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OPINIONPAPERZoochorous dispersal of freshwater bivalves: an overlooked
vector in biological invasions?

Neil E. Coughlan

, Andrew L. Stevens

, Thomas C. Kelly

, Jaimie T.A. Dick


Marcel A.K. Jansen
Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Medical Biology Centre,
97 Lisburn Rd, Belfast BT9 7BL, Northern Ireland
Centre for Environmental Research, Innovation & Sustainability, Institute of Technology Sligo, Ash Lane, Co. Sligo, Ireland
School of Biological, Earth and Environmental Sciences, University College Cork, Distillery Field, North Mall, Cork, Ireland
Center for Limnology, University of Wisconsin-Madison, Madison, WI, USA
Vectors that underpin the natural dispersal of invasive alien species are frequently unknown.
In particular, the passive dispersal (zoochory) of one organism (or propagule) by another, usually more
mobile animal, remains poorly understood. Field observations of the adherence of invasive freshwater
bivalves to other organisms have prompted usto assess the importance of zoochory in the spread of three
prolific invaders: zebra musselDreissena polymorpha; quagga musselDreissena bugensis; and Asian
clamCorbiculafiuminea.Anextensive,systematicsearchoftheliterature wasconductedacrossmultiple
on-line scientific databases using various search terms and associated synonyms. In total, onlyfive
publications fully satisfied the search criteria. It appears that somefish species can internally transport
juvenileD.polymorphacanadheretotheexternalsurfacesofwaterbirds.Overall, literature suggeststhat
zoochorous dispersal of invasive bivalves is possible, but likely a rare occurrence. However, even the
in a substantial population. Here, we highlight knowledge gaps, identify realistic opportunities for data
collection, and suggest management protocols to mitigate the spread of invasive alien species.Keywords:ectozoochory / endozoochory / freshwater ecosystems / ichthyochory / invasive alien / secondary spread
Résumé–Zoochorie de bivalves d’eau douce; un vecteur négligé dans les invasions biologiques?
Les vecteurs qui sous-tendent la dispersion naturelle des espèces exotiques envahissantes sont souvent
inconnus. En particulier, la dispersion passive (zoochorie) d’un organisme (ou propagule) par un autre,
habituellement plus mobile, reste mal comprise. Les observations sur le terrain de l’adhésion des bivalves
la propagation de trois envahisseurs prolifiques : la moule zébréeDreissena polymorpha; Moule Quagga
Dreissena bugensis; et la palourde asiatiqueCorbiculafiuminea. Une recherche approfondie et
satisfait les critères de recherche. Il semble que certaines espèces de poissons puissent transporter
intérieurement des spécimens adultes viables deD. polymorphaetC.fiuminea. En outre, la littérature

eau. Dans l’ensemble, la littérature suggère que la dispersion par zoochorie des bivalves invasifs est
possible, mais probablement une occurrence rare. Cependant, même l’établissement de quelques individus
(ou un seul spécimen autofécondant deC.fiuminea) peut, aufil du temps, entraîner une population
importante. Ici, nous mettons en évidence les lacunes en matière de connaissances, identifions des
opportunités réalistes pour la collecte de données et proposons des protocoles de gestion pour atténuer la
propagation d’espèces exotiques envahissantes.*Corresponding author:neil.coughlan.zoology@gmail.comKnowl. Manag. Aquat. Ecosyst. 2017, 418, 42
©N.E. Coughlanet al., Published byEDP Sciences2017


Knowledge &

Management o


www.kmae-journal.orgJournal fully supported by Onema
This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use,
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Mots-clés :ectozoochorie / endozoochorie / écosystèmes d’eau douce / ichthychorie / espèce exotique invasive /

propagation secondaire

1 Introduction
The majority of primary introductions of invasive alien
species (IAS) are considered to have occurred via anthropo-
genic means (Hulmeet al., 2008;Solarzet al., 2017).
However, the natural (or‘unaided by humans’)dispersalof
organisms can also result in the arrival of an IAS in a new
region (Hulmeet al., 2016). More importantly,the secondary
be facilitated by natural dispersal vectors, including water
et al., 2017b). Recent European Union (EU) and United
States of America (USA) legislation (EU Regulation 1143/
2014 and Safeguarding the Nation from the Impacts of
Invasive Species–amendment to Executive Order 13112,
respectively) seek to prevent, control and eradicate IAS
within both territories. In order to develop comprehensive
IAS prevention and control measures, species risk assess-
ments must consider not only broad invasion pathway
categories, but also specific vectors (Esslet al., 2015).
processes operating between hydrologically unconnected
water bodies remains limited (Soomerset al., 2013;
Incagnoneet al.,2015;Coughlanet al.,2017a).
Zoochorous transport of one organism by another more
mobile animal can facilitate dispersal of various taxa (see
Fig. 1)(Reynoldset al., 2015;Green, 2016;Coughlanet al.,
2017a). Many organisms, particularly propagule stages (e.g.,
seeds, spores, eggs, ephippia, gemmules, statoblasts, or cysts)
(gut), or upon the exterior surfaces of other animals. The
association where one organism (or propagule) is externally
transported by another organism is categorised under various
biological relationships which include,inter alia, ectozoo-
chory, phoresis, commensalism, and fouling. Ectozoochory
(synonyms epizoochory, exozoochory), a term originally used
to describe the dispersal of plant propagules via external
adherence to animal vectors, is now widely employed to refer
Green, 2016;Coughlanet al., 2017a). Endozoochory, a term
originally used to describe seed dispersal, now encompasses
the internal dispersal of a variety of taxa.
The spread of invasive alien bivalves represents a major
Vander Zanden, 2010;Doudaet al., 2017). In particular, zebra
musselDreissena polymorpha(Pallas, 1771), quagga mussel,
fiuminea(Müller, 1774) are prolific invaders, whose presence
canhave damaging ecologicalandeconomicconsequences for
invaded habitats (Pimentelet al., 2005;Sousaet al., 2014;
range expansion of these bivalves has been observed (e.g.,
Aldridgeetal.,2014;Benson,2014;Caffreyetal.,2016).Underoptimal conditions, these bivalve species display rapid growth
fluminea, from even one self-fertilising individual (McMahon,
2002). In contrast to many freshwater bivalve species, the life
cycles oftheseinvaders do not includea parasitic larval stages
(Mackie, 1991). Rather, planktonic larval (e.g., veliger) stages
post-veliger (e.g., juvenile) stages occurs. Both up-stream and
between catchment dispersal of these bivalves has been
ly by recreational water users (e.g., anglers, boaters, and
canoeists) (Kappes and Haase, 2012;Banhaet al., 2016).
Nevertheless, possible alternative natural vectors of passive
dispersal remain under-researched, even though these vectors
Banhaet al., 2016). Field observations ofD. polymorpha
attachment to more mobile freshwater organisms (seeFig. 2)
have prompted us to assess the importance of zoochory in the
spread of invasive freshwater bivalves. Here, we examine the
freshwater bivalves:D. polymorpha;D. bugensis; andC.

2 Methods
We systematically searched for relevantmaterial usingthe
on-line scientiflc databases Thomson-ReutersWeb of Science
andScopus. An additional search for relevant material was
preformed usingGoogleandGoogle Scholar. All searches
were undertaken in December 2016, and focused on various
terms used in the literature. For example, the principle search
term used to derive relevant material was: (mussel OR clam
OR bivalv* OR dreissena OR corbicula) AND (external OR
*chory OR *zoon OR phor* OR gut OR *intestinal) AND
(dispersal OR dispersion). Species scientiflc names (D.
polymorpha,D. bugensisandC.fluminea) and common
search terms (e.g., epizoon, entozoon, ectozoochory, endo-
zoochory, passive dispersal, fouling, phoresy) were further
Moreover, reference lists from all retrieved books and articles
were screened for other relevant publications. Selected
literature was then appraised for inclusion within this paper
based upon pertinence to the core topic,e.g., studies which
directly evaluate zoochorous mediated dispersal ofD.
polymorpha,D. bugensisorC.fluminea. There was no
restriction on publication year.

3 Results and discussion
The search yielded 219 and 161 publications fromWeb of
ScienceandScopus, respectively.GoogleandGoogle Scholar
did not provide any additional pertinent material, within the
Page 2 of8N.E. Coughlanet al.: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 42
flrst ten search-pages. Numerous studies suggested zoochory
as a potential dispersal mechanism for various freshwater
bivalves and other Mollusca species, however, many did not
reference a citation for this assumption. Studies selected for
inclusion within this paper are those which attempted to
experimentally examine zoochorous dispersal ofD. poly-
morpha,D. bugensis,orC.fluminea. In total, onlyflve
publications met the full search criteria (Tab. 1).

3.1 Endozoochorous dispersal
Many studies have reported the consumption of invasive
1988;Hamilton and Davison Ankney, 1994;Tuckeret al.,
1996). In most cases, gut contents or faecal samples appear to
suggest that the consumer can effectively digestD. poly-
morpha,D. bugensisandC.fluminealeaving only shell
fragments (e.g.,Hamilton and Davison Ankney, 1994;
do not examine endozoochorous dispersal and, therefore, do
not attempt to assess the survival and viability of intact
specimens (if any) found within retrieved gut or faecal
clams (Sphaeriidae), valve snails (Valvatidae), pond snails
(Lymnaeidae) and mussels (Mytilidae), have been shown to
survive gut passage through differentflsh and waterbird
Belzet al., 2012;van Leeuwenet al., 2012).
Literature reviewed here (and manyflsh and waterbird
dietary studies) indicate (or imply) thatD. polymorpha,D.
Remarkably,Gatlinet al.(2013)recorded the survival ofC.
flumineaandD. polymorphathat have passed through the gut
of migratory blue catflsh (Ictalurus furcatus), a species which
travels up to 689km in a year (Trippet al., 2011). However,
much shorter distances as dictated by gut retention times.
unable to survive gut passage throughI. furcatus

in waters
above 21.1°C, however, this is unlikely to overly inhibit
dispersal potential as migrations typically occur when water
temperatures are between 8 and 18°C. Incidentally, we
hypothesise that the observed increase in bivalve mortality
temperatures may increase digestion efflciency of someflsh
species (Mizanuret al., 2014;Deet al., 2016). Conversely,
higher water temperature can also result in reduced retention
times within the gastrointestinal tract (Deet al., 2016).
The feeding ecology offlsh and waterbird species, and
associated digestive morphological traits, will likely influence
Fig. 1.Overland long distance dispersal (LDD) (A), short distance dispersal (SDD) (B), and‘stepping stone’dispersal (C) of invasive bivalve
Moreover, zoochorous vectors may intensify invader spread across large aquatic areas (e.g., large lakes). Dashed lines indicate water current.
Fig. 2.(A & B) Two adult zebra musselsDreissena polymorpha
attached to the dorsal carapace of an odonata nymphEpicorduliasp.
(Corduliidae) larva. The nymph was collected on Lake Mendota,

Madison, WI (43°04



W) on 24th October 2016
viaa minnow trap in 2m of water (Photo credits, A.L. Stevens). The
criteria used to identify species are described byBouchardet al.
(2004). (C) Adult crayfish specimen extensively fouled byD.
polymorpha(Photo credit, Minnesota Department of Natural
Page 3 of8N.E. Coughlanet al.: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 42
success of endozoochorous dispersal. Vector species that are
acclimated to a diet containing bivalves are less likely to
facilitate transport than individuals or species which are not.
For example,Mack and Andraso (2015)documented no
survival of dreissenids after gut passage through the round
goby (Neogobius melanostomus). Previously, however,
Andrasoet al.(2011)had noted that matureN. melanostomus
in molluscivorousfish to prey on dreissenid mussels. Age,
genetic and environmental factors are suggested to influence
pharyngeal remodelling. Moreover, Index of Relative Impor-
tance analysis ofN. melanostomusgut contents indicate a
diet selective of veliger and juvenile dreissenid
mussels (Thompson and Simon, 2014). Incontrast,I.furcatus
appears to be preferentially more piscivorous, although it is
often described as an omnivorous opportunistic feeder
paribus, the digestion of bivalves byI. furcatusmay be less

cient than digestion by adultN. melanostomus.
(Piersmaet al.,1993;Hamilton and Davison Ankney, 1994).
Thompson and Sparks(1977)observedthatlesserscaupducks
(Aythya affinis) digestedC.flumineacompletely. However,A.

nisis a preferential rather than opportunistic consumer of
macroinvertebrates (Gurneyet al., 2017). Within phylogenetic
to acclimation of the gastrointestinal tract to the presence of
bivalves within their diet, some waterbirds may facilitate
snailspeciesfromfaecalsamplesobtainedfromsmallermallardducks compared to larger individuals. This was surmised to

ect shorter retention times by smaller ducks, given that gut
length and gizzard size are generally correlated to body mass.
Accordingly, snails likely experienced less exposure to both
high internal body temperatures of waterbirds (42°C), and
possibly hypoxia, can induce high mortality ofC.fluminea,
which generally does not tolerate water temperatures above
38°C(McMahon, 1979;Lucyet al., 2012). Similarly, the
upper thermal limit ofD. bugensisis likely between 25 and
36°C(Spidleet al., 1995). However, warm water (>15°C)
acclimatedD. polymorphacan survive water temperatures up
to40°C forbetween 20and75minutes, dependingon therate
of temperature increase (McMahon and Ussery, 1995;Spidle
et al., 1995;Beyeret al., 2011) and therefore, may survive
rapid passage through the avian gut if exposed to minimal
abrasive damage. Accordingly, bothflsh and waterbird
consumer species which are not acclimated to the presence
of bivalves within their diet may potentially facilitate a
dispersal event.

3.2 Ectozoochorous dispersal
Several publications cited anecdotal accounts detailing
ectozoochorous dispersal of various bivalve species (seeRees
(1965)for a collection of these accounts), no anecdotes
bugensisorC.flumineawere found. However,Johnson and
Carlton (1996)observed that walking mallard ducks (Anas
platyrhynchos) could transport larvae and juvenileD.
polymorphaa distance of 2.5m between ponds, albeit at a

Table 1.Studies addressing zoochorus dispersal of zebra musselDreissena polymorpha, quagga mussel,Dreissena bugensisand Asian clam
Corbiculafluminea. The bivalve species examined, method of investigation used, and a summary offlndings are identifled.
Reference Species Method Summary offlndings

Thompson and Sparks (1977)CorbiculaflumineaFaecal sample
collectionLiveC.flumineafeed to lesser scaup ducks
(Aythya affinis) did not survive gut passage.
Johnson and Carlton (1996)Dreissena polymorphaFaecal sample
collectionFaecal samples recovered from mallard ducks
(Anas platyrhynchos), which consumed juvenile
mussels or concentrated suspensions of veligers,
did not contain any viable specimens.

Gatlinet al.(2013)Corbiculafluminea

Dreissena polymorphaFaecal sample
collectionTwelve percent ofD. polymorphaand 39 % of

C.flumineaconsumed in cool water (
survived gut passage through migratory blue
catflsh (Ictalurus furcatus).
Mack and Andraso (2015)Dreissena bugensis

Dreissena polymorphaFaecal sample
collectionNo dreissenids survived passage through the
gut of round goby (Neogobius melanostomus).

Johnson and Carlton (1996)Dreissena polymorphaExperimental
attachmentVeligers and juvenileD. polymorphatransported
(2.5m) between ponds by walking mallard ducks,

Banhaet al.(2016)Dreissena polymorphaExperimental
attachmentLarvae ofD. polymorphacan adhere and remain
attached to a mallard duck carcass during

simulated swims (0.5ms

) andights (75kmh
Page 4 of8N.E. Coughlanet al.: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 42
recorded the adherence and continued attachment ofD.



be transported 145km by ducks in a long-distance dispersal
(LDD) event, with a 50% chance of survival.
The adherence (or biofouling) ofD. polymorphato other
freshwater inhabitants such as Gastropoda, crayfish species,
and dragonfly (Insecta: Odonata) nymphs has been well
documented (e.g.Fincke and Tylczak, 2011). In particular,D.
polymorpha, which is capable of secondary settlement and
active reattachment, has been observed to attach, detach and
subsequently reattach to Odonata nymphs and crayfish hosts

et al., 2007;Hughes and Fincke, 2012). Interestingly, both
Odonata nymphs and freshwater crayfish species are capable
of short overland translocation between waterbodies. More-
over, these host species can shed their entire‘mussel load’
upon cuticle moult, which is likely to deposit any adhering
bivalves within the freshwater system (fiuri

?set al., 2007;
Hughes and Fincke, 2012). Surprisingly, our review of the
invertebrates has not been examined in the context of
zoochorous dispersal.
Equally, no experimental studies concerning the role of
birdsor indeed, large semi-aquatic and/or mud wallowing
vertebrate species (e.g.otters, boars, muskrats etc.)as
possible vectors of ectozoochorous dispersal forD. bugensis
orC.flumineawere obtained from the literature. Both
Johnson and Carlton (1996)andBanhaet al.(2016)have
shown that waterbirds, such as ducks, can facilitate short-
distance dispersal (SDD) ofD. polymorphaveligers.
(Fig. 1)(Coughlanet al., 2017a,2017b). Additionally, while
Johnson and Carlton (1996)suggest that the rate of

attachment ofD. polymorpha

to waterbirds is low, only
scant experimental detail is provided. Studies such asÁguas
et al.(2014),Anastácioet al.(2014),andBanhaet al.(2016)
have highlighted the importance of aquatic invertebrate
of aquatic invertebrate contact and attachment with water-
birds. Accordingly, the density of waterbirds will also
and subsequent bird-mediated ectozoochorous dispersal
(Coughlanet al., 2017a). While ectozoochorous dispersal
ofD. bugensisandC.flumineahas not been examined, these
species are likely to adhere to waterbirds in a similar fashion
toD. polymorpha. In particular, the production of ctenidial
mucillagineous (byssal) threads by juvenileC.flumineaare
thought to aidfloatation, zoochory and anthropogenic
dispersal (McMahon, 1982).
translocation process. This will likely become particularly
arduous should a vector leave the aquatic medium.Ricciardi
et al.(1995)indicated that adultD. polymorphacan survive
(77.5% of specimens) 24hrs aerial exposure at 30°C and 50%
under colder conditions (20°C and50%RH). In contrast, only
colderconditions(20°Cand50%RH).Inaddition,Byrneetal.(1988)observed a 50% mortality rate in adultC.fluminea
aerially exposed to 25°C and 53% RH for 73hrs. However,
specimens exposed to warmer conditions (35°C and 53%RH)
found to vary with the external anatomical surfaces (e.g.,
highest temperature and lowest RH combination found within
mallard plumage, entangled adultD. polymorphaand
flumineamay survive for up to 24hrs, if not longer. Bivalves
adhering to the feet of waterbirds are likely to be exposed to
cooler temperatures, particularly in more temperate regions.
local conditions.

3.3 Post dispersal
suitable freshwater habitats. Equally, detachment of an
when attachment fails. Waterbirds frequently move between
freshwater sites, and therefore, it is likely that detachment can
occur at a suitable location. In particular, bivalves adhering to
birdsviathe‘grip’of their closed gape, may release when
brought into contact with freshwater by a vectorbird. For
example,Banhaet al.(2014)observed that non-native snails
road vehicle) forcirca100km, and subsequent detachment
was promoted by contact with freshwater. Moreover, many
waterbird species will often preen and wash themselves with
freshwater, which may facilitate detachment of plumage
enmeshed bivalves in a suitable environment.

4 Conclusion and recommendations
Our systematic search of the literature revealed onlyflve
studies that speciflcally attempted to examine zoochorous
dispersal of invasiveD. polymorpha,D. bugensis,orC.
fluminea. Overall, when taken together, these publications
suggest that zoochorous dispersal of invasive freshwater
species consistently move between invaded and non-invaded
if not rare, occurrence (Coughlanet al., 2017a). Correspond-
ingly, the recorded rate of natural up-stream dispersal and
overland translocation of these invasive bivalves to adjacent
(and hydrologically unconnected) waterbodies is slow (Voelz
with postulations found within the literature, anthropogenic
vectors likely present a higher potential for invasive bivalve
dispersal (e.g.,Voelzet al., 1998;Kappes and Haase, 2012;
Page 5 of8N.E. Coughlanet al.: Knowl. Manag. Aquat. Ecosyst. 2017, 418, 42
Moreover, in agreement withSolarzet al.(2017), given the
the challenging question of zoochorous dispersal cannot be a
priority management issue. However, there remain substantial
knowledge gaps concerning zoochorous dispersal of freshwa-
ter IAS, and in order to comply with good preventative
biosecurity practices, potential vectors will need to be
examined in more detail. Here, we identify key areas for
further study, realistic opportunities for data collection, and
management protocols for mitigation of IAS spread.
The ability offreshwaterflshto disperse invasive bivalves
merits further investigation. In particular, knowledge of gut
retention times for a catalogue of potential vector species is
needed (Gatlinet al., 2013). Gut retention and survival of
endozoochory can be analysed throughex situfeeding trials,
or faecal samples. Such knowledge can be used to mitigate
against further bivalve spread, by developing minimum
quarantine times forflsh caught and relocated for restocking
purposes. Equally, other potential zoochorous vectors also
need to be considered. For example, large semi-aquatic
mammals have been shown to externally transport various
aquatic invertebrates (Waterkeynet al., 2010). Moreover,
possible dispersal of bivalves by other freshwater inhabitants
such as crayflsh, freshwater turtles, and Odonatanymphs
should be examined in greater detail. While management of
natural dispersal by vector organisms is problematic in the
at risk of invasion, should be examined for the external
adherence of‘hitch-hikers’. This is of particular importance if
the animal is to be relocated and released into an uninvaded
situdata collection needs to be promoted. Avariety of nature
enthusiasts, photographers, ecologists, conservationists, game
hunters, wildlife andflsheries offlcers, bird ringers andfleld
ornithologists come in contact with, deliberately observe, and
often handle a variety of wildlife. It is not unlikely that
instances of zoochory have been observed but remain
undocumented. Notable examples includeGreen and Figuer-
ola (2005)andTøttrupet al.(2010), who documented the
adherence of live cockleCerastoderma eduleto shorebirds
(n=4),andtheattachment ofnon-nativebarnacles (upto>30
individual adult specimens) to migratory lesser black-backed
gullsLarus fuscus(n=7), respectively. Moreover, inseveral
of invertebrates to waterbirds (e.g.,Reynolds and Cumming,
2015). Therefore, in order to accurately determine the
frequency of bird-mediated ectozoochory, bird ringers and
game hunters should be incentivised to work with research
groups to provide greater access to samples. Citizen science
initiatives to increase the collection and cataloguing of such
observations across all potential vector taxa should be
encouraged by IAS managers and research groups. Equally,
as part of citizen science initiatives, anglers or game hunters

birds and report any intact adult bivalves found.
While this review has focused on zoochorous dispersal of
invasive freshwater bivalves, a growing body of research
of IAS, including gastropoda, amphipoda and freshwaterarthropoda (e.g., juvenile crayflsh) (Swanson, 1984;Reynolds
et al., 2015;Green, 2016). Notably, New Zealand mud snails
(Potamopyrgusantipodarum), an emerging freshwater invader
in the USA, has been shown to survive gut passage through
severalflsh species (seeBruceet al.,2009). Accordingly, the
mitigate against local invader spread.
Acknowledgments.N.E. Coughlan and J.T.A. Dick are
supported by the Irish EPA Research grant 2015-NC-MS-4:
Prevention, control and eradication of invasive alien species.
We thank anonymous reviewers for helpful comments.

Author contributions
NEC conceived and designed the review; NEC and ALS
conducted the review and analysis; all authors contributed to
the writing of the manuscript, which was led by NEC.

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Cite this article as: Coughlan NE, Stevens AL, Kelly TC, Dick JTA, Jansen MAK. 2017. Zoochorous dispersal offreshwater bivalves: anoverlooked vector in biological invasions?Knowl. Manag. Aquat. Ecosyst., 418, 42.

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