1. Available at http://planet.uwc.ac.za/nisl Threats to biological diversity 3: Exotic Species Vanessa Couldridge & Sam Hopkins Biodiversity & Conservation Biology Department Matteo Garbelotto University of California

2.  The Invasion Biology course discusses exotic species in detail.  Rather than repeat everything, the following examples of invasive species have been selected for discussion:  Rinderpest  The black rat (Rattus rattus)  The toad/platanna – Xenopus laevis  Chestnut blight Introduction

3.  Viral disease that affects primarily cattle (also known as cattle plague)  All cloven-hoofed wild and domestic are animals susceptible to the disease  Belongs to the genus Morbillivirus  Affects gastrointestinal and respiratory systems  Highly contagious and usually fatal; it can wipe out entire populations  Death occurs 6-12 days after the first symptoms http://www.virology.net Rinderpest

4.  Introduced to Africa from Asia in 1887  Disease was present in Indian cattle imported to the east coast of Africa to feed the Italian army, which was invading Ethiopia at the time  Quickly spread to local cattle and wildlife populations  From there the disease swept across eastern and southern Africa, with devastating consequences  Within 10 years it had reached South Africa Rinderpest: Introduction to Africa

5.  This map shows the spread of the disease across the African continent  The fauna and flora of Africa south of the Sahara changed completely as a result Rinderpest: Spread in Africa

6.  Millions of animals died, both wild and domestic  Reports indicate more than 90% of cattle and wildebeest were wiped out http://www.Aleffgroup.com Rinderpest: Plague of 1890s

7.  Wildlife killed by rinderpest included wildebeest, buffalo, giraffe, warthog, eland, kudu, and other buck species  Predators also suffered as their prey species disappeared; lions reportedly became man- eaters  Pastoralists depending on cattle for their livelihood faced severe hardship and death  Ox-wagon transport was brought to a standstill  Loss of grazers transformed the landscape Rinderpest: Devastation Caused

8.  The disease was eventually brought under control through early attempts at vaccination and natural immunity among surviving animals  In the early 1960s a more reliable vaccine was developed and between 1962 and 1976 there was a large-scale attempt to eradicate rinderpest entirely from Africa through mass vaccination  This was largely successful – 15 out of 17 countries were freed of the disease  Outbreaks still occur from time to time, but none as severe as the original plague of the 1890s Rinderpest: Control

9.  Vaccination of cattle in the 1960s eliminated rinderpest from wildlife populations, as cattle could no longer act as a reservoir for the disease  Wildebeest numbers in the Serengeti increased by about six-fold over a period of 15 years; Buffalo numbers also increased dramatically http://geoimages.berkeley.edu Rinderpest: Recovery

10.  This had an impact on the environment by changing grassland into woodland – an increase in grazers eliminated the fuel for fires that control tree growth. Fires are now less frequent and do not burn as hot 19802003 http://www.circa.gbif.net/Public/irc/gbif/pr/library?!=/ science_symposia/2006/mduma_ppt/_EN_1.0_&a=d Rinderpest: Landscape Change

11.  Ironically, it has been suggested that eradication of rinderpest has led to an increase in canine distemper among lions  Lions feeding on wildebeest infected with rinderpest may have gained immunity to canine distemper, since the two viruses are very similar to each other (both Morbilliviruses) http://www.eecs.umich.edu Rinderpest and Canine Distemper

12.  The Black Rat (Rattus rattus) was originally from Asia  It made its way to the near East in Roman time  It was in Europe in the 8 th century  From Europe it had a boat ticket to the rest of the world  Rats are nocturnal  Rats are omnivorous  They are good breeders The Rat 1

13.  The rat and a number of other rodents are largely responsible for out breaks of plague through history  Humans as carriers of rats also participated in the spread of the disease  Often the rats would then infect native rodents with the disease The Rat and the plague 2

14.  An early example is the plague of Justintian 3  544, The first great plague 4  1348, Black Death 5  1665, Great Plague 6  1899, Plague in South Africa 7  Recent plague – 2005/ 2006 DRC 8,9 History of the Plague

15.  Lundy island is off the coast of North Devon, UK  Rats reached the island 200 years ago  Rat numbers reached 40,000  Extermination started in 2003  Puffin and Manx Shearwater numbers had declined  Now rats gone, hopefully bird numbers will increase Other effects of rat invasion – Lundy Puffins 10, 11

16.  Reached Pacific Islands in the 17 th century  Now established on 28 groups of islands  Eat native snails, beetles, spiders, moths, stick insects, and fruit, eggs and young of birds  Largest threat to the Rarotonga flycatcher  Other Island birds affected  Sooty terns, Seychelles  Bonin Petrels, Hawaii  Galapagos dark-rumped petrels Galapagos islands  White tailed tropic birds Bermuda Other effects of rat invasion – Pacific Islands 12,13

17.  Xenopus laevis is the common platanna in Southern Africa  It is mainly aquatic  Females reach 130 mm  Eats insects, small fish, young and larvae of its own species or other species of frogs  Adults can breed more than once per season The Toad – Xenopus laevis 14

18.  Xenopus laevis is found about the world owing to  Lab animals  Pet trade  Pregnancy tests  These animals escape and can form viable populations  Now found in USA, Chile, Mexico, France, Indonesia and the UK  These frogs are a great invader owing to  Good in disturbed environments  Has a varied diet  High reproductive rate  High salt tolerance  Disease resistant  Can move overland or through rivers and streams The Toad – Xenopus laevis 14

19.  Xenopus laevis are a problem because they  Predate upon and compete with native species  Are toxic to predators  Make water turbid The Toad – Xenopus laevis 14

20.  Seen in Southern California  X. laevis has been present since the 1960s  Preys on the Tide Water Goby  Preys on the Endangered Red-legged frog  Also managed to establish parasites that need alternate hosts 15  In South Wales, Xenopus were found to have a very varied diet ranging from zooplankton to bank voles to Xenopus eggs 16 The Toad – Xenopus laevis

21.  In South Africa X. laevis is an invasive  Animals are moved out of their natural range by fisherman  Animals make use of the habitat disturbed by humans  Have hybridized with Xenopus gilli The Toad – Xenopus laevis 17

22. Chestnut Blight (Cryphonectria parasitica)

23. The American Chestnut (Castanea dentata)

24. American Chestnut: Range  Maine to Georgia and west to Ohio and Tennessee. (Braun, 1950)  Commonly made up 25% or more of mixed stands  Formed pure stands on many dry Appalachian ridgetops and near densely populated areas. Map of Historical Range of Castanea dentata (Saucier, 1973)

25. American Chestnut: Habitat  Common on midslopes and other moderately dry soils  Shared moist meso-phytic soils with many other species  Tap root 4 to 5 ft down

26. “Redwoods of the East”  Mature chestnuts could be 600 years old and average up to five feet in diameter and 100 feet tall  Many specimens of 8 to 10 feet in diameter were recorded

27. American Chestnut: Ecological Importance  Wildlife depended on the abundant crop of chestnuts  Many species of insects fed on the leaves, flowers, and nuts

28. American Chestnut: Economic Importance  Throughout much of the range chestnut had the most timber volume of any species  Half the standing timber volume of CT  Was the major source of tannin for leather pro- duction (6-11 % tannin content)  Chestnuts

29. “From cradle to casket…”  Fast growing  reached half ultimate height by 20 th year  Resistant to decay  Straight and tall  often branch free for 50 feet  Only white pine & tulip poplar could grow taller

30. “From cradle to casket…”  Posts & railroad ties  Telephone poles (65 feet)  Construction  Fuel  Fine furniture & musical instruments

31. American Chestnut: Economic Importance  Scientific forest management in the US was just getting started when the country lost its most important hard wood species (Smith, 2000)  Foresters had begun to develop comprehensive plans for intensive management

32.  Near densely populated areas Chestnut often formed nearly complete stands  due to rapid growth from stump sprouts  repeated coppicing for fuelwood

33.  Experts estimate that American Chestnut represented half the commercial value of all Eastern North American hardwoods Pure stand of Chestnut in CT 90 years after clear-cutting, 1905.

34. “… the most valuable and usable tree that ever grew in the Eastern United States.”

35. Introduction of Cryphonectria parasitica  In 1904, Herman Merkel, a forester at the New York Zoological Garden, found odd cankers on American chestnut trees in the park

36. Introduction of Cryphonectria parasitica  "rapid & sudden death of many branches stems & trees"

37. Introduction of Cryphonectria parasitica  American Chestnut produces a sweet but small nut  Chinese chestnut produces a large but generally tasteless nut

38. Introduction of Cryphonectria parasitica  Thomas Jefferson  imported European or Spanish chestnut (Castanea sativa)  grafted it onto native root stocks at Monticello.  In 1876, a nurseryman in Flushing, NY, imported the Japanese chestnut (C. crenata).  More were brought over in 1882 and 1886.  Chinese chestnut (C. Molissima) was brought here from Ichang in 1900.  to hybridize for ornamentals and nut production

39. Cryphonectria parasitica  Ascomycete  Produces both conidia & ascospores  Pycnidia stromata break through the lenticels and produce conidia and perithecia producing ascospores are formed

40. Cryphonectria parasitica: Life Cycle

41. Dispersal  Animals and insects  Ascospores are shot into the air after rain storms in the fall  Rain (conidia)

42.  Infects trunk and branches  Only above ground parts of trees active growth & sporulation

43. How does it kill the tree?  Enters through fissures or wounds in the bark  Grows in and under the bark, girdling the cambium.  Kill the tree above the point of infection.

44.  Causes swollen or sunken orange-colored cankers on the limbs and trunks of the chestnut trees.

45. How does it kill the tree?  The leaves above the point of infection die, followed by the limbs.  Within two to ten years the entire tree is dead.  Not uncommon to find many cankers on one tree

46. How does it kill the tree?  The fungus has girdled the tree and is producing yellow conidia asexual spores

47. Host Range  Like most cankers - fairly specific host range  Serious pathogen: American & European (infects Japanese and Chinese much less)  Moderate pathogen: Chinquapin & Live Oak  Can also be found infecting/living on numerous oak species in the US

48. Rate of Spread  Aggressive attempts to halt the spread of the blight were made by PA and NY  removed chestnut over a large area to halt southward spread  In 1911-1913, the U.S. Congress appropriated special funds to enable foresters to study and control the blight

49. Rate of Spread  Horticulturalists, found a blight-free area in Pennsylvania and quickly imported trees to form an experiment station  transported the blight and created a new epicenter  Accelerated spread in PA  Cuts in funding for Chestnut blight research:  With the onset of World War I in 1914  The evident futility of control efforts

50.  By 1926, fungus reported throughout native range  By 1940, virtually all (an estimated 4 billion) were dead or infected with the blight  Chestnut was the dominant wood processed at PA sawmills in the early 1920s,  salvage logging to make use of the dead and dying trees

51.  “…a tragic loss, one of the worst natural calamities ever experienced by this nation”

52. Cumulative Impacts  Chestnut in Southern range was first affected by Phytophtera cinnamomum  Now affecting hybrids

53. Cumulative Impacts  In 1974, the Oriental Chestnut Gall Wasp (Dryocosmus kuriphilus) was brought to the US  Female lays eggs in chestnut vegetative buds  Galls suppress shoot elongation and reduce fruiting  Heavy infestations can kill the trees (afflicts both American and Chinese chestnuts at the southern end of their ranges)  Threatening complete extinction (Anagnostakis, 1994)

54. Varying Outcomes: Europe  The fungus was later introduced into Europe (for tree breeding) from America  Moved through Europe killing European Chestnut  However, it was observed that many trees, while infected and full of cankers, did not die

55. Instead of sunken diffuse cankers, surviving European chestnuts had swollen cankers with evidence of "healing" along the margins.

56.  Many forest pathologists began working on this healing canker  Speculation that:  European Chestnut was less susceptible  That the fungus had mutated  That it was a different fungus altogether

57.  Noticed that a different colored fungus was recovered from "healing cankers"  Instead of the typical orange colored Cryphonectria parasitica fungus, a white-colored fungus was found.  White fungus was slower growing and produced fewer spores  When you "sprayed" the white fungus on a "killing canker" the "killing canker" became a "healing canker" (Europe)

58.  Determined that the white hypovirulent strains had become infected with a simple dsRNA virus  This virus was making the fungus "sick“  A slower fungus allowed the tree to respond to a point where the tree could survive infection

59. Varying Outcomes: Europe  Grente reported in 1965 that ‘hypovirulent’ strains from Italy did not kill chestnut trees  Began a program of active intervention when blight was found in France  blight strains with dsRNA passed hypovirulence to lethal strains  Treatment of new cankers as they formed resulted in a successful ‘biological therapy’ of the disease.  treat every canker for several years

60.  For a number of reasons biological control of chestnut blight does not work as well in the US  Different mating types of the fungus  Lack of chestnut to support conversion of the fungus by the virus  The many different types of virus in the United States

61. Varying Outcomes: Michigan  Hypovirulent strains were found in the United States  Most notably in Michigan  Successful because:  Few mating types  High number of Chestnut  Isolated from the native range  Less diversity of pathogen in MI so that hypovirulence can transfer more readily

62.  The transmission of hypovirulence from strain to strain of the fungus is restricted by a genetic system of vegetative incompatibility  Six loci, each with two alleles in a system of heterogenic incompatibility which keep the strains of the fungus from fusing and passing hypovirulence (Huber and Milgroom)  Virus transfer is restricted when there are different alleles at the vegetative incompatibility loci

63. Current Status  Reduced to a short lived sprouting understory tree  Fungus can not survive below the ground.  roots continue to live and they send up stump sprouts.

64. Current Status  Stump sprouts grow until infected  the stump re-sprouts again  Little chance for resistance to evolve  sprouts typically killed before they become sexually mature  sexual reproduction rare

65. Last remaining stand of American Chestnut  Largest living (>3 ft dbh) about 20 miles east of La Crosse, WI.  10 chestnuts planted in 1885  Seeds propagated around 50 acres and more than 3000 trees  Trees were blight free due to isolation until a canker was found in 1986  Now over 1600 cankers are present on 530 trees.  Virus was introduced in 1992 – not successful

66. Where are we now?  Upper slopes – scarlet oak, hickory, black gum  Mid slopes – red and white oak, red maple, & hickory  Coves – Poplar, hard maple, beech  Understory - American chestnut sprouts still persist, however they become infected between 1-12 yrs of age.

67.  Approaches:  Hypovirulent strains  Asian blight resistance  Natural resistance  Forest management practices Blight Control and Restoration

68. Hypovirulent Strains  Italian and French scientists observed non-lethal cankers growing on trees in Italy (1960’s)  Found that strains of the fungus associated with the blight produced colonies of abnormal shape and pigment  Demonstrated that these strains contained some “contagious factor” responsible for the inability to produce lethal infections (i.e., Hypoviruses)  In North America, hypovirus-infected strains have been found in stands in Michigan.

69. Hypovirulent Strains  In the last two decades, scientists have attempted to debilitate the fungus by infecting it with a virus, a process called hypovirulence.  Hypovirulence gives chestnut trees a much less potent form of the disease and gives chestnuts a fighting chance for survival (i.e., fungus is restricted to the outer bark).  Once introduced into a few trees, hopes are that hypovirulence will spread throughout the forest, offering hope to surrounding trees as well.

70.  Varied success  increase in stem size and stem number (Anagnostakis 2001)  strains do not persist (Peever et al. 1997) Virulent strains Hypovirulent strains

71. Graph of Numbers of Living Stems of Intensively treated American Chestnuts Intensively treated - cankers sampled, paired with hypovirulent strains, and reintroduced into the canker.

72. Graph of Numbers of Living Stems of American Chestnuts with Limited Treatment Limited treatment - cankers were sprayed with a mixture of conidia from Hypovirus-infected strains that had been used for treatment of the intensively treated plot.

73. Graph of Numbers of Living Stems of American Chestnuts with the Control Treatment Control Treatment

74. Factors contributing to failure  High blight susceptibility  Abundance of virulent inoculum  Restricted movement of the hypovirulence viruses among the many strains  Europe and Michigan strains

75. Factors contributing to failure  The transmission of hypovirulence from strain to strain of the fungus is restricted by a genetic system of vegetative incompatibility.  Genetic studies found that there are six loci, each with two alleles in a system of heterogenic incompatibility which keep the strains of the fungus from fusing and passing hypovirulence (Milgroom and Cortesi).

76. More factors contributing to failure  Environmental stress  Superficial canker instability (i.e., hypovirulent cankers produced change back into a killing canker after one or more winters)

77. Asian blight resistance  Early breeding efforts unsuccessful:  Poor form  < 50% AC parentage  Poor survival  1981 backcross breeding method proposed (Burnham)  Better form  Field blight resistance

78.  Resistant Asian X Susceptible American  Partially resistant X American again  1 out of the 4 will have 1 copy of both resistant genes  Process repeated until a final cross of 2 trees with partial resistance yields 1 having 2 copies of both resistant genes making it fully resistant

79. American chestnut resistance  Breeding programs  Scions were grafted into chestnut rootstocks to establish seed orchards  Seeds and seedlings have been distributed that have low levels of blight resistance by artificial inoculation with a standard virulent strain

80. Site Factors  High vs. low elevation  High elevation sites contain the highest density of chestnut sprouts  Studies found the superficiality rating of cankers to decrease greatly (disease developed at the vascular cambium) after several winters at high elevation sites  May be a result of physiological stress from low temperatures in mid- to late winter which may decrease host defense mechanisms in chestnut towards weak pathogens, such as hypovirulent strains

81. Site Factors  Xeric vs. mesic sites  Blight control greatest on mesic sites  Competition- high levels of hardwood competition, especially on mesic sites  Browse damage

82. Restoration  Combination of the four approaches can bring the chestnut back  Individual or group selection openings- an integrated management system using grafted trees, inoculating them with hypovirulent strains, and controlling hardwood competition  Timber production- backcross approaches

83.  The selected examples demostrate the damage that invasive species can do to both the natural environment and human interests.  For more information on invasive species see the Invasion Biology course. Concluding Remarks

84. 1.Wikipedia contributors, Black Rat, [accessed 2006 July 30] Wikipedia, The free Encyclopaedia, Available from:En.wikipedia.org/wiki/Black RatEn.wikipedia.org/wiki/ 2.Gross, L. (1995). How the plague bacillus and its transmission through fleas were discovered: Reminiscences from my years at the Pasteur Institute in Paris. Proceedings of the National Academy of Science 92: 7690-7611. 3.Dols, M. (1974) Plague in Early Islamic History Journal of the American Oriental Society 94:371-383 4.Maddicott, J. R.(1997) Plague in Seventh -Century England. The past and present society 5.Davis, D. The Scarcity of rats and the black death: an ecological history, Journal of Interdisciplinary history 16: 455-470 6. Storey of the Plague,(2006) channel 4 [accessed July 30 th 2006]. Found at http://www.channel4.com/history/microsites/H/history/plague/experts.html 7.May, J. M. (1952). Map of the world distribution of plague. Geographical review 42:628-630. 8.BBC news (2005) DR Congo plague outbreak spreads [accessed July 30 th 2006] news.bbc.co.uk/1/hi/world/africa/4290783.stm 9. the world health organization (2006). Plague in the DRC. [accessed July 30 th 2006] www.who.int/csr/don/2006_06_14/en/index.html www.who.int/csr/don/2006_06_14/en/index.html 10. Lundy shore office [accessed July 30 th 2006] http://www.lundy_ island.co.uk 11.BBC news (2005) Lundy Rats. [accessed 30 th July 2006] www.bbc.co.uk/devon/content/articles/2005/06/08/lundy_rats_feature.shtml) www.bbc.co.uk/devon/content/articles/2005/06/08/lundy_rat 12. Atkinson, I. A. E and Atkinson, T. J. (2000) Land vertebrates as invasive species on islands served by the south pacific regional ENVIRONMENT PROGRAMME. In: Invasive species in the pacific: A Technical review and draft regional strategy. South Pacific regional environment program Samoa: 19-84 13.G. McCormack. (2005). The Status of Cook Island Birds 1996, Cook Island Biodiversity and natural heritage http://cookislands.bishopmuseum.org/showarcticle.asp?id=7 http://cookislands.bishopmuseum.org/showarcticle.asp?id=7 14.Measy, J. (2004). Global Invasive species database Xenopus laevis. [accessed 30 th July 2006] Found at http://www.issg.org/database/species/ecology.asp?si=ISO&fr=1&sts=sss http://www.issg.org/database/species/ecology.asp?si=ISO&fr=1&sts=sss 15.Lafferty, K. and Page, C. (1997) Predation on the endangered Tide Water Goby, Eucyclobius newberryi, by the introduced African clawed frog I, Xenopus laevis, with notes on the frogs parasites. Copeia 1997: 589-592. 16.Measey, G. J. (1998) Diet of feral Xenopus laevis (Daudin) in South Wales, UK. Jnl Zool. 246:287-298 17.Measy G. J. (2004) Xenopus laevis. In Atlas and red data book of the frogs of South Africa, Lesotho and Swaziland, eds Minter, L. et al. References for the Rat and the Toad