and E. lucius were
field blanks were also analysed. captured across all three electrofishing sessions (Figure 1b).
DNA was extracted from the water samples using the DNeasy A total of 104,055 sequence reads (after all filtering steps;
powerwater kit and from the sediment samples using the DNeasy Supporting Information Methods and Table S1 in File S1) were
PowerMax Soil Kit (both Qiagen; wwww.qiagen.com) in the labora- retrieved, allowing for the detection of 16 species in the eDNA survey
tory. All field blanks were extracted first, and extractions were com- (Table S2). All nine species from the electrofishing survey were identi-
pleted following the manufacturer’s protocol. Owing to the nature of fied, with the addition of brown trout Salmo trutta (L. 1758), common
the sediment, it was not always possible to collect 10 g free of minnow Phoxinus phoxinus (L. 1758), European eel Anguilla anguilla
MCDEVITT ET AL.
FISH 3

(L. 1758), grayling Thymallus thymallus (L.1758), salmon Salmo salar 2018). While traditional methods cannot be replaced when investigat-
(L. 1758), stone loach Barbatula barbatula (L. 1758) and the three- ing size, age class distribution, and, for now, abundance, we find that
spined stickleback Gasterosteus aculeatus (L. 1758). The results pro- the power, speed and cost-effectiveness of eDNA metabarcoding
vided by eDNA were more consistent, with 12 out of the 16 species may often represent a highly efficient tool to assess and monitor
being detected in all three sampling sessions (Figure 1b). Electrofish- whole fish communities in canal systems.
ing failed to detect seven species, and a low number of species and
individuals within each species were recorded in two of three
AC KNOW LEDG EME NT S
stretches of canal (Figure 1b and Supporting Information Table S1 in
File S1). In addition, the selectivity of the method may hamper the We are grateful to Thomas King and Linda Butterworth at the Canal
detection of species difficult to capture due to their morphological or and River Trust for advice and discussions, and to MEM Fisheries for
behavioural characteristics (small body size fish species such as access to their data from the electrofishing surveys. Thanks to Bernd
P. phoxinus, G. aculeatus, or solitary and nocturnal fish such as Hänfling and the anonymous reviewers for improving the manuscript.
B. barbatula).
Owing to the expected relatively fast degradation of DNA mole-
AUTHOR CONTRIBU TIONS
cules (Seymour et al., 2018), the detection of species through this
method suggests their recent presence and provides an overview of C.B. and A.D.M. conceived and A.D.M, C.B., I.C., N.G.S., S.S.B. and
the contemporary fish community. However, eDNA molecules might S.M., designed the study. A.D.M., S.S.B. and A.O.S. carried out the
persist in the water column for more than a few days and thus, allow fieldwork. N.G.S. and A.D.M. performed the laboratory work.
the detection of transient species not necessarily present in the sys- N.G.S. and O.S.W. performed the bioinformatics. A.D.M., N.G.S.,
tem at the collection time (Dejean et al., 2011). DNA molecules can be I.C. and C.B.. analysed the data. A.D.M., N.G.S., C.B., I.C., S.S.B. and
transported long distances so fish may be detected far away from A.O.S. wrote the paper, with all authors commenting on the
their occurrence (Jane et al., 2015) or even originating from different manuscript.
sources. Therefore, the detection of certain species (e.g., S. trutta and
S. salar) in this study could be due to an external source, such as
human consumption. Putative false positives should be taken into OR CID

account and carefully analysed before drawing a conclusion about the


Allan D. McDevitt https://orcid.org/0000-0002-2677-7833
occurrence of these species in the Huddersfield Narrow Canal, and to
understand their origin (e.g., endogenous or exogenous, regional or
local). RE FE RE NCE S
As demonstrated in previous studies, eDNA obtained from the
Balasingham, K. D., Walter, R. P., Mandrak, N. E., & Heath, D. D. (2018).
water column yielded better results when compared with sediment Environmental DNA detection of rare and invasive fish species in two
samples (Koziol et al., 2019; Shaw et al., 2016), with 14 out of 16 spe- great lakes tributaries. Molecular Ecology, 27, 112–127.
cies recovered, but sediment samples outperformed water samples Dejean, T., Valentini, A., Suparc, A., Pellier-Cuit, S., Pompanon, F.,
Taberlet, P., & Miaud, C. (2011). Persistence of environmental DNA in
only by detecting A. anguilla and P. phoxinus. eDNA recovered from
freshwater ecosystems. PLoS One, 6, e23398.
sediment samples allowed the detection of only five species Evans, N. T., & Lamberti, G. A. (2017). Freshwater fisheries assessment
(A. anguilla, S. trutta, S. salar and B. barbatula; Supporting Information using environmental DNA: A primer on the method, its potential, and
Table S1). These could originate from historical depositions rather shortcomings as a conservation tool. Fisheries Research, 197, 60–66.
Goldberg, C. S., Turner, C. R., Deiner, K., Klymus, K. E., Thomsen, P. F.,
than contemporary records (Turner et al., 2015). Given the associated
Murphy, M. A., … Taberlet, P. (2016). Critical considerations for the
effort and costs of obtaining sediment samples from aquatic environ- application of environmental DNA methods to detect aquatic species.
ments, we would not recommend incorporating them in future bio- Methods in Ecology and Evolution, 7, 1299–1307.
monitoring using eDNA in canals. Hänfling, B., Lawson Handley, L., Read, D. S., Hahn, C., Li, J., Nichols, P., …
Winfield, I. J. (2016). Environmental DNA metabarcoding of lake fish
While many studies have shown the advantages of using eDNA
communities reflects long-term data from established survey methods.
metabarcoding in lotic (flowing streams and rivers; Balasingham et al., Molecular Ecology, 25, 3101–3119.
2018) and lentic (still lakes and ponds; (Hänfling et al., 2016; Harper Harper, L. R., Buxton, A. S., Rees, H. C., Bruce, K., Brys, R., Halfmaerten, D.,
et al., 2018) systems, they also raise concerns about the influence of … Hanfling, B. (2018). Prospects and challenges of environmental DNA
flow in DNA dispersal in fast running water and the need to sample (eDNA) monitoring in freshwater ponds. Hydrobiologia, 826, 25–41.
Hill, D., Fasham, M., Tucker, G., Shewry, M., & Shaw, P. (2005). Handbook
multiple locations in lentic waters. Canals represent man-made envi-
of biodiversity methods: Survey, evaluation and monitoring. Cambridge,
ronments with a semi-lotic regime and regulated flow, which minimise UK: University Press.
the risk of detection of species present too far away, while at the Jane, S. F., Wilcox, T. M., McKelvey, K. S., Young, M. K., Schwartz, M. K.,
same time allowing enough water movement to reduce the need for Lowe, W. H., … Whiteley, A. R. (2015). Distance, flow, and PCR inhibi-
tion: eDNA dynamics in two headwater streams. Molecular Ecology
extra sampling akin to that undertaken in lentic systems. Here we
Resources, 15, 216–227.
showed that eDNA corroborates the data obtained by electrofishing, Koziol, A., Stat, M., Simpson, T., Jarman, S., DiBatista, J. D., Harvey, E. S., …
but also provides a wider snapshot of fish assemblages (Pont et al., Bunce, M. (2019). Environmental DNA metabarcoding studies are
4
FISH MCDEVITT ET AL.

critically affected by substrate selection. Molecular Ecology Resources, DNA metabarcoding and conventional fish survey methods in a river
19, 366–376. system. Biological Conservation, 197, 131–138.
Mainstone, C. P., Hall, R. A., Hatton-Ellis, T. W., Boon, P. J., Bean, C. W., & Seymour, M., Durance, I., Cosby, B. J., Ransom-Jones, E., Deiner, K.,
Lee, A. S. L. (2018). In Guidelines for the selection of biological SSSIs. Part Ormerod, S. J., … Edwards, F. (2018). Acidity promotes degradation of
2: Detailed guidelines for habitats and species groups. Chapter 6 Freshwa- multi-species environmental DNA in lotic mesocosms. Communications
ter habitats. Peterborough, UK: Joint Nature Conservation Committee. Biology, 1, 4.
http://jncc.defra.gov.uk/pdf/SSSI_chapter6feshwater_2018.pdf Taberlet, P., Coissac, E., Hajibabaei, M., & Rieseberg, L. H. (2012). Environ-
Miya, M., Sato, Y., Fukunaga, T., Sado, T., Poulsen, J. Y., Sato, K., … mental DNA. Molecular Ecology, 21, 1789–1793.
Iwasaki, W. (2015). MiFish, a set of universal PCR primers for Turner, C. R., Uy, K. L., & Everhart, R. C. (2015). Fish environmental DNA
metabarcoding environmental DNA from fishes: Detection of more is more concentrated in aquatic sediments than surface water. Biologi-
than 230 subtropical marine species. Royal Society Open Science, 2, cal Conservation, 183, 93–102.
259–291.
Natural England. (2011). Protecting England’s natural treasures: Sites of spe-
cific scientific interest. Catalogue code: NE306. Retrieved from www. SUPPORTING INF ORMATION
naturalengland.org.uk/publications
Additional supporting information may be found online in the
Pont, D., Rocle, M., Valentini, A., Civade, R., Jean, P., Maire, A., …
Dejean, T. (2018). Environmental DNA reveals quantitative patterns of Supporting Information section at the end of this article.
fish biodiversity in large rivers despite its downstream transportation.
Scientific Reports, 8, 10361.
Sales, N. G., Wangensteen, O. S., Carvalho, D. C., & Mariani, S. (2018). How to cite this article: McDevitt AD, Sales NG, Browett SS,
Influence of preservation methods, sample medium and sampling time et al. Environmental DNA metabarcoding as an effective and
on eDNA recovery in a Neotropical river. bioRxiv. doi: https://doi.org/
rapid tool for fish monitoring in canals. J Fish Biol. 2019;1–4.
10.1101/489609
Shaw, J. L. A., Clarke, L. J., Wedderburn, S. D., Barnes, T. C., https://doi.org/10.1111/jfb.14053
Weyrich, L. S., & Cooper, A. (2016). Comparison of environmental

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