Facilitative interactions among aquatic invaders: is an "invasional meltdown" occurring in the Great Lakes?
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2513
PERSPECTIVE
Facilitative interactions among aquatic invaders:
is an “invasional meltdown” occurring in the Great
Lakes?
Anthony Ricciardi
Abstract: A widely cited hypothesis in ecology is that species-rich communities are less vulnerable to invasion than
species-poor ones, owing to competition for limiting resources (the “biotic resistance” model). However, evidence for
biotic resistance in aquatic ecosystems is equivocal. Contrary to the view that communities become more resistant to
invasion as they accumulate species, the rate of invasion has increased over the past century in areas that have received
frequent shipping traffic. Furthermore, introduced species may facilitate, rather than compete with, one another. A review
of invasions in the Great Lakes indicates that direct positive (mutualistic and commensal) interactions among introduced
species are more common than purely negative (competitive and amensal) interactions. In addition, many exploitative
(e.g., predator–prey) interactions appear to be strongly asymmetric in benefiting one invading species at a negligible cost
to another. These observations, combined with an increasing invasion rate in the Great Lakes, tentatively support the
Simberloff – Von Holle “invasional meltdown” model. The model posits that ecosystems become more easily invaded as
the cumulative number of species introductions increases, and that facilitative interactions can exacerbate the impact of
invaders. It provides a theoretical argument for substantially reducing the rate of species introductions to the Great Lakes.
Résumé : Une hypothèse couramment citée en écologie veut que les communautés riches en espèces soient moins
vulnérables aux invasions que les plus pauvres, à cause de la compétition pour les ressources limitantes (le modèle de
la « résistance biotique »). Cependant, les preuves de l’existence d’une telle résistance biotiques dans les écosystèmes
aquatiques sont équivoques. En contradiction avec l’opinion qui prétend que les communautés deviennent plus
résistantes lorsqu’elles accumulent plus d’espèces, le taux d’invasion a augmenté au cours du siècle dernier dans les
régions qui reçoivent un important trafic maritime. De plus, les espèces introduites peuvent même faciliter leur
coexistence mutuelle plutôt qu’entrer en compétition. Une étude des invasions dans les Grands-Lacs révèle que les
interactions directes positives (de mutualisme et de commensalisme) parmi les espèces introduites sont plus fréquentes
que les interactions purement négatives (de compétition et d’amensalisme). De plus, plusieurs des interactions
d’exploitation (e.g., de type prédateur-proie) semblent être fortement asymétriques en avantageant l’un des envahisseur
à un coût négligeable pour l’autre. Ces observations ainsi que le taux croissant des invasions dans les Grands-Lacs
semblent vouloir appuyer le modèle d’ « effondrement des communautés à la suite des invasions » de Simberloff – Von
Holle. Le modèle prédit que les écosystèmes deviennent de plus en plus faciles à envahir à mesure que le nombre
cumulatif d’espèces introduites y augmente et que des actions facilitantes viennent exacerber l’impact des envahisseurs.
Il s’agit donc d’un argument théorique pour limiter de façon importante le taux d’introduction d’espèces dans les
Grands-Lacs.
[Traduit par la Rédaction] Ricciardi 2525
Introduction sion ecology is that species-rich communities are more resis-
tant to invasion than species-poor ones because the former
Biological invasion studies often focus on interactions be- use limiting resources more completely and are also more
tween introduced species and native species. When interactions likely to have competitors or predators that can exclude po-
involving introduced species are considered, competition is tential invaders (Elton 1958). This concept is the basis of the
typically emphasized (Moulton and Pimm 1983; Case 1990; “biotic resistance model”, which predicts that successive in-
Case and Bolger 1991). A widely cited hypothesis in inva- vasions will cause a community to accumulate stronger com-
Received November 21, 2000. Accepted August 29, 2001. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on
December 20, 2001.
J16095
A. Ricciardi. Redpath Museum & McGill School of Environment, McGill University, 859 Sherbrooke St. West, Montreal,
QC H3A 2K6, Canada (e-mail: tony.ricciardi@mcgill.ca).
Can. J. Fish. Aquat. Sci. 58: 2513–2525 (2001) DOI: 10.1139/cjfas-58-12-2513 © 2001 NRC Canada
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2514 Can. J. Fish. Aquat. Sci. Vol. 58, 2001
Fig. 1. Temporal trend in the cumulative number of successful through mutualism, commensalism, or habitat modification
invasions as predicted by (a) the biotic resistance model and (e.g., animals pollinating and dispersing plants). They cited
(b) the invasional meltdown model. European colonization of the New World as an example of a
mutualistic process in which coevolved European animals,
plants, and pathogens formed a “synergistic juggernaut” that
facilitated their domination of native ecosystems. Further-
more, Simberloff and Von Holle (1999) suggested that such
facilitation is a common phenomenon largely ignored by re-
search that has focused on competitive interactions among
invaders. Richardson et al. (2000) similarly concluded that
facilitative interactions are widespread and important in ac-
celerating the invasion of natural communities by plants. No
such analysis has been done for aquatic invasions.
In this paper, I evaluate which of these models (biotic re-
sistance or invasional meltdown) best explains the invasion
history of the Great Lakes. First, I test two key components
of the invasional meltdown model: (i) the premise that
facilitative (positive) interactions are at least as common as
negative interactions among introduced species; and (ii) the
prediction of “an accelerating accumulation of introduced
species” (Simberloff and Von Holle 1999), i.e., that the rate
of invasion of the Great Lakes is increasing with time. Sec-
ond, I examine evidence for biotic resistance in the aquatic
ecology literature by reviewing studies that have explicitly
tested the relationship between invasion success and the
composition (diversity, trophic structure) of the resident
community.
Methods
To test the first prediction of the invasional meltdown model, I
petitors, more efficient predators, and well-defended prey reviewed all available published data for interactions among
(Moulton and Pimm 1983; Case 1990). Thus, the rate of es- sympatric nonindigenous species in the Great Lakes. Literature
tablishment of new species in a community should become sources were obtained primarily from references cited in Mills et
increasingly limited over time. al. (1993) and MacIsaac (1999), as well as from the electronic
Aquatic Sciences and Fisheries Abstracts (ASFA) database
Contrary to the idea that areas become less vulnerable to (http://webspirs3.silverplatter.com). Species interactions were cate-
invasion as they accumulate species, the rate of invasion is gorized as follows: mutualism, in which the interaction is benefi-
increasing in several aquatic ecosystems (e.g., Ribera and cial to the survival and (or) population growth of both species;
Boudouresque 1995; Leppäkoski and Olenin 2000). Even the commensalism, in which one species benefits from the presence of
most speciose aquatic ecosystems on the planet have been another species that is unaffected by the interaction; exploitation,
invaded multiple times (Kaufman 1992; Dumont 1998; Hall in which one species benefits at the expense of another (e.g., pre-
and Mills 2000), whereas some species-poor ecosystems dation, parasitism); amensalism, in which one species is inhibited
have shown remarkable resistance to invasion (e.g., Baltz while the other is unaffected; and antagonism, which is defined
and Moyle 1993). An alternative to the biotic resistance here as any mutually detrimental interaction (e.g., resource compe-
model has been proposed by Simberloff and Von Holle tition, interference, allelopathy). Only direct pairwise interactions
were tabulated. In cases where one invader had various positive
(1999), who suggested that if communities are the outcome and negative effects on another’s abundance and survival, the net
of a nonrandom sorting and adjustment process, then fre- effect was estimated when information allowed at least a subjective
quent species introductions may generate an increasing ranking of the various effects; otherwise, the interaction was omit-
threat to community integrity in two ways: (i) as the cumula- ted. For less than 5% of the cases, when Great Lakes data were un-
tive number of attempted (including unsuccessful) introduc- available, an interaction was assumed to occur between sympatric
tions increases, populations of resident species are disrupted species because it was observed between these species in another
and the community thus becomes more easily invaded; and region.
(ii) once established, some invaders alter habitat conditions The resulting dataset contained 101 pairwise interactions (Ta-
in favor of other invaders, thereby creating a positive feed- ble 1). Obviously, this is a small sample of the actual set of interac-
back system that accelerates the accumulation of non- tions among Great Lakes invaders, because it includes only cases
that are supported by empirical evidence, whereas the ecological
indigenous species and their synergistic impacts. This interactions of most invaders are untested. Moreover, the dataset
defines the “invasional meltdown” model, which emphasizes omits indirect interactions, such as indirect commensalisms in
facilitative (rather than antagonistic) interactions among in- which one invader reduces the abundance or survival of another’s
troduced species (Fig. 1). Simberloff and Von Holle (1999) enemies. Examples of this in the Great Lakes include the indirect
reviewed several cases, primarily from terrestrial ecosys- enhancement of both the alewife Alosa pseudoharengus and the
tems, where one invading organism facilitated another rainbow smelt Osmerus mordax owing to the suppression of native
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Ricciardi 2515
Table 1. Ecological interactions among nonindigenous species established in the Great Lakes – St. Lawrence River system.
Species pairs Reference
Mutualism (+/+) (3 cases)
Bithynia tentaculata / Dreissena polymorpha Ricciardi et al. 1997
Myriophyllum spicatum / Dreissena polymorpha MacIsaac 1996; Skubinna et al. 1995
Potamogeton crispus / Dreissena polymorpha MacIsaac 1996; Skubinna et al. 1995
Commensalism (+/0) (14 cases)
Acineta nitocrae + / Nitocra hibernica 0 Grigorovich et al. 2001
Acineta nitocrae + / Nitocra incerta 0 Grigorovich et al. 2001
Bithynia tentaculata + / Myriophyllum spicatum 0 Vincent et al. 1981
Dugesia polychroa + / Dreissena polymorpha 0 Ricciardi et al. 1997; Ricciardi unpublished data
Dugesia polychroa + / Dreissena bugensis 0 Ricciardi et al. 1997; Ricciardi unpublished data
Echinogammarus ischnus + / Dreissena polymorpha 0 Stewart et al. 1998a, 1998b, 1998c
Echinogammarus ischnus + / Dreissena bugensis 0 Stewart et al. 1998a, 1998b, 1998c
Gammarus fasciatus + / Dreissena polymorpha 0 Ricciardi et al. 1997
Gammarus fasciatus + / Dreissena bugensis 0 Ricciardi et al. 1997; Dermott and Kerec 1997
Lophopodella carteri + / Myriophyllum spicatum 0 Wood 1989
Lophopodella carteri + / Potamogeton crispus 0 Wood 1989
Proterorhinus marmoratus + / Potamogeton crispus 0 Jude et al. 1995
Valvata piscinalis + / Dreissena polymorpha 0 Ricciardi et al. 1997
Valvata piscinalis + / Dreissena bugensis 0 Ricciardi et al. 1997
Exploitation (+/–) (73 cases)
Herbivory
Dreissena polymorpha + / Stephanodiscus binderanus – Holland 1993; MacIsaac 1999
Dreissena polymorpha + / Stephanodiscus subtilis – Holland 1993; MacIsaac 1999
Dreissena polymorpha + / Skeletonema subsalum – Holland 1993; MacIsaac 1999
Dreissena polymorpha + / Cyclotella cryptica – Holland 1993; MacIsaac 1999
Dreissena polymorpha + / Cyclotella pseudostelligera – Holland 1993; MacIsaac 1999
Predator–prey relationships
Alosa pseudoharengus + / Osmerus mordax – Smith 1970
Alosa pseudoharengus + / Eubosmina coregoni– Mills et al. 1995
Alosa pseudoharengus + / Bythotrephes longimanus – Grigorovich et al. 1998
Alosa pseudoharengus + / Cercopagis pengoi – E. Mills, personal communication
Alosa pseudoharengus + / Dreissena polymorpha – Mills et al. 1995
Bythotrephes longimanus + / Eubosmina coregoni – Grigorovich et al. 1998
Cordylophora caspia + / Dreissena polymorpha – Molloy et al. 1997; Olenin and Leppakoski 1999
Cyprinus carpio + / Dreissena polymorpha – Tucker et al. 1996
Cyprinus carpio + / Dreissena bugensis – Ricciardi, unpublished data
Cyprinus carpio + / Sphaerium corneum– Ricciardi, unpublished data
Cyprinus carpio + / Bithynia tentaculata – Ricciardi, unpublished data
Gymnocephalus cernuus + / Gammarus fasciatus – Fullerton et al. 1998
Gymnocephalus cernuus + / Megacyclops viridis – Ogle et al. 1995
Morone americana + / Bythotrephes longimanus – Grigorovich et al. 1998
Neogobius melanostomus + / Dreissena polymorpha – Ray and Corkum 1997; Molloy et al. 1997
Neogobius melanostomus + / Dreissena bugensis – Molloy et al. 1997
Neogobius melanostomus + / Gammarus fasciatus – Ray and Corkum 1997; Jude et al. 1995
Neogobius melanostomus + / Echinogammarus ischnus – Shorygin 1952
Oncorhynchus tshawytscha + / Alosa pseudoharengus – Jude et al. 1987
Oncorhynchus tshawytscha + / Osmerus mordax – Conner et al. 1993; Jude et al. 1987
Oncorhynchus tshawytscha + / Bythotrephes longimanus – Grigorovich et al. 1998
Oncorhynchus gorbuscha + / Alosa pseudoharengus – Smith 1970
Oncorhynchus gorbuscha + / Osmerus mordax – Conner et al. 1993
Oncorhynchus gorbuscha + / Bythotrephes longimanus – Grigorovich et al. 1998
Oncorhynchus kisutch + / Alosa pseudoharengus – Jude et al. 1987
Oncorhynchus kisutch + / Osmerus mordax – Conner et al. 1993; Jude et al. 1987
Oncorhynchus nerka + / Alosa pseudoharengus – Smith 1970
Oncorhynchus nerka + / Osmerus mordax – Conner et al. 1993
Oncorhynchus mykiss + / Alosa pseudoharengus – Jude et al. 1987
Oncorhynchus mykiss + / Osmerus mordax – Conner et al. 1993; Jude et al. 1987
Oncorhynchus mykiss + / Bythotrephes longimanus – Grigorovich et al. 1998
Osmerus mordax + / Eubosmina coregoni – Mills et al. 1995
Osmerus mordax + / Dreissena polymorpha – Mills et al. 1995
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2516 Can. J. Fish. Aquat. Sci. Vol. 58, 2001
Table 1 (concluded).
Species pairs Reference
Osmerus mordax + / Bythotrephes longimanus – Grigorovich et al. 1998
Proterorhinus marmoratus + / Dreissena polymorpha – Molloy et al. 1997
Proterorhinus marmoratus + / Dreissena bugensis – Molloy et al. 1997
Salmo trutta + / Alosa pseudoharengus – Jude et al. 1987; Smith 1970
Salmo trutta + / Osmerus mordax – Conner et al. 1993; Jude et al. 1987
Salmo trutta + / Bythotrephes longimanus – Grigorovich et al. 1998
Parasite–host relationships
Acanthostomum sp. + / Gymnocephalus cernuus – Pronin et al. 1997b
Acentropus niveus + / Myriophyllum spicatum – Mills et al. 1993
Acentropus niveus + / Potamogeton crispus – Mills et al. 1993
Acentropus niveus + / Trapa natans – Mills et al. 1993
Aeromonas salmonicida + / Salmo trutta – Mills et al. 1993
Aeromonas salmonicida + / Carassius auratus – Mills et al. 1993
Aeromonas salmonicida + / Cyprinus carpio – Mills et al. 1993
Argulus japonicus + / Carassius auratus – Mills et al. 1993
Dactylogyrus amphibothrium + / Gymnocephalus cernuus – Cone et al. 1994
Dactylogyrus hemiamphibothrium + / Gymnocephalus cernuus – United States Department of the Interior 1993
Glugea hertwigi + / Osmerus mordax – Mills et al. 1993
Ichthyocotylurus pileatus + / Neogobius melanostomus – Pronin et al. 1997a
Myxobolus cerebralis + / Oncorhynchus tshawytscha – Mills et al. 1993
Myxobolus cerebralis + / Oncorhynchus gorbuscha – Mills et al. 1993
Myxobolus cerebralis + / Oncorhynchus kisutch – Mills et al. 1993
Myxobolus cerebralis + / Oncorhynchus nerka – Mills et al. 1993
Myxobolus cerebralis + / Oncorhynchus mykiss – Mills et al. 1993
Myxobolus cerebralis + / Salmo trutta – Mills et al. 1993
Neascus brevicaudatus + / Gymnocephalus cernuus – United States Department of the Interior 1993
Petromyzon marinus + / Oncorhynchus tshawytscha – Pearce et al. 1980
Petromyzon marinus + / Oncorhynchus mykiss – Berst and Wainio 1967
Petromyzon marinus + / Oncorhynchus gorbuscha – Noltie 1987
Petromyzon marinus + / Oncorhynchus kisutch – Pearce et al. 1980
Petromyzon marinus + / Oncorhynchus nerka – Pearce et al. 1980
Petromyzon marinus + / Cyprinus carpio – Christie and Kolenosky 1980
Sphaeromyxa sevastopoli + / Neogobius melanostomus – Pronin et al. 1997a
Sphaeromyxa sevastopoli + / Proterorhinus marmoratus – Pronin et al. 1997a
Trypanosoma acerinae + / Gymnocephalus cernuus – United States Department of the Interior 1993
Overgrowth
Lophopodella carteri + / Dreissena polymorpha – Lauer et al. 1999
Amensalism (–/0) (4 cases)
Habitat alteration
Potamogeton crispus – / Cyprinus carpio 0 Lundholm and Simser 1999
Myriophyllum spicatum – / Cyprinus carpio 0 Lundholm and Simser 1999
Interference
Elimia virginica – / Bithynia tentaculata 0 Harman 1968
Sphaerium corneum – / Dreissena polymorpha 0 Lauer and McComish 2001
Antagonism (–/–) (7 cases)
Predation vs. allelopathy
Oncorhynchus kisutch / Alosa pseudoharengus Fitzsimons et al. 1999
Interspecific predation of larvae
Proterorhinus marmoratus / Neogobius melanostomus Jude et al. 1995
Resource competition
Echinogammarus ischnus / Gammarus fasciatus Dermott et al. 1998
Dreissena polymorpha / Dreissena bugensis Mills et al. 1999
Sphaerium corneum / Dreissena bugensis Dermott and Kerec 1997
Lythrum salicaria / Typha angustifolia Mal et al. 1997
Oncorhynchus mykiss / Salmo trutta Landergren 1999
Note: +, Enhanced survival or population growth; –, survival or population growth negatively affected; 0, unaffected.
predatory salmonids by introduced sea lamprey Petromyzon marinus might have facilitated population expansion of large nonindigenous
during the 1940s and 1950s (Smith 1970; Christie 1974). Simi- zooplankton such as Bythotrephes longimanus and Cercopagis
larly, by preying heavily upon planktivores, introduced salmonids pengoi (Jude et al. 1987; Conner et al. 1993). Indirect
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Ricciardi 2517
commensalism also occurs when one invader augments the food Fig. 2. Positive feedback mechanisms of the invasional meltdown
resources of another invader; for example, the zebra mussel model. An example of direct facilitation is the provision of
Dreissena polymorpha increases the diversity and abundance of in- biodeposits and shelter by an introduced mussel for an introduced
vertebrate prey for benthivorous fishes like the ruffe Gymno- detritivore. An example of indirect facilitation is the reduction of
cephalus cernuus, whose growth rate may increase as a result piscivores by an introduced parasite (e.g., sea lamprey), paving the
(Thayer et al. 1997). In the invasional meltdown model, both direct
way for invasion by a planktivore (e.g., alewife).
and indirect facilitation accelerate the establishment of non-
indigenous species through positive feedback loops (Fig. 2).
I tested the second prediction of the invasional meltdown model
using linear regression analysis of data on the number of Great
Lakes invasions documented between 1810 and 2000. Only those
species known to be established (i.e., having formed reproducing
populations) were included; therefore, some introduced species
such as skipjack herring Alosa chrysochloris (Fago 1993) and grass
carp Ctenopharyngodon idella (Crossman et al. 1987) were omit-
ted. My review yielded a total of 162 invaders (see Appendix A for
species additional to those listed by Mills et al. 1993).
Finally, to assess evidence of biotic resistance in aquatic sys-
tems, I searched the ASFA database for published studies that con-
tained the following combinations of key words: (INVAD* or
INTRODUCED or NONINDIGENOUS or ALIEN or EXOTIC)
and RESISTANCE. The ASFA database contained studies pub-
lished from 1978 to 2000, inclusive. My intention was to determine
whether negative relationships between invasion success and spe-
cies diversity within a community have been demonstrated for
freshwater, brackish-water, or marine communities.
mussel larvae and the cladoceran Eubosmina coregoni may
have aided the invasion of blueback herring, Alosa aestivalis,
in Lake Ontario (Molloy et al. 1997; MacNeill 1998).
Results and discussion
Evidence of an invasional meltdown in the Great Lakes
Facilitative versus antagonistic interactions among The invasional meltdown model is supported by the in-
invaders in the Great Lakes creasing rate of invasion in the Great Lakes over the past
Contrary to the biotic resistance model, which assumes two centuries (Fig. 3). Among the 162 nonindigenous spe-
the dominance of negative interactions among introduced cies in the system, 40 were recorded during the first half of
species, the number of cases of direct positive interactions (3 the 20th century and 76 during the latter half of the 20th
mutualisms and 14 commensalisms) exceeds the number of century. Since 1970, on average, there has been one invader
cases of purely negative interactions (4 amensalisms and 7 recorded every eight months. The number of species estab-
antagonistic interactions) (Table 1). All mutualisms and lished per decade has increased with time, and none has sub-
commensalisms listed here are facultative. About 72% sequently become extirpated. The trend in the cumulative
(73/101) of interactions in the dataset are exploitative, being number of successful invasions over the past two centuries is
mostly predator–prey and parasite–host relationships. These best described by a quadratic function (Fig. 3), which ex-
cannot be interpreted as purely negative interactions, be- plains 4% more variance than a simple linear function. This
cause one invader clearly benefits from the other’s presence. trend might partially reflect recent awareness and monitoring
Moreover, in many cases, the interaction is probably efforts to locate invaders; however, much of the taxonomic
strongly asymmetric such that the prey and (or) host popula- and survey work on Great Lakes biota was carried out sev-
tion is only weakly affected because of its high recruitment eral decades ago. Undoubtedly, some invasions have gone
rate or because of the relatively low abundance of the preda- unnoticed, and there are several species of cryptogenic inver-
tor or parasite, i.e., prey abundance may control predator tebrates (species of uncertain origin but assumed to be
abundance, but not vice versa. These interactions appear to holarctic or cosmopolitan) that may have been introduced in
have such a negligible cost to the host or prey species that the distant past (Mills et al. 1993).
they could be considered commensal (examples include the Another potential explanation for the increasing invasion
moth Acentropus niveus and its plant hosts; some rate is the strong positive relationship between the number
molluscivorous fishes and their zebra mussel prey; plankti- of nonindigenous species established per decade and ship-
vorous fishes and zebra mussel larvae; Mills et al. 1993; ping activity (net tonnage of cargo ships) in the Great Lakes
Molloy et al. 1997). (Fig. 4). Shipping activity explains 62% of variation in the
In about one third (25/73) of the cases of exploitation, the invasion rate, despite the fact that nearly half of all invasions
newcomer benefited from the presence of a previously estab- that occurred over the past century are attributable to other
lished invader. For example, the presence of abundant and vectors. Shipping still accounts for more invasions than any
widespread zebra mussel populations likely facilitated the other single vector, and its influence has grown in recent de-
establishment and spread of the round goby Neogobius cades: 77% (36 of 47) of invasions since 1970 were likely
melanostomus, one of the mussel’s principal predators in the caused by transoceanic shipping (see Mills et al. 1993 and
Ponto–Caspian (Black and Caspian Seas) region (Shorygin references in Appendix A). Surprisingly, the relationship ob-
1952; Ray and Corkum 1997). Similarly, the prior establish- tained using data for all invaders is stronger than the one ob-
ment of abundant zooplanktonic prey in the form of zebra tained using only species assumed to have been transported
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2518 Can. J. Fish. Aquat. Sci. Vol. 58, 2001
Fig. 3. Changes in the numbers of nonindigenous species estab- Fig. 4. Invasion rate versus shipping activity in the Great Lakes
lished in the Great Lakes as a function of time (decades) in which from 1900 to 1999 (y = 0.062x, r 2adj = 0.62, P < 0.004).
the species was discovered or presumed introduced. (a) Number of Shipping activity is measured in net tonnage (1 ton (Imperial) =
invaders per decade (y = 0.79x, r 2adj = 0.71, P < 0.0001). (b) Cu- 0.9842 t) of cargo ships (both foreign and domestic vessels)
mulative number of invaders over time (y = 1.50x + 0.37x 2, r 2adj = averaged over all years within each decade; data are from Lake
0.997, P < 0.0001). Least-squares regression lines are shown. Data Carriers’ Association (1999).
are from Mills et al. (1993) and references are given in Appendix A.
not differ from previous decades (15 in the 1980s, 17 in the
1970s, 15 in the 1960s) despite regulations requiring in-
bound ships to exchange their freshwater–estuarine ballast
with oceanic water. Voluntary ballast water exchange guide-
lines were initiated by the Canadian government in 1989,
and approximately 90% of ships complied with the proce-
dure even before it became mandatory by U.S. regulation in
1993 (Locke et al. 1993). In theory, mid-oceanic ballast
water exchange should reduce the risk of invasion because
freshwater organisms would be purged from the ballast
tanks or killed by incoming seawater, and be replaced by
marine organisms that could not survive if released into the
Great Lakes. However, owing to the position of the pump
intake, it is impossible to empty ballast tanks completely, so
oceanic salinities are rarely achieved (Locke et al. 1993).
Therefore, ballast water exchange may not prevent invasions
with ships, either in ballast water or as fouling organisms on by species with broad salinity tolerance and by species with
ship hulls (r 2 = 0.43, P < 0.023). The stronger correlation resistant resting stages that are unlikely to be removed by
may be due, in part, to factors coincident with increasing exchange nor killed by contact with seawater.
shipping activity, such as changing trade patterns that have Indeed, since the early 1990s, ships have continued to in-
resulted in an increased diversity of donor regions linked to troduce species including the amphipod Echinogammarus
the Great Lakes. Alternatively, invasions may be succeeding ischnus, the copepod Schizopera borutzkyi, and the waterflea
more easily now than ever before because of facilitation Cercopagis pengoi (Witt et al. 1997; MacIsaac et al. 1999;
among invaders. A positive feedback cycle of invasion Horvath et al. 2001). A living specimen of another amphi-
should yield a stronger correlation involving all invaders pod, Corophium mucronatum, was collected in Lake St.
rather than only a subset of species associated with a partic- Clair in 1997, but the species has apparently not become
ular vector. Unfortunately, it is not possible to clearly sepa- established (Grigorovich and MacIsaac 1999). Other failed
rate the effects of facilitation and inoculation pressure (e.g., species introductions during the 1990s include non-
caused by to increased ship traffic) on the rate of invasion. reproducing European flounder (Platichthys flesus) and Chi-
Although shipping activity likely contributes to the in- nese mitten crab (Eriocheir sinensis) (E.L. Mills, Cornell
creased accumulation of invaders in the Great Lakes, the University, Biological Field Station, Bridgeport, N.Y., per-
number of invaders recorded in the 1990s (15 species) does sonal communication). Thus, during the 1990s there was a
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Ricciardi 2519
Fig. 5. Density of the Ponto–Caspian amphipod Echinogammarus sel beds might also offer amphipods a refuge from fish pre-
ischnus as a function of Dreissena mussel density in the Great dation (Gonzalez and Downing 1999). In addition, by colo-
Lakes (least-squares regression of log-transformed data, y = nizing fine sediments in western Lake Erie, Dreissena has
1.61 + 0.53x, r 2adj = 0.32, P < 0.017). Data are from Stewart et facilitated the expansion of Echinogammarus into habitats
al. (1998a, 1998b, 1998c) and R. Dermott, Department of Fish- that were previously unsuitable (Bially and MacIsaac 2000).
eries and Oceans, Burlington, Ont. (personal communication). !, Thus, the introduced mussels stimulate a prey resource for
Western Lake Erie; 䉱, eastern Lake Erie; 䉲, St. Clair River. juvenile round gobies, which feed predominantly on
gammarid amphipods in their native range, whereas adult
gobies feed preferentially on the mussels themselves
(Shorygin 1952; Ray and Corkum 1997). Another benefi-
ciary is the Ponto–Caspian hydroid Cordylophora caspia,
which consumes zebra mussel larvae and uses mussel shells
as substrate (Olenin and Leppäkoski 1999). After having
been relatively inconspicuous in the Great Lakes for de-
cades, Cordylophora has been observed growing luxuriantly
on mussel beds in Lake Michigan in recent years (T. Lauer,
Ball State University, Muncie, Ind., personal communica-
tion). In Lake St. Clair and Saginaw Bay, Lake Huron, zebra
mussel filtration has substantially increased water transpar-
ency, thereby stimulating the growth of exotic and native
macrophytes (Skubinna et al. 1995; MacIsaac 1996), which
in turn provide substrate for settling juvenile mussels and fa-
cilitate their dispersal (Horvath and Lamberti 1997). In the
St. Lawrence River, the European faucet snail, Bithynia
tentaculata, has tripled its abundance in association with the
growth of dense mussel populations, whose shells support
rich microflora and provide the small snail with increased
grazing area (Ricciardi et al. 1997) as well as potential ref-
uge from large predators (Stewart et al. 1999). In return, the
strong shift toward introductions of euryhaline animal spe- grazing activities of the snail reduce fouling sponge colonies
cies, most of which originate from Ponto–Caspian basins. that can overgrow and smother mussels (Ricciardi et al.
The recent influx of Ponto–Caspian invaders is attribut- 1995; A. Ricciardi, unpublished data).
able to strong invasion corridors (i.e., transportation vectors If co-evolution reduces the intensity of interspecific inter-
and dispersal pathways) linking the Great Lakes with Eur- actions (Case and Bolger 1991), then successive introduc-
asia (Ricciardi and MacIsaac 2000). Invasion corridors shunt tions of species originating from the same endemic region
large numbers of propagules from particular donor pools may not be limited by competition, contrary to predictions
into new regions, thereby assembling co-evolved alliances of community assembly models. In addition to the Great
and foreign food webs in the recipient habitat like pieces of Lakes, facilitation among invaders and reassembly of co-
an ecological jigsaw puzzle. For example, sequential inva- evolved food webs have also been observed in the Baltic
sions by Ponto–Caspian species have completed the parasitic Sea, where most of the invaders discovered since 1990 are of
life cycle of the trematode Bucephalus polymorphus in Ponto–Caspian origin (Leppäkoski and Olenin 2000). How-
Western Europe. The introductions of its first intermediate ever, positive interactions in the Great Lakes and the Baltic
host (the zebra mussel) and its definitive host (the pike- Sea often involve species that share no evolutionary history.
perch Stizostedion lucioperca) allowed the trematode to In the Great Lakes, for example, the Asian bryozoan Lopho-
spread into inland waters and cause high mortality in local podella carteri commonly uses Eurasian macrophytes as
populations of cyprinid fishes, which act as secondary inter- substrate (Wood 1989). The amphipod Gammarus fasciatus,
mediate hosts (Combes and Le Brun 1990). In the Great native to the Atlantic region of North America, thrives in
Lakes, facultative host–parasite complexes of nonindigenous Ponto–Caspian mussel beds (Ricciardi et al. 1997). In the
species have become established, including parasites of Baltic Sea, shells of the American barnacle Balanus
introduced gobies (N. melanostomus and Proterorhinus improvisus provide shelter for Ponto–Caspian amphipods
marmoratus) and of the ruffe Gymnocephalus cernuus (Pronin (Olenin and Leppäkoski 1999). Balanus itself uses zebra
et al. 1997a, 1997b; Cone et al. 1994). These parasites were mussels as substrate (Olenin and Leppäkoski 1999), and
probably introduced simultaneously with their hosts. may benefit from direct exposure to mussel filtration cur-
Ponto–Caspian invaders have also been facilitated by hab- rents as it does in its commensal relationship with Mytilus
itat alterations caused by dreissenid mussels (Dreissena (Laihonen and Furman 1986).
polymorpha and Dreissena bugensis). Dreissena spp. are in-
volved in all three cases of mutualism and 8 of the 14 cases Is the biotic resistance hypothesis generally valid for
of commensalism (e.g., Fig. 5). Food (in the form of fecal aquatic communities?
deposits) and habitat complexity produced by mussel beds Elton’s (1958) proposition that species-rich communities
have stimulated a 20-fold increase in the biomass of the am- are more resistant to invaders is supported by mathematical
phipod E. ischnus in Lake Erie (Stewart et al. 1998a). Mus- models and some field studies (e.g., Moulton and Pimm
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2520 Can. J. Fish. Aquat. Sci. Vol. 58, 2001
1983; Case 1990; Reusch 1998). The evidence is equivocal, been responsible for preventing the expansion of the alewife
however. As noted by Levine and D’Antonio (1999), mathe- from the St. Lawrence River into the Great Lakes, prior to
matical models are based on communities that are at equilib- the construction of the Erie Canal (Smith 1970). However,
rium prior to invasion, whereas many natural communities predator diversity does not appear to be a good predictor of
appear to be unsaturated or successional (Cornell 1999). invasibility. Although European studies suggest that fish
Various studies have found the relationship between inva- predation may exclude the waterflea Bythotrephes
sion success and community diversity to be negative, posi- longimanus (=cederstroemi) from lakes within its natural
tive, or insignificant (reviewed by Levine and D’Antonio range (Grigorovich et al. 1998), selective predation by
1999). Negative relationships, when observed, occur at small planktivorous fishes did not prevent Bythotrephes or another
spatial scales (e.g., ~1 m2 or less). Positive relationships waterflea, Cercopagis pengoi, from becoming established in
tend to occur at regional scales (thousands of square metres) Lake Ontario (MacIsaac et al. 1999), which has the highest
and suggest that the same environmental properties that sup- degree of planktivory among the Great Lakes (Rand et al.
port a rich diversity of native species may also support a 1995). Both species were established in Lake Ontario prior
rich diversity of introduced species (Levine and D’Antonio to invading other Great Lakes. Bythotrephes also became es-
1999). tablished in Harp Lake, Ontario, despite the presence of (i) a
Biotic resistance is hypothesized to occur at two stages of rich, stable zooplankton community, and (ii) intense plankti-
invasion: at the establishment stage and, if establishment is vory from lake herring Coregonus artedii and from a diverse
successful, during subsequent population growth, when the assemblage of macroinvertebrate predators including Lepto-
abundance of the invader (and thus its community-wide im- dora kindtii, opossum shrimp Mysis relicta, phantom midge
pact) is limited by resident species richness (Elton 1958; Chaoborus punctipennis, and the jellyfish Craspedacusta
Case 1990; Shurin 2000). I have found only four docu- sowerbyi (Yan and Pawson 1997; Coulas et al. 1998). Simi-
mented studies (published before 2001) that have explicitly larly, rainbow smelt have colonized a wide variety of inland
tested biotic resistance to establishment in aquatic communi- lakes possessing sparse to rich communities of predators
ties; two of these support the biotic resistance model. After (Evans and Loftus 1987). There are also several examples of
inoculating fishless ponds with nonindigenous zooplankton, marine algae that have become established in the presence
Shurin (2000) found that both the proportion of successful of a diverse assemblage of invertebrate grazers (Trowbridge
introductions and the biomass of introduced species was 1995). In fact, there are theoretical reasons for predicting a
negatively correlated with native species richness. In the sec- positive relationship between invasibility and predator diver-
ond study, using experimental communities of sessile marine sity. Pimm (1989) hypothesized that communities having a
invertebrates, Stachowicz et al. (1999) reported that large variety of predators might be more vulnerable to inva-
survivorship among introduced species declined with in- sion because predators reduce interspecific competition at
creasing community richness, apparently because of compe- lower trophic levels. Interference competition among preda-
tition for space. However, they tested communities tor species may also reduce pressure on introduced prey or-
composed of only 0 to 4 epifaunal species. Experiments with ganisms (Soluk 1993).
small communities may have little predictive power if the
relationship between invasibility and species richness is
asymptotic over the range of community sizes commonly Evolved versus contrived community diversity
found in nature. Are rich communities of co-evolved fauna more resistant to
The two remaining studies do not support the biotic resis- invasion? Perhaps so, but numerous examples demonstrate the
tance model. In an analysis of 125 North American vulnerability of such communities. Lake Victoria had one of
drainages, Gido and Brown (1999) found a weak negative the richest endemic fish communities on the planet, but was
correlation between the number of introduced fish species devastated by a single invader, Nile perch Lates niloticus,
and the number of native fish species historically present in which encountered neither predation nor competition from na-
a drainage. However, their random simulations showed that tive fishes (Kaufman 1992). Rich, co-evolved communities in
this pattern was due to a statistical artifact: drainages with the Caspian Sea, Lake Baikal, Lake Biwa, and Lake Titicaca
low native diversity may receive introductions from a greater have also been invaded multiple times (Dumont 1998; Hall
pool of potential invaders in neighboring drainages. Further- and Mills 2000). Mississippi River fish communities are
more, not all drainages with low native diversity were colo- among the most speciose of all temperate rivers, but have
nized by large numbers of introduced fishes; relatively fewer been invaded by several nonindigenous fishes including com-
invasions occurred in drainages situated in extreme northern mon carp Cyprinus carpio, goldfish Carassius auratus, grass
environments and in drainages whose river flow was less carp Ctenopharyngodon idella, striped bass Morone saxatilis,
regulated. rainbow smelt Osmerus mordax, rainbow trout Oncorhynchus
Contrary to the notion that species-poor communities are mykiss, and white catfish Ictaluris catus (Burr and Page
highly vulnerable to invasion, Baltz and Moyle (1993) ob- 1986). The zebra mussel has become established at high den-
served that a depauperate fish assemblage in an unregulated sities throughout the Mississippi River basin, which contains
stream resisted invasion, despite inoculation pressure from the world’s richest endemic assemblage of freshwater mussels
several nonindigenous fishes inhabiting other parts of the (Ricciardi et al. 1998). However, Lake Victoria cichlids and
drainage basin. Their analysis suggested that abiotic factors Mississippi River mussels are rapidly evolving species flocks
and the presence of native predators were more important that developed in the absence of predators like the Nile perch
than interspecific competition in maintaining community in- and biofoulers like the zebra mussel, and thus were ecologi-
tegrity. Similarly, an abundance of large piscivores may have cally naïve to their effects.
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Ricciardi 2521
The hypothesis that a community is less likely to be in- small number of native molluscivores were necessary to limit
vaded when introduced species encounter diverse competi- the abundance of the introduced marine mussel Musculista
tors is suggested by terrestrial field studies (Moulton and senhousia in a southern California bay; 65% of mussel mor-
Pimm 1983; Case and Bolger 1991), but is difficult to test tality was caused by one species of muricid snail (Reusch
rigorously because of the scarcity of data on failed introduc- 1998). Thus, a single predator or parasite species might be
tions. Nevertheless, numerous counterexamples suggest that sufficient to prevent an introduced species from becoming
this hypothesis is not broadly valid in aquatic systems. The dominant. Conversely, even when an introduced species en-
presence of ecologically or taxonomically similar native spe- counters predation pressure from a diverse assemblage of
cies has not prevented the establishment of several non- consumers it may not necessarily be prevented from becom-
indigenous algae in coastal marine communities worldwide ing dominant, as demonstrated by both the Bythotrephes
(Trowbridge 1995; Ribera and Boudouresque 1995). Follow- longimanus and the round goby, N. melanostomus, invasions
ing the opening of a major shipping canal between the Don in the Great Lakes (Jude et al. 1995; Yan and Pawson 1997).
and Volga rivers, the Caspian Sea was invaded by several Clearly, statistical syntheses are needed to test the generality
Mediterranean invertebrates, including a mussel Mytilaster of biotic resistance in aquatic communities.
lineatus that caused the extinction of a confamilial endemic
mussel Dreissena caspia (Dumont 1998). Echinogammarus Conclusion
ischnus, a deposit-feeding amphipod that inhabits zebra The invasion history of the Great Lakes is explained better
mussel beds in Europe (Köhn and Waterstraat 1990), is re- by the invasional meltdown model than by the biotic resis-
placing the previously dominant amphipod G. fasciatus from tance model. Mutualistic, commensal, and asymmetric ex-
mussel-covered substrate in Lake Erie, Lake Ontario, and ploitative interactions facilitate the survival and population
the upper St. Lawrence River (Dermott et al. 1998; A. growth of many Great Lakes invaders. Direct positive inter-
Ricciardi, unpublished data). Moyle (1986) noted that North actions are more common than negative ones, and often
American cold-water lakes and streams often contain several involve species that have no co-evolutionary history. The re-
species of salmonids not co-evolved; brook trout Salvelinus cent influx of Ponto–Caspian animals suggests that Great
fontinalis, rainbow trout O. mykiss, and brown trout Salmo Lakes communities remain highly susceptible to invasion.
trutta coexist in many streams because of their differing Further colonization by Ponto–Caspian species is likely be-
temperature preferences and spawning times. Similarly, nu- cause current ballast water controls apparently cannot pre-
merous cyprinid minnows have become established in North vent the delivery of euryhaline organisms; Ricciardi and
American lakes and rivers where rich communities of native Rasmussen (1998) identified 17 additional Ponto–Caspian
cyprinids were already present (Moyle 1986). species that are probable future invaders of the Great Lakes
Unsuccessful introductions are less likely to be reported, based on their invasion histories in Europe and their likeli-
or even noticed, than successful ones; this bias could ob- hood of surviving overseas transport in ship ballast tanks.
scure evidence of communities that have resisted invasion. There is no compelling evidence that rich aquatic assem-
However, where failed introductions are documented, they blages resist invasion when organisms are introduced repeat-
are often attributable to an invader’s inability to adapt to edly. If abiotic conditions are suitable and dispersal
abiotic conditions. For example, the Chinese mitten crab opportunities exist, aquatic species will likely invade regard-
E. sinensis and the European flounder P. flesus have been less of the composition of the resident community. If biotic
frequently introduced to the Great Lakes in ship ballast resistance to establishment exists only at a low frequency of
water over the past few decades (Emery and Teleki 1978; attempted introductions, then invasional meltdown might be
MacIsaac 1999), but the environment is not saline enough a threshold effect of inoculation pressure, which is high in
for their successful reproduction. Reproducing populations aquatic systems subject to frequent ballast water discharge.
of the Asiatic clam Corbicula fluminea in western Lake Moreover, biotic resistance appears more likely to operate
Erie, southern Lake Michigan, and the St. Clair River are re- only at small scales (Levine and D’Antonio 1999), while
stricted to waters artificially heated by discharge from power invasional meltdown is hypothesized to operate at multiple
plants (Mills et al. 1993); Corbicula’s absence from most of scales—from communities to ecosystems (Simberloff and
the Great Lakes is better explained by its narrow thermal tol- Von Holle 1999).
erance rather than biotic factors. Other examples are pro- The invasional meltdown model has important implica-
vided by introduced fishes, which often fail to invade rivers tions for ecosystem management and biodiversity. If an in-
with extreme natural flow regimes (Meffe 1991; Baltz and creased frequency of introduction causes an ecosystem to be
Moyle 1993), but may do so when river flow is stabilized by more susceptible to invasion, then efforts to severely reduce
impoundment (Moyle 1986; Gido and Brown 1999). the rate of invasion are warranted. This refutes the criticism
Some studies support the hypothesis that the abundance of that resources allocated toward prevention are wasted if
an invading species is limited by resident species richness. some future invasions are inevitable. Furthermore, because
Shurin (2000) found that introduced zooplankton achieved the impact of an invader is a function of its abundance, and
higher biomasses in enclosures where the resident species because its abundance may be enhanced by facilitative inter-
biomass was artificially reduced; therefore, he concluded actions with other invaders, frequent introductions may re-
that invaders were suppressed by strong interactions with sult in synergistic impacts (Simberloff and Von Holle 1999).
resident species. Using fish exclusion cages, Robinson and Complex combinations of interactions may render these im-
Wellborn (1988) found a 29-fold reduction in the density of pacts unpredictable. Finally, although invasional meltdown
C. fluminea in the presence of a diverse assemblage of may increase local diversity through the accumulation of
molluscivores within a Texas reservoir. Conversely, only a introduced species, the continuing replacement of endemic
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2522 Can. J. Fish. Aquat. Sci. Vol. 58, 2001
species by widespread invaders will inevitably reduce diver- Dermott, R., and Kerec, D. 1997. Changes to the deepwater benthos
sity among habitats and among regions (e.g., Rahel 2000). of eastern Lake Erie since the invasion of Dreissena: 1979–1993.
Invasional meltdown may accelerate the homogenization of Can. J. Fish. Aquat. Sci. 54: 922–930.
ecosystems. Dermott, R., Witt, J., Um, Y.M., and Gonzalez, M. 1998. Distribu-
tion of the Ponto-Caspian amphipod Echinogammarus ischnus in
the Great Lakes and replacement of native Gammarus fasciatus.
Acknowledgements J. Gt. Lakes Res. 24: 442–452.
Dumont, H.J. 1998. The Caspian Lake: history, biota, structure,
I thank Hugh MacIsaac, Norm Yan, and two anonymous and function. Limnol. Oceanogr. 43: 44–52.
referees for their comments on the manuscript. Ron Dermott Edlund, M.B., Taylor, C.M., Schelske, C.L., and Stoermer, E.F. 2000.
kindly provided unpublished data on amphipod and zebra Thalassiosira baltica (Grunow) Ostenfeld (Bacillariophyta), a new
mussel densities, and Marg Dochoda provided ship traffic exotic species in the Great Lakes. Can. J. Fish. Aquat. Sci. 57:
data. Financial support from the Killam Trusts is gratefully 610–615.
acknowledged. Elton, C.S. 1958. The ecology of invasions by animals and plants.
Methuen, London.
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