Ecological Consequences of the Introduction and ...

Ecological Consequences of the Introduction and Dissemination of New Plant Species: An Analogy with the Release of Genetically Engineered Organisms Ingo Kowarik Synopsis: Nearly half a millenium ago, Columbus' journey to North America initiated a biological process of worldwide significance: 1t ended to geographical isolation of organisms lacking the roeans to cross the dividing seas, organisms

that had evolved in separate worlds for thousands of years and were integrated in their different ecological systems. Global trade and travel mixed the flora of areas that had been isolated from one another. This transfer of non-native species into completely new ecologica! systems is analog to releasing genetically engineered organisms into the environment. Both processes involve crossing barriers impenctrable by natural means: genetic barriers bctwecn species und geni as weIl as those preventing dissemination bctween contincnts. The sauree cf the 'new' species resulting from said release Cf introduction is not cf the same order (in the ODe case astrange continent, in the other a laboratory), although this cannot be said of the possible 'surprise effecC on the environment inherent in bath instances. The possibility of predicting the reaction of 'new species' and the response of their environment is still limited. A time-lag of some decades (or even centuries in sorne cases) may exist between the release and the spontaneous spread. Meanwhile, the site conditions determining the behaviour of the released species could have been changed by external causes. As a consequence of this ecolagical perspective, it is necessary to minimize the risk of releases. If it is not possible to stop releases, the control mechanisms must be in place over lang periods of time.

Synopsis: Fast genau vor einem halben Jahrtausend setzte Kolumbus' Reise nach Nordamerika einen biologischen Prozeß von

weltweiter Bedeutung in Gang: die Aufhebung der geographischen Isolation von Organismen. die nicht aus eigener Kraft trennende Meere überwinden konnten, die über Jahrtausende ohne Kontakt zueinander die Evolution durchlaufen hatten, in verschiedene Ökosysteme integriert waren. Weltweiter Handel und Verkehr verursachten eine Vermischung der Floren bislang voneinander isolierter Gebiete. Diese Verbringung von nichteinheimischen Arten in völlig neue ökosystemare Zusammenhänge beinhaltet eine Analogie zur Freisetzung gentechnisch veränderter Organismen in die Umwelt. In heiden Fällen werden Barrieren überbrückt, die auf natürlichem Weg nicht überwunden werden können: genetische Barrieren zwischen Arten und Gattungen ebenso wie die Ausbreitungshindernisse zwischen Kontinenten . Der Ursprung der freigesetzten beziehungs-

weise eingeführten 'neuen Arten' ist unterschiedlich (hier fremder Kontinent, dort Labor) , nicht jedoch die Möglichkeit eines 'Überraschungseffektes' rur ihre neue Umwelt.

Vorhersagen des Verhaltens neuer Arten sind bislang nur sehr eingeschränkt möglich. Zwischen Ersteinführung und Beginn spontaner Ausbreitung können Zeitverzögerungen von Jahrzehnten (bis zu Jahrhunderten in einigen Fällen) auftreten. Inzwischen können für das Verhalten der Arten entscheidende Standortveränderungen eintreten, deren Auswirkungen schwer vorhersehbar sind. Die Konsequenz aus dieser ökologischen Perspektive bedeutet die Notwendigkeit einer strikten Strategie der Risikominimierung bei Freisetzungen. Sollte es nicht möglich sein, Freisetzungen zu unterlassen, muß eine intensive und vor allen Dingen langfristige Kontrolle etwaiger Freisetzungsexperimente gewährleistet sein.

Introduction

involving interconnected ecological risks has been

largely hypothetical up to now. Experience in releasing How do such genetically engineered plants, animals or micro-organisms behave in the environment? How great is the risk of uncontrolled dissemination? Are existing ecosystems in imminent danger, as weil as the environ-

ment as a whole and its human occupants? Can plants and animals with new characteristics be controlled and is

their behaviour predictable? Discussion of this question

such plants into nature has been Iimited, and extracting from results of controlIed laboratory and greenhouse experiments to the vastly more complex natural environment is a questionable venture at best.

There are historieal paralleis to the ecological challenge presented by the release of organisms whose genes have been manipulated. Nearly halfa millenium ago, Co-

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lumbus' journey to North America initiated a biologieal process of worldwide significance: lt ended the geograph-

dangerous
Mimosa pigra is eontro11ed by phytophagous inseets, but not in Southeastern Asia. It grows in a wide variety of

habitats, also penetrating into natural bodies ofwater and the eeonomieally vital irrigation systems. The plant reproduees and grows rapidly, slowing the drainage flow of the water and inereasing sedimentation and bank erosion. The damage is that serious that internationally coordinated control programmes have been initiated

(LAMAR ROBERT and HABECK, 1983; MILLER, 1983) . The courses of many streams and rivers show changes

in vegetation in Central Europe as weil. These ehanges derive from North American and East Asian garden

since the beginning of this century, is just as bad. This North Ameriean forest Iree was planted in the Netherlands and in Northern Germany in order to improve poor forest soils because of favourable C/N proportion in its leaves. These habitats were, indeed, improved in the desired manner, but then an unexpectedly strong spontaneous dissemination began starting from the planting sites. Prunus scrotina can completely dominatc shrub-Ievel forest growth. Among the undesirable results are: the change in structure in the layers of forest vegetation, the suppression of forest-floor vegetation and prevention of the natural rejuvenation of native woody plants. Thc

higher density of Prunus serotina at the shrub and tree levels leads to fewer species at the herbaceous level (STARFINGER, 1989). The history of the introduction of Prunus serotina

shows that next to nothing happened for 250 years following its initial introduction as an ornamental tree. The pop~lation then increased through plantings in forests,

whieh led to the unexpeeted resuhs mentioned above. 50 years after the systematic plantings in the wild, equally systematic control methods became necessary, which rn~y

in turn cause side-cffects on thc ecosystems in-

volved (conf. Illustr. 4 in KOWARIK and SUKOPP, 1986). Just as with Spartina. this was a matter of the ecolog-

ical failure of economically motivated import plantings. You may call this a 'Zauberlehrling' effect l : Speeies originally cuhivated in hopes ofpositive effects prove extremely difficult to contain behaving differently than they had been expected to. Possible ecologieal effects of introduced plant species

plants eseaped (golden rod, asters, knot-grass, ete.). The spread of the tuberous sunflower (Helianthus tuberosus) presents a partieularly serious problem. The plant is a

(I) The species composition and strueture of existing

strang competitor for native species. Its root suckers grow under existing vegetation from the side. whereu-

communities can be changed as a result of invasion by new species. Native species are suppressed, then dis-

pon the plant sueessfu11y eompetes with other speeies by shading them. The tuberous sunflower also endangers the banks of waterbodies, sinee the plant dies off down to it tuberous roots after the first frost. Rodents dig up the tubers, exacerbating the erosion of the banks (LOHMEYER, 1971). Spartina angliea has been planted for land reaeclamation in various parts of the tidal mud flats along the German North Sea Coast sinee 1927. The a11opolyploid plant, a hybrid of its native Spartina speeies with a North

placed entirely. This results in a levelling out of flora and vegetation

can be surnmarised as folIows:

in clear contradiction to the goal of preserving nature.

(2) These alterations can resuh in kick-back effects on the entire ecosystem, since the I new ' species cannot al-

ways fulfill the functions of those species they replaced. This is true of dependent organisms that lose their source of nutrition as weil as of habitat factars such as erosion prevention.

(3) Since disrupting agri- and silvicultural use of the

American one, does not, however, grow only in the glasswort zone where it is supposed to support land reacc1amation. It also spreads inland into bordering coastal

land, such alterations have an economic dimension in addition to the ecological one. Same of them need to be

grasslands, where it displaees valuable grazing grasses

verse the mass dissemination cf a species and its consequences.

such as Puccinella maritima due to its higher and denser growth, rendcring the overall cconomic success of the

plantings at least questionable (KÖNIG, 1949; DOODY, 1984). The eeonomie effeets of the American black eherry Prunus serotina, which has been planted on a large scale

regarded as irreversible, it being hardly possible to re-

Predictability of behaviour of 'new' species An important safety consideration in releasing geneti-

cally engineered organisms is the probability with which

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ecologieal implications can be predicted resulting from such gene alterations. Thc history of biological invasions cf non-native speeies cao serve as a basis for cxploring the extent to wh ich the future environmental behaviour cf organisms cao be

predicted from knowledge ofthe presence or lack of certain features. The available data are fairly extensive:

Since approximately the mid-19th ccntury, specific data have becn collected on the occurrence cf non-native speeies in a new environment. First, the variety cf newly occurring species was described. then they were classi-

fied according to various parameters (e.g. WATSON, 1847; THELLUNG, 1905). Later, alterations in the flora of extended areas were evaluated (e.g. THELLUNG, 1912; LINKOLA, 1916/21). The effects cf new introductions were recognised

with characteristic B?). Organisms are disseminated in a historical process that may take decades, or centuries. Thus, it is not just a quest ion of whether a 'new' species will be capable of dissemination or wh ich alterations it might cause. It is also of primary importance when all of this occurs. Current studies on the history of cultivation and dissemination of non-native woody plants in Berlin have already shown that a considerable time-lag, in some cases longer than a century (e.g . in the case of Prunus serotina, see above) . separates the first evidence of cultivation of a species and the onsel of spontaneous dissemination. How surprising the course oftbe dissemination history

early 002 . However. questions about the operative interconnecting factars were not analysed exhaustively until

of 'new' species may be is illustrated by the example of the tree of heaven (Ailanthus altissima ; cf. KOWAR1K and BÖCKER, 1984), brought to Europe from China between 1740 and 1750: Although Ailanthus had often

ELTON (1958). (Why are some species successful invaders, while elosely related specics are not? Why are same ecosystems more susceptible to aherations than athers?)

as early as 1780, there had been no spontaneous dissemination until the 1950's. A mass dissemination began after 170 years, which has made the tree ofheaven the sec-

Sinee then, numerous case studies have been com-

ond most common non-native tree after the robinia in

pleted; these were analysed in national groups within the

Berlin's inner city by now. Two factors made this prolonged, but stable, success possible: (a) The formation ofan 'island of warmth' in the city improved living conditions for this thermophileous spedes. (b) Destruction du ring WW II suddenly opened large ar-

framework of an international research programme titled

been planted as an ornamental tree in Berlin beginning

'Ecology of Biological Invasions' (SCOPE 37): USA (MOONEY and DRAKE, 1986), Great Britain (KORNBERG and WILLIAMSON, 1986), The Netherlands (JOENJE et al., 1987), South Africa (MACDONALD ct . eas in which the competitive conditions were complete ly al. , 1986) and Australia (GROVES and BURDON , new. Back in the 18th century, when the tree of heaven 1986). An overall evaluation has now been accomplished was first planted in Berlin, it would have been hardly pos(DRAKE et al. , 1989). sible to take these two factors into account in formulating The results - when it comes to the ques tion of pre- a dissemination prognosis. dictability - are sobering. The British report summarJÄGER (1988) used several species as examples to ises as folIows: 'Although cerlain habitat and biological show that the rate varies widely at which the potential features increase the probability ofinvasion and establishment, these features are neither necessary nor sufficient.

pear to guarantee success such as short generation cy-

area ofdissemination is populated after the onset of spontaneous dissemination: In most cases, aperiod between several decades and two centuries is necessary. The new arrivals can also switch biotopes in an unpredictable manner in this process . as shown by the small-blossomed

eies, fast growth, genetic variability, broad ecological amplitude, etc ., may not in fact work; on the other hand,

touch-me-not (Impatiens parviflora), which was introduced in Europe from Central Asia (TREPL, 1984).

The prediction of invasions is not yet pos~ible' (WILLIAMSON and BROWN, 1986). Features that would ap-

even species that lack these features can be quite success-

Impatiens parviflora was first observed in the wild in

ful. Tables of supposed key features of successful invaders must still be understood as collections of hypothcscs that are confirmed in some studies and rejected in others.

Europe about 1830. For the following 50 years, it then grew solely in disturbed habitats near settlements (along gardens, paths and fences). Today, the plant is the most

Until now wide-ranging theories have not provided ac-

commen non-native species to be found in Central

curate predictions in individual cases.

Europe's forests. No-one could have predicted this accelerated leap from garden weed to a plant spreading explosively in wood-Iands. The causes behind this phenomenon are assumed to lie in the surpassing of a critical population threshhold as weil as the increased dis turban ce of forest habitats.

One of the basic problems in predicting the success of introduced non-native species also applies to organisms

which genes have been altered in labs: Many studies and models are focused towards analysing the current situation. Currently known characteristics of organisms are

studied and their effects projected onto characteristics of ecosystems currently known. (What happens if an organism with characteristic A comes up against an ecosystem

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Tbe dissemination histories of the tree ef heaven and

the small-blossomed touch-me-not show c1early that consistency in the conditions dccisive for success or failure

in the invasion of a 'new' species cannot be taken as given. !t has not yet proven possible to predict future behaviour of a species under changed environmental conditions based on known reaction patterns of said species. Conclusion The introduction of alien species can be used as a model for the release of genetically engineerd organisms. From the spontaneous spread of aliens, wh ich is sometimes documentated for decades and centuries, the following conclusions can be derived: 1. The probability of a successful invasion is smalI: Only 1-3% of the introduced species of vascular plants can establish stable populations in their new environment. I Master, it's a catastrophe!! The spirits came at my behest,! And now they're haunting me. (from W. v.Goelhc , 'Der Zauberlehrling', 1797). 2 HEHN, for example (1870: 1), writes that 'native nora and fauna in the areas settled by Europeans have been replaced eilher by those from Europe or from aH over the world'. References Davis, M.B., 1981 : Quarternary History and the Stability of Forest Communities. In: West, D.C., Shugart, H.H. & BOIkin, D.B .: Forest Succession. Concepts and Application., pp. 132-153. New York, Heidelberg, Berlin. Doody, P. (ed.), 1984: Spartina anglica in Greal Dritain . Focus on Nature Conservation 6. Shrewsbery. Drake, J.A., Mooney, H.A., di Castri, F., Groves , R.H., Kruger , F.J. , Rejmanek, M. & Williamson, M., 1989: Biologicallnvasions. Agiobai perspective. Chichester etc. Elton, C.S., 1958: The ecology ofinvasions by animals and plants. London. Groves. R.H. & Bunlon. J.J. (eds.), 1986: The ecology ofbiological invasions: an Australian perspeelive. Cambridge. Hehn., V., 1870: Kulturpflanzen und Hausthiere in ihrem Übergang aus Asien nach Griechenland und Italien sowie in das übrige Europa . Berlin. Holm, L.G., Plucknell, D.L., Plancho. J. V. & H~rberger, J .P., 1977: The world's worst weeds. Vniversity Press of Hawaii. Jäger, E.J., 1988: Möglichkeiten der Prognose synanthroper Pflanzenausbreitungen. Flora 180: 101-131. Joenje, LA.W., Bakker, K., Vlijm, L. (eds.), 1987: The ecology of biological invasions . Proc. Koninklijke Nederlandse Akad. van Wetenschappen. 90: 1-80. Kornberg. H. & Williamson. M.H., 1986 (eds.): Quantitative aspects of the ecology of biological invasions. Phi!. Trans. R. Soc. Lond. B., Val 314. Kowarik, I. & Bäcker, R. 1984: Zur Verbreitung , Vergesellschaftung und Einbürgerung des Götterbaumes (Ailanthus altissima (MiII.) Swingle) in Miueleuropa. Tuexenia 4: 9-29. Kowarik, L & Sukopp, H., 1986: Ökologische Folgen der EinfUhrung neuer Pflanzenarten. Gentechnologie 10: 1 J 1-135. König, D., 1949: Spartina townsendii an der Westküste von SchleswigHolstein. Planta 36: 37-70. Lamar Robert, G. & Habeck, D.H. (eds.), 1983: Mimosa pigra management. Proc. of an intern. symposium, IPPC Doc. No. 48A-R3. Linkola, 1916121: Studien über den Einfluß der Kultur auf die Flora in den Gegenden nördlich vom Ladogasee. Acta Soc. Fauna Flom Fenn. 45 (1/2). Lohmeyer, W., 1971: Über einige Neophyten als Bestandsglieder der bach-und flußbegleitenden nitroph ilen Staudenfluren in Westdeutschland. Natur u. Landschaft 46 (6): 166-168.

2. About a third of the established species are capable to invade natural ecosystems. 3. The risk that an introduced species may become a 'pest species' causi ng severe ecological and economic damage is about I · 10-3 4. The possibility of predicting the reaction of 'new speeies' and the response of their new env ironment is still limited. A time-lag of some decades (ar even centuries in some cases) may exist between the release and the spontaneous spread. Meanwhile. the site conditions determining the behaviour of the released species, could have been changed by external causes. As a consequence of this ecological perspective, it is necessary to minimize the risk of releases. If it is not possible to stop releases, the contra I mechanisms must be in pi ace over long periods of time. Macdonald, LA.W ., Kruger. F.l. & Ferrar, A.A., 1986: The ecology and management of biological invasions in Southcrn Africa. Cape Town. McNabb, H.S., 1971 : A new look at dutch elm disease control. Thc Arnes Forester 58: 14- 18. Miller, LL. , 1983: The dist ribution and threat of Mimosa pigra in Au stralia. In: Lamar Robert & Habeck (eds.), pp. 38-50. Mooney, H.A. & Drake, J.A. (cds.): Ecology ofbiological invasions of North America and Hawaii. Ecological Studies 58. Regal, P.J., 1986: Models of genelieally engineered organisms. In : Mooney, H.A . & Drake, L A. (eds.) pp. 111·132. Rothmaler, W. (ed.), 1976: Exkursionsnora rur die Gebiete der DDR und der BRD. Kritischer Band. Berlin. Sharples, F.E., 1982: Spread of organisms with novel gcnOlypes: thoughts from an ecologieal perspective. ORNLITM-8473, Oak Ridge National Laboratory Environmental Sc iences Division Publication No. 2040, 50 p. Simberlofr, D.S., J981 ; Community effects of introduced species. In : Nitecki, M.H. (ed.): Biotic erises in ecological and evolutionary time, pp. 53-81. New York etc . Starfinger, V., 1989: Die Einbürgerung der nordamerikanischen Spilt blühenden Traubenkirsche (Prunus se rotina Ehrh.) in Mitteleuropa. Diss. TV Be rlin . Starfinger, V., in print: Black cherry (Prunus serolina Ehrh.) in Berlin. Germany - casc study of an introduction . Proc . IUCN ConL on introduced species: European poIicy al horne and abroad . 6.8.9.1988 London. Sukopp, H., 1976: Dynamik und Konstanz in der Flora der Bundesrepublik Deutschland. Sehr. R. Vegctantionskde. 10: 9-27 . Sukopp, H., 1980: Zur Geschichte der Ausbringung von Pllanzen in den letzten hundert Jahren. In : Ausbringung von Wildpflanzen . Akad. f. Naturschutz u. Landschaftspfl ., Laufen. Tagungsbericht 5/80. Thellung , A., 1905: Einteilung der Rudcral- und Adventivtlora in genetische Gruppen. In: Naegeli, O. & Thellung , A.: Die Flora des Kanton Zürich. I. Teil. Vj sch r. Naturforsch. Ges. Kanton Zürich 50; 232-236. Thellung, A .. 1912: La nore adventice de Montpellicr. Mem. Snc. Sci. Nat. Cherbourg 38: 622-647. Trepl, L., 1984: Über Impatiens parviflora D.C . als Agriophyt in Mi,· teleuropa. Diss. Bot. 73: 1-400. Watson, H.C., 1847: Cybele Brittanica 1. Weeda, E., 1987: Invasions ofvascularplants and mosses inlo the Ncth erlands. In: Jocnje, I.A.W .. Bakker, K.. Vlijm, L. (eds.). pp. 19-29. Will iamson, M., 1988. Potential effects of recombinant DNA organisms on ecosystems und their componenls. Trends in Ecol. umJ Evo!. 3 (4): 32-35. Williamson, M.H. & Drown. K.C ., 1986: The analysis and modelling ofBritish invasions. Phi!. Trans. R. Soc. Land. B 3 14: 505-522.

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