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Developmental and population growth rates of phosphine-resistant and -susceptible populations of stored-product insect pests
Journal of Stored Products Research 45 (2009) 241–246
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Developmental and population growth rates of phosphine-resistant and -susceptible populations of stored-product insect pests A.H. Sousa a, L.R.D’A. Faroni b, M.A.G. Pimentel a, R.N.C. Guedes a, * a b
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil Departamento de Engenharia Agrı´cola, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 28 April 2009
Phosphine resistance positively contributes towards an individual’s fitness under phosphine fumigation. However, phosphine resistance may place resistant individuals at a fitness disadvantage in the absence of this fumigant, which can be exploited to halt or slow down the spread of resistance. This study aimed to determine if there is a fitness cost associated with phosphine resistance in populations of the red flour beetle (Tribolium castaneum (Herbst)), the lesser grain borer (Rhyzopertha dominica (F.)) and the sawtoothed grain beetle (Oryzaephilus surinamensis (L.)). The developmental rate and population growth of phosphine-resistant and -susceptible populations of these three species of stored-product insects were therefore determined under phosphine-free environment. The majority of the phosphine-resistant populations exhibited lower developmental and population growth rates than the susceptible populations indicating that phosphine resistance is associated with fitness cost in all three species, which can potentially compromise the fixation and dispersal of the resistant genotypes. Nonetheless, some phosphine-resistant populations did not show a fitness cost. Therefore, resistance management strategies based on suppression of phosphine use aiming at eventual reestablishment of phosphine susceptibility and subsequent reintroduction of this fumigant will be useful only for insect populations exhibiting a fitness cost associated with phosphine resistance. Therefore recognition of the prevailing phosphine-resistant genotypes in a region is important to direct the management tactics to be adopted. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Fumigant resistance Tribolium castaneum Oryzaephilus surinamensis Rhyzopertha dominica Adaptive cost
1. Introduction The impairment of the reproductive performance of insecticideresistant individuals in insecticide-free environment is the result of fitness costs associated with pesticide resistance, which is often determined by resource allocation from a basic physiological process to the protection against insecticides, favoring survival at the expense of reproduction (Coustau et al., 2000; Guedes et al., 2006). Fitness costs are preliminarily recognized from demographic studies carried out with individual populations in pesticide-free environments, but the occurrence of such costs under this environmental condition is not universal, although frequent (Beeman and Nanis, 1986; Haubruge and Arnaud, 2001; Raymond et al., 2001; Fragoso et al., 2005; Oliveira et al., 2007). Fitness costs associated with resistance to grain protectants have received considerable attention lately (Fragoso et al., 2005; Guedes et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2007; Arau´jo et al., 2008a, b). However, fitness costs potentially associated with phosphine
* Corresponding author. Tel.: þ55 31 3899 4008; fax: þ55 31 3899 4012. E-mail addresses: [email protected], [email protected] (R.N.C. Guedes). 0022-474X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jspr.2009.04.003
resistance, the main fumigant currently used worldwide against stored-product insects, have received little attention and have yet to be the subject of demographic studies. The previously high prominence of phosphine as a storedproduct fumigant has been further increased by the worldwide phasing out of methyl bromide as a fumigant (Zettler and Arthur, 2000; Bell and Hutton, 2002; Fields and White, 2002). The ever increasing overuse of phosphine since the 1960’s has resulted in phosphine resistance, which was initially summarized in the FAO worldwide survey of 1976 (Champ and Dyte, 1976). Contrary to the early reports indicating low levels of phosphine resistance in Brazilian populations of stored-product insects (Champ and Dyte, 1976; Sartori et al., 1990), recent reports indicate moderate to high levels of phosphine resistance in field-collected Brazilian populations of Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae), Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), and Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) (Lorini et al., 2007; Pimentel et al., 2007, 2009). Phosphine resistance positively contributes towards an individual’s fitness under phosphine fumigation. However, phosphine resistance may place resistant individuals at a fitness disadvantage
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in the absence of this fumigant with implications for the management of these resistant populations. Fitness disadvantages associated with phosphine resistance have been inferred from genetic studies and from preliminary determinations (Lorini et al., 2007; Pimentel et al., 2007, 2009; Schlipalius et al., 2008), but have not yet been subjected to demographic studies. The objective of this study was to determine fitness costs associated with phosphine resistance in representative field-collected populations of T. castaneum, R. dominica and O. surinamensis. Fitness costs associated with phosphine resistance were expected to occur in the field-collected resistant populations studied, and consequences of these costs are important for the design of phosphine resistance management plans. 2. Materials and methods 2.1. Insects Two phosphine-resistant and two phosphine-susceptible populations of T. castaneum, R. dominica and O. surinamensis were used in the present study based on earlier studies (Pimentel et al., 2007; Sousa et al., 2008). These representative populations were collected from stored grains between June 2004 and September 2005. The phosphine-resistant populations of T. castaneum were collected at the counties of Alfenas (state of Minas Gerais) (here referred as resistant – A; 48 resistant) and Campos de Ju´lio (state of Mato Grosso) (resistant – CJ; 63 resistant), while the susceptible populations were from A´gua Boa (state of Mato Grosso) (susceptible – AB) and Brangança Paulista (state of Sa˜o Paulo) (susceptible – BP). The phosphine-resistant populations of R. dominica were from Bom Despacho (Minas Gerais) and Palmital (Sa˜o Paulo) (referred here as resistant – BD and resistant – P, with phosphine resistance levels of 39 and 71, respectively), while the susceptible populations were from Nova Era (Minas Gerais) and Piracicaba (SP) (susceptible – NE and susceptible – P, respectively). The phosphine-resistant populations of O. surinamensis were from Astolfo Dutra (Minas Gerais) and Guaxupe´ (Minas Gerais) (resistant – AD and Resistant – G, with phosphine resistance levels of 29 and 32, respectively), while the susceptible populations were from Uberlaˆndia and Unaı´ (Minas Gerais) (susceptible – Ub and susceptible – Un). The insects from each population were individually reared on insecticide-free substrates in 1.5 L glass jars at 30 2 C, 70 5% relative humidity (r.h.), and in continuous darkness after collection from the field (i.e., for ca. 10 generations). Coarsely ground maize was the feeding substrate for both T. castaneum and O. surinamensis, and whole wheat grains were the feeding substrate for R. dominica. Both feeding substrates were used at 13% moisture content and were maintained at 18 C for at least a week before use to prevent cross-infestation. 2.2. Developmental rate until adult emergence The experiments were carried out in Petri dishes (140 10 mm) containing 35 g of the respective food substrates. Each Petri dish was infested with 20 non-sexed adult insects (1–3 weeks old) and maintained at the same conditions described for rearing them. All of these parental insects were removed after 13 days to allow relative standardization of progeny development (Trematerra et al., 1996; Fragoso et al., 2005). After the removal of the parental insects, the food substrate containing the developing progeny was maintained under the same controlled conditions until adult emergence. Four replicates (with 20 adults each) were used for each population of T. castaneum and O. surinamensis, and six replicates (also with 20 adults each) were used for each population of R. dominica. Adult progenies were counted and removed from the experimental units
(i.e., Petri dishes) on alternate days starting after the first emergence, which took place 30, 28 and 33 days after first oviposition by the populations of T. castaneum, O. surinamensis and R. dominica, respectively. Daily and cumulative emergence were recorded and the cumulative data were normalized (Trematerra et al., 1996). Both data sets were subjected to non-linear regression analysis using the curve-fitting procedure of SigmaPlot (SPSS, 2001). The analysis of the cumulative emergence data was the initial focus of attention since experimental errors are less likely with it than with the daily emergence data (Trematerra et al., 1996; Fragoso et al., 2005). In addition, since the relative trends in cumulative emergence are more important than the overall data (Trematerra et al., 1996), which are not as statistically reliable, the data for each population were normalized using the time of the first adult emergence in each replicate as the starting point (Trematerra et al., 1996; Fragoso et al., 2005). This procedure minimizes the intra- and inter-population variation in the rate of development. The regression analysis of emergence was initially restricted to the models proposed earlier by Trematerra et al. (1996), but the 3-parameter sigmoid model (y ¼ a/(1 þ exp((x b)/c)) provided better fits for cumulative emergence of populations of T. castaneum and O. surinamensis, as also observed by Fragoso et al. (2005), and the 3-parameter Gompertz model (y ¼ a exp(exp((x b)/c)) provided better fits for populations of R. dominica. These models were therefore used. 2.3. Population growth The experiment on population growth was carried out in plastic jars (95 100 mm) containing 150 g of coarsely ground maize for T. castaneum and O. surinamensis, and 200 g of whole wheat grains for R. dominica. The grains were infested with 20 non-sexed adult insects (1–3 weeks old) under the same environmental conditions mentioned above. The insects were not removed in this experiment, in contrast with the experiments concerning developmental rate, and also employed four replicates for each population of T. castaneum and O. surinamensis, and six replicates for each population of R. dominica. The number of live adult insects was recorded 0, 35, 50, 65, 80, 95, and 110 days after starting the experiment for each insect population. The data were subjected to non-linear regression analysis using the curve-fitting procedure of SigmaPlot (SPSS, 2001). 3. Results 3.1. Developmental rate until adult emergence 3.1.1. Cumulative emergence The overlapping cumulative emergence from the phosphineresistant populations of T. castaneum was lower than those of both susceptible populations (Fig. 1a; Table 1). The total emergence was lower for both phosphine-resistant populations (62.6 2.2 and 77.7 2.1 insects/dish for resistant – A and resistant – CJ, respectively), than for the susceptible populations of T. castaneum (113.6 3.5 and 94.1 2.7 insects/dish for susceptible – AB and susceptible – BP, respectively). A similar trend was observed for phosphine-resistant populations of O. surinamensis, which also exhibited slower development to adulthood, than the susceptible populations of this species (Fig. 1b; Table 1). Again the total emergence was lower for the phosphine-resistant – AD population (93.0 6.6 insects/dish), followed by the susceptible – Ub and resistant – G populations (141.1 5.2 and 149.9 12.2 insects/ dish), which were statistically indistinguishable, and the susceptible – Un population, which exhibited the highest emergence (178.0 6.9 insects/dish).
A.H. Sousa et al. / Journal of Stored Products Research 45 (2009) 241–246
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Fig. 1. Normalized cumulative emergence of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 1.
The cumulative emergence of the phosphine-resistant – P and susceptible – P populations of R. dominica overlapped exhibiting quicker development than the phosphine-resistant – BD and the susceptible – NE populations (Fig. 1c; Table 1). The total emergence of the phosphine-resistant – P population was much lower (123.6 17.7 insects/dish) than that of the susceptible – NE (194.2 35.2 insects/dish), susceptible – P (218.2 16.4 insects/ dish), and resistant – BD populations (230.6 12.6 insects/dish). 3.1.2. Daily emergence Although the cumulative emergence curves indicate significant differences among populations of each insect species, the population differences in the rate of daily emergence are even larger
(Table 2; Fig. 2). The rate of daily emergence was significantly lower for the phosphine-resistant populations of T. castaneum, when compared with the phosphine-susceptible populations of this species, which reached a maximum emergence about 5 days earlier than the resistant populations (Fig. 2a). The daily emergence rate for the populations of O. surinamensis was highest for the population susceptible – Un, followed by resistant – G, susceptible – Ub, and resistant – AD, which exhibited a peak of maximum emergence about half that of the susceptible – Un and with 2 days delay (Fig. 2b). The daily emergence rate of the phosphine-resistant – P population of R. dominica was nearly half that of the resistant – BD population and both susceptible populations, which exhibited higher emergence (Fig. 2c).
Table 1 Summary of the non-linear regression analysis of the (normalized) cumulative emergence curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 1. Parameter estimates (SEM)
dferror
R2
Variable
Model
Population
a
b
Tribolium castaneum
y ¼ a/(1 þ exp((x b)/c))
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
96.8 1.0 98.9 1.1 99.5 0.9 100.0 0.7
15.4 0.3 14.6 0.3 18.1 0.2 18.1 0.2
5.2 0.2 5.0 0.2 5.2 0.2 5.4 0.1
93 93 93 93
1988.7 1638.2 3268.8 5179.8
0.97 0.97 0.98 0.99
Oryzaephilus surinamensis
y ¼ a/(1 þ exp((x b)/c))
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
98.6 0.3 97.8 0.4 98.5 0.4 97.4 0.8
15.8 0.1 16.0 0.1 17.8 0.1 16.9 0.2
4.3 0.1 4.2 0.1 3.9 0.1 4.0 0.1
89 89 89 89
18,029.0 14,230.3 12,703.6 3612.1
0.97 0.99 0.99 0.98
Rhyzopertha dominica
y ¼ a exp(exp((x b)/c))
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
114.2 2.4 99.0 0.6 101.0 0.5 98.3 0.8
18.4 0.2 19.4 0.1 19.6 0.1 16.7 0.2
9.07 0.2 9.16 0.2 9.08 0.2 9.17 0.3
183 183 183 182
5962.2 11,172.1 13,536.4 4322.3
0.98 0.99 0.99 0.97
F
c
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
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Table 2 Summary of the non-linear regression analysis of the daily emergence curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 2. Parameter estimates (SEM)
R2
Model
Population
b
c
Tribolium castaneum
y ¼ a exp(0.5((x b)/c)2)
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
9.7 0.5 8.7 0.5 6.7 0.4 5.3 0.3
15.2 0.6 14.6 0.7 18.3 0.6 18.4 0.6
9.1 0.6 8.9 0.7 9.2 0.7 9.5 0.6
93 93 93 93
82.7 74.7 73.0 81.0
0.64 0.61 0.61 0.63
Oryzaephilus surinamensis
y ¼ a exp(0.5((x b)/c)2)
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
19.6 0.6 16.1 0.5 18.4 0.6 10.7 0.4
16.5 0.2 16.5 0.2 18.4 0.2 17.1 0.3
6.9 0.2 6.5 0.2 6.0 0.2 6.5 0.3
89 89 89 89
361.7 376.5 323.3 220.0
0.89 0.89 0.87 0.83
Rhyzopertha dominica
y ¼ a exp(0.5 (ln(x/b)/c)2)
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
18.2 0.6 16.2 0.7 18.8 0.6 9.9 0.4
18.0 0.3 19.2 0.5 19.5 0.4 16.1 0.5
0.5 0.0 0.4 0.0 0.5 0.0 0.5 0.0
183 183 183 182
291.5 166.7 307.3 135.7
0.76 0.64 0.77 0.59
a
dferror
F
Variable
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
3.2. Population growth
4. Discussion
The 3-parameter sigmoid model best described the population growth of all three species of stored-product insects (P < 0.01; R2 0.77) (Table 3). Similar to the developmental rate, the population growth rate was lower in the phosphine-resistant populations of T. castaneum, in the phosphine-resistant – G population of O. surinamensis, and in the phosphine-resistant – P population of R. dominica (Fig. 3). The phosphine-susceptible populations of T. castaneum, as well as the phosphine-resistant – G population of O. surinamensis, reached a plateau in their levels at the end of the storage period as a likely result of the high population densities reached in their respective experimental units.
Fitness costs associated with insecticide resistance are frequently reported among insect pests and it is a common assumption in models of insecticide resistance evolution (Beeman and Nani, 1986; Coustau et al., 2000; Haubruge and Arnaud, 2001; Raymond et al., 2001; Fragoso et al., 2005; Guedes et al., 2006; Oliveira et al., 2007). Such costs are the likely result of an energy imbalance, diverting energy from basic physiological process (e.g., development and reproduction) to protection against insecticides, leading to insecticide resistance (Guedes et al., 2006; Arau´jo et al., 2008ab). These physiological costs are translated into fitness costs turning insecticide resistance into
Fig. 2. Daily emergence of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 2.
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Table 3 Summary of the non-linear regression analysis of the population growth curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 3. dferror
F
R2
15.7 3.9 14.5 1.5 24.0 2.0 29.3 6.4
39 39 39 39
79.1 441.3 1073.8 202.9
0.80 0.95 0.98 0.91
76.6 8.9 66.3 15.0 65.4 11.2 55.6 7.0
25.2 4.4 25.3 9.1 22.0 7.5 22.8 5.5
25 25 25 25
210.6 44.2 48.7 84.3
0.94 0.77 0.79 0.87
93.9 15.59 93.6 16.2 79.6 5.5 142.0 15.4
19.3 5.8 23.7 5.8 17.1 3.0 32.1 4.6
39 39 39 39
86.3 127.2 208.3 53.9
0.81 0.86 0.91 0.99
Variable
Model
Population
Parameter estimates (SEM) b
c
Tribolium castaneum
y ¼ a/(1 þ exp((x b)/c))
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
294.4 28.4 275.9 9.9 346.1 39.4 503.3 39.8
62.8 5.0 59.7 1.8 95.7 5.9 127.9 39.1
Oryzaephilus surinamensis
y ¼ a/(1 þ exp((x b)/c))
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
1493.4 215.4 954.5 221.7 1313.5 248.1 511.6 57.1
Rhyzopertha dominica
y ¼ a/(1 þ exp((x b)/c))
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
1194.6 419.9 1006.1 307.9 1116.43 134.3 1490.2 344.4
a
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
a disadvantageous trait in the absence of insecticides. Higher and earlier (daily) emergence among the phosphine-susceptible insect populations from our study led to higher cumulative emergence and higher population growth rates of these populations. Most of the phosphine-resistant populations exhibited lower developmental and population growth rates indicating prevalence of fitness cost associated with phosphine resistance, as frequently reported among insect species (Haubruge and Arnaud, 2001; Fragoso et al., 2005; Pimentel et al., 2009). Our findings provide support for the contention that energy allocation to insecticide resistance mechanisms can impair the reproductive performance of the resistant individuals (Coustau et al., 2000; Guedes et al., 2006; Pimentel et al., 2008, 2009).
Despite the frequent association between phosphine resistance and fitness disadvantage, there were a few instances of lack of such association, particularly regarding two phosphine-resistant populations, one of O. surinamenis and one of R. dominica (resistant – G and resistant – BD, respectively). Insecticide resistance is rarely fixed in natural populations because of its associated fitness cost and relative infrequent use of insecticides allowing (partial) reestablishment of the insecticide susceptibility (Coustau et al., 2000; Guedes et al., 2006). However, intense and extended selection for insecticide resistance may either lead to the selection of fitness modifier genes that ameliorate the cost of insecticide resistance (by decreasing its fitness disadvantage), or may favor the selection of less costly phosphine resistance genes (Coustau et al., 2000; Guedes
Fig. 3. Population growth rate of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 3.
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et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2008). Indeed this may be the case for a few Brazilian phosphine-resistant populations of stored-product insects, where phosphine resistance is increasing and becoming a problem in recent years, although not yet at the extent observed in other countries such as Australia (Lorini et al., 2007; Pimentel et al., 2007, 2009; Nayak and Collins, 2008). In a few instances, the intensive selection for phosphine resistance for several years may have favored the suppression of the deleterious effects of this trait mitigating the fitness costs usually associated with it. This seems to take place in the resistant – G and resistant – BD populations of O. surinamensis and R. dominica respectively. Such mitigation has already been reported in pyrethroid-resistant populations of Sitophilus zeamais (Coleoptera: Curculionidae) (Guedes et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2007). The potential fitness costs associated with phosphine resistance can affect the fixation and dispersal of the phosphine resistance genes due to their impact on the carrier individuals, with important implications for resistance management (Fragoso et al., 2005; Oliveira et al., 2007). From an applied perspective, the management of phosphine-resistant populations of stored-product insects can be achieved by minimizing phosphine use. This will allow the reestablishment of phosphine susceptibility when phosphine resistance is associated with a fitness cost, which seems to be frequent among phosphine-resistant populations of stored-product insects in current and previous studies (Lorini et al., 2007; Pimentel et al., 2007, 2009). However, the reestablishment of phosphine susceptibility with the brief suspension of its use should not be recommended as a management tactic for phosphine resistance when the resistant population does not exhibit an associated fitness cost, as in the cases of the resistant – G population of O. surinamensis and the resistant – BD population of R. dominica. Therefore, the recognition of the prevailing genotypes of phosphine resistance in a region should direct the selection of tactics for managing phosphine resistance. Acknowledgements Appreciation is expressed to the Minas Gerais State Agency for Research Aid (FAPEMIG), National Council of Scientific and Technological Development (CNPq), and CAPES Foundation (Brazilian Ministry of Education). The comments and suggestions provided by Dr. F. Arthur and an anonymous referee were greatly appreciated. References Arau´jo, R.A., Guedes, R.N.C., Oliveira, M.G.A., Ferreira, G.H., 2008a. Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais. Bulletin of Entomological Research 98, 417–424. Arau´jo, R.A., Guedes, R.N.C., Oliveira, M.G.A., Ferreira, G.H., 2008b. Enhanced proteolytic and cellulolytic activity in insecticide-resistant strains of the maize weevil, Sitophilus zeamais. Journal of Stored Products Research 44, 354–359.
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Developmental and population growth rates of phosphine-resistant and -susceptible populations of stored-product insect pests A.H. Sousa a, L.R.D’A. Faroni b, M.A.G. Pimentel a, R.N.C. Guedes a, * a b
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil Departamento de Engenharia Agrı´cola, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 28 April 2009
Phosphine resistance positively contributes towards an individual’s fitness under phosphine fumigation. However, phosphine resistance may place resistant individuals at a fitness disadvantage in the absence of this fumigant, which can be exploited to halt or slow down the spread of resistance. This study aimed to determine if there is a fitness cost associated with phosphine resistance in populations of the red flour beetle (Tribolium castaneum (Herbst)), the lesser grain borer (Rhyzopertha dominica (F.)) and the sawtoothed grain beetle (Oryzaephilus surinamensis (L.)). The developmental rate and population growth of phosphine-resistant and -susceptible populations of these three species of stored-product insects were therefore determined under phosphine-free environment. The majority of the phosphine-resistant populations exhibited lower developmental and population growth rates than the susceptible populations indicating that phosphine resistance is associated with fitness cost in all three species, which can potentially compromise the fixation and dispersal of the resistant genotypes. Nonetheless, some phosphine-resistant populations did not show a fitness cost. Therefore, resistance management strategies based on suppression of phosphine use aiming at eventual reestablishment of phosphine susceptibility and subsequent reintroduction of this fumigant will be useful only for insect populations exhibiting a fitness cost associated with phosphine resistance. Therefore recognition of the prevailing phosphine-resistant genotypes in a region is important to direct the management tactics to be adopted. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Fumigant resistance Tribolium castaneum Oryzaephilus surinamensis Rhyzopertha dominica Adaptive cost
1. Introduction The impairment of the reproductive performance of insecticideresistant individuals in insecticide-free environment is the result of fitness costs associated with pesticide resistance, which is often determined by resource allocation from a basic physiological process to the protection against insecticides, favoring survival at the expense of reproduction (Coustau et al., 2000; Guedes et al., 2006). Fitness costs are preliminarily recognized from demographic studies carried out with individual populations in pesticide-free environments, but the occurrence of such costs under this environmental condition is not universal, although frequent (Beeman and Nanis, 1986; Haubruge and Arnaud, 2001; Raymond et al., 2001; Fragoso et al., 2005; Oliveira et al., 2007). Fitness costs associated with resistance to grain protectants have received considerable attention lately (Fragoso et al., 2005; Guedes et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2007; Arau´jo et al., 2008a, b). However, fitness costs potentially associated with phosphine
* Corresponding author. Tel.: þ55 31 3899 4008; fax: þ55 31 3899 4012. E-mail addresses: [email protected], [email protected] (R.N.C. Guedes). 0022-474X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jspr.2009.04.003
resistance, the main fumigant currently used worldwide against stored-product insects, have received little attention and have yet to be the subject of demographic studies. The previously high prominence of phosphine as a storedproduct fumigant has been further increased by the worldwide phasing out of methyl bromide as a fumigant (Zettler and Arthur, 2000; Bell and Hutton, 2002; Fields and White, 2002). The ever increasing overuse of phosphine since the 1960’s has resulted in phosphine resistance, which was initially summarized in the FAO worldwide survey of 1976 (Champ and Dyte, 1976). Contrary to the early reports indicating low levels of phosphine resistance in Brazilian populations of stored-product insects (Champ and Dyte, 1976; Sartori et al., 1990), recent reports indicate moderate to high levels of phosphine resistance in field-collected Brazilian populations of Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae), Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), and Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) (Lorini et al., 2007; Pimentel et al., 2007, 2009). Phosphine resistance positively contributes towards an individual’s fitness under phosphine fumigation. However, phosphine resistance may place resistant individuals at a fitness disadvantage
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in the absence of this fumigant with implications for the management of these resistant populations. Fitness disadvantages associated with phosphine resistance have been inferred from genetic studies and from preliminary determinations (Lorini et al., 2007; Pimentel et al., 2007, 2009; Schlipalius et al., 2008), but have not yet been subjected to demographic studies. The objective of this study was to determine fitness costs associated with phosphine resistance in representative field-collected populations of T. castaneum, R. dominica and O. surinamensis. Fitness costs associated with phosphine resistance were expected to occur in the field-collected resistant populations studied, and consequences of these costs are important for the design of phosphine resistance management plans. 2. Materials and methods 2.1. Insects Two phosphine-resistant and two phosphine-susceptible populations of T. castaneum, R. dominica and O. surinamensis were used in the present study based on earlier studies (Pimentel et al., 2007; Sousa et al., 2008). These representative populations were collected from stored grains between June 2004 and September 2005. The phosphine-resistant populations of T. castaneum were collected at the counties of Alfenas (state of Minas Gerais) (here referred as resistant – A; 48 resistant) and Campos de Ju´lio (state of Mato Grosso) (resistant – CJ; 63 resistant), while the susceptible populations were from A´gua Boa (state of Mato Grosso) (susceptible – AB) and Brangança Paulista (state of Sa˜o Paulo) (susceptible – BP). The phosphine-resistant populations of R. dominica were from Bom Despacho (Minas Gerais) and Palmital (Sa˜o Paulo) (referred here as resistant – BD and resistant – P, with phosphine resistance levels of 39 and 71, respectively), while the susceptible populations were from Nova Era (Minas Gerais) and Piracicaba (SP) (susceptible – NE and susceptible – P, respectively). The phosphine-resistant populations of O. surinamensis were from Astolfo Dutra (Minas Gerais) and Guaxupe´ (Minas Gerais) (resistant – AD and Resistant – G, with phosphine resistance levels of 29 and 32, respectively), while the susceptible populations were from Uberlaˆndia and Unaı´ (Minas Gerais) (susceptible – Ub and susceptible – Un). The insects from each population were individually reared on insecticide-free substrates in 1.5 L glass jars at 30 2 C, 70 5% relative humidity (r.h.), and in continuous darkness after collection from the field (i.e., for ca. 10 generations). Coarsely ground maize was the feeding substrate for both T. castaneum and O. surinamensis, and whole wheat grains were the feeding substrate for R. dominica. Both feeding substrates were used at 13% moisture content and were maintained at 18 C for at least a week before use to prevent cross-infestation. 2.2. Developmental rate until adult emergence The experiments were carried out in Petri dishes (140 10 mm) containing 35 g of the respective food substrates. Each Petri dish was infested with 20 non-sexed adult insects (1–3 weeks old) and maintained at the same conditions described for rearing them. All of these parental insects were removed after 13 days to allow relative standardization of progeny development (Trematerra et al., 1996; Fragoso et al., 2005). After the removal of the parental insects, the food substrate containing the developing progeny was maintained under the same controlled conditions until adult emergence. Four replicates (with 20 adults each) were used for each population of T. castaneum and O. surinamensis, and six replicates (also with 20 adults each) were used for each population of R. dominica. Adult progenies were counted and removed from the experimental units
(i.e., Petri dishes) on alternate days starting after the first emergence, which took place 30, 28 and 33 days after first oviposition by the populations of T. castaneum, O. surinamensis and R. dominica, respectively. Daily and cumulative emergence were recorded and the cumulative data were normalized (Trematerra et al., 1996). Both data sets were subjected to non-linear regression analysis using the curve-fitting procedure of SigmaPlot (SPSS, 2001). The analysis of the cumulative emergence data was the initial focus of attention since experimental errors are less likely with it than with the daily emergence data (Trematerra et al., 1996; Fragoso et al., 2005). In addition, since the relative trends in cumulative emergence are more important than the overall data (Trematerra et al., 1996), which are not as statistically reliable, the data for each population were normalized using the time of the first adult emergence in each replicate as the starting point (Trematerra et al., 1996; Fragoso et al., 2005). This procedure minimizes the intra- and inter-population variation in the rate of development. The regression analysis of emergence was initially restricted to the models proposed earlier by Trematerra et al. (1996), but the 3-parameter sigmoid model (y ¼ a/(1 þ exp((x b)/c)) provided better fits for cumulative emergence of populations of T. castaneum and O. surinamensis, as also observed by Fragoso et al. (2005), and the 3-parameter Gompertz model (y ¼ a exp(exp((x b)/c)) provided better fits for populations of R. dominica. These models were therefore used. 2.3. Population growth The experiment on population growth was carried out in plastic jars (95 100 mm) containing 150 g of coarsely ground maize for T. castaneum and O. surinamensis, and 200 g of whole wheat grains for R. dominica. The grains were infested with 20 non-sexed adult insects (1–3 weeks old) under the same environmental conditions mentioned above. The insects were not removed in this experiment, in contrast with the experiments concerning developmental rate, and also employed four replicates for each population of T. castaneum and O. surinamensis, and six replicates for each population of R. dominica. The number of live adult insects was recorded 0, 35, 50, 65, 80, 95, and 110 days after starting the experiment for each insect population. The data were subjected to non-linear regression analysis using the curve-fitting procedure of SigmaPlot (SPSS, 2001). 3. Results 3.1. Developmental rate until adult emergence 3.1.1. Cumulative emergence The overlapping cumulative emergence from the phosphineresistant populations of T. castaneum was lower than those of both susceptible populations (Fig. 1a; Table 1). The total emergence was lower for both phosphine-resistant populations (62.6 2.2 and 77.7 2.1 insects/dish for resistant – A and resistant – CJ, respectively), than for the susceptible populations of T. castaneum (113.6 3.5 and 94.1 2.7 insects/dish for susceptible – AB and susceptible – BP, respectively). A similar trend was observed for phosphine-resistant populations of O. surinamensis, which also exhibited slower development to adulthood, than the susceptible populations of this species (Fig. 1b; Table 1). Again the total emergence was lower for the phosphine-resistant – AD population (93.0 6.6 insects/dish), followed by the susceptible – Ub and resistant – G populations (141.1 5.2 and 149.9 12.2 insects/ dish), which were statistically indistinguishable, and the susceptible – Un population, which exhibited the highest emergence (178.0 6.9 insects/dish).
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Fig. 1. Normalized cumulative emergence of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 1.
The cumulative emergence of the phosphine-resistant – P and susceptible – P populations of R. dominica overlapped exhibiting quicker development than the phosphine-resistant – BD and the susceptible – NE populations (Fig. 1c; Table 1). The total emergence of the phosphine-resistant – P population was much lower (123.6 17.7 insects/dish) than that of the susceptible – NE (194.2 35.2 insects/dish), susceptible – P (218.2 16.4 insects/ dish), and resistant – BD populations (230.6 12.6 insects/dish). 3.1.2. Daily emergence Although the cumulative emergence curves indicate significant differences among populations of each insect species, the population differences in the rate of daily emergence are even larger
(Table 2; Fig. 2). The rate of daily emergence was significantly lower for the phosphine-resistant populations of T. castaneum, when compared with the phosphine-susceptible populations of this species, which reached a maximum emergence about 5 days earlier than the resistant populations (Fig. 2a). The daily emergence rate for the populations of O. surinamensis was highest for the population susceptible – Un, followed by resistant – G, susceptible – Ub, and resistant – AD, which exhibited a peak of maximum emergence about half that of the susceptible – Un and with 2 days delay (Fig. 2b). The daily emergence rate of the phosphine-resistant – P population of R. dominica was nearly half that of the resistant – BD population and both susceptible populations, which exhibited higher emergence (Fig. 2c).
Table 1 Summary of the non-linear regression analysis of the (normalized) cumulative emergence curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 1. Parameter estimates (SEM)
dferror
R2
Variable
Model
Population
a
b
Tribolium castaneum
y ¼ a/(1 þ exp((x b)/c))
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
96.8 1.0 98.9 1.1 99.5 0.9 100.0 0.7
15.4 0.3 14.6 0.3 18.1 0.2 18.1 0.2
5.2 0.2 5.0 0.2 5.2 0.2 5.4 0.1
93 93 93 93
1988.7 1638.2 3268.8 5179.8
0.97 0.97 0.98 0.99
Oryzaephilus surinamensis
y ¼ a/(1 þ exp((x b)/c))
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
98.6 0.3 97.8 0.4 98.5 0.4 97.4 0.8
15.8 0.1 16.0 0.1 17.8 0.1 16.9 0.2
4.3 0.1 4.2 0.1 3.9 0.1 4.0 0.1
89 89 89 89
18,029.0 14,230.3 12,703.6 3612.1
0.97 0.99 0.99 0.98
Rhyzopertha dominica
y ¼ a exp(exp((x b)/c))
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
114.2 2.4 99.0 0.6 101.0 0.5 98.3 0.8
18.4 0.2 19.4 0.1 19.6 0.1 16.7 0.2
9.07 0.2 9.16 0.2 9.08 0.2 9.17 0.3
183 183 183 182
5962.2 11,172.1 13,536.4 4322.3
0.98 0.99 0.99 0.97
F
c
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
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Table 2 Summary of the non-linear regression analysis of the daily emergence curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 2. Parameter estimates (SEM)
R2
Model
Population
b
c
Tribolium castaneum
y ¼ a exp(0.5((x b)/c)2)
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
9.7 0.5 8.7 0.5 6.7 0.4 5.3 0.3
15.2 0.6 14.6 0.7 18.3 0.6 18.4 0.6
9.1 0.6 8.9 0.7 9.2 0.7 9.5 0.6
93 93 93 93
82.7 74.7 73.0 81.0
0.64 0.61 0.61 0.63
Oryzaephilus surinamensis
y ¼ a exp(0.5((x b)/c)2)
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
19.6 0.6 16.1 0.5 18.4 0.6 10.7 0.4
16.5 0.2 16.5 0.2 18.4 0.2 17.1 0.3
6.9 0.2 6.5 0.2 6.0 0.2 6.5 0.3
89 89 89 89
361.7 376.5 323.3 220.0
0.89 0.89 0.87 0.83
Rhyzopertha dominica
y ¼ a exp(0.5 (ln(x/b)/c)2)
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
18.2 0.6 16.2 0.7 18.8 0.6 9.9 0.4
18.0 0.3 19.2 0.5 19.5 0.4 16.1 0.5
0.5 0.0 0.4 0.0 0.5 0.0 0.5 0.0
183 183 183 182
291.5 166.7 307.3 135.7
0.76 0.64 0.77 0.59
a
dferror
F
Variable
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
3.2. Population growth
4. Discussion
The 3-parameter sigmoid model best described the population growth of all three species of stored-product insects (P < 0.01; R2 0.77) (Table 3). Similar to the developmental rate, the population growth rate was lower in the phosphine-resistant populations of T. castaneum, in the phosphine-resistant – G population of O. surinamensis, and in the phosphine-resistant – P population of R. dominica (Fig. 3). The phosphine-susceptible populations of T. castaneum, as well as the phosphine-resistant – G population of O. surinamensis, reached a plateau in their levels at the end of the storage period as a likely result of the high population densities reached in their respective experimental units.
Fitness costs associated with insecticide resistance are frequently reported among insect pests and it is a common assumption in models of insecticide resistance evolution (Beeman and Nani, 1986; Coustau et al., 2000; Haubruge and Arnaud, 2001; Raymond et al., 2001; Fragoso et al., 2005; Guedes et al., 2006; Oliveira et al., 2007). Such costs are the likely result of an energy imbalance, diverting energy from basic physiological process (e.g., development and reproduction) to protection against insecticides, leading to insecticide resistance (Guedes et al., 2006; Arau´jo et al., 2008ab). These physiological costs are translated into fitness costs turning insecticide resistance into
Fig. 2. Daily emergence of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 2.
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Table 3 Summary of the non-linear regression analysis of the population growth curves of Tribolium castaneum, Oryzaephilus surinamensis and Rhyzopertha dominica shown in Fig. 3. dferror
F
R2
15.7 3.9 14.5 1.5 24.0 2.0 29.3 6.4
39 39 39 39
79.1 441.3 1073.8 202.9
0.80 0.95 0.98 0.91
76.6 8.9 66.3 15.0 65.4 11.2 55.6 7.0
25.2 4.4 25.3 9.1 22.0 7.5 22.8 5.5
25 25 25 25
210.6 44.2 48.7 84.3
0.94 0.77 0.79 0.87
93.9 15.59 93.6 16.2 79.6 5.5 142.0 15.4
19.3 5.8 23.7 5.8 17.1 3.0 32.1 4.6
39 39 39 39
86.3 127.2 208.3 53.9
0.81 0.86 0.91 0.99
Variable
Model
Population
Parameter estimates (SEM) b
c
Tribolium castaneum
y ¼ a/(1 þ exp((x b)/c))
Susceptible – AB Susceptible – BP Resistant – CJ Resistant – A
294.4 28.4 275.9 9.9 346.1 39.4 503.3 39.8
62.8 5.0 59.7 1.8 95.7 5.9 127.9 39.1
Oryzaephilus surinamensis
y ¼ a/(1 þ exp((x b)/c))
Susceptible – Un Susceptible – Ub Resistant – G Resistant – AD
1493.4 215.4 954.5 221.7 1313.5 248.1 511.6 57.1
Rhyzopertha dominica
y ¼ a/(1 þ exp((x b)/c))
Susceptible – P Susceptible – NE Resistant – BD Resistant – P
1194.6 419.9 1006.1 307.9 1116.43 134.3 1490.2 344.4
a
All parameter estimates were significant at P < 0.01 by Student’s t-test and all of the models were significant at P < 0.01 by Fisher’s F-test.
a disadvantageous trait in the absence of insecticides. Higher and earlier (daily) emergence among the phosphine-susceptible insect populations from our study led to higher cumulative emergence and higher population growth rates of these populations. Most of the phosphine-resistant populations exhibited lower developmental and population growth rates indicating prevalence of fitness cost associated with phosphine resistance, as frequently reported among insect species (Haubruge and Arnaud, 2001; Fragoso et al., 2005; Pimentel et al., 2009). Our findings provide support for the contention that energy allocation to insecticide resistance mechanisms can impair the reproductive performance of the resistant individuals (Coustau et al., 2000; Guedes et al., 2006; Pimentel et al., 2008, 2009).
Despite the frequent association between phosphine resistance and fitness disadvantage, there were a few instances of lack of such association, particularly regarding two phosphine-resistant populations, one of O. surinamenis and one of R. dominica (resistant – G and resistant – BD, respectively). Insecticide resistance is rarely fixed in natural populations because of its associated fitness cost and relative infrequent use of insecticides allowing (partial) reestablishment of the insecticide susceptibility (Coustau et al., 2000; Guedes et al., 2006). However, intense and extended selection for insecticide resistance may either lead to the selection of fitness modifier genes that ameliorate the cost of insecticide resistance (by decreasing its fitness disadvantage), or may favor the selection of less costly phosphine resistance genes (Coustau et al., 2000; Guedes
Fig. 3. Population growth rate of two phosphine-susceptible (B––B, 6d6) and two phosphine-resistant populations (,—,, >–$$–>) of Tribolium castaneum (a), Oryzaephilus surinamensis (b), and Rhyzopertha dominica (c). The symbols represent the means of four replicates and the equation parameters are given in Table 3.
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et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2008). Indeed this may be the case for a few Brazilian phosphine-resistant populations of stored-product insects, where phosphine resistance is increasing and becoming a problem in recent years, although not yet at the extent observed in other countries such as Australia (Lorini et al., 2007; Pimentel et al., 2007, 2009; Nayak and Collins, 2008). In a few instances, the intensive selection for phosphine resistance for several years may have favored the suppression of the deleterious effects of this trait mitigating the fitness costs usually associated with it. This seems to take place in the resistant – G and resistant – BD populations of O. surinamensis and R. dominica respectively. Such mitigation has already been reported in pyrethroid-resistant populations of Sitophilus zeamais (Coleoptera: Curculionidae) (Guedes et al., 2006; Oliveira et al., 2007; Ribeiro et al., 2007). The potential fitness costs associated with phosphine resistance can affect the fixation and dispersal of the phosphine resistance genes due to their impact on the carrier individuals, with important implications for resistance management (Fragoso et al., 2005; Oliveira et al., 2007). From an applied perspective, the management of phosphine-resistant populations of stored-product insects can be achieved by minimizing phosphine use. This will allow the reestablishment of phosphine susceptibility when phosphine resistance is associated with a fitness cost, which seems to be frequent among phosphine-resistant populations of stored-product insects in current and previous studies (Lorini et al., 2007; Pimentel et al., 2007, 2009). However, the reestablishment of phosphine susceptibility with the brief suspension of its use should not be recommended as a management tactic for phosphine resistance when the resistant population does not exhibit an associated fitness cost, as in the cases of the resistant – G population of O. surinamensis and the resistant – BD population of R. dominica. Therefore, the recognition of the prevailing genotypes of phosphine resistance in a region should direct the selection of tactics for managing phosphine resistance. Acknowledgements Appreciation is expressed to the Minas Gerais State Agency for Research Aid (FAPEMIG), National Council of Scientific and Technological Development (CNPq), and CAPES Foundation (Brazilian Ministry of Education). The comments and suggestions provided by Dr. F. Arthur and an anonymous referee were greatly appreciated. References Arau´jo, R.A., Guedes, R.N.C., Oliveira, M.G.A., Ferreira, G.H., 2008a. Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais. Bulletin of Entomological Research 98, 417–424. Arau´jo, R.A., Guedes, R.N.C., Oliveira, M.G.A., Ferreira, G.H., 2008b. Enhanced proteolytic and cellulolytic activity in insecticide-resistant strains of the maize weevil, Sitophilus zeamais. Journal of Stored Products Research 44, 354–359.
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