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PACIFIC COOPERATIVE STUDIES UNIT

UNIVERSITY OF HAWAI’I AT MANOA
Department of Botany

3190 Maile Way

Honolulu, Hawai’i 96822

(808) 956-8218


Dr. David C. Duffy, Unit Leader

Technical Report 134
BIOLOGICAL CONTROL OF Miconia calvescens BY PHYTOPHAGOUS ARTHROPODS

Marcelo Coutinho Picanço1, Robert Weingart Barreto2, Elisangela Gomes Fidelis3, Altair Arlindo Semeão3, Jander Fagundes Rosado3, Shaiene Costa Moreno3, Emersom Cristi de Barros3, Gerson Adriano Silva3 and Tracy Johnson4
1 Departamento de Biologia Animal, Universidade Federal de Viçosa, 36571-000 Viçosa, MG, Brazil. E-mail: picanco@ufv.br

2 Departamento de Fitopatologia, Universidade Federal de Viçosa, 36571-000 Viçosa, MG, Brazil. E-mail: rbarreto@ufv.br

3 Agronomy students, Universidade Federal de Viçosa.

4 Institute of Pacific Islands Forestry, USDA Forest Service Pacific Southwest Research Station, P.O. Box 236, Volcano, Hawaii 96785

The PCSU is a cooperative program

between

The University of Hawaii

and

U.S. Geological Survey, Biological Resources Discipline,



Pacific Islands Ecosystems Research Center,

and


U.S. National Park Service, Cooperative Ecological Studies Unit
March 2005
BIOLOGICAL CONTROL OF MICONIA CALVESCENS BY PHYTOPHAGOUS ARTHROPODS

1. ABSTRACT

More than 60 species of arthropods were found associated with Miconia calvescens at two Brazilian sites in a one-year survey for potential biological control agents within the weed’s native range in Minas Gerais, Brazil. Fifty-one insect species were collected, a majority of them phytophagous. Among the sap and cell feeders were two whitefly, a thrips species Heliothrips sp.n. (Thysanoptera: Thripidae), a psyllid Diclidophlebia sp. (Hemiptera: Psyllidae), an aphid species, and six species of leaf hoppers (five were species of Cicadellidae and one species of Flatidae). The psyllid and leaf hoppers appeared to warrant further evaluation, especially for their possible association with a lethal phytoplasm disease. Defoliators causing substantial damage included the leaf-roller Ategumia sp. (Lepidoptera: Pyralidae) and Druentia cf. inscita (Lepidoptera: Mimallonidae), a sawfly Atomacera petroa (Hymenoptera: Argidae), and the leaf-cutter ant Atta sexdens rubropilosa. Stem-boring insects were discovered in low numbers and included an Agrilus sp. (Coleoptera: Buprestidae) that may be capable of killing stems. An Apion sp. (Coleoptera: Brentidae) was found associated with inflorescences. These collections include many species not discovered in earlier surveys of miconia in Brazil and Costa Rica, suggesting that additional potential arthropod agents await discovery in areas not yet explored.



2. INTRODUCTION

Miconia calvescens DC. (Melastomataceae), a tree native to Central and South America, has become an aggressive invader of forest ecosystems in French Polynesia and Hawai’i following its introduction as an ornamental (Smith & Meyer 1998). M. calvescens dominates over 65% of the island of Tahiti and has spread to nearby Moorea and Raiatea (Meyer 1996). The invasion is more recent and less advanced in Hawai’i, where efforts at containment and eradication have been underway on four islands for over a decade (Smith and Meyer 1998). However, in Hawai’i as well as Tahiti, the hope for ultimate management of this invader lies in classical biological control (Smith 2002). This method involves the importation and release of natural enemies from the plant’s native region after a series of steps including: exploration for potential biocontrol agents, agent selection, rearing, host-range evaluation, life-cycle studies, and quarantining to eliminate hyperparasites (Julien 1997).

Previous surveys of arthropods associated with M. calvescens were undertaken by the Hawai’i Department of Agriculture in 1993-94 in Costa Rica and in 1994 in Rio de Janeiro, Brazil (Burkhart 1995). These expeditions resulted in a list of over 50 species of insects belonging to the orders Lepidoptera, Coleoptera and Homoptera. Although numerous, these collections were made during very brief periods (several days for each locality). Such brief explorations are likely to miss potentially valuable biocontrol agents that may be uncommon or in life stages that are difficult to collect and identify, such as eggs or small larvae (Balciunas 2002). A more detailed study of this entomofauna was therefore regarded as necessary to complement the pioneering survey by Burkhart. Our purpose in the present study was to discover additional phytophagous arthropods with potential for biocontrol of M. calvescens by surveying repeatedly for one year at two sites in the state of Minas Gerais, Brazil. Suitability of a few species was further evaluated in attempts at rearing under controlled conditions.



3. MATERIAL AND METHODS

3.1. Entomofauna of Miconia calvescens

Surveys of arthropods associated with M. calvescens were undertaken at two sites: Viçosa and Dionísio, both in Minas Gerais, Brazil. Viçosa is at an elevation of 649 meters and located at latitude 20º45'14"S and longitude 42º52'53"W. Average temperature is 19.4oC and average rainfall is 1221 mm/year. Dionísio is at an elevation of 344 meters and located at latitude 19º50'34"S and longitude 42º46'36"W. The local average temperature is 23.2oC and average rainfall is 1003 mm/year.

Surveys were conducted at intervals of approximately three weeks beginning in June 2001 and ending in July 2002, for a total of 14-15 visits to each site. Ten M. calvescens trees per site were chosen randomly for repeated sampling. Survey plants ranged 1-7 m in height and 6-150 mm in basal diameter at Viçosa and 1-4 m in height and 20-86 mm in basal diameter at Dionisio. Occurrence of all insects on selected miconia plants and neighboring plants was observed. Whenever an insect was observed both on M. calvescens and a neighboring plant the information was recorded. For each plant ten branches were randomly selected each visit and examined for arthropods. Numbers, position on the plant (stems, leaves, buds, flowers or fruits) and feeding habit were recorded for each arthropod species. This evaluation was made in the field, but whenever necessary parts of such plants were taken into the laboratory for further examination using a 100 x dissecting microscope. After evaluation individual specimens were collected, transported to the laboratory and deposited in a reference collection. Specimens were identified initially to order and, if possible, family. Those that were regarded as having potential for biocontrol were sent to taxonomists for identification.

4. RESULTS

More than 60 species of arthropods were found on M. calvescens including at least 51 insect species, three mite species and several spiders. Among the insect species 38 were phytophagous, three predaceous, six parasitoids, and four detritivorous. Among the phytophagous species, 18 were detected at a juvenile stage. Thirty-three phytophagous arthropods were associated with leaves, six were stem borers, and one was associated with fruits and flowers. Among the leaf-feeding arthropods species 18 were sap or cell feeders and 15 were defoliators.

4.1. Cell feeders

The cell feeding arthropods included three mite species and a thrips species. Their attack resulted in similar damage: a stippled yellowing pattern on leaves. Mite fauna was similar at the two sites. Mite populations were low overall and did not appear to have a significant impact on M. calvescens (Table 1).

Thrips was among the most damaging insects attacking M. calvescens. This insect was observed forming large groups composed of nymphs and adults feeding on the undersides of leaves. Colonized leaves turned yellow and became necrotic. Thrip populations were equivalent at the two localities. They occurred throughout the year at both sites. The largest populations of both nymphs and adults occurred during periods of lower temperature (Figures 1 and 2).

4.2. Sap feeders

Sap sucking insects observed attacking M. calvescens included two species of white flies, two scale insects, one aphid, six leaf hoppers and one psyllid (Table 1).

White flies were among the most damaging insects found on M. calvescens. The presence of nymphs and adults was associated with leaf discoloration. Two species occurred at both locations throughout the year. Adults of one species (sp.1) were around 1 mm long, about half the size of sp. 2. Sp. 1 was more abundant. The two white fly species had a denser population at Dionísio than at Viçosa (Table 1). The largest density of adults belonging to Sp. 1 occurred during lower rainfall and temperature periods and the largest density of Sp. 2 occurred at periods of lower temperature (Figures 1 and 3).

Two species of scale insects were found attacking leaves of M. calvescens. The density of the two species of scale insects was larger at Dionísio than at Viçosa (Table 1). Sp. 1 had a higher population density during periods of low rainfall and lower temperature. Sp. 1 was more abundant during periods of lower rainfall and lower temperature. Sp. 2 was more abundant during cooler periods. (Figures 1 and 4).

A species of wax-producing psyllid was found attacking shoots and young leaves. Population densities of nymphs and adults of the psyllid were larger at Dionísio than at Viçosa but they were present at the two sites throughout the year (Table 1, Figure 5). A coincidence of high populations of this psyllid with a rare but highly damaging phytoplasm-induced witches’ broom disease observed on several plants at two sites (Seixas et al. 2002) suggests that this insect may be the vector of the only lethal disease so far observed in M. calvescens (Tomasi et al. 2000).

Six species of leafhoppers were found feeding on M. calvescens. Nymphs of two of these species were found on M. calvescens; for the other species only adults were found. Five of the leafhopper species belong to the Cicadellidae and one to the Flatidae. The most abundant Cicadellidae were Empoasca sp. and Scaphytopius sp. (Table 1). Leafhoppers of the family Cicadellidae are known to act as vectors for phytoplasm diseases (Casela et al. 1998), and therefore any of these species might vector the above-mentioned witches’ broom. Scaphytopius sp. had a larger population density at Viçosa than at Dionísio. Nymphs and adults of Scaphytopius sp. were observed at both sites throughout the year. Largest nymph populations occurred during drier and cooler periods (Table 1, Figures 1 and 6). Empoasca sp. was more abundant at Dionísio than at Viçosa, particularly during April and June (Table 1, Figure 7).

One aphid species was found attacking M. calvescens during May and June of 2002 at Dionísio. Three stinkbug species (Pentatomidadeae) were found but always in low numbers (Table 1, Figure 8).

4.3. Defoliators

Defoliating insects observed on M. calvescens included eight lepidopteran species, one sawfly (Atomacera petroa Smith), leaf cutter ants (Atta sexdens rubropilosa) and adults of some beetle species. Coleoptera adults occurred were uncommonly found on M. calvescens leaves. Adults of two species of Buprestidae and two Curculionidae found feeding on M. calvescens leaves, are known to have larvae that are stem-borers (Table 2).

The most damaging of all lepidopteran species was a leaf roller, Ategumia sp. (Pyralidae). This species rolled leaves longitudinally, forming cylinders where the larvae hid and eventually pupated. Adults were greyish-brown moths 1 - 1,5 cm long with yellow spots on their wings. Their eggs were green and laid in groups covered with a thin transparent sheet. Miconia plants were defoliated up to 50% following attack by this species. Potted plants of the Hawaiian biotype that were left at one field site also were attacked by this species. Ategumia sp. caterpillars were observed at the two sites throughout the year. Ategumia sp. was more damaging at Dionísio, where populations were peaked in January 2002. At Viçosa this species was found only at low densities. The largest densities of Ategumia sp. caterpillars occurred during periods of higher temperature (Table 2, Figures 1 and 9).

Druentia cf. inscita (Mimallonidae) caterpillars were observed attacking M. calvescens. These caterpillars were green with brown stripes and were approximately 5 cm long at their final stage of development. They fed mostly on apical foliage, destroying the lamina of young leaves. On older leaves this species also was a leaf roller. This species was also more abundant at Dionísio than at Viçosa. The highest damage to plants was observed from March to May of 2002. This caterpillar was more abundant during warmer periods of the year. Caterpillars collected in the field pupated in the laboratory and metamorphosed into adults, but no egg laying has been observed (Table 2, Figures 1 and 10).

Antiblemma sp. (Noctuidae) caterpillars were also observed defoliating M. calvescens. These caterpillars move like a typical Geometrideae, they are green at the beginning of the larval stage and become violet at later stages of larval development. Initially they bore small holes on the leaves but as they grow the size of these holes grow in size leading to significant loss of lamina areas. These caterpillars were found at the two locations throughout the year with no significant peaks in population density (Table 2, Figure 11).

Caterpillars of a Limacodidae species were observed attacking M. calvescens on two occasions (June 2001 and June 2002) at Dionísio. These insects were found in low densities on both occasions but were nevertheless capable of causing some defoliation of plants (Table 2, Figure 12).

One sawfly species A. petroa (Hymenoptera: Argidae) had larvae attacking M. calvescens leaves and producing distinctive linear scars on the upper lamina. Heavy damage appeared to lead to leaf drop. When common, 6 sawfly larvae up to 1 cm long could be found on the upper side of a single leaf. A. petroa larvae were observed at both sites throughout the year. A. petroa was more abundant at Dionísio, where populations peaked in November-December 2001 and April 2002. Populations at both sites peaked in a period of high air temperature. Attempts to rear this species were unsuccessful. The larvae survived for up to five days after transfer to the laboratory or the greenhouse (Table 2, Figures 1 and 13).

Intense defoliating activity by leaf cutting ants (A. sexdens rubropilosa) was observed at Dionísio. The ants were also seen harvesting fruits of M. calvescens. The attack of this ant species was observed throughout the year at both sites (Table 2, Figure 14). Unfortunately, despite the significant damage to miconia this species has no potential as a biocontrol agent of M. calvescens since it is well known as a major generalist crop pest attacking most dicotyledons cultivated in Brazil (Della Lucia, 1993, Anjos et al. 1998).



4.4. Stem borers

Adults of several species of stem boring Coleoptera were collected, but larvae of only one Agrilus sp. (Buprestidae) were confirmed as capable of boring stems of M. calvescens. Agrilus sp. larvae, judging from evidence of their feeding galleries, appeared to be capable of killing branches and even whole plants. However our observations did not allow us to establish a definite causal link between this insect and plant mortality: it is possible that it attacked tissue that was already dead or dying. Attack by the larvae started at the external part of the stems and from there they dig tunnels towards the central part of the stems. This group of insects normally lays its eggs on thinner and tender branches. Pupae were found inside the galleries. Larvae, adults and stem damage were observed at the two sites. Larvae were observed at Viçosa from November 2001 to February 2002 and in May 2002 at Dionísio. Adults were seen from June to December of 2001 in Viçosa. In Dionísio adults were seen in August 2001, January, February and June 2002 in Dionísio. Stem boring was noticed from June 2001 to January 2002 in Viçosa and in November 2001 and January 2002 in Dionísio (Table 2, Figure 15).

Two individual adults of another Buprestidae species collected at Itabira, MG were maintained for two months feeding on Brazilian and Hawaiian biotypes of miconia. This species appears to have biocontrol potential. A new visit to the area of Itabira where this insect was collected was made in June 2003 but no insects of this species were found. Another attempt will be made during a warmer period (Figure 16).

Naupactus spp. (Coleoptera: Curculionidae) was commonly encountered in low numbers. Insects of this species were most abundant at Dionísio during months with lower air temperature (Table 2, Figures 1 and 17).

4.4. Flower and fruit feeders

Apion sp. (Coleoptera: Brentidae) adults were observed on leaves of M. calvescens throughout the year, but at low densities. Their higher densities occurred during periods of higher temperature (Table 2, Figures 1 and 18). Adults were 2 - 3 mm long and were black with thin yellow legs. Larvae of this genus are known to feed on fruits, seeds and inflorescences (Norambuena & Piper, 2000) as well as superficially boring stems (Knodel & Charlet, 2002), nevertheless larvae of this beetle were not observed on flowers, fruits of stems.

4.5. Other arthropods

Eriophyid mite induced galls on M. calvescens plants similar to the Hawaiian biotype (Fig 18) were observed during a survey for miconia pathogens in Ecuador in May 2000 (R.W.B. unpublished data), and apparently also were observed by Burkhart (1995) near Rio de Janeiro in 1994. Throughout the investigations by R.W.B. in Brazil, similar galls were widely found on other species of Miconia, often causing severe damage to leaves, flowers and fruits (e.g.: Miconia prasina [Sw.] DC.), but never on M. calvescens. Galls that appeared to be caused by eriophyids were also found on M. calvescens recently by entomologists in Costa Rica (Paul Hanson, personal communication). Eriophyid mites are often regarded by entomologists as having poor biocontrol potential since they can be heavily predated by other mites, however in some cases they do appear capable of providing effective control (Piper & Andres 1995).



5. CONCLUSIONS AND RECOMMENDATIONS

Over 60 species of arthropods were found associated with Miconia calvescens during our systematic survey at two sites in the state of Minas Gerais, Brazil. The great majority of species observed during this study were different from those recorded by Burkhart (1995). Only the lepidopterous Antegumia sp. (Pyralidae), Antiblemma sp. (Noctuidae) and Druentia cf. inscita (Mimallonidae) were recorded in both studies. This indicates that a diverse entomofauna exists in association with this species, offering a range of potential candidates for use in classical biocontrol.

Observations in the field suggest that the following species are sufficiently damaging to M. calvescens to warrant further evaluation as potential biocontrol agents: a whitefly species 1, Diclidophlebia sp. (Hemoptera: Psyllidae), Heliothrips sp.n (Thysanoptera: Thripidae), Ategumia sp. (Lepidoptera: Pyralidae), Druentia cf. inscita (Lepidoptera: Mimallonidae), Atomacera sp. (Hymenoptera: Argidae), Agrilus sp. (Coleoptera: Buprestidae) and another unidentified buprestid. Additional efforts to rear and document the life cycle of these insects are needed.

Specimens of selected species were sent to taxonomists for identification but for some groups no experts are available in Brazil. Several of the insects that were collected, clearly represent new species that will require description, naming and publication. Support from taxonomic specialists will be critical.

An effort to elucidate the link of potential vectors for witches broom disease and molecular characterization of the pathogen involved (probably a phytoplasm) are recommended. This disease was observed to be highly lethal, even to adult miconia.

Expansion of the arthropod survey to new areas of occurrence of this plant in Brazil is recommended. This will probably yield a larger range of pathogens and herbivores that may be useful in miconia biocontrol. A comparison of the arthropod fauna between Brazil and Costa Rica, where a similar survey is being undertaken on a different miconia biotype, will then become feasible and will help build a more complete image of the target plant and its natural enemies.


ACknowledgements

Climatic data for Viçosa were provided by the “Estação Climatológica Principal (INEMET/ 50 DISME/ UFV)” and for Dionísio by the “Estação Meteorológica de Ponte Alta” belonging to CAF Santa Bárbara Ltda. Financial support from the U.S. Geological Survey, Biological Resources Discipline, Pacific Island Ecosystems Research Center, Haleakala National Park, U.S. National Park Service, and Hawaii Department of Agriculture by means of RCUH-FUNARBE cooperative agreement is gratefully acknowledged. The cooperative agreement was administered through the Pacific Cooperative Studies Unit, University of Hawaii.

Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.



6. LITERATURE

ANJOS, N., DELLA LUCIA, T.M.C., MAYHÉ-NUNES, A.J. Guia prático sobre formigas cortadeiras em reflorestamentos. Ponte Nova: Graff Cor, 1998. 100p.

BALCIUNAS, J. 2002. Strategies for expanding and improving overseas research for biological control of weeds. Pp. 1-6 In: SMITH, C.W., DENSLOW, J., HIGHT, S. (Eds.). Proceedings of a workshop on biological control of invasive plants in native Hawaiian ecosystems. Pacific Cooperative Studies Unit, University of Hawai'I at Manoa. 122 pp. (Technical Report 129).

BURKHART, R. 1995. Natural enemies of Miconia calvescens, Hawai’i Department of Agriculture, unpublished report Reproduced with permission on website: www.botany.Hawai’i.edu/faculty/cw_smith/mc_control.htm. Accessed: [15/10/2003].

CASELA, C.R., RENFRO, B.L., KRATTIGER, A.F. 1998. Diagnosing Maize Diseases in Latin America. ISAAA Briefs, n.9.

CHEN, P.Y., POPOVICH, P.M. Correlation: parametric and nonparametric measures Thousand Oaks: Sage, 2002. 96p.

DELLA LUCIA, T.M.C. As formigas cortadeiras. Viçosa: Folha de Viçosa, 1993. 262p.

HARLEY, K.L.S, FORNO, I.W. 1992. Biological control of weeds, a handbook for practioners and students. Melbourne: Inkata. 74p.

JULIEN, M.H. 1997. Success, and failure, in biological control of weeds. In: JULIEN, M.H., WHITE, G. (Eds.). Biological control of weeds: theory and practical application. ACIR Monograph no 9, p.9-15.

KNODEL, J.J., CHARLET, L.D. Biology and integrated pest management of the sunflower stem weevils in the Great Plains. Fargo: North Dakota State University, 2002. 8p.(NDSU Extension Service E-821).

MEYER J.Y. 1996. Status of Miconia calvescens (Melastomataceae), a dominant invasive tree in the Society Islands (French Polynesia). Pacific Science, v.50, n.1, p.66-76.

MEYER J.Y., MALET, J.P. 1997. Study and management of the alien invasive tree Miconia calvescens DC. (Melastomataceae) in the islands of Raiatea and Tahaa (Society Islands, French Polynesia): 1992-1996. Cooperative National Park Resources Studies Unit University of Hawai'i at Manoa. 56 pp. (Technical Report 111).

MEYER, J.Y., SMITH, C.W. (Eds). 1998. Proceedings of the first regional conference on miconia control. August 26-29, 1997, Papeete, Tahiti, French Polynesia. Gouvernement de Polynésie française/University of Hawai’i at Manoa/Centre ORSTOM de Tahiti, 90p.

NORAMBUENA, H., PIPER, G.L. Impact of Apion ulicis Forster on Ulex europaeus L. seed dispersal. Biological Control 17: 267–271, 2000.

PIPER, G.L., ANDRES, L.A. 1995. Rush skeletonweed. In: Nechols, J.R., Andres, L.A., Beardsley, J.W., Goeden, R.D., Jackson, C.G. (Eds.). Biological control in the western United States: Accomplishments and benefits of regional research project W-84, 1964-1989. University of California, Division of Agriculture and Natural Resources, pp. 252-255.

SEIXAS, C.D.S. 2002. Controle biológico de Miconia calvescens DC. (Melastomataceae) com fitopatógenos. Viçosa: UFV. 123p. (Tese de Doutorado em Fitopatologia).

SEIXAS, C.D.S., BARRETO, R.W., MATSUOKA, K. 2002. First report of a phytoplasm-associated witches' broom disease of Miconia calvescens. Plant Pathology 5: 801-801.

SMITH, C.W. 2002. Forest pest biological control program in Hawai’i. Pp. 91-102 in: SMITH, C.W., DENSLOW, J., HIGHT, S. (Eds.). Proceedings of a workshop on biological control of invasive plants in native Hawaiian ecosystems. Pacific Cooperative Studies Unit, University of Hawai'I at Manoa. 122 pp. (Technical Report 129).

TOMASI, F., BRANZ, A., GRANDO, M.S., FORNO, F., FORTI, D., VINDIMIAN, M.E. 2000. Individuazione di fitoplasmi del gruppo AP nelle psille presenti nei frutteti. Informatore Agrario. 56: 51-54.

WATSON, A.K. 1991. The classical approach with plant pathogens. In: TEBEEST, D.O. (Ed.). Microbiol control weeds. New York: Chapman & Hall. p.3-23.



Table 1. Individuals collected of sap feeding insects on Miconia calvescens at Viçosa and Dionísio in Minas Gerais State, Brazil. 2001/02.


Taxon

Observed stage*

Total of collected individuals

Total




Leaves




Stem




Buds




Flowers




Fruits

Viçosa

Dionísio




Viçosa

Dionísio




Viçosa

Dionísio




Viçosa

Dionísio




Viçosa

Dionísio




Viçosa

Dionísio

Acari sp.1

A

16

84




16

84




0

0




0

0




0

0




0

0

Acari sp.2

A

55

55




54

53




1

1




0

1




0

0




0

0

Acari sp.3

A

15

11




13

10




1

0




1

0




0

1




0

0

Thysanoptera: Thripidae: Panchaetothripinae

N, A




















































Heliothrips sp.n

N

948

943




948

943




0

0




0

0




0

0




0

0

Heliothrips sp.n

A

880

631




880

631




0

0




0

0




0

0




0

0


























































Hemiptera: Aleyrodidae 1























































Nymphs




543

1469




543

1469




0

0




0

0




0

0




0

0

Adults




233

178




233

178




0

0




0

0




0

0




0

0

Hemiptera: Aleyrodidae 2

N, A




















































Nymphs




212

307




212

307




0

0




0

0




0

0




0

0

Adults




43

22




43

22




0

0




0

0




0

0




0

0

Hemiptera: Diaspididae 1

N, A

67

108




67

108




0

0




0

0




0

0




0

0

Hemiptera: Diaspididae 2

N, A

127

681




111

673




0

1




7

5




9

2




0

0

Diclidophlebia sp. (Hemiptera: Psyllidae)

O, N, A




















































Nymphs




769

59




0

0




0

0




769

59




0

0




0

0

Adults




93

945




0

0




0

0




93

945




0

0




0

0

Hemiptera: Aphididae

N, A

0

30




0

30




0

0




0

0




0

0




0

0

Hemiptera: Flatidae

N, A

32

10




11

5




0

0




16

4




0

0




5

1

Nymphs




32

10




11

5




0

0




16

4




0

0




5

1

Empoasca sp. (Hemiptera: Cicadellidae)

N, A




















































Nymphs




9

161




9

145




0

0




0

8




0

1




0

7

Adults




28

244




26

221




0

8




0

9




2

5




0

1

Scaphytopius sp. (Hemiptera: Cicadellidae)

N, A




















































Nymphs




10

13




7

12




0

0




3

1




0

0




0

0

Adults




59

6




50

3




4

0




5

3




0

0




0

0

Hemiptera: Cicadellidae 1

A

10

13




7

12




0

0




3

1




0

0




0

0

Hemiptera: Cicadellidae 2

A

12

2




11

1




0

0




0

1




0

0




1

0

Hemiptera: Cicadellidae 3

A

2

9




2

8




0

0




0

0




0

1




0

0

Hemiptera: Miridae

A

16

34




12

29




3

3




0

1




0

1




1

0

Hemiptera: Pentatomidae 1

A

13

2




13

2




0

0




0

0




0

0




0

0

Hemiptera: Pentatomidae 2

A

13

0




12

0




0

0




0

0




1

0




0

0

Hemiptera: Pentatomidae 3

A

0

14




0

14




0

0




0

0




0

0




0

0
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