The casual, naturalised and invasive alien flora of Zimbabwe based on herbarium and literature records

Alien plant species invasions are causing major conservation problems in many regions of the world and are viewed as an important component of human caused global change (Vilà, Meggaro & Weber 1999; Vitousek et al. 1997). The spread of alien species is often associated with human activities which include disturbance and fragmentation of the natural environment, urbanisation, agriculture and the use of alien plants for landscaping and erosion control (Vilà et al. 1999). The transport of organisms by humans since earliest times and now through increased levels of trade and tourism has led to the widespread breaching of natural biogeographic barriers of alien species (Hulme 2009). According to Vilà et al. (1999), there is a need to document naturalised flora before investigating the ecological relationship between invader and invaded habitats. Documentation of alien species and analysing patterns of floristic status, biological attributes and geographical distribution has proved to be a useful approach in understanding alien species richness in various regions (e.g. Khuroo et al. 2007; Pyšek, Sádlo & Mandák 2003; Pyšek & Richardson 2006; Rozefelds et al. 1999; Stadler et al. 2000; Weber, Sun & Li 2008).


Introduction
Alien plant species invasions are causing major conservation problems in many regions of the world and are viewed as an important component of human caused global change (Vilà, Meggaro & Weber 1999;Vitousek et al. 1997).The spread of alien species is often associated with human activities which include disturbance and fragmentation of the natural environment, urbanisation, agriculture and the use of alien plants for landscaping and erosion control (Vilà et al. 1999).The transport of organisms by humans since earliest times and now through increased levels of trade and tourism has led to the widespread breaching of natural biogeographic barriers of alien species (Hulme 2009).According to Vilà et al. (1999), there is a need to document naturalised flora before investigating the ecological relationship between invader and invaded habitats.Documentation of alien species and analysing patterns of floristic status, biological attributes and geographical distribution has proved to be a useful approach in understanding alien species richness in various regions (e.g.Khuroo et al. 2007;Pyšek, Sádlo & Mandák 2003;Pyšek & Richardson 2006;Rozefelds et al. 1999;Stadler et al. 2000;Weber, Sun & Li 2008).
Basic information on naturalised plant species, plant invasions and their impacts is lacking in Zimbabwe.Although occasional attention has been paid to alien plants and weeds in Zimbabwe (e.g.Biegel 1977Biegel , 1980;;Drummond 1975Drummond , 1984;;Mapaura & Timberlake 2004;Maroyi 2006;Mullin 1996Mullin , 2000;;Timberlake, Fagg & Barnes 1999;Wild 1955), comprehensive studies on plant invasions are still lacking.The compilation of a catalogue of casual, naturalised and invasive species, hereafter referred to as alien flora, can serve as an initial step towards further detailed studies on the impact of alien plant species on the indigenous flora and fauna.Therefore, the primary objective of this investigation was to provide an overview of the alien species present, and their invasion status and geographical extent in Zimbabwe, based on a literature survey and herbarium records.

Compiling the list
A database of casual, naturalised and invasive alien flora occurring in Zimbabwe was compiled based on a literature survey and herbarium records.All alien plant species ever recorded in Zimbabwe's casual, naturalised and invasive alien plant species were analysed with regard to their habit, origin, mode or purpose of introduction and their invasion status in the country.This alien flora of 391 taxa belonged to 239 genera and 73 families, corresponding to 6.6% of the total flora of Zimbabwe.Of these, 153 (39.1%) plant species were casual aliens, 154 (39.4%) were naturalised and 84 (21.5%) were invasive species.Most invasions in terms of numbers of alien species were in the central and eastern parts of the country.Asteraceae (53 species), Poaceae (48 species) and Fabaceae sensu lato (49 species) families were prominent in all the floristic regions of the country.Annual and perennial herbaceous species formed the majority of life forms of the casual, naturalised and invasive alien flora of Zimbabwe.Genera with the highest number of alien species were Ipomoea with nine species, Acacia and Euphorbia with eight species each, Chenopodium and Senna with seven species each, Eucalyptus with six species, Oenothera, Physalis and Solanum with five species each.More than 49.6% of the alien plants in Zimbabwe originated primarily from South, Central and North America, followed by Europe (24.6%),Asia (23.8%),Africa (10.5%) and Australasia (5.9%).

Conservation implications:
This research provides baseline information and historical invasion patterns of casual, naturalised and invasive alien flora in Zimbabwe.This inventory is a crucial starting point in trying to understand and initiate the management of biological invasions.This is also important for monitoring new introductions and management of existing alien plants in Zimbabwe.
Zimbabwe as escapes from cultivation or naturalised at least once in the wild were included in the database.Species introduced or cultivated without any evidence of having escaped were not considered.Alien species were divided into three categories: casual, naturalised and invasive aliens.According to Pyšek et al. (2004), casual aliens reproduce occasionally outside cultivation, do not form self-sustaining populations and rely on repeated introductions for their persistence.Naturalised species are defined as aliens that reproduce consistently without direct human intervention, and invasive aliens as naturalised species producing offspring in large numbers and at considerable distances from the parent plants with the potential to spread over a large area.This definition of invasive alien species used in this study is different from the Convention on Biological Diversity (CBD) Conference of Parties' definition of an invasive alien species, where an alien is defined as a species outside its indigenous geographic range, whose introduction and spread threatens biodiversity (UNEP 2002).The National Herbarium, Harare, Zimbabwe (SRGH), was visited on numerous occasions between 1996 and 2010.Information on herbarium labels, including locality and year of collection of the plant species, was examined and recorded.

Species data
For each taxon, information on its life history traits, such as habit, origin, year when plant species was first collected, mode or purpose of introduction and its invasion status in Zimbabwe were extracted from literature and herbarium records.Economic uses were included and whether the introduction was accidental or intentional.A taxon was allocated to more than one use category if different uses applied to it.A wide range of published literature and websites was consulted (see Online Appendix).The correct identities and names of all the taxa listed were checked and, where names have changed, the currently accepted name was applied.The species nomenclature and classification generally follow Glen (2002).Infra-specific taxa up to the variety level have been recognised.Author citation abbreviations follow those given in Brummitt and Powell (1992).Each taxon's distribution in Zimbabwe was indicated by letters showing the floristic divisions used in Flora Zambesiaca (see Pope & Pope 1998): Northern region (N), Western region (W), Central region (C), Eastern region (E) and Southern region (S).

Results
The present study revealed that the casual, naturalised and invasive alien flora of Zimbabwe is comprised of 391 taxa belonging to 239 genera and 73 families, representing 6.6% of the total Zimbabwean flora.Although this checklist is not exhaustive, it provides good baseline data for future work on casual, naturalised and invasive flora of Zimbabwe.Of these, 153 (39.1%) plant species were casual aliens, 154 (39.4%) were naturalised aliens, and 84 (24.5%) were invasive aliens.Intensive collection of casual, naturalised and invasive alien plant species occurred between 1921 and 1980 (Figure 1).Nineteen twenty-one to 1940 was a period of relatively slow accumulation of casual, naturalised and invasive alien plant species records, with a total of 72 species (18.4%) collected during this period (Figure 1, Online Appendix).Most casual, naturalised and invasive alien plant species (153 in total, Page 2 of 6 39.1%) were collected between 1941 and 1960 (Figure 1).The accumulation of casual, naturalised and invasive alien plant species slowed and levelled off between 1961 and 1980, resulting in the collection of 83 species (21.2%) (Figure 1).

Discussion
The species list includes a total of 391 casual, naturalised and invasive alien plant species and infraspecific taxa is higher than 328 species listed by Maroyi (2006).(2010) showed that the number of documented invasive alien species is underestimated due to lack of information and research.
The taxonomic composition of the alien flora of Zimbabwe is not random and families with the largest number of species belong to the largest families worldwide, for example Asteraceae, Poaceae and Fabaceae.A number of taxa belonging to these families and those of Amaranthaceae, Caryophyllaceae, Chenopodiaceae and Solanaceae have been recorded as weeds of agroecosystems in Zimbabwe   1 8 6 1 -1 8 8 0 1 8 8 1 -1 9 0 0 1 9 0 1 -1 9 2 0 1 9 2 1 -1 9 4 0 1 9 4 1 -1 9 6 0 1 9 8 1 -2 0 0 0 1 9 6 1 -1 9 8 0 Time (20-year periods) (Drummond 1984;Wild 1955).Heywood (1989) examined the patterns and extent of invasions by agricultural weeds and concluded that most weeds come from the largest plant families like the Asteraceae and Poaceae.Thus, it is also not surprising that annuals and herbaceous perennials are the prevalent life forms amongst the alien flora recorded in this study, as it has been shown in other studies that the herbaceous habit is most frequent amongst the invasive species (Daehler 1998;Kolar & Lodge 2001).
The early phase of exotic plant species introduction involved early settlers who arrived and settled in major towns like Harare and Gweru (Zimbabwe central), Bulawayo (Zimbabwe west) and Mutare (Zimbabwe east).Historically, colonists from Europe brought food plants, ornamentals, structural timber species, et cetera, with them during their migration (Maroyi 2006;Mullin 1996).According to Maroyi (2006), small-scale plantings of alien plant species in Zimbabwe started with European settlement in the 1890s and early 20th century.This was a period when acclimatisation societies and botanical gardens flourished in the British colonies and economic plants were transferred from one continent to another (Maroyi 2006).Over 80% of the alien flora in Zimbabwe originated from America, Europe and Asia.Alien plants were introduced into from these regions probably through the European colonisers.The relatively lower number of alien species in the southern part of Zimbabwe is due to the harshness of the region's climate.Southern Zimbabwe is hot and dry, characterised by low and erratic rainfall.
The majority of alien plant species recorded in Zimbabwe have been introduced intentionally for economic purposes, although a sizeable proportion of species arrived in the country by accident.Several species of Eucalyptus were introduced from Australia for structural timber, furniture, poles, charcoal and medicinal oils (Mullin 1996).About An understanding of the establishment and distributional changes of alien flora over time is important for making informed decisions in managing existing introductions and predicting future invasions.Although the Zimbabwean alien flora has been noted for some time (Wild 1955), it is only in the last four decades that a profound interest has developed, owing to the important economic impacts of alien weed species on agricultural crops (Drummond 1975(Drummond , 1984)).
The majority of the species (63.2%) considered in this investigation were already casuals, naturalised or invasives in Zimbabwe by 1955, when an initial survey of exotic weeds was carried out (Wild 1955).About 30 alien species were recognised as weeds by Wild (1955).Drummond (1975) reported 45 naturalised woody plant species.Drummond (1984) Drummond (1975), but this investigation showed that they are also naturalised in other regions of the country.Information on naturalisation or rate of spread of alien plants increases with more collecting and monitoring efforts.A better understanding of their establishment and distributional changes is important for the development of appropriate alien plant species management plans.

Conclusion
The catalogue of casual, naturalised and invasive alien plant species presented in this study is a critical starting point in trying to understand and initiate the management of biological invasions; and it will serve as a foundation for future research on plant invasions in Zimbabwe.However, the documentation of casual, naturalised and invasive plant species in Zimbabwe is far from sufficient.It is here recommended that extra attention be paid at studying the ecological and socio-economic impacts of introduced plant species on the native communities in Zimbabwe.A better understanding of their establishment, spread, social and economic impacts, and distributional changes over time is vital for making informed decisions on new introductions and managing existing casual, naturalised and invasive alien plant species.Since complete eradication of introduced species is unachievable (Moles et al. 2012), there is need to have a historical invasion patterns of alien species and their long-term effects on native communities.This field of study is currently under researched in Zimbabwe and there are few examples where casual, naturalised and invasive alien plant species have been fully evaluated.The result is that, where investigations are done at all, research on such alien plants are often short-term, highly localised, sporadic, largely ad hoc and restricted to field studies without underpinning agricultural, scientific or economic studies.Therefore, elucidation of alien plant naturalisation patterns in Zimbabwe will prove crucial in the scientific management of casual, naturalised and invasive alien flora in the country.
The current figure is higher because it utilised herbarium records, an online database (http://www.zimbabweflora.co.zw/[Hyde & Wursten 2011]) and published literature (e.g.volumes of Flora Zambesiaca and Kirkia), unlike findings ofMaroyi (2006), which utilised mainly herbarium records.This figure is relatively low when compared with the 5930 indigenous Zimbabwean taxa recorded byMapaura and Timberlake  (2004).This could be a result of under-collection, as plant collectors tend to collect mainly indigenous species, ignoring alien plants(Pyšek et al. 2008).The rather small alien flora in Zimbabwe confirms the findings of Foxcroft et al. (2010), Le Floc'h, Le Houerou and Mathez (1990) and Vitousek et al. (1997) that African countries generally have few naturalised species compared to the other regions of the world.However, research by McGeoch et al. (2010), and Nuñez and Pauchard aliens; Nt, Naturalised aliens; In, Invasive aliens.

FIGURE 1 :
FIGURE 1: Cumulative number of species against date of earliest herbarium collection for 391 casual, naturalised and invasive alien plant species in Zimbabwe.

FIGURE 2 :
FIGURE 2: The distribution of the 391 casual, naturalised and invasive alien plant species in Zimbabwe.The numbers in the figure indicate the number of alien species in the five floristic regions of the country.
38.1% of the casual, naturalised and invasive alien plant species in Zimbabwe were introduced into the country as ornamentals.Similar studies in other countries have shown that most invasive plants are ornamentals (Reichard & White 2001).Previous research has shown that whilst many herbaceous ornamentals have been accidentally introduced, woody ornamentals have been almost entirely introduced intentionally, mainly for landscaping (Reichard & White 2001).The accidental introduction of alien plant species into Zimbabwe is also due both to the use of contaminated seeds in agricultural systems and as a result of human transport systems.Nowadays, intensive trade and the constant flow of people have resulted in a large plant transfer, crossing frontiers and geographical boundaries (Del Monte & Aguado 2003).
systematically recorded 62 alien species that grew as weeds in croplands, causing important economic damage in productive lands.The period between 1921 and 1980 was characterised by increased study of the Zimbabwean flora, which boosted awareness and recording of new invaders.Equally intriguing is the fact that the following ten notable introduced species classified as invasive aliens in this study were not documented until the 1960s: A. filiculoides (Azollaceae), Bidens bipinnata (Asteraceae), Cs, Casual aliens; Nt, Naturalised aliens; In, Invasive aliens.

FIGURE 3 :
FIGURE 3: The growth forms of 391 casual, naturalised and invasive alien plant species recorded in Zimbabwe.

FIGURE 4 :
FIGURE 4: Regions of origin of alien plant flora in Zimbabwe.
Azolla filiculoides Lam.(Azollaceae), Microlepia strigosa (Thunb.)C. Presl (Dennstaedtiaceae), Microsorum scandens (G.Forst.)Tindale (Polypodiaceae) and Salvinia molesta D.S. Mitch.(Salviniaceae).All five species were introduced to Zimbabwe as ornamentals (Online Appendix).Gymnosperms were represented by Cupressaceae and Pinaceae families composed of Callistris calcarata F. Muell., Cupressus lusitanica Mill., Cupressus torulosa D. Don, Pinus elliottii Engelm., Pinus patula Schltdl.and Cham.and Pinus roxburghii Sarg.; all introduced to Zimbabwe at the turn of the 19th and 20th centuries, mainly for timber and as ornamentals (Online Appendix).Dicotyledons constituted the majority of alien flora, with 323 species (82.6%), and monocotyledons contributed 58 species (14.8%).A large number of casual, naturalised and invasive alien plant species in Zimbabwe (289, 73.9%) are from 16 families (Table 1).Plant families with the highest number of casual, naturalised and invasive alien plant species were: Asteraceae (53 species), Fabaceae sensu lato (49 species), Poaceae (48 species) and Solanaceae (21 species).The genera with the highest number of casual, naturalised and invasive alien plant species were Ipomoea with nine species, Acacia and Euphorbia with eight species each, Chenopodium and Senna with seven species each, Eucalyptus with six species, and Oenothera, Physalis and Solanum with five species each.The earliest recorded dates of the alien plants in this study are based on herbarium collections (Online Appendix).The oldest collections date back to the late 1800s, with Nicotiana tabacum L. collected in 1870, Populus X canescens (Aiton) Sm collected in 1874, C. torulosa D.Don collected in 1895, Eucalyptus camaldulensis Dehnh.collected in 1897 and C. lusitanica Mill.collected in 1900.Most of the species were first collected between 1941 and 1960 (Online Appendix).

TABLE 1 :
Families with the largest number of casual, naturalised and invasive alien species (with more than 5 taxa) in Zimbabwe.

TABLE 2 :
Possible reasons for the introductions of the alien flora into Zimbabwe.Species may have been allocated to more than one category.