Non-indigenous Species

or exotic-, alien-, invasive-, non-native, foreign, harmful...

a global problem

What is non-indigenous species?

• Non-indigenous species are organism that occurs outside their native range

• Non-indigenous organisms can be viruses, bacteria, animals, plants, marine, terrestrial, etc.. even man

• This lecture focuses mainly on aquatic invaders

Why worry?

Cohen AN, Carlton, J.T. (1998)

Number of aquatic invaders in San Francisco

Bay

Number of marine invaders North America

Ruiz GM, Fofonoff PW et al (2000)

1. Global problem

2. After habitat destruction the leading cause of species extinction

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Ribera Siguan, M.A., 2002.

What’s the problem ?

• “Invader” can harm the invaded ecosystem through:– Resource competition with local species– Preying on local species– Carrying diseases which harm local wildlife– Secondary impacts

• “Invader” can affect humans– Economic impact through fisheries, shell fisheries,

biofouling and tourism– Spread of human diseases

McNeely JA, Mooney HA, et al (2001)

How does an invasion happen?

• Any movement by humans can be a potential vector

• Common ways of introductions are:– intended introduction for economic or “beneficial” purpose– release/escape from “captivity” – accidental transport within other material – breaching of natural barriers– ballast water and ship fouling communities

Multitude of vectors

Example of ratio for the different vectors for non-native plants in the Mediterranean Sea

aquarium

oyster transfer

algae culture

ballast

fouling

fishing

Suez Canal

Ribera Siguan, M.A., 2002.

Number of invasions caused by which vector on the North American coast

Ruiz GM, Fofonoff PW et al (2000)

The brown tree snake (Boiga irregularis)

• Its native in Australia and was introduced accidentally in the 1950’s• Overall responsible for the extinction of 3 out of 4 pelagic birds; 9

out of 13 forest birds; 3-5 out 12 reptile species on the Island of Guam.

• This snake caused the extirpation or serious reduction of most of the island's 25 resident bird species on the main island of Guam.

• Twelve species were likely extirpated as breeding residents on the main island, 8 others experienced declines of greater than or equal to 90% throughout the island or at least in the north, and 2 were kept at reduced population levels during all or much of the study.

• Declines of greater than or equal to 90% occurred rapidly, averaging just 8.9 years along three roadside survey routes combined and 1.6 years at a 100-ha forested study site.

Wiles GJ, Bart J, et al (2003) Fritts TH, Rodda GH (1998)

Nile Perch (Lates niloticus)

• Introduced to Lake Victoria in 1954 to increase fish yield

• Caused extinction of 200+ endemic fish species through predation, and competition

• Fish caused indirect increased erosion on land, causing higher nutrient levels in the lake.

Hauser L, Carvalho GR, Pitcher T, Oguto-Ohwayo R (1998)

Water Hyacinth (Eichhornia crassipes)

• Introduced as ornamental plant around the world• Now in 50 countries on 5 continents including US• In California it replaced the native pennywort (Hydrocotyle

umbellata) which occupies a similar habitat, leading to a marked decrease in invertebrate communities

• Limits water transport, reduces oxygen and light levels in the water

• Biological control used successfully against water hyacinth in some cases (water hyacinth weevil Neochetina spp.)

Albright TP, Moorhouse TG, et al 2004 / Toft JD, Simenstad CA, et al (2003)

Caulerpa Seaweed (Caulerpa taxifolia)

• Introduced into Mediterranean by Monaco Aquarium in 1984 by dumping aquarium waste into the sea.

• Hardier clone than the tropical species which seemed to have developed in the aquarium.

• Smothers natural seagrass beds while being toxic to herbivores• Spreads via small fragments or planktonic zygotes attached to anchors, ropes, nets or

boats• By 2000 covered 131km2 in several Mediterranean countries.• Bio-control attempts using tropical seaslugs were made but unsuccessful so far.• Recently it was discovered and eradicated (?) along the Californian coast, as well as

near Sydney.Meinesz A, Belsher T,et al 2001 / Thibaut T, Meinesz A

Meinesz A, Belsher T,et al 2001

Common crab (Carcinus maenas)

• Introduced to USA as early as 1800s on northern east coast, recently in California

• Competes with native molluscs and crustaceans for food and/or eats them

• Impact on oyster culture and local crab fishery

• Estimated annual damage in US $44 million

Grosholz ED, Ruiz GM (1996) / Audet D, Davis DS, Miron G, et al., (2003).

Zebra mussel (Dreissena polymorpha)

• Spread from its native range in the Baltic Sea via ballast water

• Spreads in Europe and North America• Kills native molluscs, changes ecosystems and

causes major biofouling• Estimated annual damage in US $3 billion

Napela T.F., Schloesser, D.W., 1992

Zebra mussel distribution in North America

Is an invasive meltdown occurring in the Great Lakes?

• It has been suggested that Ponto-Caspian foodwebs are being reconstructed in the Great Lakes

• Large zebra mussel populations provide habitat for the invasive round goby

• The invasive Echinogammarus is a deposit feeder living within zebra mussel clumps

• The invasive hydroid Cordylophora caspia markedly increased in population densities after the arrival of the zebra mussel

• The increase of water clarity by the filter feeding zebra mussels fascilitates native and invasive macrophytes, which provides substrate for juvenile mussels

Ricciardi A, Maclsaac HJ (2000)

North American Crayfish (Pacifastacus leniusculus)

The North American Crayfish has been introduced to Great Britain to replace the fisheries for the native species Austropotamobius pallipes, supported by governmental funds.

The North American Crayfish is more aggressive and larger and ejects the native crayfish out of its shelters

North American Crayfish carry the fungal Crayfish plague which has little effect on the invader but kills many native European crayfish

Holdich DM, Reeve ID (1991) Soederbaeck B (1991)

‘Jellyfish’ in the Black Sea

In the 1960’s the jellyfish eating mackerel (Scomber scombrus) became rare due to over-fishing and eutrophication.In the 1980 the resident Aurelia aurita reached 300-500 million tons biomass, making it the top-water column predator.In the late 1980’s the more euryhaline Mnemiopsis leidyi got introduced from the Atlantic via ballast water, and replaced Aurelia during a period of lowered salinity reaching 300-500 ind/m3.During the same period commercial fisheries in the Black Sea crashed, most likely due to a combination of comb jelly predation on juvenile fish and overfishingAnother accidentally introduced ctenophore, Beroe ovata, seems to reduce number of Mnemiopsis in some areas by predation, but the long term effect has to be established

Guseinov MK, Osmanov MM, Guseinov KM(2005) / Mills CE (2001)

Californian cordgrass Spartina foliosa, and its non-native sibling species Spartina alterniflora.

• The Californian native S. foliosa is a wetland species with low tolerance to tidal submersion.

• S. alterniflora was introduced in the 1970’s purposely in San Francisco bay.

• It is larger, faster growing and has a high tolerance to submersion and therefore survives lower on intertidal mudflats.

• This has detrimental effects on humans as well as birds, fish, and native and cultivated shellfish by replacing open mudflats with dense cordgrass stands

• Hybrids of both species were observed which could out-compete the native species in its original habitat

• The delphacid planthopper Prokelisia marginata was recently introduced into Willapa Bay, Washington for biological control of S. alterniflora with some success.

Ayres DR, Garcia-Rossi D, et al(1999) / Grevstad FS, Strong DR, et al (2003).

The invasion history of Cercopagis pengoi in the Great Lakes

Native to the Caspian and Black Sea, the Sea of Azov, and Aral Lake

Spread to the Baltic Sea and the lower Rhine via canals opened in the 19th century

In 1998 it was found in Lake Ontario, since then it has spread to Lake Michigan, Lake Erie, Muskegon Lake and the finger lakes (NY)

It reduces the native zooplankton community significantly

mtDNA markers were used to assess the source of the North American population

A severe genetic bottleneck was foundCristescu MEA, Hebert PDN, et al (2001) / MacIsaac HJ, Grigorovich IA, et

al(1999)

Cercopagis pengoi

Cristescu MEA, Hebert PDN, et al (2001)

The Chinese mitten Crab, Eriocheir sinensis• Spread from China to Europe in 1912 were it reached a widespread

distribution by the 1930’s• In the 1990’s it arrived in San Francisco bay and reached high

population levels there• European population is most likely caused by ballast water

introductions, but this species is also a valuable aquaculture organism

Herborg L-M, Rushton SP, et al (2003)

Eriocheir sinensis• Microsatelite study showed a

population bottleneck in all European populations.

• A mt DNA study found that the Californian population is closer related to the European ones than the Native ones.

• This has important management implications. PCA 1

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Elbe

Schelde

Malaeren

Thames

Weser

Tagus

Hanfling B, Carvalho GR, et al (2002) / Herborg L-M, Rushton SP, et al (2003)

The paradox of the Argentine Ant (Linepithema humile)

• The Argentinean Ant was introduced to the US in 1891 and spread by 1907 to California.

• Once established this species replaced almost all native ant species, which is in contrast with its behaviour in the native range

• In the native range this species shares it habitat with other ant species and strongly compete between con-specific colonies.

Tsutsui ND, Suarez AV, et al (2000)

The invasion of the brown anole lizard, Anolis sagrei.

• Native to Cuba, with several distinct populations.• Invaded Florida, Hawaii and several other locations in

the last century.• Genetic diversity actually increased in the invasive

populations versus the native populations.

Sequence divergence

mean 1.7%

mean 3.5%

Kolbe, Glor et al, 2004

Summary

• Many different vectors can lead to an introduction

• The types of impact can be as far reaching as remodelling a whole ecosystem

• Genetics can identify source populations, vectors and propagule supply

• The degree of genetic diversity varies widely between invaders

References

Vectors

Impacts• Ribera Siguan, M.A., 2002. Review of non-native plants in the Mediterannean SeaIn: Leppaekoski E, Gollasch S,

Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and managment. Kluwer Academic Publishers, pp 217-231

• Guseinov MK, Osmanov MM, Guseinov KM(2005). Characteristics in the pelagic ecosystem of the Dagestan region of the Caspian Sea under the impact of the ctenophore Mnemiopsis leidyi (A-agassiz) OCEANOLOGY 45 (1): 62-65

• Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451: 55-68

• Bilio M, Niermann U (2004) Is the comb jelly really to blame for it all? Mnemiopsis leidyi and the ecological concerns about the Caspian Sea. MARINE ECOLOGY-PROGRESS SERIES 269: 173-183

• Soederbaeck B (1991) Interspecific dominance relationship and aggressive interactions in the freshwater crayfishes Astacus astacus (L.) and Pacifastacus leniusculus. Canadian Journal of Zoology 69: 1321-1325

• Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: Lessons from the multiple invasions of the European green crab Carcinus maenas. Biological Conservation 78: 59-66

• Toft JD, Simenstad CA, Cordell JR, Grimaldo LF (2003). The effects of introduced water hyacinth on habitat structure, invertebrate assemblages, and fish diets. ESTUARIES 26 (3): 746-758

• Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of Island ecosystems: A Case History of Guam. Annual Review of Ecology and Systematics 29: 113-140

• Ricciardi A, Maclsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology & Evolution 15: 62-65

Genetics• Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological

invasion by a Cuban lizard. Nature 431: 177-181• Cristescu MEA, Hebert PDN, Witt JDS, MacIsaac HJ, Grigorovich IA (2001) An invasion history for Cercopagis pengoi

based on mitochondrial gene sequences. Limnology and Oceanography 46: 224-229• Hanfling B, Carvalho GR, Brandl R (2002) mt-DNA sequences and possible invasion pathways of the Chinese mitten

crab. Marine Ecology-Progress Series 238: 307-310• Ayres DR, Garcia-Rossi D, Davis HG, Strong DR (1999) Extent and degree of hybridization between exotic (Spartina

alterniflora) and native (S-foliosa) cordgrass (Poaceae) in California, USA determined by random amplified polymorphic DNA (RAPDs). Molecular Ecology 8: 1179-1186

• Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America 97: 5948-5953

• Hauser L, Carvalho GR, Pitcher T, Oguto-Ohwayo R (1998) Genetic affinities of an introduced predator: Nile perch in Lake Victoria, East Africa. Molecular Ecology 7: 849-857

Spread / Distribution• Holdich DM, Reeve ID (1991) Distribution of Fresh-Water Crayfish in the British-Isles, with Particular Reference to Crayfish Plague,

Alien Introductions and Water-Quality. Aquatic Conservation-Marine and Freshwater Ecosystems 1: 139-158• Audet D, Davis DS, Miron G, et al., (2003). Geographical expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova

Scotian shore into the southeastern Gulf of St. Lawrence, Canada. JOURNAL OF SHELLFISH RESEARCH 22 (1): 255-262• Meinesz A, Belsher T, Thibaut T, Antolic B, Mustapha KB, Boudouresque C, Chiaverini D, Cinelli F, Cottalorda JM, Djellouli A, El Abed

A, Orestano C, Grau AM, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, de Vaugelas J, Zavodnik N, Zuljevic A (2001) The Introduced Green Alga Caulerpa taxifolia Continues to Spread in the Mediterranean. Biological Invasions 3: 201-210

• Albright TP, Moorhouse TG, McNabb J 2004. The rise and fall of water hyacinth in Lake Victoria and the Kagera River Basin, 1989-2001. JOURNAL OF AQUATIC PLANT MANAGEMENT 42: 73-84

• MacIsaac HJ, Grigorovich IA, Hoyle JA, Yan ND, Panov VE (1999) Invasion of Lake Ontario by the Ponto-Caspian predatory cladoceran Cercopagis pengoi. Canadian Journal of Fisheries and Aquatic Sciences 56: 1-5

• Herborg L-M, Rushton SP, Clare AS, Bentley MG (2003) Spread of the Chinese mitten crab (Eriocheir sinensis, H. Milne Edwards) in Continental Europe: analysis of a historical data set. Hydrobiologia 503: 21-28

• Wiles GJ, Bart J, Beck RE, Aguon CF (2003). Impacts of the brown tree snake: Patterns of decline and species persistence in Guam's avifauna.  CONSERVATION BIOLOGY 17 (5): 1350-1360

• Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: Apparent patterns, processes, and biases. Annual Review of Ecology and Systematics 31: 481-531

Control / Managment• Thibaut T, Meinesz A, Amade P, Charrier S, De Angelis K, Ierardi S, Mangialajo L, Melnick J, Vidal V 2001. Elysia subornata (Mollusca)

a potential control agent of the alga Caulerpa taxifolia (Chlorophyta) in the Mediterranean Sea. JOURNAL OF THE MARINE BIOLOGICAL ASSOCIATION OF THE UNITED KINGDOM 81 (3): 497-504

• McNeely JA, Mooney HA, Neville LE, Schei P, Waage JK (2001) A Global Strategy on Invasive Alien Species. IUCN Gland, Switzerland, and Cambridge, U.K., in collaboration with the Global Invasive Species Programme.

• Grevstad FS, Strong DR, Garcia-Rossi D, Switzer RW, Wecker MS (2003). Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results BIOLOGICAL CONTROL 27 (1): 32-42

Further reading:

• Alexander Meinesz, 1999. “Killer Algae”, p1-360, The University of Chicago Press.• Napela T.F., Schloesser D.W. eds, 1992. Zebra mussels, biology, impacts, and control,Lewis Publishers