What have we learned from freshwater invasions? Anthony Ricciardi Redpath Museum and McGill School of Environment McGill University, Montreal, Canada tony.ricciardi@mcgill.ca
Ten generalizations regarding aquatic invasions 1. Rates of discovery are increasing worldwide.
Rate of discovery of invaders in aquatic systems Great Lakes Baltic Sea Cumulative number of invaders San Francisco Bay Mediterranean Sea
Rates of discovery of invaders in large aquatic systems Hudson River Columbia River Modern (since 1960) Longterm (over 200 yrs) North Sea Baltic Sea Pearl Harbor Great Lakes Chesapeake Bay Port Phillip Bay, Australia San Francisco Bay Ricciardi (2006) Number of species per year
Ten generalizations regarding aquatic invasions 2. Many introductions fail to establish sustainable populations.
Barriers to species invasion Species pool: A B C D E F G Geographic barrier Physiological barrier Demographic barrier Biotic resistance Invading species: G
Nonindigenous freshwater fishes introduced to 149 regions worldwide Number of established species Slope = 0.67± 0.03 Number of introduced species
Ten generalizations regarding aquatic invasions 3. Propagule pressure is the most consistent predictor of establishment success.
Success of introduced salmonids versus propagule pressure Successful invaders Failed invaders Magnitude Introduction attempts log 10 (# individuals) Propagule pressure Colautti (2005)
Ten generalizations regarding aquatic invasions 4. All aquatic systems are invasible, but some are more invasible than others.
Impounded lakes are invaded more frequently than natural lakes Johnson et al. (2008)
Effect of land use on the proportion of endemic versus exotic fishes at 36 sites in two river basins. Scott & Helman (2001) % invaders % endemics Land use intensity (deforested area + # buildings/ha + km roads/ha)
Ten generalizations regarding aquatic invasions 5. The impacts of exotic species are context dependent.
Impacts of invasive fishes vary across regions (Data from 153 invaders) Number of regions where species is high-impact Gambusia Oreochromus affinis niloticus Ricciardi & Kipp (2008) Total number of regions invaded
Impact Abundance Abundance Environmental variable Impact Exotic species abundance Environmental variables
Effect of predation on the clam Corbicula fluminea in a Texas reservoir Corbicula density (# per Ekman sample) 100 75 50 25 3.0 2.0 1.0 Predators excluded Exposed to predators Robinson & Wellborn (1988) 0 May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar
Ten generalizations regarding aquatic invasions 6. The potential impact of an exotic species is not correlated with its invasiveness.
Invasiveness vs impact of exotic species on native species populations Rate of spread (km/yr) Ricciardi & Cohen (2007) Impact ranking
Invasiveness vs impact of exotic species on native species populations Establishment success (%) Ricciardi & Cohen (2007) Impact ranking
Invasiveness vs impact of exotic species Ricciardi & Cohen (2007)
Ten generalizations regarding aquatic invasions 7. The introduction of an uncontrolled generalist consumer often has cascading effects in aquatic food webs.
Food web of Flathead Lake (Montana, USA) Grizzly bear Bald eagle Zooplankton (cladocerans, copepods) Kokanee salmon Phytoplankton Spencer et al. (1990)
Food web of Flathead Lake (Montana, USA) after introduction of opossum shrimp Mysis relicta Grizzly bear Bald eagle Zooplankton (cladocerans, copepods) Kokanee salmon Phytoplankton Spencer et al. (1990)
Trophic cascade caused by introduced brown trout Invertebrate biomass (g m -2 ) NS * * Algal biomass (AFDM mg cm -2 ) NS Flecker & Townsend (1994) No fish Native Trout fish
The effect of Peacock Cichlid Cichla ocellaris on the food web of Gatun Lake, Panama herons & kingfishers adult Cichla young Cichla terrestrial insects phytoplankton benthic algae Before introduction After introduction Zaret & Paine (1973)
Seasonal abundance of malarial mosquitoes near Gatun Lake 7000 Number of mosquitoes 5000 3000 1000 1969 1970 1971 Post-invasion 1968 Pre-invasion 0 Month Zaret & Paine (1973)
Lake trout Minnows Zooplankton Reference lake Pelagic Littoral Bass Lake trout Minnows Zooplankton Invaded lake Pelagic Littoral Vander Zanden et al. (1999)
Lake trout response to smallmouth bass removal: Changes in proportion of prey in lake trout diet Littoral prey Pelagic prey Profundal prey Diet proportion Lepak et al. (2006) Year Bass removal
Ten generalizations regarding aquatic invasions 8. The largest impacts are caused by species introduced to systems where no similar species exist.
Impact of exotic trout on frogs (Rana muscosa) in alpine lakes in California Knapp et al. (2001) Frog abundance # frogs/ m of shoreline % lakes containing frogs
Impact of Nile perch (Lates niloticus) on Lake Victoria cichlids Catch of native cichlids vs Nile perch Cichlids Nile perch Kaufman et al. (1992)
Impact of sea lamprey on lake trout in the Great Lakes Lake trout production (10 3 tonnes) 3 2 1 0 3 2 1 0 3 2 1 0 1930 Lamprey invade Lake Huron Lake Michigan Lake Superior 1935 1940 1945 1950 1955 1960 1965 Lawrie (1970)
Causes of freshwater fish extinctions in North America Physical habitat alteration Exotic species invasions 68% 73% Pollution Hybridization 38% 38% Overfishing 15% Miller (1989)
High-impact invaders tend to belong to novel taxa Low-impact spp High-impact spp Rhine River NS (p=0.49) Lake Biwa NS (p=0.23) Potomac River NS (p=0.07) Hudson River p=0.0007 Great Lakes p=0.00002 Proportion of genera that are novel After Ricciardi & Atkinson (2004) Fisher s Combined Test: 2 = 45.8, P<0.0001
Colonization of the Great Lakes by invaders from the Black Sea
Impacts of inter- vs intra-continental invasions California fishes Dill & Cordone 1997; Knapp & Matthews 2000; Moyle 2002 Great Lakes fishes Mills et al. 1993; Crawford 2001 NS NS Inter Intra Mammals (global) Long 2003 p<0.05 Ricciardi & Simberloff (2009) % invaders with strong impacts
Ten generalizations regarding aquatic invasions 9. The invasion history of a species is the best predictor of its invasiveness and impact.
Ecosystem impacts of the zebra mussel = increase, = decrease
Effects of Dreissena on invertebrate communities (as revealed by meta-analysis) negative effect positive effect Ward & Ricciardi (2007)
Declines in N. American native mussel populations following zebra mussel invasion % Pre-invasion density Upper St. Lawrence Lake Erie Lake St. Clair Rideau Canal Hudson River After Strayer & Malcom (2007) Years since invasion
Native mussel mortality versus zebra mussel fouling in North America % Recent mortality 100 80 60 40 20 sin -1 (y 0.5 ) = 0.5 log x +1.03 R 2 = 0.75 P <0.0001 0 0.01 0.1 1 10 Fouling intensity (zebra mussel mass / native mussel mass) Ricciardi (2003)
Ten generalizations regarding aquatic invasions 10. Synergistic effects may result from the interactions of multiple invaders.
Facilitation of alewife invasion by sea lamprey in the Great Lakes Lawrie (1970); Kitchell & Crowder (1986) + Sea lamprey - + - + Lake trout Alewife
Facilitation of bullfrog invasion of ponds by nonindigenous fish Adams et al. (2003) - + Bluegill + + - Dragonfly nymphs (Aeshnids) Bullfrog tadpoles
Facilitation of exotic plants by zebra mussels Skubinna et al. (1995); Vanderploeg et al. (2002) suspended solids phytoplankton Water clarity Filtration
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 Round goby Waterfowl Zebra & Quagga mussels Clostridium botulinum
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