Establishment of Ageniaspis citricola (Hymenoptera: Encyrtidae) for Biological Control of Phyllocnistis citrella (Lepidoptera: Gracillariidae) In Florida

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ESTABLISHMENT OF AGENIASPIS CITRICOLA (HYMENOPTERA: ENCYRTIDAE) FOR BIOLOGICAL CONTROL OF PHYLLOCNISTIS CITRELLA (LEPIDOPTERA: GRACILLARIIDAE) IN FLORIDA

Mark A. Pomerinke and Philip A. Stansly
Southwest Florida Research and Education Center
Institute of Food and Agricultural Science
University of Florida
P.O. Drawer 5127
Immokalee, FL 34143-5002

Abstract

The parasitoid Ageniaspis citricola (Hymenoptera: Encyrtidae), originally from Thailand and obtained from Australia, was released at 52 sites in Southwest Florida between May 1994 and September 1995 as part of a statewide program of biological control of citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae). Establishment and over-wintering was confirmed during spring of 1995 and 1996 in spite of frosts experienced during the previous winters. Parasitism from A. citricola at monitored groves increased from 2% in May 1994 to 86% in October 1995, apparently unhindered by native parasitoids. In contrast, apparent parasitism of citrus leafminer from endemic parasitoids fell from 30% to 2% during the same period. Wind-aided dispersal of A. citricola occurred in all directions and was documented to a maximum of 48 km from the nearest release point. A. citricola is now ubiquitous throughout the region and will probably remain a permanent component of the entomophagous complex using citrus leafminer.

Key Words: citrus leafminer, Ageniaspis citricola, biological control, Phyllocnistis citrella

Resumen

El parasitoide Ageniaspis citricola (Hymenoptera: Encyrtidae), que originalmente es de Tailandia pero qué fue obtenido para este proyecto en Australia, fue liberado en 52 sitios de la zona citrícola del sudoeste de Florida entre Mayo de 1994 y Septiembre de 1995 como parte de un programa estatal del control biológico del minador de los cítricos, Phyllocnistis citrella (Lepidoptera: Gracillariidae). Durante las primaveras de 1995 y 1996 se confirmó su establecimiento a pesar de algunas heladas durante los inviernos anteriores. Parasitismo por A. citricola en plantaciones monitoreadas aumentó del 2% en Mayo de 1994 al 86% en Octubre de 1995, aparentemente sin impedimento por parasitoides nativos. En cambio, parasitismo del minador por parasitoides nativos bajó del 30% al 2% durante el mismo período. Se documentó la dispersión de A. citricola, aparentemente por medio del viento, en todas direcciones, con el máximo de 48 km de distancia del sitio de liberación más cercano. Ya se encuentra A. citricola en toda la región y se espera que sea un componente permanente del complejo entomófago que utiliza a P. citrella.

Citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), was detected in May, 1993 infesting Persian limes in Dade County, Florida (Heppner 1993). The moth spread quickly across Florida, and within several months was found in all citrus growing regions of the State (Knapp et al. 1993). It has since been detected throughout the Caribbean, Central America (Heppner 1995), South America, and most Mediterranean countries (Knapp et al. 1993, Hoy and Nguyen 1997). Citrus leafminer had previously been reported as a major pest of new flush in southeast Asia, Australia, Japan, Taiwan, and South Africa (Heppner 1995). Larvae feed by mining the epidermal layer of leaves (Sonhi and Verma 1965), stems, and occasionally fruit.

Evidence from the United States, India, Japan, and Israel indicate that citrus leafminer can be managed by biological control from native and introduced parasitoids (Peña et al. 1996, Batra and Sandhu 1981, Ishii 1953, Argov and Rossler 1996). Surveys in 1993 and 1994 revealed that the leafminer was attacked by a complex of native parasitoids in the families Eulophidae, Encyrtidae, Elasmidae, Eurytomidae and Pteromalidae (LaSalle and Schauff 1996). Peña et al. (1996) found that generalist native parasitoids provided low to moderate levels of P. citrella parasitism in lime orchards in southeast Florida. They suggest that this reduction in effectiveness of native parasitoids may be the result of pesticide applications for the control of citrus pests. Given the apparent low levels of control by native parasitoids and difficulty in achieving good chemical control due to the biology of citrus leafminer (Knapp et al. 1995) the importation and release of additional biological control agents was deemed necessary.

Citrus leafminer had been detected in Australia in 1912 (Beattie 1993), and the gregarious parasitoid Ageniaspis citricola Logvinovskaya from Southeast Asia was introduced there in 1989 (Neale et al. 1995). Ageniaspis was imported from Australia to Florida with permission from that government in spring 1994. Federal and Florida state permits to release A. citricola from quarantine were granted for adults field-collected as pupae in May of that year (Hoy & Nguyen 1994). A. citricola is an internal koinobiont parasitoid of Citrus leafminer. Eggs are laid into eggs or first instar leafminer and parasitoids pupate inside the host prepupa, located within its pupal cell (Pomerinke, personal observation). The only reported host of A. citricola is Citrus leafminer (Hoy 1994), although development in the Mahogany leafminer, Phyllocnistis erechtiisella Chambers, has been observed (Stansly, unpublished data).

The following study was conducted to document establishment and dispersal of A. citricola, and its effects on incidence of native parasitoids. We report results of 13 releases at 10 groves (a total of 2,625 A. citricola adults) in 1994, and 39 releases at 25 groves (a total of 9,757 A. citricola adults) in 1995 made in five counties in Southwest Florida: Henry, Lee, Collier, Charlotte, and Glades.

Materials and Methods

Parasitoids were received from Gainesville, Florida, rearing facilities in plastic 50 ml vials containing an average of 100 adults. Wasps were provided with strips of filter paper moistened with pure honey and packed in Styrofoam boxes (21 × 21 × 31 cm) cooled with EverCold® gel refrigerant or Freez Pak Icicle®. Shipments were made by overnight courier and arrived midmorning the following day.

Release sites for A. citricola where chosen partly on the basis of a questionnaire which queried growers in the five county area on location, block size, variety, leafminer status, management practices and their willingness to suspend all pesticide applications for one year post-release. In 1994, 1995 and 1996, 13, 39 and 2 releases were made in 10, 25 and 2 groves respectively. Releases were generally made an hour or so before dusk, in trees with ample emerging foliage on which eggs and young Citrus leafminer were present. Vials were opened and wasps allowed to crawl out onto young leaves introduced into the opened neck of the vial to facilitate transfer in the field.

Sampling for evidence of leafminer pupae parasitized by A. citricola was conducted at least once, two weeks after each release in 1994 to confirm a first generation. No attempt was made to confirm establishment at 1995 and 1996 releases sites because close proximity to previous release sites would have made it difficult to distinguish between establishment and immigration.

Establishment and Apparent Parasitism

Four 1994 release sites near Immokalee were monitored bi-weekly in 1994 and monthly in 1995 and 1996: Youngquest grove in Lee County, Foundation and Corkscrew groves in Collier County and A. Duda & Sons grove in Hendry County. An additional location, Rosbough grove, directly west of Corkscrew grove was added in late 1994 after A. citricola was found to have dispersed there. All groves were sampled for confirmation of establishment and overwintering.

Sampling of A. citricola was conducted from time of release/discovery at monitored release blocks through late October when citrus normally becomes dormant (Jackson 1991), and reinitiated in May 1995 and 1996. Samples were obtained by examining 100 intact pupal chambers of citrus leafminer chosen at random or the number encountered in 30 minutes. Pupal chambers were sampled since A. citricola and native parasitoids pupate outside the host co-incident with or previous to host pupation. The “sausage link” pupae of A. citricola within the host pre-pupal skin of the last host larval instar were easily distinguished from pupae of leafminers or native parasitoids, all of which were noted (Fig. 1). The resulting estimate of parasitoid incidence provided a convenient measure for comparing parasitoid activity among groves (Southwood 1978).

Dispersal

Dispersal was documented by surveying 23 citrus groves for the presence of A. citricola outward along 2 transects originating from each of 6 release sites between July and October, 1995. Intact citrus leafminer pupal chambers were examined at all encountered groves for 30 minutes or until A. citricola was discovered, whichever came first. Transects were followed until the end of contiguous grove was reached or another release site was encountered and ranged from 1.6-30 miles (2.6-48.3 Km).

Grove structure

Release sites were categorized as either single or multiple aged groves. Multiple aged groves contained blocks of trees consisting of the original planting, usually 15 years or older, along with resets of various ages comprising approximately 50% of the trees. A grove with 60% or more of the trees being uniform in size and age was considered single aged. By these criteria, 6 of the 11 release sites in 1994 were multiple-aged and 5 were single-aged blocks. In 1995, 4 of 17 release sites were multiple-aged and 13 single-aged.

Weather

Weather stations were monitored at two sites; Corkscrew grove and at the University of Florida’s Southwest Florida Research and Education Center adjacent to the Foundation grove near Immokalee, Florida. Temperature and humidity (HMP35C probe), wind direction (024A probe) and speed (014B probe) were continuously recorded using a CR10 weather station (Campbell Scientific, Inc. Logan Utah 84321) at both sites in 1995 and 1996.

Results

Weather

Climatic conditions for 1995 and 1996 at the research center and 1996 at Corkscrew grove are presented in Table 1. Temperatures at the research center ranged from highs of 36.1°C and 35.5°C in August 1995 and July 1996, to lows of -1.6°C and -2.7°C in February 1995 and 1996 respectfully. Highs at Corkscrew grove reached 36.2°C in September, and dropped to -2.5°C in February. On February 4th, 17th, and 18th, 1996, three freezes were recorded with temperatures at -2.4, -1.9, and -0.9°C respectively at Corkscrew grove, and -2.7, -2.2, and 0°C respectively at the research center. An additional freeze was recorded at the research center on January 9th dropping temperatures to -1.1°C. No freeze lasted more then 9 hours.

Average relative humidity at the research center ranged from 87% in April to 73.1% in November in 1995 and 85% to 79.9% in April and March respectively in 1996 (Table 1). Average humidity at Corkscrew grove ranged from 79.5% in March to 89.7% in August, 1996.

Establishment

Wasps were often observed to immediately initiate searching movements accompanied by antennation, and to pause over leafminer eggs or small larvae, apparently to oviposit. Recoveries were made at five release sites in two counties during the May, 1995 survey (Table 2). Recoveries ranged from 10 of 25 pupal chambers yielding 29 A. citricola pupae to 2 of 25 yielding 6 A. citricola pupae. A mean 2.3 (SE = .13, N = 35) A. citricola pupae per pupal chamber were found in 1995.

During the May 1996 survey, A. citricola was recovered at 14 of 28 release sites in three counties (Table 2). Four recoveries were made at groves where A. citricola had been released in 1994 and recovered in 1995; the remaining 10 recoveries were made at 1995 release sites. Recoveries ranged from 41 of 100 pupal chambers yielding 94 A. citricola pupae to 1 of 100 yielding 2 A. citricola pupae. Again, a mean 2.3 (SE = .06, N = 145) A. citricola pupae were recovered from parasitized citrus leafminer pupae/pupal chambers.

Apparent Parasitism

A detectable reproducing population of A. citricola was observed at Corkscrew grove 2 weeks after initial release in 1994. Incidence of A. citricola increased to 50% within 3 weeks and remained above 10% through 12 October, 1994, climbing to 83% by June 1995 (Fig. 2A). In contrast, parasitization by native parasitoids, in the genera Pnigalio and Horismenus, peaked at 30% 4 weeks following the release of Ageniaspis, and declined to 8% by June 1995.

Incidence of A. citricola at the Youngquest grove was documented on 30 May, 1995, at 10%, ultimately peaking at 90% by October 1995. In 1996, parasitism was documented at 20% on 20 May, peaked at 51% in June, falling to 41% by September. Incidence of Pnigalio and Horismenus fluctuated between 1% and 19% during the same time period, peaking in August, 1995 at 21% (Fig. 2B).

Table 2. Release sites, grove structure, number of Ageniaspis citricola released, and parasitism levels from samples of 25 and 100 Phyllocnistis citrella intact pupal chambers during May 1995 and 1996 surveys of 1994 and 1995 release blocks, respectively.

Grove Structure1
Date
Total2
Ageniaspis 1995/19964
CLM
1995/1996
Native Parasitoids3 1995/1996
MA
3 May 94
75
6/0
17/98
2/2
MA
16 May 94, 12 Apr 95
225
0/0
25/100
0/0
MA
10 Aug 945
0
10/10
12/89
2/1
MA
26 Aug 94
200
9/2
11/95
5/3
MA
1, 25 May,
22 Jul 94
515
8/10
16/89
1/1
MA
20, 28 Sep 95
401
0
99
1
MA
19 Jul 95
300
2
82
16
MA
25 Oct 94
109
2/10
21/82
2/8
MA
28 Oct,
17 Nov 94; 22 May 95; 26 Jun 96
1289
0/0
25/100
0
MA
13 Sep 95
500
35
59
6
MA
7 Jul 95
600
4
80
16
SA
28 Feb 95
285
19
67
14
SA
23 Dec 94;
16 Mar,
20 Jul 95
750
0/0
20/95
5/5
SA
1, 17, 22 Mar,
31 May 95
1125
0
99
1
SA
26 Oct 94,
20 Jul 95
287
0/0
25/97
0/3
SA
25 Oct 94
119
0/0
18/100
7/0
SA
25 Apr,
9 Jun,
4 Aug 95
640
41
58
1
SA
17 May 95
100
3
95
2
SA
16 Jun 95
500
0
40
0
SA
21 Jun 95
235
0
40
0
SA
25 Oct 94
136
0/2
25/97
0/1
SA
16 May 95
300
9
87
4
SA
20 Jul,
4 Aug 95
600
1
89
10
SA
15 Aug 95
100
2
98
0
SA
20 Jan,
5, 22, 31 May 95
921
0
94
6
SA
1 Mar 95
150
1
98
1
SA
27 Jun 95
300
0
98
2
SA
28 Jun 95
300
0
99
1

1. MA = Multiple aged grove; SA = Single aged grove.
2. Total number of Ageniaspis released at each individual grove from 1994 to 1996.
3. Two most prevalent species Pnigalio and Horismenus.
4. Single numbers indicate that sampling was only conducted in 1996.
5. Date Ageniaspis was discovered at Rosbough grove in Lee county.

A. citricola was recovered on 12 October 1994, with an incidence of 1% in the Foundation grove, and again on 31 May 1995 at 2%, increasing to 51% by mid October. In 1996, A. citricola was recovered on 23 July with an incidence of 9%, and increasing to 50% by mid September. Parasitism by Pnigalio and Horismenus fluctuated between 3% and 8% during the same time period, with a maximum of 16% observed on August 9, 1995 (Fig. 2C).

A. citricola was first recovered at Duda grove on 28 November, 1994 with an incidence of 1%, increasing to 15% on 19 June, 1995 and peaking at 86% on 19 October, 1995. Parasitism from Pnigalio and Horismenus fluctuated between 1% and 40% during the same time period with maximum parasitism observed on 28 November 1994 at 40% (Fig. 2D).

A. citricola was discovered on 17 August 1994 at Rosbough grove, 3 months following their initial release at the adjacent Corkscrew grove. This was the first documented case of A. citricola dispersal from grove to grove in Southwest Florida. Incidence of A. citricola was 7% on August 17, peaking at 26% on October 6, 1994. Incidence of A. citricola increased over the 1995 season to a peak of 76% by October. High levels of parasitism were again recorded in 1996, reaching 85%. Parasitism from Pnigalio and Horismenus never exceed 7% and was almost undetectable in 1996 (Fig. 2E).

Grove structure

A. citricola was detected during the 1995 survey in 5 of the 7 multiple-aged release blocks but in none of the 4 single-aged release blocks (Table 2). The parasitoid was recovered at 7 of the 11 multiple-aged blocks and 8 of the 17 single-aged release blocks during the May 1996 survey (Table 2).

Nine groves where parasite establishment was not initially documented received more than one release between 1994 and 1996, 4 were multiple-age, the remaining 6 single-age. Establishment of A. citricola occurred in both types of grove structure with the probability of successful establishment being higher in multiple-aged groves (70%) then in single-aged groves (47%).

Dispersal

Dispersal of A. citricola was documented from July to October 1995. Maximum dispersal was documented on 25 October from Green Horizon grove in Collier County to Stoney’s Citrus Groves, 16.1 miles (25.9 km) to the southwest (Fig. 3). In July, 1996 it was found through casual observation on Marco Island, 30 miles (48.2 km) south measured from Green Horizon Grove. A. citricola was recovered at all sample sites during the survey.

Discussion

A. citricola appeared to establish more quickly in multiple aged blocks compared to single-aged blocks. Parasitoid survival may have been favored in multiple-aged blocks by the shelter and a clement microclimate provided by large trees, and a continual source of host material provided by rapidly growing small trees. In comparison, blocks of uniform age and size are characterized by synchronous flush, and a less stable microclimate that appeared to slow establishment of A. citricola. Number of releases required before establishment was documented also appeared to be an indicator of the importance of grove structure. Nevertheless, A. citricola eventually was established uniformly throughout the region, demonstrating that overall, conditions are favorable for this species.

These conditions include long growing season with hot, humid summers and mild winters despite two freezes in 1995 and four in 1996. Edwards and Hoy (in press) found that survivorship of A. citricola was best at humidities between 80% and 95%, within the average range for Southwest Florida during most of 1995 and 1996 (Table 1). Probability of establishment may have been enhanced by releasing early in the rainy season, May through August, maximizing the interval of warm, humid weather and ideal growing conditions.

Parasitism of citrus leafminer by A. citricola steadily increased at most sites following initial release, whereas the proportion of host pupal chambers with native parasitoids tended to decline (Fig. 2). A. citricola develops internally, pupates in the leafminer pupal chamber and probably does not have alternate hosts of ecological significance in the area, although there are at least 3 other species of Phyllocnistis present (unpublished data). In contrast, native parasitoids of citrus leafminer such as Pnigalio spp. etc. are generalists capable of parasitizing many different types of leafminers (Browning et al. 1996, Peña et al. 1996). Also, delayed internal development leaves hosts containing A. citricola open to parasitism from quickly developing external native parasitoids such as Pnigalio spp, unlikely to distinguish between parasitized and unparasitized citrus leafminer (Pomerinke, personal observation). Yet, in spite of these apparent disadvantages, A. citricola came to dominate the nitch provided by citrus leafminer.

Lack of alternate hosts means A. citricola populations must track host populations, themselves dependent on the cyclic patterns of flush, which is largely arrested during the winter (Jackson 1991) when generalist native parasitoids would have the greatest advantage. As a likely consequence A. citricola was largely absent during the May 1996 samples, whereas native parasitoids where relatively abundant. However A. citricola numbers later rebounded, apparently at the expense of native parasitoids. Possibly, the superior host-finding ability that comes with host specificity conferred a key advantage in the competition for hosts.

Superior searching ability was illustrated in the dispersal of A. citricola to new groves. In spite of impediments that a small size (approximately 1 mm in length according to Evans 1995 and Logvinoskaya 1983) should pose to directed flight, A. citricola was able to disperse over large distances, rapidly colonizing widely scattered citrus plantings over an extensive area (Fig. 3). Ageniaspis was found to have dispersed equivalent distances in the Indian river, Homestead, and Orlando citrus growing areas (Hoy et al. 1995). Dispersal distances in Southwest Florida are also consistent with documented dispersal in Louisiana (United States), Bahamas, Honduras, and Australia (Hoy and Nguyen 1997). In this ability A. citricola was not unlike its leafminer host which dispersed throughout Florida over a single growing season. Given successful reproduction, overwintering and dispersal throughout Southwest Florida, we feel confident that A. citricola has become a permanent addition to the fauna of the region, contributing a significant component of natural mortality to citrus leafminer populations.

Acknowledgments

The authors would like to thank Dr. Marjorie A. Hoy and Janel Smith (Entomology and Nematology, IFAS, University of Florida, Gainesville), and Dr. Ru Nguyen (FDACS, DPI, Gainesville, Florida) for making available parasitoids for release. We would also like to recognize the cooperation of participating citrus growers, especially A. Duda & Sons, Berry’s, Rousbough, and Youngquest citrus groves. Florida Agricultural Experiment Station Journal Series number R-06309.

Literature Cited

Argov, Y., and Y. Rossler. 1996. Introduction, release and recovery of several exotic natural enemies for biological control of the citrus leafminer, Phyllocnistis citrella, in Isreal. Phytoparasitica. 24(1): 33-38.

Batra, R. C., and G. S. Sandhu. 1981. Differential population of citrus leafminer and its parasites on some commercial citrus cultivars. J. Res. Punjab Agric. Univ. 18: 170-176.

Beattie, G. A. C. 1993. Integrated control of citrus leafminer. NSW Agriculture. Agfact H2.AE.4

Browning, H. W., J. E. Pena, and P. A. Stansly. 1996. Evaluating impact of indigenous parasitoids on populations of citrus leafminer. Proceedings from Managing the citrus leafminer. Orlando, Florida April 23-25, 1996.

Edwards, O. R., and M. A. Hoy. 1998. Biology of Ageniaspis citricola (Hymenoptera: Encyrtidae), a parasitoid of the citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae). Ann. Entomol. Soc. AM. In Press.

Evans, G. A. 1995. Discovery of the male of Ageniaspis citricola (Hymenoptera: Encyrtidae), parasitoid of the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae). Florida Entomol. 78(1): 134-136.

Heppner, J. B. 1993. Citrus leafminer, Phyllocnistis citrella, in Florida (Lepidoptera: Gracillariidae: Phyllocnistinae). Trop. Lepid. 4: 49-64.

Heppner, J. B. 1995. Citrus leafminer (Lepidoptera: Gracillariidae) on fruit in Florida. Florida Entomol. 78(1): 83-186.

Hoy, M. 1994. Field release of a nonindigenous wasp (Ageniaspis citricola Logvinovskaya) for biological control of citrus leafminer (Phyllocnistis citrella Stainton). United States Department of Agriculture-Biological Assessment and Taxonomic Support. Environmental Assessment.

Hoy, M., and R. Nguyen. 1994. Classical biological control of the citrus leafminer in Florida: a progress report. Citrus Industry. June 1994, p. 61-62.

Hoy, M., R. Nguyen, D. Hall, R. Bullock, M. Pomerinke, J. Peña, H. Browning, and P. Stansly. 1995. Establishment of citrus leafminer parasitoid, Ageniaspis citricola in Florida. Citrus Industry. December 1995, p. 12-17.

Hoy, M., and R. Nguyen. 1997. Classical biological control of the citrus leafminer Phyllocnistis citrella Stainton. Torp. Lepid. 8(suppl. 1): 1-19.

Ishii, T. 1953. A report of the studies of the parasite wasps of injurious insects. Bull. Fac. Agric. Tokyo Univ. Agric. Tech. 1: 1-10.

Jackson, L. K. 1991. Citrus growing in Florida, 3rd Edition. University of Florida Press, Gainesville. 293 pp.

Knapp, J. L., L. G. Albrigo, H. W. Browning, R. C. Bullock, J. B. Heppner, D. G. Hall, M. A. Hoy, R. Nguyen, J. E. Peña, and P. A. Stansly. Citrus leafminer, Phyllocnistis citrella Stainton: Current status in Florida—1995. Knapp, J. L. Editor. University of Florida. March, 1995.

Knapp, J., J. Peña, P. Stansly, J. Heppner, and Y. Yang. 1993. The citrus leafminer, Phyllocnistis citrella, a new pest of citrus in Florida. Florida Cooperative Extension Service. Document SP 156.

LaSalle, J., and M. E. Schauff. The genera of chalcid parasitoids (Hymenoptera: Chalcidoidea) of citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae): a workshop presentation. Proceedings from Managing the citrus leafminer. Orlando, Florida April 23-25, 1996.

Logvinoskaya, T. V. 1983. A new species of Ageniaspis Dahlbom, 1857 (Hymenoptera: Encyrtidae) from Vietnam. Entomological Review 62: 150-151.

Neale, C., D. Smith, G. A. C. Beattie, and M. Miles. 1995. Importation, host specificity testing, rearing and release of three parasitoids of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in eastern Australia. J. Aust. Ent. Soc. 34: 343-348.

Peña, J. E., R. Duncan, and H. Browning. 1996. Seasonal abundance of Phyllocnistis citrella (Lepidoptera: Gracillariidae) and its parasitoids in south Florida citrus. Environ. Entomol. 25(3): 698-702.

Southwood, T. R. E. 1984. Ecological Methods, 2nd Edition. Chapman and Hall, London. 524 pp.

Sohi, G. S., and G. C. Verma. 1966. Feeding habits of Phyllocnistis citrella Stainton in relation to the anatomical structure of the leaf. Indian J. Ent. (New Delhi), 27: 483-485.

 

Table 1. Maximum, minimum and average temperature (Co) along with average relative humidity (%) at Southwest Florida research and education center, Immokalee, Florida in 1995 and 1996, and Corkscrew grove, Collier county, in 1996.

Southwest Florida Research and Education Center—1995

Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
Maximum
27.7
30.0
31.1
32.2
35.0
35.0
35.0
36.1
34.4
33.3
31.6
28.8
Minimum
1.6
-1.6
0.0
10.5
17.2
16.6
21.1
21.1
21.6
15.5
5.0
-0.5
Average
16.6
17.2
20.3
23.0
26.6
26.6
27.5
28.0
27.7
25.8
19.7
16.9
Avg RH
80.0
86.2
85.8
87.0
84.4
82.9
82.5
83.2
84.7
87.0
78.7
NA
Southwest Florida Research and Education Center—1996
Maximum
28.8
30.0
30.5
33.8
32.7
34.4
35.5
34.4
35.0
32.2
31.1
29.4
Minimum
-1.1
-2.7
1.1
7.2
16.6
16.1
20.5
19.4
18.8
11.1
5.5
3.8
Average
16.6
16.4
18.0
21.6
25.5
26.3
28.3
27.7
27.2
24.1
20.7
18.3
Avg RH
80.8
75.7
73.7
74.1
85.0
83.0
80.0
84.2
83.0
84.1
77.6
80.0
Corkscrew—1996
Maximum
30.7
31.3
35.0
34.0
35.3
34.6
35.8
35.6
36.2
32.7
32.0
30.7
Minimum
10.6
-2.5
1.1
6.2
15.6
14.7
19.0
18.9
18.0
10.5
10.1
2.3
Average
18.8
16.9
17.8
21.3
24.8
25.6
27.3
26.1
26.2
23.4
19.8
17.5
Avg RH
84.5
79.5
77.8
79.7
84.0
88.0
86.4
89.4
86.7
89.0
83.9
84.6
NA, not available.

Fig. 1. Pupae Pnigalio minio (Walker) (top), Ageniaspis citricola Logvinovskaya (middle), and Phyllocnistis citrella Stainton (bottom).
Fig. 2. Percent apparent parasitism of citrus leafminer pupae by Ageniaspis citricola and endemic parasitoids at five monitored groves. Samples taken weekly from 25 May to 21 Oct 1994, monthly from 1 May to 24 Oct 1995 and 23 May 1996 to Sep 1996.
Fig. 3. Dispersal of Ageniaspis citricola documented from six release sites in 1996. Relative direction and distance depicted by arrows. Numbers in parenthesis indicate number of months recovery followed release. Arrows and map are not to scale.