1789

Ecological Applications, 11(6), 2001, pp. 1789–1799 q 2001 by the Ecological Society of America

OVERLAND DISPERSAL OF AQUATIC INVASIVE SPECIES: A RISK

ASSESSMENT OF TRANSIENT RECREATIONAL BOATING

LADD E. JOHNSON,

1,3 ANTHONY RICCIARDI,2 AND JAMES T. CARLTON1

1

Maritime Studies Program, Williams College–Mystic Seaport, Mystic, Connecticut 06355 USA 2Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1

Abstract. Predictions of the geographic spread of introduced species are often limited

by a lack of data on their mechanisms of dispersal. We interviewed boaters and inspected

boating equipment at public boat launches on Lake St. Clair (Michigan, USA) to assess

the potential for the zebra mussel, an invasive bivalve, to be dispersed overland to inland

waters by transient recreational boating activities. Several mechanisms associated with

recreational boating were found to be capable of transporting either larval or adult life

stages. Larvae were found in all forms of water carried by boats (i.e., in live wells, bilges,

bait buckets, and engines) but were estimated to be 40–1003 more abundant in live wells

than other locations. Dilution in receiving waters should, however, greatly reduce the risk

of establishing new populations by the introduction of larvae. Contrary to common belief,

mussel dispersal from these boat launches did not occur by direct attachment to transient

boats. Rather, adult and juvenile mussels were transported primarily on macrophytes entangled on boat trailers and, less frequently, on anchors (5.3% and 0.9% of departing boats,

respectively). Combining these data with estimates of survival in air and reported boater

destinations, we predict that a maximum of 0.12% of the trailered boats departing these

access sites delivered live adult mussels to inland waters solely by transport on entangled

macrophytes. While this is a small probability, high levels of vector activity resulted in a

prediction of a total of 170 dispersal events to inland waters within the summer season

from the primary boat launch studied. Many other potential vectors remain to be assessed,

but the dispersal of zebra mussels by trailered boats, particularly by ‘‘piggybacking’’ on

macrophytes entangled on the trailers, must be controlled in order to limit further range

expansion of the zebra mussel within North America.

Key words: aquatic weeds; biological invasions; Dreissena polymorpha; exotic species; fouling;

geographic spread; nonindigenous; zebra mussel.

INTRODUCTION

After the intercontinental transport and introduction

of a species by some human-mediated vector, further

regional spread can occur through the action of additional mechanisms including both natural and humanmediated vectors. Ultimately, it is this secondary spread

that will determine the scale of any ecological and economic impact of a biological invasion (Lodge et al.

1998). While it would be best to prevent initial introductions in the first place (e.g., through agricultural inspections or ballast water management), it is still critical

to prevent further spread after initial establishment. Even

efforts that only slow spread can provide the time needed

to assess potential impacts and, if necessary, develop

additional control strategies. Thus knowledge of the

mechanisms of secondary dispersal of an introduced species can provide a basis for predicting its further spread

(e.g., Ludwig and Leitch 1996, Schneider et al. 1998),

Manuscript received 16 July 1999; revised 12 October 2000;

accepted 19 October 2000; final version received 1 December

2000. 3 Present address: De ́partement de biologie and GIROQ,

Universite ́ Laval, Que ́bec, QC, Canada G1K 7P4.

E-mail: ladd.johnson@bio.ulaval.ca

and for effectively allocating resources towards preventing or slowing the spread.

Freshwater habitats offer a particularly tractable system for investigating the spread of exotic species, in

that the habitats (e.g., lakes, streams) have well-defined

borders and connections (Johnson and Padilla 1996).

Dispersal between hydrographically isolated waters requires specific adaptations for overland transport and

survival in inhospitable terrestrial environments or further assistance from human vectors. This phenomenon

is well illustrated by the invasion of North America by

the Eurasian zebra mussel (Dreissena polymorpha), a

freshwater bivalve with many of the attributes of marine mussels (e.g., attachment by byssal threads to hard

surfaces, a planktotrophic larval stage that spends 2–

5 wk feeding in the water column before settling to the

bottom). Since its introduction to North America in the

mid-1980s, the zebra mussel has spread rapidly across

a large portion of the continent (O’Neill and Dextrase

1994, Johnson and Carlton 1996). Most of this spread

has been confined to interconnected waterways, aided

by the natural downstream transport of planktonic larvae (Horvath et al. 1996); upstream spread has also

occurred, most likely through the movement of adult

stages fixed to the bottoms of ships or barges (Keevin
1790 LADD E. JOHNSON ET AL. Ecological Applications

Vol. 11, No. 6

et al. 1992). However, saltatory dispersal to isolated

inland waters has resulted in the establishment of zebra

mussel populations in a number of inland lakes in the

regions surrounding the Great Lakes (Kraft and Johnson 2000). An understanding of the dispersal mechanisms available to this nuisance species is essential for

predicting the rate and direction of its spread, as well

as for implementing effective control strategies.

While overland dispersal of the zebra mussel can

result from the actions of a wide variety of potential

natural and human-mediated mechanisms (Carlton

1993), transient recreational boating is commonly perceived as the primary means by which the species is

transported between unconnected bodies of water. This

perception exists not only among researchers (e.g.,

Griffiths et al. 1991, Neary and Leach 1992, Carlton

1993, Schneider et al. 1998, Buchan and Padilla 1999),

but also policy makers (OMNR 1991, Tyrus et al.

1994), outreach agencies (e.g., Kelch 1992) and the

general public. As a result, costly boater education and

boat cleaning programs have been implemented to prevent infestations and slow the spread. Transient boating

activity has been invoked to explain distribution patterns of zooplankton (e.g., Yan et al. 1992, Havel et

al. 1995), and the initial zebra mussel invasions of

inland waterbodies in Wisconsin occurred almost entirely in those waterbodies used by boaters who also

used waters with established populations of zebra mussels (Padilla et al. 1996). Recreational boating activity

has previously been demonstrated as a vector for the

unintentional overland transport of exotic aquatic macrophytes (Scales and Bryan 1979, Dove and Malcolm

1980, Dove and Wallis 1981, Dove and Taylor 1982,

Johnstone et al. 1985, Joyce 1992), but only recently

has its role in the transport of aquatic animals begun

to be assessed (Johnson and Carlton 1996, Havel and

Stelzleni-Schwent 2001). Thus, although intuitively

appealing, the putative ability of recreational boats to

disperse zebra mussels remains largely unexamined,

and the mechanistic basis of any transport is known

only from anecdotal observations (e.g., Griffiths et al.

1991, Janik 2001; but see Johnson and Carlton 1996).

The impressive biofouling ability of the zebra mussel

has led to visions of boats departing infested waters

with hulls encrusted with zebra mussels—certainly a

worst-case scenario. However, in reality, there is a suite

of mechanisms by which recreational boats might transport zebra mussels, including other mechanisms involving the transport of adults (e.g., on anchors or on

entangled macrophytes) or larvae (i.e., in locations

where water might accumulate such as live wells, bilges, bait buckets, and engine cooling systems).

The objectives of this study were to (1) determine

the extent to which zebra mussels are transported by

transient recreational boating; (2) identify precisely the

mechanisms involved and evaluate their relative probability of transporting zebra mussels between unconnected bodies of water; and (3) illustrate a simple modeling approach for use in the risk assessment of these

various mechanisms.

METHODS

To identify and estimate the relative importance of

the mechanisms by which zebra mussels could be transported from infested waters, boaters were interviewed

and boats and trailers were inspected and sampled at

three public boat launches on the northwestern shore

of Lake St. Clair (Michigan, USA), the body of water

where zebra mussels were first reported in North America (Hebert et al. 1989). The two principal sites were

the boat launches at the Ensign Public Access Site and

the Metrobeach Public Access Site, with more limited

sampling at the Selfridge Public Access Site. A total

of 920 interviews were conducted on 24 different dates

from 20 June to 4 September 1992: 617 at the Ensign

launch on 21 dates, 280 at the Metrobeach launch on

11 dates, and 23 interviews at the Selfridge launch on

one date. Of all the interviews, 99% were conducted

during weekend periods (Friday noon until Sunday

evening) and holidays and were usually conducted as

boaters departed the access site (77%), a moment when

they were more receptive to being interviewed. On any

given date, interviews were usually conducted for a

block of 5–7 h between 0900 and 2100 (local time), as

initial observations indicated that boaters rarely departed before then. All departing boaters were solicited

for interviews until the rate of departures exceeded the

capacity of the interviewer, at which time the most

recently retrieved boat was selected for the next interview. If no boaters were departing, then interviews

were solicited from arriving boaters. Boaters rarely refused to be interviewed (,3%), and most refusals were

from boaters interviewed before. The interviews, which

were part of a larger study aimed at documenting the

habits and demography of boaters using waters infested

by the zebra mussel, consisted of 25–30 questions and

lasted an average of 5–10 min. Questions relevant to

this study pertained to the duration of the outing, activities and devices associated with fishing, the use of

anchors, and the anticipated time and location of the

boat’s next use (Table 1). The interview was modified

over time as additional mechanisms of transport became apparent. These modifications and incomplete interviews produced sample sizes , 920 for certain types

of information. During the summer, interviews were

conducted by three people who rotated among these

and other launches.

A visual inspection lasting 30–60 s was made of the

boat exterior for any zebra mussels attached to the hull

or motor, with particular attention paid to irregularities

where zebra mussels were first likely to accumulate.

During the course of the study, it became apparent that

a previously unrecognized mechanism for the overland

transport of zebra mussels existed: the transport of

mussels attached to aquatic macrophytes entangled on

boats or on boat trailers. Aquatic macrophytes often
December 2001 DISPERSAL OF ZEBRA MUSSELS BY BOATS 1791

TABLE 1. Survey questions asked of boaters departing public boat launches on Lake St. Clair

(Michigan, USA).

1) How long were you out on the lake today? (number of hours, days or weeks)

2) Were you fishing today? (yes/no)

3) Were you equipped with a live well or similar device? (yes/no)

If ‘‘yes,’’ then

a) Did you use this device today? (yes/no)

b) What was the fate of any water in it?

(dumped in lake/dumped at ramp/taken from ramp/unknown)

4) What kind of bait did you use today? (minnows, worms, artificial, other)

If minnows,

a) Did you use a bait bucket today? (yes/no)

b) What was the fate of any water it contained?

(dumped in lake/dumped at ramp/taken from ramp/unknown)

5) Did you use your anchor today? (yes/no)

6) Where is your next planned use of this boat? (return here/other Great Lake launch/inland

lake/unknown)

7) When do you plan to use this boat next? (Number of days or weeks/unknown)

Notes: For arriving boats, Questions 1–5 were framed in the present or future tense. Type

of data or possible responses recorded are in parentheses.

FIG. 1. An extreme example of the entanglement of aquatic macrophytes on recreational

boats and trailers. The photograph was taken at

the boat launch area of the Ensign Public Access

Site, Lake St. Clair, Michigan, USA, in the summer of 1993.

fragment or become uprooted and then accumulate

along the shoreline, where they can become entangled

on boat trailers and equipment (Fig. 1; Johnstone et al.

1985). Zebra mussels can colonize macrophytes (Lewandowski 1982) and then be indirectly transported by

boats when the macrophytes become entangled, i.e.,

‘‘piggyback’’ dispersal. Thus, beginning in mid-July,

we also examined departing boats and trailers for the

presence of entangled aquatic macrophytes. Time and

safety constraints permitted only the observation of

entangled macrophytes on departing boats and not their

examination for any attached zebra mussels. Therefore,

to estimate the occurrence of macrophyte-associated

zebra mussels (MAZM), we also examined empty boat

trailers parked at these sites for the frequency of

MAZM on entangled macrophytes. In addition, the percentage of parked trailers with entangled macrophytes

was used as an independent estimate of the frequency

of macrophyte entanglement. However, the inspection

of parked trailers could underestimate this parameter,

as macrophytes can also become entangled on the boat

or motor or be caught between the trailer runners and

the boat hull as the boat is placed on the trailer (Fig.

1). Boat trailers were inspected on 2–5 weekend dates

(depending on the site) in August and early September,

usually at midday, but occasionally at multiple times

during the day. In the latter case, trailers were marked

to avoid repeated sampling. The number of trailers sampled at any given launch on any given date ranged from

30 to 305. The quantity of macrophytes entangled was

scored categorically as ‘‘None’’ (no plants visible),

‘‘Few’’ (1–5 separate plant strands), ‘‘Many’’ (.5 separate strands), or ‘‘Clumps’’ (1 or more masses of entangled fragments; Fig. 1 represents an extreme example of ‘‘clumps’’). Each strand or clump of macrophytes was removed from the trailer and macroscopically examined for attached zebra mussels (limit of

detection near 2 mm in shell length), which were then

counted and measured to the nearest 0.1 mm.

On six dates in August, water was sampled from

areas where it might accumulate or be stored on a boat.

Typically 5 to 15 samples were collected on any given

day from boats chosen haphazardly. These included

samples from live wells (containers designed to keep
1792 LADD E. JOHNSON ET AL. Ecological Applications

Vol. 11, No. 6

bait or captured fish alive, usually a built-in feature of

the boat that pumps water directly from the lake, but

sometimes simply an ice chest; n 5 54), bait buckets

(n 5 9), bilge water (water that inadvertently accumulates between the hull and the floorboards; n 5 22),

and engine cooling water (n 5 2). Sample volumes

were 200–2000 mL, depending on the volume and time

available for processing. Samples were concentrated

using a 63-mm mesh (which retains the shelled larval

stage of the zebra mussel; Marsden 1992) and stored

on ice until returned to the laboratory where they were

refrigerated pending examination. Samples were

screened for the presence of larvae within 4 d using

cross-polarized light microscopy (Johnson 1995). For

a haphazardly selected subset of these samples, concentrations of larvae in the samples were also determined at the same time. To calculate the number of

larvae transported by an individual boat (i.e., per

event), these concentrations were multiplied by the volumes typical for these areas, which were estimated

from observations or information from the manufacturers of boating and fishing equipment. Samples were

also taken from the docks at the launches to document

the presence of larvae in the lake. Using an 18-L bucket, 90–180 L of water were collected from the surface

and filtered through a 63-mm mesh plankton net.

We also attempted to collect samples from the hulls

of boats to look for mussel larvae that might have recently settled there. We used a rubber scraper (a squeegee, normally used for removing water from windows)

but found that the hull usually dried too quickly, making it impossible to collect water in this manner. We

therefore discontinued these efforts and assumed that,

because zebra mussels have no dormant or resting

phase, larvae transported on the external surfaces of

boats, motors, and trailers could not survive aerial exposure during transit. The possibility remained that active settlement could have occurred in irregularities

(e.g., seams, rivets), but the lack of a biofilm, which

is used as a settlement cue for larvae (Wainman et al.

1996), would reduce this possibility.

To assess the risk of transporting zebra mussels

associated with each mechanism, we estimated the

probability that any randomly selected boat would

transport zebra mussels away from the site (Ptransport).

This probability was calculated from the probability

of a boat’s ‘‘exposure’’ to a potential mechanism

(Pexposure) multiplied by the conditional probability

that zebra mussels were indeed being transported if

exposed (Ptransportzexposure). Estimates of Pexposure were

calculated from interview data for anchors, live

wells, bait buckets, and from inspections during the

interview for entangled macrophytes. For example,

if 40 of 100 boaters indicated that they had used their

anchors during the voyage, Pexposure would be 0.40.

An independent estimate of Pexposure to macrophyte

entanglement was also calculated as the proportion

of trailers with entangled macrophytes in parking

areas. Pexposure for the exterior boat surfaces and engine cooling water systems was assumed to be 1

(5100%), because the use of any motorized boat in

infested waters would, by definition, expose the hull

to larvae in the water column and bring water with

larvae into the cooling system. Bilges were difficult

to inspect, and thus for gross comparative purposes

we estimated the exposure at 80%, based on the observation that during almost any excursion some lake

water either leaks in or is unintentionally brought

aboard (e.g., while swimming, water-skiing, or fishing).

For both live wells and bait buckets, Pexposure does

not simply depend on the presence of the device, but

also on its use and the fate of any water it contained.

Thus, Pexposure for these mechanisms was calculated

from the proportion of boats equipped with the device (Pequipped), multiplied by the proportion of fishers

who indicated that they had used the device during

their outing (Pusedzequipped) and intended to transport the

water contained in the device away from the boat

launch (Pexposurezused). In other words, if a boat’s live

well or bait bucket was not used or was emptied

before leaving, the boat was not considered ‘‘exposed’’ with regard to this mechanism of transport.

For example: if 200 of 300 boaters indicated that

there was a live well on their boat, but only 60%

indicated that they had used the device and half of

those then indicated that they had dumped the water

from their live well in the lake or at the launch, we

would estimate Pexposure 5 (200/300) 3 0.6 3 0.5 5

0.02.

Ptransportzexposure for each mechanism was estimated from

the inspections of boat hulls and anchors of departing

boats, from the inspections of parked trailers for entangled macrophytes, and from water samples of live

wells, bait buckets, engine cooling systems, and bilges.

Continuing with the above example, if zebra mussel

larvae were found in 20 of 40 live wells sampled,

Ptransportzexposure would be 0.5. Thus Ptransport, the product of

the two probabilities, would be 0.02 3 0.5 5 0.01 (or

1 out of any 100 departing boats).

Exportation of propagules from a source population

involves only the first of a series of steps, each with

an associated probability, that are necessary for the

successful establishment of a new population. For the

dispersal of zebra mussels on macrophytes, we were

able to extend our simple probabilistic modeling approach to the two subsequent steps of the dispersal

process: (1) the movement patterns of the vector (e.g.,

from infested to uninfested waters), and (2) the survival

of propagules during transit. By combining the probability of transport (Ptransport) calculated above with the

probability of vector movement between source and

target waterbodies (Pmove) and survival of the life stage

during transit to target waterbodies (Psurvivalzmove), we estimated the maximum probability that a boat departing
December 2001 DISPERSAL OF ZEBRA MUSSELS BY BOATS 1793

TABLE 2. Probabilities of different steps in the dispersal of zebra mussels by various potential mechanisms of transport

associated with transient recreational boating and fishing activities at public boat launches on Lake St. Clair (Michigan,

USA).

Mechanism Life stage Pexposure (n)† Ptransportzexposure (n)† Ptransport

1) Boat exterior (hull/motor)

2) Anchors

3) Entangled macrophytes

4) Engine cooling system

5) Bilge

6) Live wells (fishing only)

7) Bait buckets (fishing only)

ad/juv

ad/juv

ad/juv

larvae

larvae

larvae

larvae

1.0a (···)

0.44c (149)

0.33b (535)

1.0a (···)

0.8f (···)

0.086c (835)

0.024c (869)

0.0b (822)

0.02b (49)

0.16d (383)

1.0e (2)

0.64e (22)

0.83e (54)

0.44e (9)

0.0

0.009

0.053

1.0

0.51

0.071

0.011

Notes: ‘‘Life stage’’ indicates whether adults or juvenile (ad/juv) or larvae were transported. Pexposure is the probability of a

boat’s ‘‘exposure’’ to a particular mechanism, Ptransportzexposure is the conditional probability that zebra mussels are transported if

the boat is exposed, and Ptransport, the product of the two preceding probabilities, is the probability that any randomly selected

departing boat would transport zebra mussels away from the site. Ptransportzexposure values for live wells and bait buckets are derived

from Table 5 and include only cases in which water was taken from the boat launch. Numbers in parentheses are sample sizes.

†Sources of estimates: a

By definition; bInspection of departing boats; cInterviews with boaters; dInspection of parked boat

trailers; e

Water samples; fEducated guess (see Methods for additional discussion).

TABLE 3. Duration in water of boats launched from public

access sites on Lake St. Clair in summer 1992 (n 5 799).

Duration Frequency (%)

1–12 h (day trip)

13–36 h (overnight)

2–7 d

1–4 wk

1–3 mo

88

4

4

1

3

the source waterbody will deliver living zebra mussels

to source waters, Pdelivery. Specifically,

P 5 (P )(P )(P ). delivery transport move survivalzmove

Estimation of Ptransport is described above. Pmove was estimated from information obtained during the interviews, specifically the intended location for the next

use of the boat. Psurvivalzmove can be estimated here in two

ways. The simpler method is to use the laboratory estimate of #5 d of aerial exposure for maximal survival

time for mussels out of water under typical temperate

summer conditions of 208C and 50% relative humidity

(Ricciardi et al. 1995), multiplied by the proportion of

those boaters destined for inland waters who plan to

use their boat within 5 d. A second, more conservative,

method uses these same measurements of laboratory

survival to estimate the probability that at least one

mussel of a group of z mussels will survive the transit

between infested and uninfested waters. In this case,

Ps(d), the probability of survival of a single mussel for

d days out of water, can be used to calculate the probability that at least one mussel out of a group of z

mussels will survive d days:

P 5 z 1 2 (1 2 P ) s(d,z) s(d)

i.e., the probability of at least one mussel surviving is

1 minus the probability of all the mussels dying, which

is the product of the probability of each individual

dying. To then determine the conditional probability

that any departing boat that is transporting zebra mussels will deliver at least one living mussel to uninfested

waters,

P 5 O (P )(P )(P ) survivalzmove d z s(d,z)

where Pd 5 probability that a boat visiting inland waters will do so in d days, and Pz 5 probability that a

boat will transport z mussels.

This approach assumes that (1) Pd and Pz are independent, which is reasonable, and (2) that the survivorship of individual mussels is independent of z (number of mussels transported), which is reasonable for

small numbers of mussels.

To convert these probabilities to estimates of the

absolute numbers of dispersal events, data on the absolute numbers of boaters using these boat launches

were obtained from the Michigan Department of Natural Resources (unpublished data) for the period 1988–

1991. This extension of the probability model was only

applied to transportation of zebra mussels on entangled

macrophytes as the survival data on open-air desiccation is most applicable to this situation.

RESULTS

Zebra mussels were transported by all potential

mechanisms except for the direct attachment to the hull

(Table 2). The median time that boats were in the water

was 6 h, and most boats (96%) encountered at these

sites were in the water 1 wk or less (Table 3) and thus

were not in the water long enough to be fouled. However, as discussed below, if a boat is left for a sufficient

time (i.e., weeks) in the water, the direct attachment of

zebra mussels could occur. Instead, the export of adults

occurred most frequently on entangled macrophytes.

Both the probability of exposure (i.e., how often macrophytes were entangled on boat trailers 5 Pexposure) and

the proportion of macrophytes that harbored zebra mussels (Ptransportzexposure) were extremely variable among

dates and sites (Fig. 2). Overall 33% of the departing

boats had entangled macrophytes (i.e., Pexposure 5 0.33;

Table 2), which is consistent with the observation of
1794 LADD E. JOHNSON ET AL. Ecological Applications

Vol. 11, No. 6

FIG. 2. Occurrence of entangled macrophytes and macrophyte-associated zebra mussels (MAZM) on boat trailers

parked at three public access sites (Lake St. Clair, Michigan,

USA) sampled in summer 1992. The hatched portion of each

bar represents the percentage of trailers with only entangled

macrophytes, whereas the solid portion of each bar represents

percentage of trailers with entangled macrophytes and

MAZM. Sample sizes (number of trailers) for each date are

indicated above each bar; n.d. 5 no data.

TABLE 4. Occurrence and abundance of macrophytes on

trailers and zebra mussels on macrophytes (macrophyteassociated zebra mussels 5 MAZM) in parking areas of

boat launches (n 5 1053 trailers).

Macrophyte

abundance

Trailers

with

macrophytes (%)

Macrophytes

with

MAZM

(%)

MAZM/trailer

(mean 6 1 SD) (n)

Absent

Present

64

36

···

16

···

2.3 6 1.8 (55)

Few

Many

Clumps

24

10

2

8

31

39

2.1 6 1.8 (21)

2.4 6 2.0 (27)

2.1 6 1.1 (7)

Note: See Methods for definitions of abundance.

TABLE 5. Use of live wells and bait buckets and the fate of

any water they might contain by recreational boaters using

public boat launches on Lake St. Clair in summer 1992.

Device Pequipped (n)

Pused/equipped

(n)

Pexposure/used

(n) Pexposure

Live wells

Bait buckets

0.39 (835)

0.11 (869)

0.65 (242)

1.00 (68)

0.38 (138)

0.22 (68)

0.086

0.024

Notes: Pequipped is the probability of a boat being equipped

with the device; Pusedzequipped is the conditional probability of a

boat equipped using the device during that day’s outing; Pexposurezused is the conditional probability that any device used is

carrying water as it departs the launch site (as opposed to

being dumped in the lake or at the launch). Pexposure is then

the product of the preceding probabilities; n 5 sample size.

36% of trailers in the parking areas having entangled

macrophytes (Table 4). Macrophyte-associated zebra

mussels (MAZM) were found on 16% of these trailers

(i.e., Ptransportzexposure 5 0.16), which leads to an estimate

that 5.3% of boats leaving these boat launches had

MAZM on their trailers (i.e., Ptransport 5 0.053). MAZM

were found disproportionately more often on trailers

with greater amounts of entangled macrophytes (Table

4; P , 0.001; G 5 20.5, n 5 61; G test). There was

a mean of 2.3 mussels per trailer (range 1–8; n 5 55);

the number did not vary with the quantity of macrophytes entangled on the trailer (Table 4). The average

zebra mussel length was 4 mm and 13 mm for the two

cohorts apparent from the size frequency (data not

shown).

Anchors were used frequently by boaters (Pexposure 5

0.44), but mussels were found on anchors only once

out of 49 inspections. Neither the abundance nor size

of mussels on the anchor was recorded.

Larvae were found in all areas where water accumulated on the boats (Table 2). Pexposure in these areas

ranged from 0.024 to 1.0 and was particularly low for

mechanisms associated with fishing (i.e., live wells and

bait buckets) due to (1) low frequencies of boats

equipped with these devices (Pequipped), and (2) the low

probability of taking water away from the site even

when the device was used (Pexposurezused; Table 5). Thus,

Ptransport was much lower for activities associated with

fishing than for more general mechanisms transporting

larvae. The highest estimates of Ptransport were found for

engine cooling water and bilge water due to high values

for both Pexposure and Ptransportzexposure for these mechanisms

(Table 2). Although these parameters are based on either low sample sizes (Ptransportzexposure of engine cooling

water) or qualitative observations (Pexposure of bilge water), precision is not important in these cases (i.e., both

would remain the most likely methods of transport even

if estimates of both parameters were reduced by 50%).

However, as discussed below, the number and survival

of larvae transported by these means will influence the

importance of these mechanisms.

The concentration of larvae in these areas ranged

from 5.9 to 19 larvae/L, but was highly variable (Table
December 2001 DISPERSAL OF ZEBRA MUSSELS BY BOATS 1795

TABLE 6. Estimates of the numbers of larvae transported in water accumulated in various

locations on recreational boats using public boat launches on Lake St. Clair (Michigan, USA)

in August 1992.

Location (n)

Volume†

(L)

Concentration

(larvae/L)‡

Larvae

transported

per event

Likelihood of

survival§

Engine cooling system (2)

Bilge (13)

Live well (38)

Bait bucket (3)

1

2

65

4

16 6 1

5.9 6 13

19 6 34\

7.8 6 8.4

16

12

1230

31

high

low

moderate

moderate

Notes: Larvae transported per event is the product of the estimated volume and the measured

concentration of larvae; n is the sample size of water samples used for determining concentrations.

† The engine cooling system volume was estimated by determining the mean of the manufacturers’ specifications for a 35-horsepower outboard, a 100-horsepower outboard, and a 100-

horsepower inboard/outboard (1 horsepower 5 746 W). Bilge volume ranged from 0 to 20 L

(L. E. Johnson, personal observation). The live well volume was determined by the mean of

the two most common sizes (56.8 and 75.7 L) encountered at various internet listings (n 5 10

locations). The bait bucket volume was an estimate based on bait buckets sold at fishing supply

stores and L. E. Johnson (personal observation).

‡ Mean 6 1 SD.

§ Predictions based solely on presumed water quality in each location (see Discussion).

\ Incorrectly reported as 111 (222) larvae/L in Johnson and Carlton (1996) due to calculation

error.

FIG. 3. Values of PdPzPs(d,z), the component of the conditional probability of survival if moved between infested

sites and inland lakes, for different numbers of macrophyteassociated zebra mussels (MAZM) and for different transit

times (1 and 3 d). Numbers above the pairs of bars indicate

the absolute number of times that number of MAZM was

observed. These numbers were used to calculate values for

Pz, the probability of transporting z mussels.

6), due perhaps to the use of different locations within

the lake. As larval densities usually peak earlier in the

season, these samples probably underestimated the

density of larvae for the entire season. The range of

values is consistent with measurements of larval abundance in water collected at the boat launches (mean 6

1 SD 5 25 6 22 larvae/L; n 5 4). Using the estimated

average volumes of lake water that could accumulate

in each area and the observed larval concentrations,

live wells had the potential to export 40–100 times

more larvae on a per-trip basis than did other mechanisms, due both to the large volume of this structure

and to higher concentrations of larvae (Table 6). While

the probability of transport of zebra mussel larvae in

engine cooling water is very high (probably near

100%), the small volume of the cooling system severely

limits the total number of larvae transported per event.

Based on the reported next use of boats, Pmove, the

probability of boat movement between these infested

waters and inland lakes (which at the time were not

known to be infested) was 0.089 (68 of 766). Of the

boaters destined for inland waters, 27% intended to use

their boats within 1 d or less, 25% within 2–5 d, 37%

within 5–10 d, and 12% in . 10 d. From Ricciardi et

al. 1995, Ps(d) (the survival of an individual mussel surviving d days out of water) for mussels 10–18 mm in

length is Ps(1) 5 0.73, Ps(3) 5 0.03, and Ps(5) 5 0. Thus,

for the simpler estimate, Psurvivalzmove 5 (0.27 1 0.25) 5

0.52, i.e., the proportion of boats intended to be used in

inland lakes within 5 d after their use in infested waters.

This estimate assumes that at least one mussel will survive for periods up to 5 d, an unlikely assumption given

the low numbers of MAZM per boat (Table 4) and low

survival after a 3-d exposure. For the more complex

model, Psurvivalzmove 5 0.25, which is influenced by the

much higher survival rates for the 1-d period and the

low number of mussels carried by individual boats (Fig.

3). Combining this latter, more realistic, value with the

probabilities of transport (Ptransport; Table 2) and movement (Pmove, above), we can estimate the maximum probability that an individual boat might deliver a live zebra

mussel on aquatic macrophytes to inland waters as

Pdelivery 5 (0.053) 3 (0.089) 3 (0.25) 5 0.0012. In other

words, we estimate that a maximum of 12 of every

10 000 boaters who used these Great Lakes boat launches transported live (juvenile and adult) zebra mussels on

entangled macrophytes to inland waters.

What does this mean in absolute terms of overland

dispersal? An annual average of 96 800 boaters used

the Ensign launch during the period 1988–1991 (Mich-
1796 LADD E. JOHNSON ET AL. Ecological Applications

Vol. 11, No. 6

igan Department of Natural Resources, unpublished

data). Based on the above model and data specific to

that site (i.e., 7.6% of departing trailers with MAZM

and 8.8% of departing boaters destined for inland waters; thus Pdelivery 5 (0.076) 3 (0.088) 3 (0.25) 5

0.0017), we predict that this site alone was the source

of 170 (5 0.0017 3 96 800) events having the potential

to transport a live zebra mussel into inland waters within that single season. Clearly, the data for MAZM were

variable between public boat launches (Fig. 2), and care

is needed in extrapolating results from this one site.

For example, applying the model to data from the Metrobeach launch (i.e., 0.4% of departing trailers with

MAZM and 7.8% of departing boaters destined for inland waters), gives an overall probability of an individual boat delivering live mussels to inland waters

that is less than 5% that for the Ensign launch (P 5

0.00008 vs. P 5 0.0017, respectively). Still, these public access sites represented only a fraction of the transient boating activity on Lake St. Clair, suggesting that

hundreds and perhaps thousands of dispersal events

have occurred each year within this region.

DISCUSSION

As most bodies of water connected to the Great Lakes

have been colonized by the zebra mussel, further range

expansion will largely occur through interbasin dispersal, and thus should be determined by the availability and

effectiveness of overland transport mechanisms. Overland dispersal has already occurred (Kraft and Johnson

2000), and although there are a myriad of vectors with

the potential to transport zebra mussels overland (Carlton 1993), recreational boating has generally been assumed to be the primary vector of dispersal (Padilla et

al. 1996, Schneider et al. 1998, Buchan and Padilla

1999). The results of this study clearly demonstrate the

potential for recreational boating to transport zebra mussels away from infested waters. However, the mere existence of a vector does not assess its importance relative

to other potential vectors (e.g., Johnson and Carlton

1996). Other vectors, including other classes of recreational boats (see following paragraphs), may also be

operating and should be similarly assessed.

Our results clearly demonstrate that recreational

boating must be considered as a suite of mechanisms

that can be categorized according to the stage of the

life cycle transported (i.e., larvae vs. attached stages)

or by specific human activities (e.g., fishing vs. other

recreational activities). Overall, larvae appear to be

more commonly transported than adults due to their

occurrence in the lake water that accumulates in a variety of places on boats. Although engine cooling water

may be the most likely means in which larvae are transported, live wells may present a greater overall risk

due to their larger volume and thus larger number of

larvae transported (Table 6 and below). However, boaters who took lake water away from boat launches in

the live well often indicated that they intended to empty

or clean it (typically at home) before the next use of

their boats. Thus, our calculation of the probability of

export is likely to be an overestimate of the transport

of water in live wells and bait buckets between lakes.

Contrary to expectations, adults were not found on

the boat hull itself, but instead only on aquatic macrophytes entangled on the boat trailer or on the anchor.

Given the short duration that most recreational boats

spent in the water (Table 3), this result is not surprising,

as there was insufficient time for the development of

the biofilm necessary as a settlement cue for larvae

(Wainman et al. 1996). Moreover, most boaters who

use public boat launches store their boats out of water

(e.g., in a driveway), and neither larvae nor recent

metamorphosed juveniles are adapted for living out of

water. The domain of this study, namely recreational

boats using public access sites, did not, however, include ‘‘resident boats,’’ those boats that are seasonally

moored in infested waters. Although these boats are

unlikely to be transported between unconnected bodies

of water, they have a tremendous potential for transporting large numbers of juvenile and adult mussels,

for example when their owners change residences. All

of the infested boats intercepted at California inspection stations appear to have been resident boats commercially hauled from the Midwest (Janik 2001), suggesting this type of dispersal may be especially important at larger spatial scales.

The entanglement of macrophytes occurred frequently, either on 33% or 36% of the trailers, depending on

the assessment method used. These estimates are consistent with those from New Zealand (27%; Johnstone

et al. 1985), but much higher than those found in British

Columbia, Canada (3.9%; Dove and Malcolm 1980,

Dove and Wallis 1981, Dove and Taylor 1982). This

latter study, however, only examined one species of

aquatic macrophyte, underestimating the general phenomena, and included many nontrailered boats (e.g.,

canoes) which were less likely to entangle macrophytes. As with our data, there was substantial variation

among boat launches in these studies, presumably due

to differences in macrophyte abundance and distribution, location of the launches, and species characteristics (e.g., propensity to fragment). Not surprisingly,

the probability of transporting MAZM increased with

the amount of macrophytes entangled, but it is not clear

why the number of MAZM per trailer did not follow

the same pattern (Table 4). The low numbers of MAZM

per strand may reflect low colonization levels of macrophytes or a propensity of more heavily colonized

plants to sink and thus not accumulate near launches.

Identification of the relative importance of the mechanisms in which zebra mussels are transported is critical both for modeling the geographic spread of zebra

mussels and for control strategies. Past modeling efforts (Neary and Leach 1992, Schneider et al. 1998,

Buchan and Padilla 1999) have treated all boating activity as equivalent in terms of the abilities of boats to
December 2001 DISPERSAL OF ZEBRA MUSSELS BY BOATS 1797

transport zebra mussels. Our results demonstrate that

boats can vary in this capacity depending on the exact

activity (e.g., fishing, use of anchors) and can vary

substantially in space and time (e.g., macrophyte entanglement; Fig. 2). As stressed by Schneider et al.

(1998), data on vector movement and probabilities of

transport are needed for developing models of invasion

risk. For example, given the data available at the time,

Schneider et al. assumed a probability of export of 1%,

which likely underestimates this parameter (Table 2).

Further information is also needed on the demographic

conditions needed for establishing new populations.

Knowledge of the details of transportation is also

needed for preventing or delaying the further spread of

zebra mussels. For example, early guidelines for boaters included measures aimed at sterilizing the exterior

surfaces of boats with chlorine solutions, hot water, or

long periods out of water (e.g., Kelch 1992). Given that

these procedures were both inconvenient and voluntary, compliance rates were undoubtedly quite low.

Moreover, as no mention of the removal of aquatic

plants was made, boaters were directed away from the

more likely mechanism of transport. Detailed information about dispersal mechanisms, especially their

relative frequency of occurrence, can help guide the

development of such programs.

This study primarily addressed transport from infested

waters. Survival during transit is the next key aspect.

Unfortunately, there are only limited survival data for

these mechanisms. Maximum survival of adults in air

is estimated at ø3 wk under conditions that minimize

desiccation (low temperature [,58C], high humidity

[$95% relative humidity], and no wind; McMahon

1996). At more typical summer outdoor conditions

(208C, 50% relative humidity) survival is likely to be

3–5 d (Ricciardi et al. 1995), but desiccation of adult

zebra mussels might be reduced when they are attached

to moist macrophytes. Conditions in the small volumes

of water transported in recreational boats (e.g., temperature, pH, dissolved oxygen) are likely to differ from

natural conditions, and we hypothesize that survival

rates of larvae will be low (Table 6). Conditions in bait

buckets and live wells are likely to be degraded by fish

excretions, and may even be worse in bilge water where

other contaminants (e.g., fuel) accumulate. Thus water

trapped in the intake of the engine cooling system, where

temperatures are not elevated, is likely to be the most

suitable, and on one occasion we found a living larva

in engine cooling water collected from a boat that had

been recently used in zebra mussel-infested waters (Lake

Erie) as it was preparing to launch in an uninfested

inland lake (L. E. Johnson, personal observation). Still,

the small volumes involved suggest the absolute number

transported per event is low (Table 6).

In spite of the dominance of mechanisms transporting larvae (Table 2), adults are hypothesized to have a

greater potential to establish new populations (Johnson

and Padilla 1996). Gamete dilution, which decreases

fertilization rates of benthic invertebrates in marine

systems (Levitan et al. 1992), requires that introduced

populations must be either very large or spatially aggregated to become established. Thus, the incidental

release of small numbers of larvae by recreational boats

is not likely to meet these conditions, as larvae will

become diluted and suffer high mortality (Sprung

1993). We concur that interbasin range expansion from

transient recreational boating is most likely to continue

by the dispersal of adult or juvenile stages, especially

those attached to entangled macrophytes.

The simple probability model developed here predicted

that hundreds to thousands of potential dispersal events

occurred during the period of the study. How does this

estimate of ‘‘propagule pressure’’ (sensu Ricciardi and

MacIsaac 2000) compare with subsequent patterns of inland invasion in adjacent areas? As of 1997, zebra mussel

populations had been found in 11 of the 36 lakes .50

ha in area within the four-county region of Michigan

bordering Lake St. Clair (Kraft and Johnson 2000), but

six of these were most likely the result of secondary

dispersal of zebra mussels downstream (L. E. Johnson

and C. E. Kraft, unpublished data). Given the abundance

of lakes in this region, this number is surprising low

considering the number of potential colonizing events.

This discrepancy can be explained in a number of ways.

First, we only made observations as boats and trailer were

leaving infested waters, and not as they arrived at inland

lakes. Although MAZM have been observed arriving at

uninfested inland lakes (Johnson and Carlton 1996), we

do not know the proportion of MAZM that fall off en

route, that are removed by boat owners, or that are not

released upon arrival (i.e., that are retained on the trailer).

Second, individual inoculations may often fail to found

new populations (the ‘‘Noah Fallacy,’’ Johnson and Carlton 1992), or multiple deliveries may be required to attain

a minimum viable population. Indeed, for modeling purposes, Schneider et al. (1998) chose a threshold of 2000

visitations by infested boats to establish new populations

of zebra mussels. Last, boaters do not visit lakes randomly

(Johnson and Padilla 1996, Padilla et al. 1996, Buchan

and Padilla 1999), and thus invasions may be more likely

for popular lakes. However, it is not the overall use of

recreational boats on a given a lake, but rather the frequency of ‘‘promiscuous’’ behavior (i.e., the sequential

use of multiple waterbodies by boaters) that will likely

determine the likelihood of invasion, all other factors being equal (Padilla et al. 1996).

The presence of adult zebra mussels on trailered

boats, coupled with a high frequency of multilake usage

by boaters (Gunderson 1994, Padilla et al. 1996, Buchan and Padilla 1999; this study), suggests that transient

recreational boating activities may play an important

role in the colonization of isolated inland lakes (but

see the previous comments concerning resident boats).

Recreational boating has already been implicated in the

spread of exotic macrophytes (Dove and Taylor 1982

and references therein, Johnstone et al. 1985, Joyce
1798 LADD E. JOHNSON ET AL. Ecological Applications

Vol. 11, No. 6

1992). Because zebra mussels attach frequently to submerged macrophytes (Lewandowski 1982, UWSGI

1993, Lewandowski and Ozimek 1997, Horvath and

Lamberti 1997) and macrophyte abundance is predicted

to increase in lakes infested with zebra mussels (Griffiths 1993), we contend that the interbasin transport of

macrophytes entangled on boat trailers and equipment

(e.g., motors, propellers) must be targeted to prevent

or slow the further invasion of inland waters. Fortunately, the importance of removing macrophytes from

boats and trailers, both to prevent the spread of zebra

mussels and the macrophytes themselves, is beginning

to be integrated into educational efforts (e.g., MSG

2000). Guidelines for the control of zebra mussels and

other epiphytes must emphasize the potential interaction between macrophytes and boat trailers, not only

for the obvious danger of dispersing exotic macrophytes, but also for dispersing associated exotic animals including, but not limited to, the zebra mussel.

Although we focused specifically on the further regional expansion of the zebra mussel, our results are

applicable to the dispersal of other aquatic species,

including the past, present and future invaders of North

American inland waters (Mills et al. 1993, Ricciardi

1998, Ricciardi and Rasmussen 1998). Besides the obvious relevance to the dispersal of macrophytes and

any associated fauna and flora, the transport of small

quantities of water could play a major role in the spread

of species possessing planktonic life stages, particularly those capable of parthenogenetic reproduction,

e.g., the invasive cladocerans Bythotrephes cederstroemi (Yan et al. 1992) and Daphnia lumholtzi (Havel et

al. 1995, Havel and Stelzleni-Schwent 2001).

This study examined in detail the diverse mechanisms of dispersal associated with one vector, namely

transient recreational boating, but our approach is

widely applicable to other vectors and other invasive

species. Dispersal can be inherently difficult to study

even in a qualitative manner, and thus the vectors of

dispersal are often ignored by researchers who instead

focus on the ecological and economic impacts of invaders. Still, as we have demonstrated here, one can

make the key observations needed to demonstrate that

a suspected vector is indeed capable of transporting the

species in question. Beyond this basic requirement, one

can then compare different mechanisms by which organisms can be transferred and ideally make comparisons among different vectors (Johnson and Carlton

1996). Finally, the overall risk of any particular mechanism can be assessed by quantifying the various probabilities associated with each step in the process of

dispersal. For the case of the zebra mussel, intuition

and anecdote have served in the absence of any formal

risk assessment as the only basis for policy decisions

and educational efforts (e.g., the 100th meridian project; Tyrus et al. 1994). Quantitative approaches to dispersal and geographical spread can help develop a more

rigorous science on which to base these decisions.

ACKNOWLEDGMENTS

This research was supported by the NOAA National Sea

Grant College Program (Connecticut Sea Grant R/ER-5 to J.

T. Carlton). Our appreciation to Drs. Alfred Beeton and David

Reed of the Great Lakes Environmental Research Laboratory

(NOAA) for providing space and facilities during the course

of this study, and to the Michigan Department of Natural

Resources and the Metroparks Commission for permission to

work at their public access sites and access to unpublished

data. Discussions with David Garton, Cliff Kraft, Ellen Marsden, Ransom Myers, Jerrie Nichols, and Dianna Padilla contributed to many of the ideas incorporated into this paper.

Our thanks to Joe Anicka and Rich Doneen for the long hours

spent in the field, and to the many boaters who willingly put

up with the seemingly endless questions and troublesome

sampling of their boats.

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