Anthony Ricciardi
Redpath Museum and McGill School of Environment
McGill University, Montreal, Canada
What have we learned from
freshwater invasions?
1. Rates of discovery are increasing
worldwide.
Ten generalizations
regarding aquatic invasions
Cum
ula
tive n
um
ber
of
invaders
Rate of discovery of invaders in aquatic systems
Great Lakes Baltic Sea
San Francisco Bay Mediterranean Sea
Rates of discovery of invaders in large aquatic systems
San Francisco Bay
Port Phillip Bay, Australia
Pearl Harbor
Great Lakes
Baltic Sea
Hudson River
Columbia River
Chesapeake Bay
North Sea
Number of species per year
Longterm (over 200 yrs)
Modern (since 1960)
Ricciardi (2006)
2. Many introductions fail to establish
sustainable populations.
Ten generalizations
regarding aquatic invasions
Geographic barrier
G Invading species:
Barriers to species invasion
Biotic resistance
Demographic barrier
Physiological barrier
B D E G A C F Species pool:
Num
ber
of
esta
blis
hed s
pecie
s
Number of introduced species
Slope = 0.67± 0.03
Nonindigenous freshwater fishes
introduced to 149 regions worldwide
3. Propagule pressure is the most
consistent predictor of establishment
success.
Ten generalizations
regarding aquatic invasions
Propagule pressure
Introduction
attempts
log10 (# individuals)
Success of introduced salmonids
versus propagule pressure
Successful invaders
Failed invaders
Colautti (2005)
Magnitude
4. All aquatic systems are invasible,
but some are more invasible than
others.
Ten generalizations
regarding aquatic invasions
Johnson et al. (2008)
Impounded lakes are invaded more frequently
than natural lakes
% invaders
%
endem
ics
Effect of land use
on the proportion
of endemic versus
exotic fishes
at 36 sites in two
river basins.
Scott & Helman (2001)
Land use intensity (deforested area + # buildings/ha + km roads/ha)
5. The impacts of exotic species are
context dependent.
Ten generalizations
regarding aquatic invasions
Num
ber
of
regio
ns
where
specie
s is ‘hig
h-im
pact’
Total number of regions invaded
Impacts of invasive fishes vary across regions (Data from 153 invaders)
Oreochromus niloticus Gambusia affinis
Ricciardi & Kipp (2008)
Impact
Exotic species
abundance
Environmental
variables
Ab
un
dan
ce
Environmental variable
Imp
act
Abundance
Effect of predation
on the clam
Corbicula fluminea
in a Texas reservoir
Robinson & Wellborn (1988)
1.0
2.0
3.0
0
25
50
75
100
May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar
Predators excluded
Exposed to predators C
orb
icu
la d
ensity (
# p
er
Ekm
an s
am
ple
)
6. The potential impact of an exotic
species is not correlated with its
invasiveness.
Ten generalizations
regarding aquatic invasions
Impact ranking Ricciardi & Cohen (2007)
Rate
of
spre
ad (
km
/yr)
Invasiveness vs impact of exotic species
on native species populations
Esta
blis
hm
ent
success (
%)
Impact ranking Ricciardi & Cohen (2007)
Invasiveness vs impact of exotic species
on native species populations
Invasiveness vs impact of exotic species
Ricciardi & Cohen (2007)
7. The introduction of an uncontrolled
generalist consumer often has
cascading effects in aquatic food webs.
Ten generalizations
regarding aquatic invasions
Phytoplankton
Kokanee salmon
Bald eagle
Zooplankton (cladocerans, copepods)
Food web of Flathead Lake (Montana, USA)
Grizzly bear
Spencer et al. (1990)
Phytoplankton
Kokanee salmon
Bald eagle
Zooplankton (cladocerans, copepods)
Grizzly bear Mysis relicta
Food web of Flathead Lake (Montana, USA)
after introduction of opossum shrimp
Spencer et al. (1990)
Flecker & Townsend (1994)
No fish Native Trout
fish
Alg
al
bio
mass
(A
FD
M m
g c
m-2
)
Invert
eb
rate
bio
mass
(g m
-2)
NS
*
*
NS
Trophic cascade caused by introduced brown trout
Before introduction After introduction
phytoplankton benthic algae
young
Cichla
adult
Cichla
terrestrial insects
herons & kingfishers
The effect of Peacock Cichlid Cichla ocellaris
on the food web of Gatun Lake, Panama
Zaret & Paine (1973)
1968 Pre-invasion
1971 1970
1969
Num
ber
of
mosquitoes
Month
Post-invasion
Seasonal abundance of malarial mosquitoes
near Gatun Lake
7000
5000
3000
1000
0
Zaret & Paine (1973)
Invaded lake
Reference lake
Minnows
Lake trout
Zooplankton
Bass
Zooplankton
Minnows
Vander Zanden
et al. (1999)
Lake trout
Pelagic Littoral
Pelagic Littoral
Bass removal Lepak et al. (2006)
Lake trout response to smallmouth bass removal:
Changes in proportion of prey in lake trout diet
Littoral prey
Profundal prey
Pelagic prey
Die
t pro
port
ion
Year
8. The largest impacts are caused by
species introduced to systems where
no similar species exist.
Ten generalizations
regarding aquatic invasions
Impact of exotic trout
on frogs (Rana muscosa)
in alpine lakes in
California
Knapp et al. (2001)
Fro
g a
bu
nd
an
ce
% l
akes c
on
tain
ing
fro
gs
# f
rogs/
m o
f shore
line
Impact of Nile perch (Lates niloticus)
on Lake Victoria cichlids
Kaufman et al. (1992)
Nile perch
Cichlids
Catch of native cichlids vs Nile perch
Impact of sea lamprey
on lake trout in the
Great Lakes
Lawrie (1970)
1935 1940 1945 1950 1955 1960 1965 1930
0
1
2
3
0
1
2
3
0
1
2
3 Lake t
rout
pro
duction
(10
3 t
onnes)
Lake Huron
Lake Michigan
Lake Superior
Lamprey
invade
Causes of freshwater fish extinctions
in North America
73%
68%
38%
15%
38%
Physical habitat alteration
Exotic species invasions
Pollution
Hybridization
Overfishing
Miller (1989)
High-impact invaders tend to belong to novel taxa
Rhine River
Lake Biwa
Potomac River
Hudson River
Great Lakes
Low-impact spp High-impact spp
Proportion of genera that are novel
p=0.00002
p=0.0007
NS (p=0.07)
NS (p=0.23)
NS (p=0.49)
Fisher’s Combined Test: 2 = 45.8, P<0.0001 After Ricciardi & Atkinson (2004)
Colonization of the Great Lakes
by invaders from the Black Sea
Impacts of inter- vs intra-continental invasions
Inter
Intra
% invaders with strong impacts
Mammals (global)
Great Lakes fishes
California fishes Dill & Cordone 1997; Knapp & Matthews 2000; Moyle 2002
Mills et al. 1993; Crawford 2001
Long 2003
NS
NS
p<0.05
Ricciardi & Simberloff (2009)
9. The invasion history of a species is
the best predictor of its invasiveness
and impact.
Ten generalizations
regarding aquatic invasions
Ecosystem impacts of the zebra mussel
= increase, = decrease
positive effect negative effect
Effects of Dreissena on invertebrate communities (as revealed by meta-analysis)
Ward & Ricciardi (2007)
After Strayer & Malcom (2007) Years since invasion
% P
re-invasio
n d
ensity
Declines in N. American native mussel populations
following zebra mussel invasion
Upper St. Lawrence
Lake Erie
Lake St. Clair
Rideau Canal
Hudson River
Ricciardi (2003)
% R
ecent
mort
alit
y
0
20
40
60
80
100
10 1 0.01 0.1
R2 = 0.75
P <0.0001
sin-1(y0.5) = 0.5 log x +1.03
Fouling intensity (zebra mussel mass / native mussel mass)
Native mussel mortality versus zebra mussel fouling in North America
10. Synergistic effects may result from
the interactions of multiple invaders.
Ten generalizations
regarding aquatic invasions
Alewife
-+
+
Facilitation of alewife invasion
by sea lamprey in the Great Lakes
Lake trout
Sea lamprey
-
+
Lawrie (1970); Kitchell & Crowder (1986)
Facilitation of bullfrog invasion of ponds
by nonindigenous fish
Bluegill
-
+
-+
+
Bullfrog tadpoles Dragonfly nymphs
(Aeshnids)
Adams et al. (2003)
Facilitation of exotic plants by zebra mussels
phytoplankton
suspended solids • • • • • •
• • •
• • •
Filtration
Water
clarity
Skubinna et al. (1995); Vanderploeg et al. (2002)
Dreissenid mussel activities forced the
James A. Fitzpatrick nuclear reactor at Oswego, N.Y.
to shut down 3 times in Fall 2007
Cladophora (filamentous algae)
Recent outbreaks of avian botulism
in the Great Lakes
• > 90,000 birds (fish-eating
waterfowl) killed since 1999
• Also affects benthic fishes
• Cause: Type-E botulism from
dreissenid mussels
Transfer of botulism from dreissenid mussels
to fish & birds in Lake Erie
Clostridium botulinum
Round goby Waterfowl
Zebra & Quagga mussels
Conclusions
• All aquatic systems are invasible, given
sufficient propagule pressure.
• An invader’s impacts are context dependent,
but its invasion history may reveal patterns.
• Ecologically-distinct invaders are more likely
to disrupt food webs.
• Multiple invaders may interact synergistically.
Acknowledgements
• Natural Sciences and Engineering Research
Council (Canada)
• Canadian Aquatic Invasive Species Network
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