DISTRIBUTION AND POTENTIAL IMPACT OF FERAL COTTON ON THE REINTRODUCTION OF COTTON IN THE SOUTHERN HIGHLANDS, TANZANIA

O Shilla1, TP Hauser2 and FI Tibazarwa3 1Tropical Pesticides Research Institute (TPRI), Plant Quarantine and Biosafety Office, P.O. Box 3024. 2Department of Agriculture and Ecology, Faculty of Life Sciences, University of Copenhagen, Rolighedsvej 21, DK- 1958 Frederiksberg Denmark. 3Department of Botany, University of Dar es Salaam, P.O Box 35060, Dar es Salaam, Tanzania [email protected] or [email protected], [email protected], [email protected] Corresponding author: FI Tibazarwa

ABSTRACT Cotton ( hirsutum) production is limited by bollworms that cause declining yields and poor lint quality. Generally, farmers manage pests by employing Integrated Pest Management (IPM) strategies, which include biological, cultural, physical and chemical approaches. Pest management by quarantine and pesticide sprays reduce production area and lead to resistance build-up. The Red bollworm, Dipsaropsis castanea is an important cotton pest of significant economical importance to Tanzania. The pest invaded the Southern Highlands (SH) of Tanzania in 1960’s from southern neighbour countries causing the Government to quarantine cotton production from 1968 as measure to limit the spread of the red bollworm. Transgenic Bt cotton with insecticidal properties presents a potential solution to the bollworm infestation in Tanzania. However, concerns associated with transgenic crops viz.; transgene flow to wild and feral relatives, increased potential for resistance evolution, need to be addressed prior to adoption of any transgenic crop. Information from national herbaria, research stations and a field survey established sparse distribution and diversity of feral cotton species G. barbadense, an exotic ornamental from Brazil though as isolated garden plants. Informal interviews revealed medicinal and fibre value of the ornamental. Diploid wild cotton relatives such as G. longicalyx and Gossypoides kirkii were also recorded but are incompatible to G. hirsutum. Field observations indicate continued red bollworm presence in the SH on feral cotton, but low in number as plants are few and isolated. Cluster analysis indicates presence of hybrid remnants of G. hirsutum and G. barbadense suggesting potential for gene flow.

Keywords: Bt cotton, bollworms, quarantine, insecticides, resistance, feral cotton, refuge plant

INTRODUCTION self-pollinating allotetraploids of the AD- Cotton is the world most important fibre genome. Other Gossypium species that also crop that is mainly produced by two species produce fibres are G. arboreum and G. Gossypium hirsutum and G. barbadense. G. herbaceum are diploid, A-genome species hirsutum accounts for over 95% of (Rana et al. 2007). commercial cotton and G. barbadense also known as Pima cotton provides less than 5% Cotton production is limited by insect pests (Lukonge et al. 2008). These two species are and diseases that cause decline in yield and

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poor lint quality in most producing following a decade of use (Martin et al. countries. The yield losses from insect pests 2002). Furthermore, insecticide use is alone are estimated at 24% in Sub-Saharan discouraged due to side effects on human Africa, 13% in South America and only 7% and health, contamination of the in Australia where control has been more environment and cost (Aldridge, 1998; effective but expensive (Oerke and Dehne Martin et al. 2002; Sinzogan et al. 2004; 2004; Deguine et al. 2008). Of all the cotton Achaleke et al. 2009). Biotechnological insect pests, the bollworms are of particular options such as transgenic cotton genetically economic importance as they cause engineered to incorporate Bacillus significant destruction of crop (Kabissa and thuringiensis (Bt) with insecticidal Nyambo, 1989). Bollworms are extremely properties are currently commercially destructive in their larval stages feeding on employed in several cotton growing cotton leaves, flowers and boring into the countries (James C 2003). Bt cotton is bolls (Deguine et al. 2008). widely grown in the United States of America, China and India where yields have In Africa, the red bollworm, been higher than non-Bt cotton (James C castanea and other species Helivicopera 2003). armigera, H. zea and Heliothis armigera have caused cotton losses of up to 75% in Despite the potential benefits of Bt cotton, Mozambique and Zambia, while in Malawi there are concerns regarding production of 70% losses is due to the red bollworm alone transgenic crops. These risks include (Kabissa and Nyambo, 1989). In Makathini, undesirable transgene flow to wild and feral South Africa in addition to D. castanea relatives that can in turn lead to increased other bollworm species H. armigera, Earias rates of resistance development where wild biploga, and E. insulana have also caused and/ or feral relatives act as refugia to the considerable damage (Ismael et al. 2002; pests. For Bt cotton, it is argued that Morse et al, 2004). In Tanzania D. castanea transgenes through hybridisation may cross infestation led to a quarantine of cotton into wild Gossypium species and if the production in the Southern Highlands (SH) hybrids express the Bt toxin it may influence of Tanzania to prevent spread to other the selection pressure which may enable growing areas since 1968 (Kabissa and bollworms evolve resistance to the Bt toxin. Nyambo, 1989). Despite this cotton remains This is a real concern as two crop pests; the the second most important cash crop in Plutella Xyllostella (diamondback ) and Tanzania, contributing about 15% per year Trichoplusia ni have already evolved to the foreign currency exchange earning resistance to conventional Bt sprays in the and approximately 40% of the population field; and laboratory tests have shown depend solely on cotton for their selection of resistance in Heliothis/ employment (Lukonge et al. 2005). (Tabashink et al. 1994, 2003; Fitt, 2000; Chilcutt and Tabashnik 2004; Insecticide sprays are the main means for Morin et al. 2004; Soberon et al. 2007; bollworm control. Cotton utilizes more Raymond et al. 2007). Resistance to insecticides than any other single crop in the transgenic Bt cotton and other Bt crops has world (James 2003). Insecticide sprays have been observed in certain areas but it is limited efficiency due to the development of argued that good integrated pest resistance over time (Rashid et al. 2008). H. management practices and appropriate armigera for example developed resistance mitigation measures such as refugia can to pyrethroids in the U.S.A and likewise in significantly delay resistance development Australia, Burkina Faso, Benin and Mali

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(Bourguet 2004; Tabashnik et al, 2003 and Namatuhi, Lilambo, Kitanda-A, Kitanda-B Tabashnik 1994a). and Naikesi in Ruvuma region; and Mng’elenge-A and Mng’elenge-B in Iringa In the event, Tanzania considers region. introduction of Bt cotton in the SH this would revive farmer incomes, and make Sampling and morphological significant contribution to total cotton characterisation was done using the production. The present study was thus International Board for Plant Genetic undertaken to establish the presence and Resources (IBPGR 1985) and Union for the distribution of feral cotton and socio- Protection of new Varieties, (UPOV 2001) economic values/ issues associated with it in targeting the flowering period for the SH. This information is necessary to morphological character scoring. At each provide premises for informed-decision location four individual plants were sampled making prior to adoption of Bt cotton. and presence of bollworm larvae recorded. Three different people noted the MATERIALS AND METHODS morphological characters using the Wild and Feral Cotton Distribution in designated codes that were later converted to Tanzania a binary matrix system. Scored characters Wild and feral cotton distribution in included; petal colour, basal petal spot, Tanzania was established using documented pollen colour, boll (shape, surface and information from two herbaria viz. National colour), leaf (colour, hairiness and shape), Herbarium of Tanzania (NHT), the seed (fuzzy/no fuzz, fuzz colour, nature, University of Dar es Salaam and two cotton number per boll) and locules per boll. research centres i.e. Lake Zone Agricultural Principal component analysis (PCA) from Research and Development Institute the R-2.9.2 software program was used to (LZARDI)-Ukiriguru and Agricultural test variation in specimen based on Research Institute (ARI)-Ilonga in 2006. morphological markers. Twenty two Information housed at these institutions herbarium vouchers were collected from the provided specimen records, collection sites, SH, fourteen of which had complete floral and phenology. Selection of sites for the and vegetative information were sent to the field survey in the SH were decided Royal Botanical Gardens, Kew, United following information from collected Kingdom for identification and the specimen records and consultation with ARI remaining eight that did not have complete staff. information were deposited at the Botany Department herbaria, University of Dar es Survey in the Southern Highlands (SH) Salaam. Cotton Quarantine Zone Selected villages in Ruvuma (East), Mbeya Informal interviews (open-ended questions) and Iringa (West) regions in the SH of were conducted with four randomly selected Tanzania were surveyed from end of August villagers at each of the twenty sampling to early September 2006 to establish points (Table 2) to gather information on localities of wild and/ or feral cotton plants. feral cotton. The questions were focused on The specimens were collected from the use of the plants, whether the plants were following sites/locations of the SH; Ipinda, planted intentionally or grew on their own Ushirika, Lutusyo, Ikulu, Magamba, Ifumbo, and where seeds were sourced. The Ifumbo-makona, Mbala, and in Mbeya information was used to establish whether region; Hanga-A, Hanga-B, Sinai-A, Sinai- there was a single source or mixed seed B, Sinai-C, Luhimbililo, Likuyufusi, source that would enable inference to be

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drawn on the observed variations within the brasilience as G. barbadense and listed feral cotton surveyed. characteristics of the species as having a yellow corolla with dark red or purple centre RESULTS (petal spot), free or fused seeds, 3-7 lobed Wild and Feral Cotton Distribution leaves and glabrous, pitted, elongate bolls Herbaria records indicated the presence of with 3 locules and broadly ovate bracts of only one true wild diploid cotton species; epicalyx. The FTEA also discourages use of Gossypium longicalyx (F-genome) and a the variety names; mariegalante and species of the sister tribe Gossypieae; brasilience. The eight voucher specimens Gossypioides kirkii to occur in Tanzania. that had not been sent to the Royal Botanical Gossypioides kirkii records are from the Gardens, Kew were also identified as G. Coast, Arusha and Tanga regions and G. barbadense using the FTEA in Dar es longicalyx records are from Dodoma and Salaam. The morphological characters used Iringa regions. The records show that both in the FTEA classification were adopted for species are found in habitats ranging from this study with some exceptions that not all forest edge to lowland and seasonally wet plants had a purple spot and some plant bolls open Acacia bush land. Neither of the two were not elongated but rather oval (See species was observed in the SH. Table 1). G. barbadense plants were found to be sparsely distributed in the SH with a Records at the ARI stations by Nyambo few individuals in home gardens and no (1989) and Temu and Mrosso (1999) listed large populations. two feral species of cotton, introduced from the Americas, that is G. barbadense var. Principal Component Analysis (PCA) using brasilience Macf and G. hirsutum var. the morphological markers showed two mariegalante Watt. G. hirsutum may have main groupings of individuals collected established as feral populations after from the Eastern villages (Ruvuma) and previous cultivation. G. barbadense var. Western villages (Mbeya and Iringa) (See brasilience was cited as being a common Figure 1). The distances between collecting bush in East Africa also known as kidney areas ranged from 150Km to 270Km. The cotton. In Tanzania the records indicated the overall variation as explained by PCA is distribution of G. barbadense to be Songea 66%, which infers that variations between Highlands at the head of Lake Nyasa. G. individual plants were significant. barbadense was introduced by the Arabs Individuals grouped according to during their colonial era as an ornamental. geographical region with some exception The two populations of cotton may have such as individuals from Lutusyo village adapted to the unmanaged conditions and which is in Mbeya region grouped with the persisted in the environment as feral cotton. Eastern individuals and those from Mng’elenge_A and Mng’elenge B grouped Confirmation of Feral cotton identity with the Western individuals from Ruvuma All the 14 specimens sent to the Royal region. It is likely that some seeds have been Botanical Gardens, Kew were identified as dispersed between Ruvuma and Mng’elenge feral G. barbadense using morphology as (Iringa) as these places border each other or documented in the Flora of Tropical East moved by farmers from one location to the Africa (FTEA) Family Malvaceae of 2007. other as the feral cotton was primarily The FTEA re-classified G. barbadense var. introduced as an ornamental.

93 Shilla et al. - Feral Cotton in the Southern Highlands of Tanzania … Table 1: Morphological Markers Scored from different individual Plants

Petal Pollen Seed Leaf Petal Boll Boll colour Boll Seed leaf Village Region colour colour natue hair spot shape surface fuzzy colour deep deep fused- deep Hanga A absent oval deep green pitted naked short yellow yellow black green deep deep fused- deep Hanga B absent oval light green pitted naked short yellow yellow black green deep deep singly- deep Kitanda A present oval deep green pitted naked short yellow yellow black green light deep green- deep Kitanda B absent oval deep green pitted singly short yellow yellow fuzzy green deep singly- deep Likuyufusi absent cream conical light green pitted naked short yellow black green deep singly- deep Lilambo present cream conical deep green pitted naked glabrous yellow black green deep deep singly- deep Luhimbililo present oval light green pitted naked glabrous yellow yellow black green

Ruvuma Region light pale singly- deep Naikesi absent oval deep green pitted naked glabrous yellow yellow black green deep deep singly- deep Namatuhi present oval light green smooth naked long yellow yellow black green light deep singly- deep Sinai A absent oval deep green pitted naked short yellow yellow black green deep deep singly- deep Sinai B absent oval deep green smooth naked short yellow yellow black green deep deep green- singly- deep Sinai C present oval deep green pitted short yellow yellow fuzzy black green

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light deep fused- deep Ushirika absent conical deep green pitted naked short yellow yellow black green

light deep fused- deep Ikulu absent conical light green pitted naked short yellow yellow black green light deep green- deep Ipinda absent conical light green pitted fused short yellow yellow fuzzy green deep deep singly- deep Lutusyo present conical deep green pitted naked glabrous yellow yellow black green Ifumbo- light deep fused- deep absent conical light green pitted naked short makona Mbeya Region yellow yellow brown green light deep fused- light Ifumbo absent conical light green pitted naked short yellow yellow black green deep deep fused- deep Magamba present conical deep green pitted naked short yellow yellow brown green light deep singly- deep Mbala absent conical light green pitted naked short yellow yellow brown green Mng'elenge deep deep fused- deep absent conical deep green pitted naked long A yellow yellow black green Mng'elenge deep deep fused- deep Iringa Region absent conical deep green pitted naked long B yellow yellow brown green

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Figure 1: PCA analysis of the G. barbadense individuals collected in the East and West SH; crossed squares indicate the accessions identified at Kew

Red bollworm larvae were observed on stronger than that from G. hirsutum. cotton plants at two different locations; Furthermore the lint was used to make local Ipinda (4 larvae) and Ushirika (3 larvae) all mattresses and wicks. Local names for feral in Kyela district. In other areas dry bored G. barbadense varied between regions, in bolls indicated presence of larvae, as the ‘Undendeule’ in Ruvuma region it is called organisms were not observed. ‘Litonje’, in the Kyela district in Mbeya region it is called ‘Masapa’ while in several Consulted communities and individuals in other regions it is known as ‘pamba pori’in the SH indicated medicinal and lint value of Kiswahili. feral G. barbadense. G. barbadense serves as an antiseptic for cleaning wounds, leaf DISCUSSION and root concoctions treat convulsions and The present study established the presence, stomach ache and the oil from seeds cures distribution and the reasons why feral G. ear aches. G. barbadense fibre is considered

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barbadense plants are maintained by found that the tree cotton of G. barbadense communities in the SH. had a characteristic feature of naked seeds fused to form a typical kidney structure in Identification by experts from Kew Royal each locule of the capsule, whereas Acland Botanical Gardens and the FTEA Malvaceae (1971) and Purseglove (1968) showed that (2007) using keys indicate that all the G. barbadense has dark brown and pitted collected voucher specimens to be feral G. bolls, usually 3 locules with 5 to 8 seeds per Barbadense, the PCA grouping using the locules. It can be argued that the characterised morphological markers morphological grouping observed in the separates individuals from different PCA diagrams is due to these differences as geographic areas. PCA groupings suggest examination of the individuals from subtle phenotypic variations within the Magamba, Mng’elenge-A and Mng’elenge- recorded G. barbadense individuals. For B show grouping based on shared characters instance, some plants lacked purple spots, of yellow petals, deep yellow pollen; conical there was variation in petal yellowness and pitted bolls with non-fuzz fused seeds, ranging from deep to pale yellow and boll deep green leaves lacking a petal spot. The shape which was recorded as oval or conical distinction between G. barbadense (see Table 1). The observed variations can populations using morphological characters be plausibly argued on two fronts; firstly provides some insight to parent origin but environmental factors that are known to for purposes of taxonomic grouping all influence morphological markers may individuals collected from the SH are account for the different groupings (Lihova considered one species i.e. G. barbadense. et al. 2007). Secondly, the variations may have arisen from natural intraspecific The presence of the Red bollworm larvae on crossing, where offspring deviate from their feral G. barbadense suggests that the pests parents for some of the characters. Lastly, continue to thrive on other plants in the the informal consultations revealed that absence of the quarantined G. hirsutum. seeds from good lint producing plants have Temu and Mrosso 1999 postulate G. been exchanged between villages and barbadense to be the main host for the regions with minimal monitoring and this bollworm as it was not found on any other may explain variation of characters such as plant species, in this survey similar the colour and spots. Furthermore, observations were made though the intraspecific crossing is also a strong examination of all species was not possibility taking into account that these comprehensive. plants have co-existed together for a significant period. Under normal Implications to G. hirsutum circumstances the intraspecific crosses in G. barbadense and G. hirsutum have the cotton is very low (1-5%) in the absence of same ploidy level and related genomes. This large pollinators like bees as cotton pollen is suggests that the two species can hybridise heavy. giving rise to the probability of cultivar-to- feral out crossing and the likelihood of gene The findings of this study complement that flow (Brubaker et al. 1999). Transgenic G. of Fontes et al. (2005) who observed two hirsutum with the Bt gene insert is distinct G. barbadense populations based on physiologically and genetically similar to seed form; one with unattached seed and the conventional cultivars. The presence of G. other with attached seeds (kidney cotton). barbadense in the SH that continues to Other studies also show similar distinctions thrive showing relative tolerance to the Red in seed form for example Singh et al. (2003) bollworm may be of some concern for

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resistance evolution against Bt toxin if the to consider management options that would G. barbadense is allowed to remain in the safeguard the minor likelihood of area. However as the distribution of G. hybridisation between the two species. barbadense is sparse with no distinct Furthermore as the survey was limited to the populations at any one point this may be a SH it would be of added value if similar barrier to pollen mediated gene flow. This studies were conducted in other cotton postulation however, requires confirmation growing areas to establish the potential for through surveys in other parts of the country gene flow and resistance development where that will inform on the potential for gene introduction of Bt cotton may be considered. flow. The value attached to the feral cotton by the communities may be due to the lack of G. A lack of clear differences in geographically hirsutum and or access to modern clinics, an isolated individuals suggests that there has extended study in other parts of the country been movement of genes between the would serve to confirm this assumption. locations, as confirmed by the consultations. For introduction of Bt cotton management ACKNOWLEDGEMENT strategies that ensure seed movement The authors thank ARI-Ilonga for the between growing areas is monitored to avoid technical assistance in the field survey and spread of transgenes are necessary. staff from the three Tanzania herbaria for the key botanical information. Furthermore the Public participation in implementing communities of the SH who contributed management options is vital since the study their knowledge through the interviews are has shown that feral plants are of value to acknowledged. This work was sponsored by some of them and that is why plants are a grant from the BioSafeTrain Project (An found not very far from farmyards and along ENRECA-DANIDA project number DFC the roadsides. Furthermore, if Bt cotton is to 720-AU2, this is paper Number 22 of the be introduced in the SH apart from gene project). flow other pest management and socio- economic concerns would need to be REFERENCES addressed in the risk assessment such as the Achaleke J, Vaissayre M and Brevault T capacity for adoption, need for refugia 2009 Evaluating Pyrethroid Alternatives among others. for the Management of Cotton Bollworms and Resistance in Cameroon. CONCLUSION Exp. Agric. 45(1):35-46. Based on the findings of the study it can be Acland, J. D 1971 East African crops, concluded that feral G. Barbadense FAO\Longman, ISBN, London distribution in the SH does not pose a Aldridge, S 1998 “Insect resistance: From significant threat to the introduction of Bt mechanisms to management”, New Sci. cotton. This is because the isolated 160: 1-4 occurrence of the feral individual plants Brubaker CL, Brown AHD, Stewart JM, would not facilitate significant gene flow Kilby, MJ and Grace JP 1999 Production between the transgenic and feral plants. of fertile hybrid germplasm with diploid Likewise despite the occurrence of the red Australian Gossypium species for cotton bollworm on the feral cotton, individual improvement. Euphytica. 108(3):199- plants do not offer sufficient refugia to allow 213. the pest to grow populations that would Chilcutt CF and Tabashnik BE 2004 facilitate resistance build up to Bt. However, Contamination of refuges by Bacillus prior to Bt cotton introduction it is necessary thuringiensis toxin genes from transgenic

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