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Adaptation of Bemisia tabaci biotype B (Gennadius) to cassava, Manihot esculenta (Crantz)
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Crop Protection 24 (2005) 643–649 www.elsevier.com/locate/cropro
Adaptation of Bemisia tabaci biotype B (Gennadius) to cassava, Manihot esculenta (Crantz)$ A. Carabalia, A.C. Bellottia,, J. Montoya-Lermab, M.E. Cuellara a
International Center for Tropical Agriculture (CIAT), A.A. 6713, Cali, Colombia b Universidad del Valle, Cali, Colombia
Received 13 February 2004; received in revised form 4 November 2004; accepted 8 November 2004
Abstract Bemisia tabaci is a recognized pest in cassava (Manihot esculenta) crops in Asia and Africa, where it transmits the cassava mosaic geminiviruses (CMGs) (family: Geminiviridae, genus: Begomovirus). A general consensus exists that B. tabaci is a complex of morphologically indistinguishable populations with different biological biotypes. In the Americas, though the polyphagous B. tabaci biotype B appears to feed on cassava, it is postulated that the absence of CMGs is related to the inability of this biotype to colonize this crop effectively. However, its potential adaptation is considered a threat for cassava production in the Neotropics. This study was initiated to verify whether B. tabaci can become gradually adapted to M. esculenta. Trials in rearing chambers were carried out measuring population development of whitefly individuals passed through a series of intermediate hosts, previously selected and based on phylogenetic closeness to Manihot. The capacity of biotype B to adapt gradually to cassava, started on a legume (Phaseolus vulgaris), followed on two Euphorbiaceae (Euphorbia pulcherrima and Jatropha gossypiifolia) until, finally reaching a commercial cassava variety. B. tabaci female mean longevity on cassava, coming from P. vulgaris, E. pulcherrima and J. gossypiifolia was 3.1, 5.6 and 3.3 days, respectively. The highest oviposition rate (2.6 eggs/female/2 days), the shortest development time (44.4 days) and the highest value of rm (0.48 day1) were for populations coming from J. gossypiifolia, where 27.5% of the individuals coming from this host survived and reproduced on cassava. The importance and potential impact of phylogenetically close plants as intermediate hosts faciliting the adaptation of B. tabaci biotype B to cassava is discussed. r 2004 Published by Elsevier Ltd. Keywords: Bemisia tabaci; Biotype B; Manihot esculenta; Adaptation; Hosts
1. Introduction Bemisia tabaci (Homoptera: Aleyrodidae) is considered one of the most important pests in tropical and subtropical agriculture, as well as in production systems in glasshouses in temperate zones (Byrne and Bellows, 1991; Byrne et al., 1990). Since the 1980s, it has caused considerable economic losses in the southern United States, Mexico, Venezuela, the Eastern Caribbean $
Recent evidence suggests that B. tabaci represents a species complex with numerous biotypes and two described cryptic species. The binomial B. tabaci is used here in the broadest sense to include all members of the species complex. Corresponding author. Fax: +57 2 450073. E-mail address: [email protected] (A.C. Bellotti). 0261-2194/$ - see front matter r 2004 Published by Elsevier Ltd. doi:10.1016/j.cropro.2004.11.008
Basin, and Central and South America due to its proven efficiency as a virus vector, together with damage caused by direct feeding and excretion of honeydew (Brown et al., 1995; Oliveira et al., 2001). Many biotypes have been identified in different regions of the world, which suggests that B. tabaci may be a complex of species and biotypes (Perring, 2001; Abdullahi et al., 2003) undergoing continuous evolutionary changes. In the Americas there are complex associations between some hosts and various B. tabaci biotypes. In Puerto Rico, for example, the Sida biotype, which colonizes many species of plants including the genus Sida, to which it transmits several geminiviruses (family Geminiviridae: genus Begomovirus), and the Jatropha biotype, monophagous only on Jatropha gossypiifolia L., to which it specifically transmits
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the Jatropha mosaic virus (Brown et al., 1995), co-exist in the same geographic area but in different niches. After its first report and identification in the USA, the B. tabaci biotype B has become important due to its unique biochemical and biological characteristics. B. tabaci species complex adapts easily to new hosts and geographic regions. With the exception of Antarctica, it has been reported throughout the world (Martin et al., 2000) associated with almost 600 species of plants (Mound and Halsey, 1978; Secker et al., 1998). These include many cultivated and noncultivated species, annuals and perennials, which act as host plants, favoring its feeding and/or reproduction (Bedford et al., 1992; Brown et al., 1995; Butler and Henneberry, 1986). The families with the highest number of host species are Fabaceae, Asteraceae, Malvaceae, Solanaceae and Euphorbiaceae (Mound and Halsey, 1978). The introduced biotype B displays one of the broadest host range known among Bemisia whiteflies (Brown et al., 1995). However, unlike its West African counterpart the biotype B exhibits a wide polyphagous habit but cassava appears to be a nonsuitable host. Further, it had been speculated that the absence of cassava-infecting begomoviruses in South America is in part related to the inability of B. tabaci to colonize cassava (Bellotti and Arias, 2001; Costa and Russell, 1975). Nevertheless, B. tabaci was found feeding on cassava in Cuba (Va´squez et al., 1995) and specifically the biotype B in the Dominican Republic (Brown et al., 1995). These facts, together with the economic impact that affected southern USA, were attributed to the introduction and establishment of this highly invasive biotype B and its association to viral diseases (Brown et al., 1995; Brown and Bird, 1995). These examples indicate a potentially serious threat of the possible introduction of cassava mosaic geminiviruses (CMGs) to the Americas, especially because most traditional cassava cultivars in the Neotropics are highly susceptible to the disease. In addition, the B. tabaci species complex is the vector of viruses on several other crops often grown in association with or in proximity to cassava (e.g. beans, cowpea, sweet potatoes, string beans, tomatoes, cotton, soy bean) (Bellotti and Arias, 2001; Costa and Russell, 1975). The possibility of viral diseases moving among these crops or the appearance of new viruses represents a potential threat, e.g. tomato-yellow leaf curl virus infecting common bean (Navas-Castillo et al., 1999). In order to anticipate these events and as a prerequisite for developing any control measure (especially one that entails quarantine), research was initiated to evaluate the adaptative capacity of B. tabaci biotype B. The main goal of the present study was to verify, experimentally, the capacity of the biotype B to adapt on cassava. Specifically, it was evaluated, in a hypothetical but quantifiable manner (through life tables), possible ways in which this adaptation could occur in Colombia.
2. Materials and methods 2.1. Biotype B of Bemisia tabaci A strain of B. tabaci1 biotype B was obtained from individuals of a colony established at CIAT by the Bean Project in 1997, originating from Dapa County (Cauca Valley, Colombia). The strain was reared for five generations on Phaseolus vulgaris plants (variety ICAPijao) in cages made of tulle and wood (1 1 1 m) under controlled conditions (2572 1C, 7075% RH and a 12-h photophase) according to methodology proposed by Eichelkraut and Cardona (1989). Periodically, the purity of adult biotype B specimens in the colony was checked using RAPD-PCR (CIAT, 1999). 2.2. Adaptation of B. tabaci from P. vulgaris to M. esculenta (MCol 2063) The experimental hypothesis was that B. tabaci could become gradually adapted to M. esculenta by passing firstly through a series of intermediate hosts, previously selected based on phylogenetic closeness to Manihot (Burkill, 1994) and susceptibility to whiteflies. The adaptation process was initiated on a highly susceptible host (P. vulgaris L.), phylogenetically distant from M. esculenta; passing through two Euphorbiaceae (Euphorbia pulcherrima Willd. ex. Klotzch ‘‘poinsettia’’ and Jatropha gossypiifolia L. ‘‘jatropha’’), both intermediate hosts to B. tabaci, being relatively familiar and phyllogenetically close to Manihot. As the final host, the cassava cultivar MCol 2063 ‘‘var. Secundina’’ was selected for its known susceptibility to the whiteflies Aleurotrachelus socialis Bondar and B. tuberculata Bondar (Bellotti et al., 1999). Eight, 40 days old E. pulcherrima plants, divided into two cages (1 m 1 m 1 m) were each infested with an average of 4400 B. tabaci pupae on P. vulgaris leaves. These individuals had passed through five generations on the latter host. Later, young leaves of E. pulcherrima infested with an average of 5880 fifth generation B. tabaci pupae, were used to infest 8, 40 days old plants, of J. gossypiifolia using the above described methodology. Lastly, young J. gossypiifolia leaves containing an average of 7600 fifth generation B. tabaci pupae were used to infest 8, 35 days old M. esculenta (var MCol 2063) plants (Fig. 1). 2.3. Biology and demographic parameters of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia In order to determine the relative importance of each host involved in the sequence to reach the adaptation of 1 Unless a more specific designation is indicated, for practical reasons, the binomial B. tabaci is used here thereafter to refer to its Biotype B, which is so far the only one reported in Colombia.
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1 P.vulgaris (five generations)
2 E. pulcherrima (five generations)
3 J. gossypiifolia (five generations)
4 M. esculenta
Fig. 1. Host species sequence for the gradual adaptation of B. tabaci from P. vulgaris to M. esculenta. (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima and (4) on M. esculenta passed sequencially through P. vulgaris and E. pulcherrima and J. gossypiifolia.
B. tabaci on M. esculenta (Fig. 1), fecundity, longevity and development time, survival rate, proportion of females and demographic parameters were estimated and evaluated for individuals of B. tabaci on M. esculenta var. MCol 2063. All these data were obtained from individuals which in their previous five generations were reared: (1) only on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima (Fig. 2). All experiments were conducted at CIAT (Palmira, Colombia) in growth chambers under controlled conditions (2572 1C, 7075% RH and 12-h photophase). 2.4. Longevity and fecundity of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Forty pairs (males: females) of B. tabaci, recently emerged and coming from each of the three hosts of the sequence of adaptation: (1) P. vulgaris (2) E. pulcherrima and (3) J. gossypiifolia, were introduced in to clip cages (2.5 cm in diam. and 2 cm in depth), using a manual aspirator (impregnated with wax from the wings of adult whitefly to reduce the mortality due to manipulation), and placed on the undersides of M Col 2063 leaves. Every 48 h the adults were removed to a new area of the leaf until the natural death of females occurred. Males were replaced as they died. Fecundity was estimated by
B. tabaci / P. vulgaris
1
B. tabaci / E. pulcherrima
2
B. tabaci / J. gossypiifolia
3
Manihot esculenta MCol 2063
Fig. 2. Evaluation scheme of the biology and demographic parameters of B. tabaci on M. esculenta with individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
counting the number of eggs oviposited by the female every 48 h (in this way it was expected to reduce perturbation and mortality), while longevity was based on the maximum time (days) that a female lived. 2.5. Development time, rate of survival and proportion of females of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Fifty 2-day-old adults (males and females) of B. tabaci, originating from each of three hosts of the sequence of adaptation; (1) P. vulgaris, (2) E. pulcherrima and (3) J. gossypiifolia (Fig. 2), were placed with the aid of a manual aspirator in clip cages on the underside of M. esculenta (MCol 2063) leaves. After 6 h the adults were removed and 200 eggs were selected at random for
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rearing to adulthood. In each case, the development time from egg to adult, the survival rate of the immature stages, and the proportion of females emerged were recorded.
Table 1 Longevity (days), fecundity (eggs) and oviposition rate (eggs/female/2 days) of B. tabaci on M. esculenta (M Col 2063) of the individuals coming from host sequencea (n ¼ 40) Parameter
2.6. Demographic parameters of B. tabaci on M. esculenta with individuals coming from of host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Life tables were constructed following the methodology described by Manzano (2000). The data on the development time of the immature individuals were combined with experimental data from the lxmx reproduction to produce life tables and used to calculate the demographic parameters defined by Price (1975): (1) Net reproduction rate (Ro) or average number of female descendents that a female produces in one generation; (2) generational time (T), equivalent to the period comprised between the emergence of the parents and that of the progeny; and (3) intrinsic rate of population growth (rm), estimated by Carey’s (1993) equation: X expðrm xÞl x mx ¼ 1, where x is the age days of females, lx is the specific survival age, and mx is the proportion of females from the progeny of a female with age x. In calculating the values of rm, the corrected age X+0.5 was used; and the equation ln 2/rm was used to estimate the days needed for the population to double in number (Carey, 1993). 2.7. Statistical analyses Differences between the mean values of longevity, fecundity, oviposition rate and development time were tested by Kruskal–Wallis test. When required, Student– Newman–Keuls was further used for multiple pair-wise comparisons. Values for survival rate of immature individuals were compared using Chi-square test.
3. Results and discussion 3.1. Biology and demographic parameters of B. tabaci on M. esculenta (MCol 2063), with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia 3.1.1. Longevity, fecundity and oviposition rate of females The highest longevity mean (5.6 days) was obtained on females coming from E. pulcherrima, surpassing their counterparts coming from P. vulgaris (3.1) and J. gossypiifolia (3.3), respectively (Table 1). Both values were statistically different when compared with
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
Average longevity 3.3 b Range 2–10 Average fecundity 8.6 a Range 1–41 Average oviposition rate 2.6 a Range 0.5–8
5.6 a 2–18 7.7 a 1–48 1.4 b 0.4–3
3.1 b 2–10 1.8 b 1–19 0.6 c 0.5–3.5
Averages followed by different letters between columns differ significantly (Kruskal–Wallis Po0:0001; followed by Student–Newman–Keuls Po0:05). a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
E. pulcherrima (Student–Newman–Keuls Po0:05; after Kruskal–Wallis Po0:001); differences can clearly be seen in the survival curves (Fig. 3). Nevertheless, the populations coming from E. pulcherrima survived 39% less than those obtained by Sa´nchez et al. (1997) with B. tabaci on favorable hosts such as cotton (Gossypium hirsutum L.) and tomatoes (Lycopersicon esculentum Mill.). Independent of their origin, all biotype B females initiated oviposition during the first 2 days (Fig. 4), and by the sixth day the females coming from J. gossypiifolia and P. vulgaris had oviposited 50% of their eggs on M. esculenta. The highest oviposition rate (2.6 eggs/female/ 2 days) was found in females coming from J. gossypiifolia, being significantly higher than that of females coming from the other two hosts (Student–Newman– Keuls Po0:05; after Kruskal–Wallis Po0:001) (Table 1). Nevertheless there was variability in the maximum oviposition days, being 2, 6 or 12 days, depending on the female’s origin, established previously on J. gossypiifolia, P. vulgaris and E. pulcherrima, respectively (Fig. 4). The results obtained with the females coming from J. gossypiifolia and P. vulgaris concur with reports by Gameel (1974, cited by van Lenteren and Noldus, 1990), who found that the maximum oviposition of B. tabaci occurs in the first week of adult life. In contrast, the average fecundity on M. esculenta was 8.6 and 7.7 eggs when the females came from J. gossypiifolia and E. pulcherrima, respectively (Table 1). These values were significantly different from those obtained for females coming from P. vulgaris (1.8 eggs) (Student–Newman– Keuls Po0:05; after Kruskal–Wallis Po0:001). The analyses of the previous results show that when populations of B. tabaci are reared for some generations through the sequence of hosts: P. vulgaris–E. pulcherrima–J. gossypiifolia, they have higher rates of oviposition
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Table 2 Development time, survival and proportion of females of individuals of B. tabaci on M. esculenta (MCol 2063) coming from host sequencea
E. pulcherrima J. gossypiifolia P. vulgaris
Parameter
2
4
6
8
10
12
14
16
18
20
Age of females (days)
Fig. 3. Survival curves of B. tabaci on M. esculenta MCol 2063 with individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
9 8
Eggs/female/2 days
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
0
E. pulcherrima J. gossypiifolia P. vulgaris
7 6 5 4 3 2 1 0 0
647
2
4
6
8
10
12
14
16
18
20
Age of females (days)
Fig. 4. Curves of oviposition of B. tabaci on plants of M. esculenta (MCol 2063) of the individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
and longevity on M. esculenta than if they are transferred directly from P. vulgaris to M. esculenta. 3.1.2. Development time, rate of survival of the immature stages and proportion of females The means of development time were not significantly different (Kruskal–Wallis P ¼ 0:102). However, individuals of B. tabaci coming from J. gossypiifolia took 44.4 days to develop on M. esculenta, a shorter time by about 6 days, compared when coming from E. pulcherrima and P. vulgaris (Table 2). On the other hand, the highest survival rate in the immature stage (27.5%) was found in individuals coming from J. gossypiifolia, being significantly different (Student–Newman–Keuls Po0:05; after Kruskal–Wallis Po0:001) from those coming from E. pulcherrima (3%) and P. vulgaris (2%) (Table 2). The shortest development time of B. tabaci on M. esculenta when the populations had been established previously on J. gossypiifolia, can be interpreted as a better biological adaptation of the insect to the closest phylogenetic host. Therefore it is possible to consider J. gossypiifolia as a ‘‘principal link’’ in the gradual
Development time (days) 44.4 ns No. of insects 55 27.5 a Survival rate (%)b No. of insects 200 Proportion of females (%) 51.0 No. of insects 55
50.6 6 3.0 b 200 50.0 6
49.5 4 2.0 b 200 50.0 4
a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima. b Averages followed by different letters in the columns differ significantly, w2 ¼ 16:7; 2 df, Po0:0002; followed by Student– Newman–Keuls Po0:05:
adaptation of B. tabaci to M. esculenta, passing previously from E. pulcherrima and P. vulgaris. The proportion of females of B. tabaci biotype B, independent of the host of origin, was not affected by developing on M. esculenta as the sex ratio was 1:1. These results are similar to those reported for B. tabaci by Eichelkraut and Cardona (1989) and Sa´nchez et al. (1997). 3.1.3. Demographic parameters Based on the net reproduction rate (Ro), it was possible to determine that after one generation, on average, the populations of B. tabaci can multiply 11.6 times (individual/individual) on cassava when they come from E. pulcherrima, being 1.3 and 6.3 times higher, respectively, than when they come from J. gossypiifolia and P. vulgaris (Table 3). A generation time of B. tabaci on M. esculenta is 44.8 days when the populations come from J. gossypiifolia, 7 and 11 days less than for those populations coming from P. vulgaris and E. pulcherrima, respectively. In other words, B. tabaci biotype B can reach up to eight, seven or five generations/year on M. esculenta dependent upon previous host; J. gossypiifolia, P. vulgaris or E. pulcherrima, respectively (Table 3). The population established previously on J. gossypiifolia had the higher value of the intrinsic growth rate (0.05), which decreased slightly for E. pulcherrima (0.04) and lower still for P. vulgaris (0.02). On M. esculenta females of B. tabaci coming from J. gossypiifolia can double their population in significantly less time (14.4 days) than those from P. vulgaris (34.7 days). Results of intrinsic growth rates (rm) reveal a higher population growth on M. esculenta when coming from J. gossypiifolia, exceeding those from E. pulcherrima by 8.3% and up to 58.3% for those from P. vulgaris. In the case of individuals coming from E. pulcherrima, the rm value was favored by their fecundity as compared to
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Table 3 Demographic parameters for individuals of B. tabaci on M. esculenta (MCol 2063) coming from host sequencea (n ¼ 200) Parameter
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
8.6 Net reproductive rate (Ro) Generational time (T) 44.8 Intrinsic growth rate (rm) 0.05 Time for duplication 14.4 (TD)
11.6
1.8
56.0 0.04 17.3
51.3 0.02 34.7
a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
that of the individuals coming from J. gossypiifolia (Table 3). Our findings have both academic and economic implications. Firstly, from the analysis of our results and in light of the scientific literature, it is plausible to affirm that M. esculenta might represent, in the near future, a suitable host for B. tabaci in Colombia. Demographic parameters suggest that an increase in the capacity for adapting to M. esculenta, favored by the influence of phylogenetically related hosts, such as J. gossypiifolia, might act as gradual points in which the insect increases its biotic potential, facilitating its adaptation to M. esculenta. Indeed, this fact constitutes one of the principal findings of this study, actually confronting the apparent lack of adaptive capacity of B. tabaci on M. esculenta, a host on which, according to Costa and Russell (1975), it does not feed or reproduce in the Americas. Secondly, in view of these findings and the constant presence of cassava cultivars throughout the year, it is possible to hypothetise the host specialization of B. tabaci on Colombian cassava. The occurrence of this ‘‘host-shifting’’ can be favored by J. gossypiifolia and E. pulcherrima, acting as gradual hosts. A similar adaptative scenario is reported by Abdullahi et al. (2003) for the African B. tabaci populations associated with cassava. Although the available evidence precludes an actual estimation of the time that this specialization will demand, it is likely that B. tabaci, despite its ‘‘experimental’’ low potential for development, can in just a few generations, adapt to cassava cultivars. This situation can be anticipated based on the dramatic and rapid increases undergone by the B. tabaci populations in recent years (Brown et al., 1995; Quintero et al., 1998; Perring, 2001). On academic grounds, the experimental adaptation of B. tabaci, through different phyllogenetically related hosts to Manihot, might produce a useful model to understand the evolutive potential of this important pest. The differences on fecundity and survival detected
between individuals coming from the adaptation sequence might increase in a progressive way, the biological fitness of B. tabaci. Thus, in the long term, after several generations, a change in its phenotype can be expected.
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ARTICLE IN PRESS A. Carabali et al. / Crop Protection 24 (2005) 643–649 Oliveira, M.R.V., Henneberry, T.J., Anderson, P., 2001. History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot. 20, 709–723. Perring, T.M., 2001. The Bemisia tabaci species complex. Crop Prot. 20, 725–737. Price, P., 1975. Insect Ecology. Wiley, New York 514pp. Quintero, C., Cardona, C., Ramirez, D., Jime´nez, N., 1998. Primer registro de Biotipo B de Bemisia tabaci (Homoptera: Aleyrodidae) en Colombia. Rev. Col. Entomol. 24, 23–28. Sa´nchez, A., Geraud-Pouey, F., Esparza, D., 1997. Bionomics of the tobacco whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) and potential for population increase on five host plant species. Rev. Fac. Agron. (LUZ) 14, 193–206.
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Secker, A.E., Bedford, I.D., Markham, P.G., de Courcy Williams, M.E., 1998. Squash, a reliable field indicator for the presence of the B biotype tobacco whitefly, Bemisia tabaci. Br. Crop Prot. Counc. Brighton Conf. 3, 837–842. van Lenteren, J.C., Noldus, P.J.J., 1990. Whitefly relationships: behavioural and ecological aspects. In: Whiteflies: Their Bionomics, Pest Status and Management. Department of Entomology, Agricultural University Wageningen, Netherlands, pp. 47–89. Va´squez, L.L., Jime´nez, R., Iglesia, M., Mateo, A., Lopez, D., Vera, E.R., 1995. Moscas blancas (Homoptera: Aleyrodidae) detectadas en los principales cultivos agrı´ colas de Cuba. Manejo Integrado Plagas (Costa Rica) 36, 18–21.
Crop Protection 24 (2005) 643–649 www.elsevier.com/locate/cropro
Adaptation of Bemisia tabaci biotype B (Gennadius) to cassava, Manihot esculenta (Crantz)$ A. Carabalia, A.C. Bellottia,, J. Montoya-Lermab, M.E. Cuellara a
International Center for Tropical Agriculture (CIAT), A.A. 6713, Cali, Colombia b Universidad del Valle, Cali, Colombia
Received 13 February 2004; received in revised form 4 November 2004; accepted 8 November 2004
Abstract Bemisia tabaci is a recognized pest in cassava (Manihot esculenta) crops in Asia and Africa, where it transmits the cassava mosaic geminiviruses (CMGs) (family: Geminiviridae, genus: Begomovirus). A general consensus exists that B. tabaci is a complex of morphologically indistinguishable populations with different biological biotypes. In the Americas, though the polyphagous B. tabaci biotype B appears to feed on cassava, it is postulated that the absence of CMGs is related to the inability of this biotype to colonize this crop effectively. However, its potential adaptation is considered a threat for cassava production in the Neotropics. This study was initiated to verify whether B. tabaci can become gradually adapted to M. esculenta. Trials in rearing chambers were carried out measuring population development of whitefly individuals passed through a series of intermediate hosts, previously selected and based on phylogenetic closeness to Manihot. The capacity of biotype B to adapt gradually to cassava, started on a legume (Phaseolus vulgaris), followed on two Euphorbiaceae (Euphorbia pulcherrima and Jatropha gossypiifolia) until, finally reaching a commercial cassava variety. B. tabaci female mean longevity on cassava, coming from P. vulgaris, E. pulcherrima and J. gossypiifolia was 3.1, 5.6 and 3.3 days, respectively. The highest oviposition rate (2.6 eggs/female/2 days), the shortest development time (44.4 days) and the highest value of rm (0.48 day1) were for populations coming from J. gossypiifolia, where 27.5% of the individuals coming from this host survived and reproduced on cassava. The importance and potential impact of phylogenetically close plants as intermediate hosts faciliting the adaptation of B. tabaci biotype B to cassava is discussed. r 2004 Published by Elsevier Ltd. Keywords: Bemisia tabaci; Biotype B; Manihot esculenta; Adaptation; Hosts
1. Introduction Bemisia tabaci (Homoptera: Aleyrodidae) is considered one of the most important pests in tropical and subtropical agriculture, as well as in production systems in glasshouses in temperate zones (Byrne and Bellows, 1991; Byrne et al., 1990). Since the 1980s, it has caused considerable economic losses in the southern United States, Mexico, Venezuela, the Eastern Caribbean $
Recent evidence suggests that B. tabaci represents a species complex with numerous biotypes and two described cryptic species. The binomial B. tabaci is used here in the broadest sense to include all members of the species complex. Corresponding author. Fax: +57 2 450073. E-mail address: [email protected] (A.C. Bellotti). 0261-2194/$ - see front matter r 2004 Published by Elsevier Ltd. doi:10.1016/j.cropro.2004.11.008
Basin, and Central and South America due to its proven efficiency as a virus vector, together with damage caused by direct feeding and excretion of honeydew (Brown et al., 1995; Oliveira et al., 2001). Many biotypes have been identified in different regions of the world, which suggests that B. tabaci may be a complex of species and biotypes (Perring, 2001; Abdullahi et al., 2003) undergoing continuous evolutionary changes. In the Americas there are complex associations between some hosts and various B. tabaci biotypes. In Puerto Rico, for example, the Sida biotype, which colonizes many species of plants including the genus Sida, to which it transmits several geminiviruses (family Geminiviridae: genus Begomovirus), and the Jatropha biotype, monophagous only on Jatropha gossypiifolia L., to which it specifically transmits
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the Jatropha mosaic virus (Brown et al., 1995), co-exist in the same geographic area but in different niches. After its first report and identification in the USA, the B. tabaci biotype B has become important due to its unique biochemical and biological characteristics. B. tabaci species complex adapts easily to new hosts and geographic regions. With the exception of Antarctica, it has been reported throughout the world (Martin et al., 2000) associated with almost 600 species of plants (Mound and Halsey, 1978; Secker et al., 1998). These include many cultivated and noncultivated species, annuals and perennials, which act as host plants, favoring its feeding and/or reproduction (Bedford et al., 1992; Brown et al., 1995; Butler and Henneberry, 1986). The families with the highest number of host species are Fabaceae, Asteraceae, Malvaceae, Solanaceae and Euphorbiaceae (Mound and Halsey, 1978). The introduced biotype B displays one of the broadest host range known among Bemisia whiteflies (Brown et al., 1995). However, unlike its West African counterpart the biotype B exhibits a wide polyphagous habit but cassava appears to be a nonsuitable host. Further, it had been speculated that the absence of cassava-infecting begomoviruses in South America is in part related to the inability of B. tabaci to colonize cassava (Bellotti and Arias, 2001; Costa and Russell, 1975). Nevertheless, B. tabaci was found feeding on cassava in Cuba (Va´squez et al., 1995) and specifically the biotype B in the Dominican Republic (Brown et al., 1995). These facts, together with the economic impact that affected southern USA, were attributed to the introduction and establishment of this highly invasive biotype B and its association to viral diseases (Brown et al., 1995; Brown and Bird, 1995). These examples indicate a potentially serious threat of the possible introduction of cassava mosaic geminiviruses (CMGs) to the Americas, especially because most traditional cassava cultivars in the Neotropics are highly susceptible to the disease. In addition, the B. tabaci species complex is the vector of viruses on several other crops often grown in association with or in proximity to cassava (e.g. beans, cowpea, sweet potatoes, string beans, tomatoes, cotton, soy bean) (Bellotti and Arias, 2001; Costa and Russell, 1975). The possibility of viral diseases moving among these crops or the appearance of new viruses represents a potential threat, e.g. tomato-yellow leaf curl virus infecting common bean (Navas-Castillo et al., 1999). In order to anticipate these events and as a prerequisite for developing any control measure (especially one that entails quarantine), research was initiated to evaluate the adaptative capacity of B. tabaci biotype B. The main goal of the present study was to verify, experimentally, the capacity of the biotype B to adapt on cassava. Specifically, it was evaluated, in a hypothetical but quantifiable manner (through life tables), possible ways in which this adaptation could occur in Colombia.
2. Materials and methods 2.1. Biotype B of Bemisia tabaci A strain of B. tabaci1 biotype B was obtained from individuals of a colony established at CIAT by the Bean Project in 1997, originating from Dapa County (Cauca Valley, Colombia). The strain was reared for five generations on Phaseolus vulgaris plants (variety ICAPijao) in cages made of tulle and wood (1 1 1 m) under controlled conditions (2572 1C, 7075% RH and a 12-h photophase) according to methodology proposed by Eichelkraut and Cardona (1989). Periodically, the purity of adult biotype B specimens in the colony was checked using RAPD-PCR (CIAT, 1999). 2.2. Adaptation of B. tabaci from P. vulgaris to M. esculenta (MCol 2063) The experimental hypothesis was that B. tabaci could become gradually adapted to M. esculenta by passing firstly through a series of intermediate hosts, previously selected based on phylogenetic closeness to Manihot (Burkill, 1994) and susceptibility to whiteflies. The adaptation process was initiated on a highly susceptible host (P. vulgaris L.), phylogenetically distant from M. esculenta; passing through two Euphorbiaceae (Euphorbia pulcherrima Willd. ex. Klotzch ‘‘poinsettia’’ and Jatropha gossypiifolia L. ‘‘jatropha’’), both intermediate hosts to B. tabaci, being relatively familiar and phyllogenetically close to Manihot. As the final host, the cassava cultivar MCol 2063 ‘‘var. Secundina’’ was selected for its known susceptibility to the whiteflies Aleurotrachelus socialis Bondar and B. tuberculata Bondar (Bellotti et al., 1999). Eight, 40 days old E. pulcherrima plants, divided into two cages (1 m 1 m 1 m) were each infested with an average of 4400 B. tabaci pupae on P. vulgaris leaves. These individuals had passed through five generations on the latter host. Later, young leaves of E. pulcherrima infested with an average of 5880 fifth generation B. tabaci pupae, were used to infest 8, 40 days old plants, of J. gossypiifolia using the above described methodology. Lastly, young J. gossypiifolia leaves containing an average of 7600 fifth generation B. tabaci pupae were used to infest 8, 35 days old M. esculenta (var MCol 2063) plants (Fig. 1). 2.3. Biology and demographic parameters of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia In order to determine the relative importance of each host involved in the sequence to reach the adaptation of 1 Unless a more specific designation is indicated, for practical reasons, the binomial B. tabaci is used here thereafter to refer to its Biotype B, which is so far the only one reported in Colombia.
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1 P.vulgaris (five generations)
2 E. pulcherrima (five generations)
3 J. gossypiifolia (five generations)
4 M. esculenta
Fig. 1. Host species sequence for the gradual adaptation of B. tabaci from P. vulgaris to M. esculenta. (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima and (4) on M. esculenta passed sequencially through P. vulgaris and E. pulcherrima and J. gossypiifolia.
B. tabaci on M. esculenta (Fig. 1), fecundity, longevity and development time, survival rate, proportion of females and demographic parameters were estimated and evaluated for individuals of B. tabaci on M. esculenta var. MCol 2063. All these data were obtained from individuals which in their previous five generations were reared: (1) only on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima (Fig. 2). All experiments were conducted at CIAT (Palmira, Colombia) in growth chambers under controlled conditions (2572 1C, 7075% RH and 12-h photophase). 2.4. Longevity and fecundity of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Forty pairs (males: females) of B. tabaci, recently emerged and coming from each of the three hosts of the sequence of adaptation: (1) P. vulgaris (2) E. pulcherrima and (3) J. gossypiifolia, were introduced in to clip cages (2.5 cm in diam. and 2 cm in depth), using a manual aspirator (impregnated with wax from the wings of adult whitefly to reduce the mortality due to manipulation), and placed on the undersides of M Col 2063 leaves. Every 48 h the adults were removed to a new area of the leaf until the natural death of females occurred. Males were replaced as they died. Fecundity was estimated by
B. tabaci / P. vulgaris
1
B. tabaci / E. pulcherrima
2
B. tabaci / J. gossypiifolia
3
Manihot esculenta MCol 2063
Fig. 2. Evaluation scheme of the biology and demographic parameters of B. tabaci on M. esculenta with individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
counting the number of eggs oviposited by the female every 48 h (in this way it was expected to reduce perturbation and mortality), while longevity was based on the maximum time (days) that a female lived. 2.5. Development time, rate of survival and proportion of females of B. tabaci on M. esculenta with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Fifty 2-day-old adults (males and females) of B. tabaci, originating from each of three hosts of the sequence of adaptation; (1) P. vulgaris, (2) E. pulcherrima and (3) J. gossypiifolia (Fig. 2), were placed with the aid of a manual aspirator in clip cages on the underside of M. esculenta (MCol 2063) leaves. After 6 h the adults were removed and 200 eggs were selected at random for
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rearing to adulthood. In each case, the development time from egg to adult, the survival rate of the immature stages, and the proportion of females emerged were recorded.
Table 1 Longevity (days), fecundity (eggs) and oviposition rate (eggs/female/2 days) of B. tabaci on M. esculenta (M Col 2063) of the individuals coming from host sequencea (n ¼ 40) Parameter
2.6. Demographic parameters of B. tabaci on M. esculenta with individuals coming from of host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia Life tables were constructed following the methodology described by Manzano (2000). The data on the development time of the immature individuals were combined with experimental data from the lxmx reproduction to produce life tables and used to calculate the demographic parameters defined by Price (1975): (1) Net reproduction rate (Ro) or average number of female descendents that a female produces in one generation; (2) generational time (T), equivalent to the period comprised between the emergence of the parents and that of the progeny; and (3) intrinsic rate of population growth (rm), estimated by Carey’s (1993) equation: X expðrm xÞl x mx ¼ 1, where x is the age days of females, lx is the specific survival age, and mx is the proportion of females from the progeny of a female with age x. In calculating the values of rm, the corrected age X+0.5 was used; and the equation ln 2/rm was used to estimate the days needed for the population to double in number (Carey, 1993). 2.7. Statistical analyses Differences between the mean values of longevity, fecundity, oviposition rate and development time were tested by Kruskal–Wallis test. When required, Student– Newman–Keuls was further used for multiple pair-wise comparisons. Values for survival rate of immature individuals were compared using Chi-square test.
3. Results and discussion 3.1. Biology and demographic parameters of B. tabaci on M. esculenta (MCol 2063), with individuals coming from host sequence: P. vulgaris, E. pulcherrima and J. gossypiifolia 3.1.1. Longevity, fecundity and oviposition rate of females The highest longevity mean (5.6 days) was obtained on females coming from E. pulcherrima, surpassing their counterparts coming from P. vulgaris (3.1) and J. gossypiifolia (3.3), respectively (Table 1). Both values were statistically different when compared with
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
Average longevity 3.3 b Range 2–10 Average fecundity 8.6 a Range 1–41 Average oviposition rate 2.6 a Range 0.5–8
5.6 a 2–18 7.7 a 1–48 1.4 b 0.4–3
3.1 b 2–10 1.8 b 1–19 0.6 c 0.5–3.5
Averages followed by different letters between columns differ significantly (Kruskal–Wallis Po0:0001; followed by Student–Newman–Keuls Po0:05). a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
E. pulcherrima (Student–Newman–Keuls Po0:05; after Kruskal–Wallis Po0:001); differences can clearly be seen in the survival curves (Fig. 3). Nevertheless, the populations coming from E. pulcherrima survived 39% less than those obtained by Sa´nchez et al. (1997) with B. tabaci on favorable hosts such as cotton (Gossypium hirsutum L.) and tomatoes (Lycopersicon esculentum Mill.). Independent of their origin, all biotype B females initiated oviposition during the first 2 days (Fig. 4), and by the sixth day the females coming from J. gossypiifolia and P. vulgaris had oviposited 50% of their eggs on M. esculenta. The highest oviposition rate (2.6 eggs/female/ 2 days) was found in females coming from J. gossypiifolia, being significantly higher than that of females coming from the other two hosts (Student–Newman– Keuls Po0:05; after Kruskal–Wallis Po0:001) (Table 1). Nevertheless there was variability in the maximum oviposition days, being 2, 6 or 12 days, depending on the female’s origin, established previously on J. gossypiifolia, P. vulgaris and E. pulcherrima, respectively (Fig. 4). The results obtained with the females coming from J. gossypiifolia and P. vulgaris concur with reports by Gameel (1974, cited by van Lenteren and Noldus, 1990), who found that the maximum oviposition of B. tabaci occurs in the first week of adult life. In contrast, the average fecundity on M. esculenta was 8.6 and 7.7 eggs when the females came from J. gossypiifolia and E. pulcherrima, respectively (Table 1). These values were significantly different from those obtained for females coming from P. vulgaris (1.8 eggs) (Student–Newman– Keuls Po0:05; after Kruskal–Wallis Po0:001). The analyses of the previous results show that when populations of B. tabaci are reared for some generations through the sequence of hosts: P. vulgaris–E. pulcherrima–J. gossypiifolia, they have higher rates of oviposition
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A. Carabali et al. / Crop Protection 24 (2005) 643–649 1 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0
Table 2 Development time, survival and proportion of females of individuals of B. tabaci on M. esculenta (MCol 2063) coming from host sequencea
E. pulcherrima J. gossypiifolia P. vulgaris
Parameter
2
4
6
8
10
12
14
16
18
20
Age of females (days)
Fig. 3. Survival curves of B. tabaci on M. esculenta MCol 2063 with individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
9 8
Eggs/female/2 days
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
0
E. pulcherrima J. gossypiifolia P. vulgaris
7 6 5 4 3 2 1 0 0
647
2
4
6
8
10
12
14
16
18
20
Age of females (days)
Fig. 4. Curves of oviposition of B. tabaci on plants of M. esculenta (MCol 2063) of the individuals coming from host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
and longevity on M. esculenta than if they are transferred directly from P. vulgaris to M. esculenta. 3.1.2. Development time, rate of survival of the immature stages and proportion of females The means of development time were not significantly different (Kruskal–Wallis P ¼ 0:102). However, individuals of B. tabaci coming from J. gossypiifolia took 44.4 days to develop on M. esculenta, a shorter time by about 6 days, compared when coming from E. pulcherrima and P. vulgaris (Table 2). On the other hand, the highest survival rate in the immature stage (27.5%) was found in individuals coming from J. gossypiifolia, being significantly different (Student–Newman–Keuls Po0:05; after Kruskal–Wallis Po0:001) from those coming from E. pulcherrima (3%) and P. vulgaris (2%) (Table 2). The shortest development time of B. tabaci on M. esculenta when the populations had been established previously on J. gossypiifolia, can be interpreted as a better biological adaptation of the insect to the closest phylogenetic host. Therefore it is possible to consider J. gossypiifolia as a ‘‘principal link’’ in the gradual
Development time (days) 44.4 ns No. of insects 55 27.5 a Survival rate (%)b No. of insects 200 Proportion of females (%) 51.0 No. of insects 55
50.6 6 3.0 b 200 50.0 6
49.5 4 2.0 b 200 50.0 4
a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima. b Averages followed by different letters in the columns differ significantly, w2 ¼ 16:7; 2 df, Po0:0002; followed by Student– Newman–Keuls Po0:05:
adaptation of B. tabaci to M. esculenta, passing previously from E. pulcherrima and P. vulgaris. The proportion of females of B. tabaci biotype B, independent of the host of origin, was not affected by developing on M. esculenta as the sex ratio was 1:1. These results are similar to those reported for B. tabaci by Eichelkraut and Cardona (1989) and Sa´nchez et al. (1997). 3.1.3. Demographic parameters Based on the net reproduction rate (Ro), it was possible to determine that after one generation, on average, the populations of B. tabaci can multiply 11.6 times (individual/individual) on cassava when they come from E. pulcherrima, being 1.3 and 6.3 times higher, respectively, than when they come from J. gossypiifolia and P. vulgaris (Table 3). A generation time of B. tabaci on M. esculenta is 44.8 days when the populations come from J. gossypiifolia, 7 and 11 days less than for those populations coming from P. vulgaris and E. pulcherrima, respectively. In other words, B. tabaci biotype B can reach up to eight, seven or five generations/year on M. esculenta dependent upon previous host; J. gossypiifolia, P. vulgaris or E. pulcherrima, respectively (Table 3). The population established previously on J. gossypiifolia had the higher value of the intrinsic growth rate (0.05), which decreased slightly for E. pulcherrima (0.04) and lower still for P. vulgaris (0.02). On M. esculenta females of B. tabaci coming from J. gossypiifolia can double their population in significantly less time (14.4 days) than those from P. vulgaris (34.7 days). Results of intrinsic growth rates (rm) reveal a higher population growth on M. esculenta when coming from J. gossypiifolia, exceeding those from E. pulcherrima by 8.3% and up to 58.3% for those from P. vulgaris. In the case of individuals coming from E. pulcherrima, the rm value was favored by their fecundity as compared to
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Table 3 Demographic parameters for individuals of B. tabaci on M. esculenta (MCol 2063) coming from host sequencea (n ¼ 200) Parameter
Host of origin J. gossypiifolia E. pulcherrima P. vulgaris
8.6 Net reproductive rate (Ro) Generational time (T) 44.8 Intrinsic growth rate (rm) 0.05 Time for duplication 14.4 (TD)
11.6
1.8
56.0 0.04 17.3
51.3 0.02 34.7
a Host sequence: (1) on P. vulgaris; (2) on E. pulcherrima but previously reared on P. vulgaris, and (3) on J. gossypiifolia but were passed sequencially through P. vulgaris and E. pulcherrima.
that of the individuals coming from J. gossypiifolia (Table 3). Our findings have both academic and economic implications. Firstly, from the analysis of our results and in light of the scientific literature, it is plausible to affirm that M. esculenta might represent, in the near future, a suitable host for B. tabaci in Colombia. Demographic parameters suggest that an increase in the capacity for adapting to M. esculenta, favored by the influence of phylogenetically related hosts, such as J. gossypiifolia, might act as gradual points in which the insect increases its biotic potential, facilitating its adaptation to M. esculenta. Indeed, this fact constitutes one of the principal findings of this study, actually confronting the apparent lack of adaptive capacity of B. tabaci on M. esculenta, a host on which, according to Costa and Russell (1975), it does not feed or reproduce in the Americas. Secondly, in view of these findings and the constant presence of cassava cultivars throughout the year, it is possible to hypothetise the host specialization of B. tabaci on Colombian cassava. The occurrence of this ‘‘host-shifting’’ can be favored by J. gossypiifolia and E. pulcherrima, acting as gradual hosts. A similar adaptative scenario is reported by Abdullahi et al. (2003) for the African B. tabaci populations associated with cassava. Although the available evidence precludes an actual estimation of the time that this specialization will demand, it is likely that B. tabaci, despite its ‘‘experimental’’ low potential for development, can in just a few generations, adapt to cassava cultivars. This situation can be anticipated based on the dramatic and rapid increases undergone by the B. tabaci populations in recent years (Brown et al., 1995; Quintero et al., 1998; Perring, 2001). On academic grounds, the experimental adaptation of B. tabaci, through different phyllogenetically related hosts to Manihot, might produce a useful model to understand the evolutive potential of this important pest. The differences on fecundity and survival detected
between individuals coming from the adaptation sequence might increase in a progressive way, the biological fitness of B. tabaci. Thus, in the long term, after several generations, a change in its phenotype can be expected.
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