what have we learned from freshwater invasions? · what have we learned from freshwater invasions?...

Anthony Ricciardi

Redpath Museum and McGill School of Environment

McGill University, Montreal, Canada

tony.ricciardi@mcgill.ca

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