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Movement of greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses
Agriculture, Ecosystems and Environment 102 (2004) 341–348
Movement of greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses Rosa Gabarra a,∗ , Òscar Alomar a , Cristina Castañé a , Marta Goula b , Ramon Albajes c a b
Departament de Protecció Vegetal, IRTA-Centre de Cabrils, Cabrils, 08348 Barcelona, Spain Departament de Biologia Animal (Artròpodes), Facultat de Biologia, Universitat de Barcelona, 08028 Barcelona, Spain c Centre UdL-IRTA, Universitat de Lleida, 25198 Lleida, Spain
Received 26 November 2002; received in revised form 13 August 2003; accepted 22 August 2003
Abstract Some Mediterranean greenhouses are inserted in a landscape of open fields, non-agricultural and woody habitats. Both the greenhouse whitefly and its polyphagous predators are well adapted to protected and field crops. The phenology and intensity of whitefly and predator exchange between greenhouses and surrounding habitats were investigated in two different zones of northern Spain. Whiteflies colonised greenhouses earlier and built up high populations before predators established in the crop. Both the abundance of vegetation and the topographic characteristics of the environment surrounding greenhouses affected the numbers of predators entering the tomato crop through the greenhouse openings whereas whitefly migration was only affected by the topography around the greenhouses. These results are discussed in terms of biological control of greenhouse pests by naturally occurring predators. © 2003 Elsevier B.V. All rights reserved. Keywords: Trialeurodes vaporariorum; Macrolophus caliginosus melanotoma; Dicyphus tamaninii; Greenhouses; Predators; Crop colonisation
1. Introduction Mediterranean greenhouses are situated in a variety of agricultural landscapes with different degrees of diversity. Some are within large areas of cultivation under plastic with relatively poor habitats outside, others in patchy landscapes of annual crops in the open field, in non-agricultural or even in woody habitats (Gullino et al., 1999). Species with high dispersal capacity are allowed to move between ephemeral habitats (Wissinger, 1997) by successively colonising crops and non-agricultural plants. If non-agricultural ∗ Corresponding author. Tel.: +34-93-750-99-76. E-mail address: [email protected] (R. Gabarra).
vegetation is available as a refuge, crops may be colonised early by species coming from the permanent habitats. This pattern may be the cause of regular greenhouse colonisation by predatory insects in Mediterranean areas but there are no detailed experimental records on this. In the northeast of the Iberian Peninsula predatory mirids are well adapted to colonising both protected and unprotected crops. They contribute in particular to reducing pest densities of greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Albajes and Alomar, 1999). Two predatory species are mainly involved: Macrolophus caliginosus Wagner (=M. melanotoma Costa; Carapezza, 1995; Kerzhner and Josifov, 1999) and Dicyphus tamaninii Wagner. In
0167-8809/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2003.08.012
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winter, both predators are found on several agricultural and non-agricultural plants, such as potato, Dittrichia viscosa (L.) Greuter, Cistus spp., and Parietaria officinalis L., from which they colonise unsprayed crops in spring (Alomar et al., 1994; Goula and Alomar, 2000). The presence of these overwintering shelter plants may be associated with enhanced predation in nearby crops. Alomar et al. (2002) have shown that the proximity and complexity of the vegetation surrounding the crops influenced the colonisation of tomato fields by both predators. Both are also common in protected crops where they contribute to biologically control pest insects (Castañé et al., 2000). The role of the surrounding vegetation in the colonisation is poorly known. This work aims to assess the movement of greenhouse whitefly and its predators between greenhouses and the surrounding habitats.
2. Materials and methods Field work was conducted in El Maresme county, a major vegetable production area north of Barcelona (a strip 2–7 by 50 km along the coast). The area is limited to the west by hilly woodland and to the east by the Mediterranean Sea. Two pairs of tomato greenhouses owned by the same grower under IPM programmes were chosen. The four greenhouses were located on terraces, facing northeast. The surfaces of the greenhouses were within the range common in the area (Table 1). Structure and plastic cover were similar for the four greenhouses; i.e. a wooden structure covered by thermal polyethylene. Ventilation was provided by installing roll-up sides with a hand winch system installed at 180 cm height at both long sides, that may be opened up to 1 m. Tomato seedlings were transplanted in February and grown under similar
Table 1 Characteristics of the greenhouses studied and of nearby floraa Vegetation nearby Scarce A1
Amaranthus sp. Borago sp. Calendula sp. Centaurea sp. Conyza sp. Cynoglossum sp. Dittrichia sp. Galium sp. Geranium sp. Parietaria sp. Sonchus sp. Urtica sp. Beans Cucumber Eggplant Potato Strawberry Tomato Zucchini a
Abundant
(1200)b
A2
SWc (down)d
NEc (up)d
X
X
(1580)b
SWc (down)d
NEc (up)d
B2 (780)b
SWc (down)d
NEc (up)d
X
X
X
SWc (down)d
NEc (up)d X X
X X X
X X X X
X
X
X
X X
X X X
X
X X X X
X X X
X X
X X
X X X
X
X X X X X
All plant species are known to be potential sources of mirids. Surface (m2 ). c Greenhouse side. d Slope along greenhouse. b
B1 (950)b
X X
R. Gabarra et al. / Agriculture, Ecosystems and Environment 102 (2004) 341–348
cultural practices. Starting 1 week after transplantation, the four greenhouses were ventilated daily by opening ventilation during an increasing number of hours in the day as the season progressed. Encarsia formosa Gahan and Diglyphus isaea Walker were released to control greenhouse whitefly and leafminers as needed (Gabarra and Besri, 1999). No insecticide was applied throughout the season. Flight traps were used to determine movement of insects from April (12 or 8 weeks after transplantation) to the end of June. Flight traps consisted of clear plastic acetate sheets 19 cm × 29.5 cm coated on both sides with a layer of insect adhesive (Tangle-Trap) (Prokopy and Owens, 1978). Traps were spaced in the greenhouse 20 cm from the ventilation 7–8 m along the sides of each greenhouse. Trap faces were oriented parallel to the ventilation openings. The numbers of traps used depended on the size of the greenhouse (14 in both greenhouses of zone A, 15 and 16 in greenhouses B1 and B2, respectively). Traps were replaced weekly and the number of mirids and greenhouse whiteflies was determined in the laboratory with a stereomicroscope. Catches of predators and whiteflies on the outer and inner faces of traps estimated the numbers of insects entering or leaving greenhouses, respectively (Puche et al., 1993). The border vegetation was determined by identifying (De Bolòs and Vigo, 1995) and mapping each fortnight all plant species located within 25 m of the greenhouses. 2.1. Statistical analysis To detect differences between zones, the total number of insect-days per week and trap was calculated by the formula [(Xa + Xb )/2]Da−b , where Xa and Xb are the trap counts in two successive weeks a and b, and Da−b the number of days between two successive records (Ruppel, 1983). The influence of zone and greenhouse on the total number of whiteflies and predators was analysed within each√zone by ANOVA with original data transformed by (x + 0.5). The weekly number of whiteflies or predators caught on traps was analysed within each greenhouse by a three-way ANOVA with week, greenhouse side (southwest vs. northeast) and trap face (inner vs. outer) as main effects. As double interactions with week were statistically significant (P > 0.05) in most
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cases, the influence of greenhouse side and trap face on insect catches were analysed week by week. The effect of trap face was analysed for each greenhouse side in cases where the trap face × greenhouse side interaction was significant. To meet the assumptions, whitefly numbers were transformed by log(x √ + 1) and M. caliginosus data were transformed by (x + 0.5). When needed, means were compared by LSD.
3. Results Table 1 summarises crop characteristics and host plants recorded near the greenhouses. In zone A, the SW side of both greenhouses faced a downward slope, and was regularly weeded so that few Dicyphini host plants were recorded. During the experiment, zucchinis were transplanted near A1-SW, beans and tomatoes to A2-SW. The NE side of A1 faced an upward slope with non-host garden plants and only few weedy host plants (Centaurea spp., Conyza spp., Sonchus spp., and Galium aparine L.). The NE side of greenhouse A2, also facing an upward slope, was richer in Dicyphini hosts, including P. officinalis and some Calendula arvensis L., Sonchus spp., and, on top of the terrace, an abandoned artichoke field with D. viscosa. In zone B, greenhouses were closer to more complex vegetation, and had fallow land and stone walls to the east with many host plants (D. viscosa, P. officinalis, C. arvensis, Ononis natrix L., Borago officinalis L.). Both greenhouses were adjacent, so that the NE side of B1 and the SW one of B2 shared the same flora, although B1 was on a terrace below B2. Greenhouse B shared several hosts plants (Table 1), specially P. officinalis. The margins of the greenhouses were not fully weeded during the study period. In zone B, potatoes and beans were grown near side B1-NE, and zuchinis and eggplants were transplanted during the experiment. The total number of insect-days per trap was used to compare whitefly and predator abundance among zones. There was no significant difference in the total number of whitefly-days between zones (F = 1.02; d.f. = 1, 985; P > 0.05). In both zones, M. caliginosus was the prevalent predator, being significantly more abundant in zone B than in zone A (F = 5.02; d.f. = 1, 987; P < 0.001) (Table 2). Only 32 D. tamaninii adults were caught during the whole
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Table 2 Total number (mean ± S.E.) of insect × days caught in the four experimental greenhouses
T. vaporariorum M. caliginosus
A1
A2
B1
B2
140.5 ± 22.1 0.5 ± 0.5
2722.0 ± 467.6 8.5 ± 3.0
609.0 ± 148.8 159.6 ± 24.7
1450.1 ± 258.1 116.4 ± 13.4
trapping period in the four greenhouses and this predator was not further analysed. T. vaporariorum was the only whitefly species present in the experimental greenhouses and its numbers were already significant (P < 0.05) in the first monitoring week in all greenhouses. In the four greenhouses, trap counts were significantly (P < 0.05) influenced by: sampling week, greenhouse side, and trap face. However, the influence of each factor was
affected by the other factors as most double interactions resulted statistically significant (P < 0.05) (Table 3). Traps located on the NE side caught significantly (P < 0.05) more whiteflies than on the SW side (Table 4). In the NE side, the outer face caught significantly (P < 0.05) more whiteflies than the inner face of the trap in the four greenhouses whereas this difference was only found in one greenhouse for the SW side (Table 4). Since the influence
Table 3 ANOVAs of the total number of whitefly and predator adults caught per week and trap in four greenhouses (data log(x + 1) transformed) Source
Greenhouse whitefly d.f.
F
Predator P
d.f.
F
P
Greenhouse A1 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
8.230 1.230 1.230 8.230 8.230 1.230
20.34 49.91 57.93 7.09 2.66 60.40
<0.001 0.001 <0.001 <0.001 0.008 <0.001
8.222 1.222 1.222 8.222 8.222 1.222
1.19 0.67 2.79 0.67 1.10 2.73
Greenhouse A2 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
8.215 1.215 1.215 8.215 8.215 1.215
95.33 490.29 122.74 17.08 2.47 90.48
<0.001 <0.001 <0.001 <0.001 0.014 <0.001
8.281 1.281 1.281 8.281 8.281 1.281
6.89 7.84 11.08 1.67 1.24 5.10
<0.001 0.006 <0.001 NS NS 0.03
Greenhouse B1 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
11.323 1.323 1.323 11.323 11.323 1.323
106.86 134.58 118.52 3.21 2.63 22.47
<0.001 <0.001 <0.001 <0.001 0.003 <0.001
11.324 1.324 1.324 11.324 11.324 1.324
51.56 4.83 37.23 1.79 5.33 0.11
<0.001 0.03 <0.001 0.05 <0.001 NS
Greenhouse B2 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
11.356 1.356 1.356 11.356 11.356 1.356
308.60 269.18 148.60 4.81 7.63 124.15
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
11.347 1.347 1.347 11.347 11.347 1.347
67.58 8.04 8.21 0.48 2.13 1.70
<0.001 0.005 0.005 NS 0.02 NS
NS NS NS NS NS NS
R. Gabarra et al. / Agriculture, Ecosystems and Environment 102 (2004) 341–348
June
July
A1
M. caliginosus per trap
whiteflies per trap
May
30
outer
*
inner
*
20 10
* *
0 16
17
18
19
20
A2
21
* *
400
* * *
200
inner
0.4
1.2
15
16
17
18
19
20
21
22
15
16
17
18
19
20
21
22
A2
0.8
0.4
0
15
May
16
17
18
19
20
21
June
July
B1
*
80
*
*
60 40
14
22
*
20
M. caliginosus per trap
14
whiteflies per trap
outer
0.8
14
0
May
12
July
June
B1
* 8
4
0
0
9 10 11 12 13 14 15 16 17 18 19 20 21
B2
*
150
* *
* 100 50
M. caliginosus per trap
9 10 11 12 13 14 15 16 17 18 19 20 21
whiteflies per trap
July
A1
22
M. caliginosus per trap
whiteflies per trap
15
600
200
June
1.2
0
14
100
May
345
12
B2
* 8 4 0
0 9 10 11 12 13 14 15 16 17 18 19 20 21 weeks after transplanting
Fig. 1. Mean number of whitefly adults per trap on outer and inner trap faces in four experimental greenhouses (∗: week in which trap face catches differed significantly (P < 0.05); data log(x + 1) transformed).
9 10 11 12 13 14 15 16 17 18 19 20 21 weeks after transplanting
Fig. 2. Mean number of individuals of M. caliginosus per trap on outer and inner trap faces in four experimental greenhouses (∗: week in which trap face √ catches differed significantly (P < 0.05); data transformed by (x + 0.5)).
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Table 4 Mean number (±S.E.) of individuals of T. vaporariorum and M. caliginosus per trap in each greenhouse side and trap face in greenhouses where interaction was significant (P < 0.05)a Greenhouse
Side (slope)b
T. vaporariorum Outer face
M. caliginosus Inner face
Outer face
Inner face
NSc NS
NS NS
SW (down) NE (up)
3.21 ± 0.46 aB 13.97 ± 1.67 aA
3.30 ± 0.59 aA 2.66 ± 0.34 bA
A2
SW (down) NE (up)
28.88 ± 6.68 aB 337.76 ± 57.6 aA
23.63 ± 6.70 aA 39.81 ± 6.59 bA
0.12 ± 0.05 aB 0.41 ± 0.12 aA
0.04 ± 0.03 aA 0.07 ± 0.04 bA
B1
SW (down) NE (up)
7.78 ± 1.21 aB 34.39 ± 4.39 aA
4.81 ± 0.76 bA 10.24 ± 1.87 bA
1.10 ± 0.19 2.10 ± 0.28
1.45 ± 0.24 2.81 ± 0.40
B2
SW (down) NE (up)
12.80 ± 1.64 aB 79.24 ± 10.26 aA
14.19 ± 2.07 aA 20.57 ± 3.48 bA
NS NS
NS NS
A1
a Within each greenhouse, lower case letters indicate comparisons of trap faces (within rows) and upper case letters comparisons of √ greenhouse sides (within columns). Prior to analysis, data of whiteflies were transformed by log(x+1) and those of predators by (x + 0.5). b SW, oriented to the southwest; NE, oriented to the northeast. c Not significant.
of greenhouse side and trap face on whitefly catches varied with sampling week in most cases, catches were analysed week by week (Fig. 1). Catches were significantly (P < 0.05) higher on the outer trap face of the four greenhouses than on inner one in several of the monitoring weeks (Fig. 1). Outside movement of whitefly adults increased during the season in greenhouses with high counts, particularly after crop harvest is initiated. The total numbers of M. caliginosus remained very low in the greenhouse A1 throughout the season (Table 2) and predator catches were not significantly (P < 0.05) affected by any of the factors or interactions analysed (Table 3). On the contrary, catches were significantly (P < 0.05) affected by sampling week, greenhouse side, and trap face in the other three greenhouses (Table 3). Table 4 shows the interaction of greenhouse side × trap face found in greenhouse A2. Significant differences between the two faces were only found in the NE greenhouse side, in which the outer face caught more predators than the inner one. In greenhouse B1 the NE had higher catches than SW side (P < 0.05) (Table 4). In contrast with the observations for whiteflies, the trap face did not affect the numbers of captures and the inner face had significantly more catches (P < 0.05) in one sampling week of greenhouses B1 and B2 only (Fig. 2).
4. Discussion Whitefly adults were caught on the outer trap face during the first monitoring week. Greenhouse crops continued to receive high numbers of adults from outside during the crop season, over twofold increases in trap catches per week being common. Such unpredictable pest immigrations hampered seasonal inoculative releases of specific parasitoids in Mediterranean greenhouses (Alomar et al., 1989). There was no significant difference in the total number of whitefly-days caught between zones indicating that abundance and composition of vegetation close to the greenhouses were not a key factor. On the other hand, NE traps adjacent to an upward slope, had consistently more catches than SW ones in the four greenhouses, suggesting that presence of whitefly sources at the height of the ventilation facilitated the entrance of whitefly adults. Prevailing winds in the area are from S to E–SE during ventilation therefore did not contribute to the pattern of insect movement. For biological control to be successful it is important that predators become established when pest population is still at low density (Smith et al., 1997). Precocity in field colonisation by natural enemies is particularly relevant in ephemeral crops like greenhouse tomato. In the present work, the first predators were caught in mid- to late-May, when crop colonisation may be too
R. Gabarra et al. / Agriculture, Ecosystems and Environment 102 (2004) 341–348
late to prevent whitefly building up to high populations. The type, abundance and richness of agricultural and non-agricultural vegetations surrounding crop fields have been related to the abundance, diversity and earlier occurrence of native predators on some crops (Altieri and Letourneau, 1982; van Emden, 1990). For the predatory M. caliginosus, a number of plant species have been identified as overwintering refuges and related to the adequate colonisation of tomato fields (Alomar et al., 1994, 2002). Greenhouse A surrounded by sparse vegetation, had fewer predators than B that were surrounded by abundant vegetation. Colonisation of greenhouses from distant sources does not seem to occur as readily as observed in the open field (Alomar et al., 2002). It seems, therefore, that greenhouse cover may limit mirid immigration onto the crop even if ventilation remains open for most hours of the day, which is a common practice in the region. Greenhouse screening as sometimes recommended in the Mediterranean region (Berlinger et al., 1988), is hence likely to prevent colonization by natural enemies. Differences in trap counts between A2 greenhouse sides showed that the vicinity of D. viscosa and P. officinalis facilitated the entrance of mirid bugs. The vegetation surrounding the greenhouse B was more homogeneous but differences in predator movement between sides were nevertheless recorded. NE traps, adjacent to a slope, had more catches than SW ones. The topography of the terrain hence also plays a role in the immigration of natural enemies into greenhouses and hilly landscapes may favour the entrance of both predators and whiteflies. Predator catches began at the same time on both trap faces, but only in the last monitoring weeks were catches significantly different between faces. This suggests a continuous flux of adult predators moving to better food sources, reproduction places, or weather conditions as suggested for Coleomegilla maculata (de Geer) (Whitcomb, 1981). This should be further studied as conservation biological control by habitat management should not only seek to establish refuges as early sources of predators, but also to provide shelter or food sources for predators moving between the crop and the margin. In the present study there was only one major movement out of the greenhouse with minor entrance at the end of the season, indicating
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that greenhouses act as a source of M. caliginosus for neighbouring crops (Albajes and Alomar, 1999). The capacity of M. caliginosus to go in and out of greenhouses could regulate the density of the predator on the crop and would explain why this facultative predator does not cause damage in the open Mediterranean greenhouses in comparison with that reported for northern latitudes (Sampson and Jacobson, 1999), where the use of M. caliginosus for biological control is considered risky because of its damaging capacity on certain ornamental and tomato varieties. In conclusion, the composition of the vegetation, and possibly the topography, surrounding greenhouses may favour the colonisation of the crops by M. caliginosus but also the early immigration of whitefly adults. Composition and abundance of the vegetation and greenhouse ventilation may be managed to both enhance predator entrance into greenhouses and reduce crop colonisation by whiteflies.
Acknowledgements This research was supported by CICYT (AGF960483 and AGL2000-0354), and was possible thanks to the agreements between IRTA and the grower’s associations (ADV) in Alt Maresme and Baix Maresme. The comments of the two anonymous reviewers and the editor have greatly improved the manuscript. References Albajes, R., Alomar, O., 1999. Current and potential uses of polyphagous predators. In: Albajes, R., Gullino, M.L., van Lenteren, J.C., Elad, Y. (Eds.), Integrated Pest and Disease Management in Greenhouse Crops. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 265–275. Alomar, O., Castañé, C., Gabarra, R., Bordas, E., Adillón, J., Albajes, R., 1989. Cultural practices for IPM on protected crops in Catalonia. In: Cavalloro, R., Pelerents, C. (Eds.), Integrated Pest Management in Protected Vegetable Crops. A.A. Balkema, Rotterdam, pp. 339–346. Alomar, O., Goula, M., Albajes, R., 1994. Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonisation of tomato fields. IOBC/WPRS Bull. 17 (5), 217–223. Alomar, O., Goula, M., Albajes, R., 2002. Colonization of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric. Ecosyst. Environ. 89, 105–115. Altieri, M.A., Letourneau, D.K., 1982. Vegetation management and biological control in agroecosystems. Crop Protect. 1, 405–430.
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Berlinger, M., Dahan, R., Lebiush-Mordechi, S., 1988. Integrated pest management of organically grown tomato in Israel greenhouses. Appl. Agric. Res. 3, 233–238. Carapezza, A., 1995. The specific identities of Macrolophus melanotoma (A. Costa, 1853) and Stenodema curtecolli (A. Costa, 1853) (Insecta Heteroptera, Miridae). Nat. Siciliano S.IV XIX (3–4), 295–298. Castañé, C., Alomar, O., Goula, M., Gabarra, R., 2000. Natural populations of Macrolophus caliginosus and Dicyphus tamaninii in the control of the greenhouse whitefly in tomato crops. IOBC/WPRS Bull. 23 (1), 221–224. De Bolòs, O., Vigo, J., 1995. Flora dels Pa¨ısos Catalans, vols. 1–3. Editorial Barcino, Barcelona. Gabarra, R., Besri, M., 1999. Tomatoes. In: Albajes, R., Gullino, M.L., van Lenteren, J.C., Elad, Y. (Eds.), Integrated Pest and Disease Management in Greenhouse Crops. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 420–431. Goula, M., Alomar, O., 2000. Aportacions als m´ırids del Maresme (Insecta Heteroptera). 4es Jornades Naturalistes del Maresme, Mataró, novembre 1998. CATAM ed., Argentona, pp. 18–30. Gullino, M.L., Albajes, R., van Lenteren, J.C., 1999. Setting the stage: characteristics of protected cultivation and tools for sustainable crop protection. In: Albajes, R., Gullino, M.L., van Lenteren, J.C., Elad, Y. (Eds.), Integrated Pest and Disease Management in Greenhouse Crops. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 1–15. Kerzhner, I.M., Josifov, M., 1999. Cimicomorpha. II. Miridae. In: Aukema, B., Rieger, Chr. (Eds.), Catalogue of the Heteroptera
of the Palaearctic Region, vol. 3. Netherlands Entomological Society, Amsterdam, 577 pp. Prokopy, R.J., Owens, E.D., 1978. Visual generalist with visual specialist phytophagous insects:host selection behaviour and application to management. Entomol. Exp. Appl. 24, 409– 420. Puche, H., Funderburk, J.E., Olson, S.M., 1993. Captures of Frankliniella species (Thysanoptera: Thripidae) in tomatoes versus weather, surrounding vegetation, and orientation of sticky cards. Entomology 1, 55–62. Ruppel, R.F., 1983. Cumulative insect-days as an index of crop protection. J. Econ. Entomol. 76, 375–377. Sampson, C., Jacobson, R.J., 1999. Macrolophus caliginosus Wagner (Heteroptera: Miridae): a predator causing damage to UK tomatoes. IOBC/WPRS Bull. 22 (1), 213–216. Smith, J.W., Wiedenmann, R.N., Gilstrap, F.E., 1997. Challenges and opportunities for biological control in ephemeral crop habitats: an overview. Biol. Contr. 10, 2–3. van Emden, H.F., 1990. Plant diversity and natural enemy efficiency in agroecosystems. In: Ehler, L.E., MacKauer (Eds.), Critical Issues in Biological Control. Intecept Ltd., Andover, Hants, pp. 63–80. Whitcomb, W.H., 1981. The use of predators in insect control. In: Pimentel, D. (Ed.), CRC Handbook of Pest Management in Agriculture, vol. II. CRC Press, Boca Raton, FL, pp. 105–123. Wissinger, S.A., 1997. Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol. Contr. 10, 4–15.
Movement of greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses Rosa Gabarra a,∗ , Òscar Alomar a , Cristina Castañé a , Marta Goula b , Ramon Albajes c a b
Departament de Protecció Vegetal, IRTA-Centre de Cabrils, Cabrils, 08348 Barcelona, Spain Departament de Biologia Animal (Artròpodes), Facultat de Biologia, Universitat de Barcelona, 08028 Barcelona, Spain c Centre UdL-IRTA, Universitat de Lleida, 25198 Lleida, Spain
Received 26 November 2002; received in revised form 13 August 2003; accepted 22 August 2003
Abstract Some Mediterranean greenhouses are inserted in a landscape of open fields, non-agricultural and woody habitats. Both the greenhouse whitefly and its polyphagous predators are well adapted to protected and field crops. The phenology and intensity of whitefly and predator exchange between greenhouses and surrounding habitats were investigated in two different zones of northern Spain. Whiteflies colonised greenhouses earlier and built up high populations before predators established in the crop. Both the abundance of vegetation and the topographic characteristics of the environment surrounding greenhouses affected the numbers of predators entering the tomato crop through the greenhouse openings whereas whitefly migration was only affected by the topography around the greenhouses. These results are discussed in terms of biological control of greenhouse pests by naturally occurring predators. © 2003 Elsevier B.V. All rights reserved. Keywords: Trialeurodes vaporariorum; Macrolophus caliginosus melanotoma; Dicyphus tamaninii; Greenhouses; Predators; Crop colonisation
1. Introduction Mediterranean greenhouses are situated in a variety of agricultural landscapes with different degrees of diversity. Some are within large areas of cultivation under plastic with relatively poor habitats outside, others in patchy landscapes of annual crops in the open field, in non-agricultural or even in woody habitats (Gullino et al., 1999). Species with high dispersal capacity are allowed to move between ephemeral habitats (Wissinger, 1997) by successively colonising crops and non-agricultural plants. If non-agricultural ∗ Corresponding author. Tel.: +34-93-750-99-76. E-mail address: [email protected] (R. Gabarra).
vegetation is available as a refuge, crops may be colonised early by species coming from the permanent habitats. This pattern may be the cause of regular greenhouse colonisation by predatory insects in Mediterranean areas but there are no detailed experimental records on this. In the northeast of the Iberian Peninsula predatory mirids are well adapted to colonising both protected and unprotected crops. They contribute in particular to reducing pest densities of greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Albajes and Alomar, 1999). Two predatory species are mainly involved: Macrolophus caliginosus Wagner (=M. melanotoma Costa; Carapezza, 1995; Kerzhner and Josifov, 1999) and Dicyphus tamaninii Wagner. In
0167-8809/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2003.08.012
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winter, both predators are found on several agricultural and non-agricultural plants, such as potato, Dittrichia viscosa (L.) Greuter, Cistus spp., and Parietaria officinalis L., from which they colonise unsprayed crops in spring (Alomar et al., 1994; Goula and Alomar, 2000). The presence of these overwintering shelter plants may be associated with enhanced predation in nearby crops. Alomar et al. (2002) have shown that the proximity and complexity of the vegetation surrounding the crops influenced the colonisation of tomato fields by both predators. Both are also common in protected crops where they contribute to biologically control pest insects (Castañé et al., 2000). The role of the surrounding vegetation in the colonisation is poorly known. This work aims to assess the movement of greenhouse whitefly and its predators between greenhouses and the surrounding habitats.
2. Materials and methods Field work was conducted in El Maresme county, a major vegetable production area north of Barcelona (a strip 2–7 by 50 km along the coast). The area is limited to the west by hilly woodland and to the east by the Mediterranean Sea. Two pairs of tomato greenhouses owned by the same grower under IPM programmes were chosen. The four greenhouses were located on terraces, facing northeast. The surfaces of the greenhouses were within the range common in the area (Table 1). Structure and plastic cover were similar for the four greenhouses; i.e. a wooden structure covered by thermal polyethylene. Ventilation was provided by installing roll-up sides with a hand winch system installed at 180 cm height at both long sides, that may be opened up to 1 m. Tomato seedlings were transplanted in February and grown under similar
Table 1 Characteristics of the greenhouses studied and of nearby floraa Vegetation nearby Scarce A1
Amaranthus sp. Borago sp. Calendula sp. Centaurea sp. Conyza sp. Cynoglossum sp. Dittrichia sp. Galium sp. Geranium sp. Parietaria sp. Sonchus sp. Urtica sp. Beans Cucumber Eggplant Potato Strawberry Tomato Zucchini a
Abundant
(1200)b
A2
SWc (down)d
NEc (up)d
X
X
(1580)b
SWc (down)d
NEc (up)d
B2 (780)b
SWc (down)d
NEc (up)d
X
X
X
SWc (down)d
NEc (up)d X X
X X X
X X X X
X
X
X
X X
X X X
X
X X X X
X X X
X X
X X
X X X
X
X X X X X
All plant species are known to be potential sources of mirids. Surface (m2 ). c Greenhouse side. d Slope along greenhouse. b
B1 (950)b
X X
R. Gabarra et al. / Agriculture, Ecosystems and Environment 102 (2004) 341–348
cultural practices. Starting 1 week after transplantation, the four greenhouses were ventilated daily by opening ventilation during an increasing number of hours in the day as the season progressed. Encarsia formosa Gahan and Diglyphus isaea Walker were released to control greenhouse whitefly and leafminers as needed (Gabarra and Besri, 1999). No insecticide was applied throughout the season. Flight traps were used to determine movement of insects from April (12 or 8 weeks after transplantation) to the end of June. Flight traps consisted of clear plastic acetate sheets 19 cm × 29.5 cm coated on both sides with a layer of insect adhesive (Tangle-Trap) (Prokopy and Owens, 1978). Traps were spaced in the greenhouse 20 cm from the ventilation 7–8 m along the sides of each greenhouse. Trap faces were oriented parallel to the ventilation openings. The numbers of traps used depended on the size of the greenhouse (14 in both greenhouses of zone A, 15 and 16 in greenhouses B1 and B2, respectively). Traps were replaced weekly and the number of mirids and greenhouse whiteflies was determined in the laboratory with a stereomicroscope. Catches of predators and whiteflies on the outer and inner faces of traps estimated the numbers of insects entering or leaving greenhouses, respectively (Puche et al., 1993). The border vegetation was determined by identifying (De Bolòs and Vigo, 1995) and mapping each fortnight all plant species located within 25 m of the greenhouses. 2.1. Statistical analysis To detect differences between zones, the total number of insect-days per week and trap was calculated by the formula [(Xa + Xb )/2]Da−b , where Xa and Xb are the trap counts in two successive weeks a and b, and Da−b the number of days between two successive records (Ruppel, 1983). The influence of zone and greenhouse on the total number of whiteflies and predators was analysed within each√zone by ANOVA with original data transformed by (x + 0.5). The weekly number of whiteflies or predators caught on traps was analysed within each greenhouse by a three-way ANOVA with week, greenhouse side (southwest vs. northeast) and trap face (inner vs. outer) as main effects. As double interactions with week were statistically significant (P > 0.05) in most
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cases, the influence of greenhouse side and trap face on insect catches were analysed week by week. The effect of trap face was analysed for each greenhouse side in cases where the trap face × greenhouse side interaction was significant. To meet the assumptions, whitefly numbers were transformed by log(x √ + 1) and M. caliginosus data were transformed by (x + 0.5). When needed, means were compared by LSD.
3. Results Table 1 summarises crop characteristics and host plants recorded near the greenhouses. In zone A, the SW side of both greenhouses faced a downward slope, and was regularly weeded so that few Dicyphini host plants were recorded. During the experiment, zucchinis were transplanted near A1-SW, beans and tomatoes to A2-SW. The NE side of A1 faced an upward slope with non-host garden plants and only few weedy host plants (Centaurea spp., Conyza spp., Sonchus spp., and Galium aparine L.). The NE side of greenhouse A2, also facing an upward slope, was richer in Dicyphini hosts, including P. officinalis and some Calendula arvensis L., Sonchus spp., and, on top of the terrace, an abandoned artichoke field with D. viscosa. In zone B, greenhouses were closer to more complex vegetation, and had fallow land and stone walls to the east with many host plants (D. viscosa, P. officinalis, C. arvensis, Ononis natrix L., Borago officinalis L.). Both greenhouses were adjacent, so that the NE side of B1 and the SW one of B2 shared the same flora, although B1 was on a terrace below B2. Greenhouse B shared several hosts plants (Table 1), specially P. officinalis. The margins of the greenhouses were not fully weeded during the study period. In zone B, potatoes and beans were grown near side B1-NE, and zuchinis and eggplants were transplanted during the experiment. The total number of insect-days per trap was used to compare whitefly and predator abundance among zones. There was no significant difference in the total number of whitefly-days between zones (F = 1.02; d.f. = 1, 985; P > 0.05). In both zones, M. caliginosus was the prevalent predator, being significantly more abundant in zone B than in zone A (F = 5.02; d.f. = 1, 987; P < 0.001) (Table 2). Only 32 D. tamaninii adults were caught during the whole
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Table 2 Total number (mean ± S.E.) of insect × days caught in the four experimental greenhouses
T. vaporariorum M. caliginosus
A1
A2
B1
B2
140.5 ± 22.1 0.5 ± 0.5
2722.0 ± 467.6 8.5 ± 3.0
609.0 ± 148.8 159.6 ± 24.7
1450.1 ± 258.1 116.4 ± 13.4
trapping period in the four greenhouses and this predator was not further analysed. T. vaporariorum was the only whitefly species present in the experimental greenhouses and its numbers were already significant (P < 0.05) in the first monitoring week in all greenhouses. In the four greenhouses, trap counts were significantly (P < 0.05) influenced by: sampling week, greenhouse side, and trap face. However, the influence of each factor was
affected by the other factors as most double interactions resulted statistically significant (P < 0.05) (Table 3). Traps located on the NE side caught significantly (P < 0.05) more whiteflies than on the SW side (Table 4). In the NE side, the outer face caught significantly (P < 0.05) more whiteflies than the inner face of the trap in the four greenhouses whereas this difference was only found in one greenhouse for the SW side (Table 4). Since the influence
Table 3 ANOVAs of the total number of whitefly and predator adults caught per week and trap in four greenhouses (data log(x + 1) transformed) Source
Greenhouse whitefly d.f.
F
Predator P
d.f.
F
P
Greenhouse A1 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
8.230 1.230 1.230 8.230 8.230 1.230
20.34 49.91 57.93 7.09 2.66 60.40
<0.001 0.001 <0.001 <0.001 0.008 <0.001
8.222 1.222 1.222 8.222 8.222 1.222
1.19 0.67 2.79 0.67 1.10 2.73
Greenhouse A2 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
8.215 1.215 1.215 8.215 8.215 1.215
95.33 490.29 122.74 17.08 2.47 90.48
<0.001 <0.001 <0.001 <0.001 0.014 <0.001
8.281 1.281 1.281 8.281 8.281 1.281
6.89 7.84 11.08 1.67 1.24 5.10
<0.001 0.006 <0.001 NS NS 0.03
Greenhouse B1 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
11.323 1.323 1.323 11.323 11.323 1.323
106.86 134.58 118.52 3.21 2.63 22.47
<0.001 <0.001 <0.001 <0.001 0.003 <0.001
11.324 1.324 1.324 11.324 11.324 1.324
51.56 4.83 37.23 1.79 5.33 0.11
<0.001 0.03 <0.001 0.05 <0.001 NS
Greenhouse B2 Week Greenhouse side Trap face Week × greenhouse side Week × trap face Greenhouse side × trap face
11.356 1.356 1.356 11.356 11.356 1.356
308.60 269.18 148.60 4.81 7.63 124.15
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
11.347 1.347 1.347 11.347 11.347 1.347
67.58 8.04 8.21 0.48 2.13 1.70
<0.001 0.005 0.005 NS 0.02 NS
NS NS NS NS NS NS
R. Gabarra et al. / Agriculture, Ecosystems and Environment 102 (2004) 341–348
June
July
A1
M. caliginosus per trap
whiteflies per trap
May
30
outer
*
inner
*
20 10
* *
0 16
17
18
19
20
A2
21
* *
400
* * *
200
inner
0.4
1.2
15
16
17
18
19
20
21
22
15
16
17
18
19
20
21
22
A2
0.8
0.4
0
15
May
16
17
18
19
20
21
June
July
B1
*
80
*
*
60 40
14
22
*
20
M. caliginosus per trap
14
whiteflies per trap
outer
0.8
14
0
May
12
July
June
B1
* 8
4
0
0
9 10 11 12 13 14 15 16 17 18 19 20 21
B2
*
150
* *
* 100 50
M. caliginosus per trap
9 10 11 12 13 14 15 16 17 18 19 20 21
whiteflies per trap
July
A1
22
M. caliginosus per trap
whiteflies per trap
15
600
200
June
1.2
0
14
100
May
345
12
B2
* 8 4 0
0 9 10 11 12 13 14 15 16 17 18 19 20 21 weeks after transplanting
Fig. 1. Mean number of whitefly adults per trap on outer and inner trap faces in four experimental greenhouses (∗: week in which trap face catches differed significantly (P < 0.05); data log(x + 1) transformed).
9 10 11 12 13 14 15 16 17 18 19 20 21 weeks after transplanting
Fig. 2. Mean number of individuals of M. caliginosus per trap on outer and inner trap faces in four experimental greenhouses (∗: week in which trap face √ catches differed significantly (P < 0.05); data transformed by (x + 0.5)).
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Table 4 Mean number (±S.E.) of individuals of T. vaporariorum and M. caliginosus per trap in each greenhouse side and trap face in greenhouses where interaction was significant (P < 0.05)a Greenhouse
Side (slope)b
T. vaporariorum Outer face
M. caliginosus Inner face
Outer face
Inner face
NSc NS
NS NS
SW (down) NE (up)
3.21 ± 0.46 aB 13.97 ± 1.67 aA
3.30 ± 0.59 aA 2.66 ± 0.34 bA
A2
SW (down) NE (up)
28.88 ± 6.68 aB 337.76 ± 57.6 aA
23.63 ± 6.70 aA 39.81 ± 6.59 bA
0.12 ± 0.05 aB 0.41 ± 0.12 aA
0.04 ± 0.03 aA 0.07 ± 0.04 bA
B1
SW (down) NE (up)
7.78 ± 1.21 aB 34.39 ± 4.39 aA
4.81 ± 0.76 bA 10.24 ± 1.87 bA
1.10 ± 0.19 2.10 ± 0.28
1.45 ± 0.24 2.81 ± 0.40
B2
SW (down) NE (up)
12.80 ± 1.64 aB 79.24 ± 10.26 aA
14.19 ± 2.07 aA 20.57 ± 3.48 bA
NS NS
NS NS
A1
a Within each greenhouse, lower case letters indicate comparisons of trap faces (within rows) and upper case letters comparisons of √ greenhouse sides (within columns). Prior to analysis, data of whiteflies were transformed by log(x+1) and those of predators by (x + 0.5). b SW, oriented to the southwest; NE, oriented to the northeast. c Not significant.
of greenhouse side and trap face on whitefly catches varied with sampling week in most cases, catches were analysed week by week (Fig. 1). Catches were significantly (P < 0.05) higher on the outer trap face of the four greenhouses than on inner one in several of the monitoring weeks (Fig. 1). Outside movement of whitefly adults increased during the season in greenhouses with high counts, particularly after crop harvest is initiated. The total numbers of M. caliginosus remained very low in the greenhouse A1 throughout the season (Table 2) and predator catches were not significantly (P < 0.05) affected by any of the factors or interactions analysed (Table 3). On the contrary, catches were significantly (P < 0.05) affected by sampling week, greenhouse side, and trap face in the other three greenhouses (Table 3). Table 4 shows the interaction of greenhouse side × trap face found in greenhouse A2. Significant differences between the two faces were only found in the NE greenhouse side, in which the outer face caught more predators than the inner one. In greenhouse B1 the NE had higher catches than SW side (P < 0.05) (Table 4). In contrast with the observations for whiteflies, the trap face did not affect the numbers of captures and the inner face had significantly more catches (P < 0.05) in one sampling week of greenhouses B1 and B2 only (Fig. 2).
4. Discussion Whitefly adults were caught on the outer trap face during the first monitoring week. Greenhouse crops continued to receive high numbers of adults from outside during the crop season, over twofold increases in trap catches per week being common. Such unpredictable pest immigrations hampered seasonal inoculative releases of specific parasitoids in Mediterranean greenhouses (Alomar et al., 1989). There was no significant difference in the total number of whitefly-days caught between zones indicating that abundance and composition of vegetation close to the greenhouses were not a key factor. On the other hand, NE traps adjacent to an upward slope, had consistently more catches than SW ones in the four greenhouses, suggesting that presence of whitefly sources at the height of the ventilation facilitated the entrance of whitefly adults. Prevailing winds in the area are from S to E–SE during ventilation therefore did not contribute to the pattern of insect movement. For biological control to be successful it is important that predators become established when pest population is still at low density (Smith et al., 1997). Precocity in field colonisation by natural enemies is particularly relevant in ephemeral crops like greenhouse tomato. In the present work, the first predators were caught in mid- to late-May, when crop colonisation may be too
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late to prevent whitefly building up to high populations. The type, abundance and richness of agricultural and non-agricultural vegetations surrounding crop fields have been related to the abundance, diversity and earlier occurrence of native predators on some crops (Altieri and Letourneau, 1982; van Emden, 1990). For the predatory M. caliginosus, a number of plant species have been identified as overwintering refuges and related to the adequate colonisation of tomato fields (Alomar et al., 1994, 2002). Greenhouse A surrounded by sparse vegetation, had fewer predators than B that were surrounded by abundant vegetation. Colonisation of greenhouses from distant sources does not seem to occur as readily as observed in the open field (Alomar et al., 2002). It seems, therefore, that greenhouse cover may limit mirid immigration onto the crop even if ventilation remains open for most hours of the day, which is a common practice in the region. Greenhouse screening as sometimes recommended in the Mediterranean region (Berlinger et al., 1988), is hence likely to prevent colonization by natural enemies. Differences in trap counts between A2 greenhouse sides showed that the vicinity of D. viscosa and P. officinalis facilitated the entrance of mirid bugs. The vegetation surrounding the greenhouse B was more homogeneous but differences in predator movement between sides were nevertheless recorded. NE traps, adjacent to a slope, had more catches than SW ones. The topography of the terrain hence also plays a role in the immigration of natural enemies into greenhouses and hilly landscapes may favour the entrance of both predators and whiteflies. Predator catches began at the same time on both trap faces, but only in the last monitoring weeks were catches significantly different between faces. This suggests a continuous flux of adult predators moving to better food sources, reproduction places, or weather conditions as suggested for Coleomegilla maculata (de Geer) (Whitcomb, 1981). This should be further studied as conservation biological control by habitat management should not only seek to establish refuges as early sources of predators, but also to provide shelter or food sources for predators moving between the crop and the margin. In the present study there was only one major movement out of the greenhouse with minor entrance at the end of the season, indicating
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that greenhouses act as a source of M. caliginosus for neighbouring crops (Albajes and Alomar, 1999). The capacity of M. caliginosus to go in and out of greenhouses could regulate the density of the predator on the crop and would explain why this facultative predator does not cause damage in the open Mediterranean greenhouses in comparison with that reported for northern latitudes (Sampson and Jacobson, 1999), where the use of M. caliginosus for biological control is considered risky because of its damaging capacity on certain ornamental and tomato varieties. In conclusion, the composition of the vegetation, and possibly the topography, surrounding greenhouses may favour the colonisation of the crops by M. caliginosus but also the early immigration of whitefly adults. Composition and abundance of the vegetation and greenhouse ventilation may be managed to both enhance predator entrance into greenhouses and reduce crop colonisation by whiteflies.
Acknowledgements This research was supported by CICYT (AGF960483 and AGL2000-0354), and was possible thanks to the agreements between IRTA and the grower’s associations (ADV) in Alt Maresme and Baix Maresme. The comments of the two anonymous reviewers and the editor have greatly improved the manuscript. References Albajes, R., Alomar, O., 1999. Current and potential uses of polyphagous predators. In: Albajes, R., Gullino, M.L., van Lenteren, J.C., Elad, Y. (Eds.), Integrated Pest and Disease Management in Greenhouse Crops. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 265–275. Alomar, O., Castañé, C., Gabarra, R., Bordas, E., Adillón, J., Albajes, R., 1989. Cultural practices for IPM on protected crops in Catalonia. In: Cavalloro, R., Pelerents, C. (Eds.), Integrated Pest Management in Protected Vegetable Crops. A.A. Balkema, Rotterdam, pp. 339–346. Alomar, O., Goula, M., Albajes, R., 1994. Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonisation of tomato fields. IOBC/WPRS Bull. 17 (5), 217–223. Alomar, O., Goula, M., Albajes, R., 2002. Colonization of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric. Ecosyst. Environ. 89, 105–115. Altieri, M.A., Letourneau, D.K., 1982. Vegetation management and biological control in agroecosystems. Crop Protect. 1, 405–430.
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