Eupalopsellidae and Stigmaeidae (Acari: Prostigmata) within citrus ...

Exp Appl Acarol (2014) 64:187–205 DOI 10.1007/s10493-014-9815-x

Eupalopsellidae and Stigmaeidae (Acari: Prostigmata) within citrus orchards in Florida: species distribution, relative and seasonal abundance within trees, associated vines, and ground cover plants Carl C. Childers • Eduard A. Ueckermann

Received: 25 November 2013 / Accepted: 8 April 2014 / Published online: 27 April 2014 Ó Springer International Publishing Switzerland 2014

Abstract Seven citrus orchards on reduced- to no-pesticide spray programs were sampled for predacious mites in the families Eupalopsellidae and Stigmaeidae (Acari: Prostigmata) in central and south central Florida. Inner and outer canopy leaves, fruit, twigs, and trunk scrapings were sampled monthly between August 1994 and January 1996. Open flowers were sampled in March from five of the sites. Two species of eupalopsellid mites (Exothorhis caudata Summers and Saniosulus harteni (van-Dis and Ueckermann)) were identified from 252 specimens collected within citrus tree canopies within the seven citrus orchards of which 249 were E. caudata. Only two E. caudata were collected from ground cover plants within five of the seven orchards. Eight species of Stigmaeidae were identified from 5,637 specimens: Agistemus floridanus Gonzalez, A. terminalis Gonzalez, Eustigmaeus arcuata (Chandhri), E. sp. near arcuata, E. segnis (Koch), Mediostigmaeus citri (Rakha and McCoy), Stigmaeus seminudus Wood, and Zetzellia languida Gonzalez were collected from within citrus tree canopies from seven orchard sites. Agistemus floridanus was the only species in either family that was abundant with 5,483 collected from within citrus tree canopies compared with only 39 from vine or ground cover plants. A total of 431 samples from one or more of 82 vines and ground cover plants were sampled monthly between September 1994 and January 1996 in five of these orchards and one or

C. C. Childers (&) Emeritus Professor, Entomology and Nematology Department, IFAS, Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred, FL 33850, USA e-mail: [email protected] C. C. Childers 26 Wood Sorrel Lane, Hendersonville, NC 28792, USA E. A. Ueckermann Agricultural Research Center, Plant Protection Research Institute, Private Bag X134, Queenswood, Pretoria 0121, South Africa e-mail: [email protected] E. A. Ueckermann School of Environmental Sciences and Development, North-West University, Potchefstroom Campus, Potchefstroom 2520, South Africa

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more eupalopsellids or stigmaeids were collected from 19 of these plants. Richardia brasiliensis (Meg.) Gomez had nine A. floridanus from 5 of 25 samples collected from this plant. Solanum sp. had five A. floridanus from three samples taken. Both eupalopsellid and stigmaeid species numbers represented \1 % of the total numbers of phytoseiid species taken from the same plants. The two remaining orchards were on full herbicide programs and ground cover plants were absent. Agistemus floridanus was more abundant in the citrus orchards with on-going or recent herbicide programs compared with orchards having welldeveloped ground cover plants. Agistemus floridanus was most abundant on inner leaves between January and April and again during September through November. Additional collection records of E. caudata, S. harteni, A. terminalis, M. citri, Z. languida, and Zetzellia sp. near silvicola within Florida citrus orchards between 1989 and 2004 are included. Four species of Eupalopsellidae and ten species of Stigmaeidae occur within Florida citrus orchards. Keywords Eupalopsellus Exothorhis Saniosulus Agistemus Eustigmaeus Mediostigmaeus Stigmaeus Zetzellia Ground cover plants

Introduction Species of mites in the families Eupalopsellidae and Stigmaeidae are recognized as predators of different phytophagous insects and mites in various horticultural crops (Ehara and Wongsiri 1982; Oomen 1982; Ehara and Oomen-Kalsbeek 1983; Santos and Laing 1985; Thistlewood et al. 1996; Bellini et al. 2005). The two families are among nine included in the superfamily Raphignathoidea (Krantz and Walter 2009). The most recent state-wide survey of the two families within Florida citrus orchards was published by Muma (1975) with most of the work done prior to 1961 (Muma 1961). Major changes in arthropod pests and diseases, pesticides used and their frequencies of application, irrigation techniques, spray application technology, increased herbicide usage, newer citrus varieties, tree size, and tree densities per hectare have all evolved since the previous survey. A more accurate and current assessment of the important predacious and pest mites within Florida citrus was since needed to develop improved integrated pest management methods. This has become a more serious issue given the recent introductions of the bacterial disease, Huanglongbing (citrus greening) and its vector, the Asian citrus psyllid, Diaphorina citri Kuwayama (Insecta: Psyllidae). Infrequent qualitative surveys of over 50 commercial citrus orchards were conducted across Florida between 1980 and 2003 (Childers, unpublished data). Very low numbers of predacious mites were recovered from fruit and leaf samples in orchards prior to 1994, and most often, no beneficial mites were found. Records of selected species of Eupalopsellidae and Stigmaeidae from those surveys along with more recent field sampling are included in this paper. An extended and more intensive quantitative study was initiated in August 1994 to identify and compare the species complex of phytophagous, fungivorous, and predacious mites in seven selected commercial citrus orchards that were on minimal-, modified-, or no-pesticide spray programs. Multiple sites with minimal- to no-foliar pesticide programs were chosen to optimize the diversity of beneficial mite species that might be found,

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including mites in the families Eupalopsellidae and Stigmaeidae. Specific objectives of the research reported in this paper were to: (1) identify the Eupalopsellidae and Stigmaeidae within each of the seven selected sites; (2) compare and contrast eupalopsellid and stigmaeid species numbers, distributions, and seasonal differences; (3) assess the impact of ground cover and vine species within the citrus orchards; (4) include selected collection records of mites in these two families between 1989 and 2004; and (5) identify potential key rust mite or general arthropod predators within the mite species collected. The family Phytoseiidae was reported in Part I of a series of papers on the predacious and phytophagous mite complex within Florida citrus orchards (Childers and Denmark 2011). The ultimate objective of this research is to optimize biological control of the phytophagous mites on Florida citrus, especially the citrus rust mite, Phyllocoptruta oleivora (Ashmead), and the pink citrus rust mite, Aculops pelekassi (Keifer).

Materials and methods Seven citrus orchards in Polk, Lake, and DeSoto Counties in central and south-central Florida on reduced- to no-pesticide spray programs were sampled monthly over an 18 months interval between August 1994 and January 1996 for Eupalopsellidae and Stigmaeidae. The Trask, Pollard, and Yarborough orchards were located in the Highlands City vicinity in Polk County (Table 1). The two Hart orchards were northwest of Mascotte in Lake County and the Mixon orchards were located in southeastern Arcadia in DeSoto County. Only the Pollard and Hart II orchards remain as of January 2013 due to the citrus canker eradication program and/or urban sprawl. Eupalopsellid and stigmaeid species were collected separately from the following substrates: (1) 100 inner leaves, (2) 100 outer leaves, (3) 10–20 twigs, (4) 25 immature fruits or individual mature fruit samples, (5) trunk scrapings, and (6) 100 open citrus flowers. Each sample type was collected separately into a 5-l bucket containing about 250 ml of 80 % ethanol. Tree trunk scrapings were collected following the same procedures. A stiff brush was used to make 15–20 firm, short, downward strokes on the surface of the main trunk and scaffold limbs of each citrus tree sampled, and scrapings were directed into a bucket placed directly below to collect the arthropods. Loose bark or debris and lichens when present were also collected from the tree trunks. Citrus flowers were collected directly into 80 % ethanol from most of the sites during bloom. Different trees were sampled on different dates. Each of the sample types was collected individually from the same randomly selected trees within each orchard and replicated six to eight times. Many of the mite species would rapidly leave a disturbed leaf or fruit during one sampling. Therefore, rapid preservation of the fauna was intended to accurately measure what was present within each sample. Individual flowers, fruits, leaves, or twigs were collected and dropped immediately into a bucket containing about 250 ml of 80 % ethanol, vigorously agitated in the solution, and then discarded. The alcohol wash per sample was then transferred into a labeled glass jar and returned to the laboratory for processing. Mean numbers and standard error values were calculated for Agistemus floridanus and statistical differences were assessed using a paired t test between randomly selected inner and outer leaf samples (Statistics 2008) collected from the same trees. Selection of sample trees on each collection date differed. Each sample date represented different sets of randomly selected leaves from different trees. A total of 431 samples from one or more of 82 ground cover plants or vines were also sampled from five of the seven orchard sites. The two Mixon sites were treated with

123

123 Glyphosate ? Diuron (twice per year) 1995, 1996 Glyphosate ? Diuron (twice per year) 1995, 1996

N 28°360 2500 W 81°530 4600

N 28°350 2500 W 81°530 1800

N 27°110 1600 W 81°490 2500

N 27°100 5000 W 81°500 4100

Hart Ib Lake County ‘Ambersweet’ orange

Hart IIb Lake County navel orange

Mixon I DeSoto County ‘Marsh’ grapefruit

Mixon II DeSoto Co. ‘Valencia’ orange

b

Mowed 17–18 July 1995

Ground cover plants were tilled on 26 October 1995

Not applied since 1992

N 27°570 2000 W 81°540 1500

Pollarda Polk County ‘Duncan’/‘Marsh’ grapefruit

a

Glyphosate 1994, 1995

N 27°570 0700 W 81°530 2800

Yarborough Polk County ‘Hamlin’ orange

Glyphosate 1993, 1995



N 27°580 4400 W 81°530 3000

Traska Polk County ‘Hamlin’ orange

Herbicides

Coordinates

Orchard



Ethion ? petroleum oil (Spring and Summer 1992) Fenbutatin oxide 1992

Ethion ? petroleum oil (Summer 1994) Fenbutatin oxide (Spring 1993) Propargite (Fall 1993 and 1994)


Petroleum oil ? (Mn and Zn) - May 1994 Petroleum oil only - July 1994 Petroleum oil ? (Mn and Zn) - June 1995


Insecticides/acaricides



Aliette 1992 Copper 1992

Never applied


Copper 1994


Fungicides

Table 1 Pesticide spray programs for the Trask, Pollard, Yarborough, Hart I and II, and Mixon I and II citrus orchards sampled for mite species in Florida between 1994 and 1996

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herbicides and lacked ground cover plants for sampling. Selection of plants varied at each location and depended upon their prevalence. Each plant species that was sampled included leaves, stems, and flowers (when present). A sufficient volume of one or more ground cover plant or vine species was gathered to fill a 473 ml glass jar containing 50–100 ml of 80 % ethanol to near capacity. Each labeled jar containing one or more plants of one species was returned to the laboratory for processing. A representative sample of each plant was also collected and placed in a plant press in the field between sheets of newspaper for eventual identification. Plant identifications to species were completed by Kent Perkins at the Herbarium, University of Florida, Gainesville. Collection data were included with samples in both the jars and the plant press and included location, date, and code (e.g., weed A, B, C). Each mite species within each processed sample was recorded and then placed into a labeled vial containing 80 % ethanol. Eventually, each vial was processed, mite species removed, and individually slide-mounted in Hoyer’s mounting medium (Krantz and Walter 2009), then oven—cured for at least 3 weeks at 45–47 °C. Genera and species names in this paper follow those reported by Sepasgosarian (1985, 1990), Smith Meyer and Ueckermann (1989), and Fan and Walter (2005). Qualitative samples collected from other orchard sites in Florida consisted of 20 or 50 mature leaves from the new spring flush or samples of 20 fruit. All samples were immediately washed in 80 % ethanol as stated above.

Results and discussion Eupalopsellidae fauna Muma (1975) found two species of eupalopsellid mites on Florida citrus: Exothorhis caudata Summers and Saniosulus nudus Summers with the later species rarely found. Rakha and McCoy (1985) identified three species of eupalopsellid mites: E. caudata, S. nudus, and Eupalopsellus rostridius Summers on citrus in Lake Alfred. The authors failed to identify where on citrus S. nudus was collected while indicating that E. rostridius was collected in low numbers from citrus branches. Saniosulus nudus feeds on the eggs of Lepidosaphes pallida Maskell, L. beckii (Newman), L. ulmi (L.), Chrysomphalus aonidium (L.), and C. dictyospermi Morgan, and on the crawlers of Aonidiella aurantii (Maskell) (Zaher et al. 1982). Gerson and Blumberg (1969) reported that S. nudus fed on chaff scale, Parlatoria pergandii Comstock. In Israel, this mite peaked during late summer on citrus and was found primarily on the bark (Gerson 1971). Eupalopsellus rostridius Summers was collected on citrus in Lake Alfred, Florida by Rakha and McCoy (1985). This was the only record of this mite being found in Florida and its feeding habits are unknown. A total of 249 Exothorhis caudata were identified from within citrus tree canopies and two specimens from vines or ground cover plants within the seven orchard sites (Tables 2, 3, 4). One or two E. caudata were collected from an occasional 100 leaf, 25 immature fruit, or 10 twig sample in this study. Exothorhis caudata was found on all citrus tree sample types except flowers and was most abundant on twigs and fruit. The mite was collected from citrus leaves from January through April and again in September; from twigs during January, April, May, August, October, and November; and from fruit during January through April, October, and November. Exothorhis caudata was collected on trunk scrape samples from January through March. Muma (1975) usually found one E. caudata in a sample of citrus leaves or fruit. In Brazil, E. caudata was found in association with scale insect species: Parlatoria cinerea Doane and Hadden, Coccus viridis Green, Saisetia

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Table 2 Distribution and comparative numbers of Eupalopsellidae and Stigmaeidae species within the Trask, Pollard, Yarborough, Hart I and II, and Mixon I and II citrus orchards in Florida between September 1994 and January 1996 Mite family and species

Habitat Twigsa

Total from ground cover or vines

Total within tree

Flowersa

Trunk scrapea

52

0

31

249

2

1

1

0

0

3

0

0

0

0

0

0

0

5

3,352

1,205

208

714

0

4

5,483

39

Agistemus terminalis (Quayle)

4

4

0

0

0

0

8

0

Eustigmaeus arcuata (Chandhri)

0

0

0

3

0

19

22

0

Eustigmaeus sp. near arcuata

0

0

0

0

0

58

58

0

Eustigmaeus segnis (Koch)

2

0

0

0

0

8

10

2

Mediostigmaeus citri (Rakha and McCoy)

1

0

3

0

0

2

6

0

Stigmaeus seminudus Wood

1

0

0

5

0

0

6

0

Zetzellia languida Gonzalez

2

0

0

1

0

0

3

0

2

4

16

17

0

2

41

11

Inner leaves

Outer leaves

Exothorhis caudata Summers

30

23

113

Saniosulus harteni (van-Dis and Ueckermann)

1

0

0

Agistemus floridanus Gonzalez

Fruit

Eupalopsellidae

Eupalopsellids Stigmaeidae

Stigmaeids a

Limited samples were taken compared with leaves or fruit

Table 3 Comparative distribution of Exothorhis caudata in the seven citrus orchard sites Orchard

Inner leaves

Outer leaves

Twigsa

Fruit

Flowersa

Trunk scrapea

Total from within tree

Total from vines and ground cover

Trask

4

3

13

3

0

8

31

Pollard

4

1

33

15

0

2

55

0

10

5

24

6

0

0

45

0

Hart I

1

10

7

0

0

5

23

0

Hart II

0

1

4

10

0

16

31

2 (2)b

Mixon I

10

3

24

18

0

0

55

–

Mixon II

1

0

8

0

0

0

9

–

30

23

113

52

0

31

249

2

Yarborough

Totals: a


b

Total number of vine and ground cover plants with this mite species

123

0

[small eyebane]

Euphorbia hyssopifolia (L.) Small

[garden spurge]

Euphorbia hirta (L.) Millsp.

Euphorbiaceae

[Asiatic hawkweed]

Youngia japonica (L.) DC

1/9

1/8

3/10

1/5

Taraxacum officinalis Wiggers

[dandelion]

1/1

Sonchus sp.

4/17 Apr

Agistemus floridanus




Nov

Nov

Jan

Jan

Nov

Stigmaeidae Agistemus floridanus

Jan, Feb, Mar

Apr

Feb

Oct

May


Eupalopsellidae

[cudweed]

Gnaphalium pensylvanicum Willd.

Agistemus floridanus Eustigmaeus segnis

2/63

[beggar tick]

Bidens alba (L.) DC var. radiata

Compositae

[Jerusalem oak; Mexican tea]

Stigmaeidae

1/13

Chenopodium ambrosioides L.

Jan

Jan

Feb

Eustigmaeus segnis Exothorhis caudata

Feb

Jan, Feb, Jul

Months found


Eupalopsellidae

Mite species


1/6

3/34

Number of samplesa

[lamb’s quarter]

Chenopodium album (L.)

Caryophyllaceae

[spiny amaranth]

Amaranthus spinosus L.

Amaranthaceae

Family/Plant species/[common name]

1

2

1

1

1

1

Trask

1

1

1

1

1

1

Pollard

1

3

Yarborough

1

1

Hart I

3

1

1

3

1

1

Hart II

Table 4 Eupalopsellidae and Stigmaeidae collected from selected vine and ground cover plants within the Trask, Pollard, Yarborough, and Hart I and II citrus orchards between September 1994 and January 1996

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123

123

a

5/18

Apr Feb, May, Jul

Stigmaeidae

Jan


Exothorhis caudata

Jan, Feb, Nov

Feb, Mar, Jul

Jul

Jan

Jul

Feb, May

Apr, Jul, Oct, Nov

Nov

Sep

Nov

Months found

2

5

3

1

1

5

1

1

Trask

Number of times plant had one or more eupalopsellid or stigmaeid mites/total number of times plant was sampled

[common lantana]

Lantana camara L.

Verbenaceae


3/3

Solanum sp.

Eupalopsellidae


Stigmaeidae



Eupalopsellidae



Mite species


4/26

1/1

1/2

2/5

5/25

1/1

1/5

Number of samplesa

[night shade]

Solanum americanum L.

[ground cherry]

Physalis angulata L.

Solanaceae

Smilax auriculata Walt.

Smilacaceae

[goat weed]

Scoparia dulcis L.

Scrophulariaceae

[Brazilian pusley]

Richardia brasiliensis (Meg.) Gomez

Rubiaceae

[blood berry]

Rivina humilis L.

Phytolacaceae

[wood sorrel]

Oxalis intermedia A. Rich.

Oxalidaceae

Family/Plant species/[common name]

Table 4 continued Pollard

1

Yarborough

2

4

1

Hart I

2

1

1

1

Hart II

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Table 5 Comparative distribution of Agistemus floridanus in the seven citrus orchard sites Orchard

Twigsa

Flowersa

Trunk scrapea

86

0

0

878

21 (10)b

15

73

0

0

374

3 (3)

16

56

0

1

980

5 (3)

30

73

0

2

504

7 (3)

Inner leaves

Outer leaves

Trask

586

183

23

Pollard

155

131

Yarborough

576

331

Hart I

276

123

Fruit

Total from within tree

Hart II

93

29

5

16

0

1

144

Mixon I

709

258

78

330

–

0

1,375

Mixon II Totals:

Total from vines and ground cover

3 (3) –

957

150

41

80

–

0

1,228

–

3,352

1,205

208

714

0

4

5,483

39

a


b

Total number of vine and ground cover plants with this mite species

coffeae Walker, Selenaspidus articulatus (Morgan), Orthezia praelonga Douglas, and Pinnaspis aspidistrae (Signoret) (Matioli et al. 2002). Only one E. caudata each was recovered from Chenopodium ambrosiodes and Lantana camara during January 1996, both in Hart II (Table 3). Thirteen separate samples of C. ambrosiodes were taken from Pollard, Hart I, and Hart II between May and November; and, 18 separate samples of L. camara were taken from Pollard, Yarborough, Hart I, and Hart II between January and November. This mite appears to overwinter primarily within the citrus tree. Exothorhis caudata was frequently collected in low numbers (1–3 individuals) from citrus leaf samples in Florida between 1998 and 2004. One to three individuals were collected from 20 leaf samples of ‘Hamlin’ orange in Lake County, Florida between June and November 1998. One or two E. caudata were collected from 50 leaf samples of ‘Valencia’ orange in Highlands County, Florida between February and April 2000 or from ‘Hamlin’ orange in DeSoto County, Florida between March and June. Three larvae, twelve nymphs, and three female E. caudata were collected from bud and twig galls on Kumquat trees in Pasco County, Florida on 19 February 2004. This represented the highest number of this species collected from a single sample from Florida citrus. Single specimens of Saniosulus harteni were collected from fruit in Pollard during January, from inner leaves during January in Yarborough, and from inner twigs in June from Mixon I. This is a new record for this species in the United States and was originally described from Yemen (Van Dis and Ueckermann 1993). Nothing is known about its biology or feeding habits. Two nymphs and eight female S. harteni were collected from 20 clustered fruit on grapefruit trees in Hendry County, Florida during November 1998. Samples of 20 clustered grapefruit collected in October 1998 from the same orchard yielded one male; one nymph and four females; and one nymph and seven females from three other samples. Stigmaeidae fauna Muma (1975) found nine species of stigmaeid mites in five genera including: Agistemus floridanus Gonzalez, A. terminalis (Quayle), two undescribed species of Eryngiopus, Ledermuelleria plumifer (Halbert) and L. segnis (Koch), both of which are now in the genus

123

123

3.0 ± 0.6

0.3 ± 0.3

Nov 24-Dec 2

Dec 19–20

6.8 ± 1.4

6.8 ± 2.6*

2.2 ± 0.7

Oct 23–27

Nov 20–21

Jan 18, 1996

Jan 29–30

1.5 ± 0.6

Sep 18–20

1.5 ± 0.4

1.8 ± 0.7

5.2 ± 1.4

3.8 ± 1.8

3.2 ± 3.2

1.2 ± 0.7

1.2 ± 0.7

0.7 ± 0.5

0

0.2 ± 0.2

0

2.3 ± 1.4

1.2 ± 0.5

0.3 ± 0.2

1.2 ± 0.7

Aug 21–28

1.0 ± 0.4

Jul 21–28

0

2.0. ± 0.9

4.3 ± 3.9

1.8 ± 0.4

4.3 ± 1.4

0.2 ± 0.2

2.5 ± 1.1

2.8 ± 1.0

2.5 ± 1.0

Inner

0

2.8 ± 2.3

7.17 ± 1.9*

2.8 ± 1.5

4.8 ± 1.4

5.0 ± 2.3

0.5 ± 0.3

1.7 ± 0.3

1.8 ± 0.4

0

Outer

a

Pollard

May 22–26

May 15–17

Apr 26–27

Apr 17–19

Mar 30

7.3 ± 1.6

18.3 ± 3.7**

Feb 6–8

Mar 15

39.3 ± 7.5**

Jan 18–19

Jan 12, 1995

1.0 ± 0.4

0

Inner

a

Trask

Nov 1

Oct 18

Sep 13

Sep 6–7

Aug 31, 1994

(a)

Date

–

0.7 ± 0.5

0.5 ± 0.3

0.7 ± 0.3

0

1.0 ± 0.7

0

0.2 ± 0.2

0.3 ± 0.2

1.2 ± 0.8

1.8 ± 1.0

7.5 ± 2.9

1.3 ± 0.8

3.3 ± 1.0

1.5 ± 0.7

2.7 ± 1.2

Outer

0

0.4 ± 0.4

0.7 ± 0.3

0.2 ± 0.2

0

0

0.7 ± 0.3

5.2 ± 2.3

11.7 ± 1.4

27.0 ± 9.3*

40.8 ± 19.8

3.5 ± 1.3

3.2 ± 1.2

2.3 ± 0.8

1.0 ± 0.5

Inner

a

Yarborough

0.5 ± 0.3

0.5 ± 0.3

0

0.2 ± 0.2

0

0

0.3 ± 0.3

1.0 ± 0.4

8.2 ± 3.8

12.3 ± 3.8

20.5 ± 8.0

4.0 ± 1.4

2.0 ± 0.6

3.0 ± 0.7

0.8 ± 0.5

Outer

3.0 ± 1.3

0.6 ± 0.4

0.8 ± 0.5

4.2 ± 1.4

7.2 ± 2.2 7.2 ± 1.7*

3.2 ± 0.9

2.3 ± 1.2

0.3 ± 0.2

0.2 ± 0.2

0.5 ± 0.3

1.7 ± 0.7

0.5 ± 0.3

0.3 ± 0.2

0

0

0.7 ± 0.5

4.8 ± 1.1

Outer

8.2 ± 4.4

2.3 ± 0.9

1.5 ± 1.5

1.0 ± 1.0

1.3 ± 0.6

1.5 ± 0.4

4.0 ± 1.4*

2.0 ± 1.4

0.3 ± 0.2

0.3 ± 0.2

0.3 ± 0.2

4.5 ± 1.4

Innera

Hart I

Table 6 Comparative mean (± SEM) numbers of Agistemus floridanus on 100 inner and 100 outer leaf samples within the (a) Trask, Pollard, Yarborough, and Hart I orchard sites (b) Hart II, Mixon I, and Mixon II orchard sites

196 Exp Appl Acarol (2014) 64:187–205

0

0

Oct 23–27

Nov 20–21

4.0 ± 3.8

0

0

Sep 13

Sep 18–20 0.2 ± 0.2

16.0 ± 5.9

3.7 ± 1.8

0.7 ± 0.7

0

Aug 21–28

0

1.7 ± 0.9 2.3 ± 0.9

0

3.0 ± 1.0*

0

0

0

0.5 ± 0.2

20.7 ± 5.7* 15.2 ± 3.6*

May 22–26

0.2 ± 0.2

0.7 ± 0.7

2.5 ± 2.1 0.7 ± 0.3

0

Jul 21–28

May 15–17

Apr 26–27

Apr 17–19

Mar 30

Mar 15

3.7 ± 1.3*

Feb 6–8

Mar 7

2.7 ± 0.8

3.8 ± 1.0*

Jan 18–19

Jan 12, 1995

0

0.2 ± 0.2

Dec 19–20

Dec 29

0.5 ± 0.3 1.7 ± 0.8

0.8 ± 0.4

1.0 ± 0.6

Inner

0.3 ± 0.2

0

0

Outer

a

Mixon I

Oct 25

0

0.2 ± 0.2

Inner

a

Hart II

Nov 24-Dec 2

Oct 18

Sep 6–7

Aug 31, 1994

(b)

Date

Table 6 continued

4.0 ± 1.3

3.8 ± 3.0

11.7 ± 4.2*

0.5 ± 0.3

3.8 ± 1.1

1.8 ± 1.3 0

4.3 ± 2.8*

0.2 ± 0.2

11.8 ± 4.0*

61.3 ± 15.4**

19.8 ± 7.4*

0

0.8 ± 0.4

0.8 ± 0.4

0.8 ± 0.5

Innera

2.7 ± 1.1

0.2 ± 0.2

6.0 ± 2.2

7.0 ± 2.8

0

1.5 ± 0.7

0.8 ± 0.5

1.0 ± 0.7

Outer

Mixon II

0.3 ± 0.3

0.5 ± 0.3

1.5 ± 0.5

0.7 ± 0.3

0.8 ± 0.7

0.8 ± 0.7

5.0 ± 3.9

4.5 ± 2.2

0

0.8 ± 0.5

0.8 ± 0.4

0.7 ± 0.3

Outer

Exp Appl Acarol (2014) 64:187–205 197

123

123

a

1.0 ± 1.0

Inner

a

Hart II

0.2 ± 0.2

Outer

17.4 ± 4.6*

15.2 ± 5.2*

Inner

a

Mixon I

Differences between means of inner versus outer leaf samples were determined by using a paired t test

*P B 0.05, **P B 0.01

Jan 29–30

Jan 18, 1996

Nov 30

Date

Table 6 continued

1.7 ± 0.9

3.7 ± 1.8

Outer

4.8 ± 3.0

2.2 ± 0.8

Innera

Mixon II

0.2 ± 0.2

2.2 ± 1.8

Outer

198 Exp Appl Acarol (2014) 64:187–205

Exp Appl Acarol (2014) 64:187–205

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Eustigmaeus, an undescribed species of Stigmaeus, Zetzellia languida Gonzalez, and an undescribed species of Zetzellia. Eight species of stigmaeid mites were identified from 5,637 specimens collected within citrus tree canopies and 52 specimens from vines or ground cover plants within the seven orchard sites (Tables 2, 4, 5). Agistemus floridanus (5,483) was the only stigmaeid considered abundant. Only two species of phytoseiid mites (Euseius mesembrinus (Dean) with 20,948 specimens and Typhlodromalus peregrinus (Muma) with 8,628 specimens) were more abundant within the tree canopies than A. floridanus in this study (Childers and Denmark 2011). Only 39 A. floridanus were identified from vines or ground cover plants (Table 4). In contrast, eight different species of phytoseiids were more abundant on the same vines or ground cover plants sampled (Childers and Denmark 2011). Agistemus floridanus was found in all within-tree sample types except flowers in all seven citrus orchards (Table 5). The mite was most abundant on leaves with significantly higher numbers on inner leaf versus outer leaf samples between January and May (Paired t test, p = 0.0004; 1,35 df). Agistemus floridanus was most abundant during January through April with a second peak from September through November (Table 6). Muma (1975) reported that A. floridanus was most abundant in the winter and spring in Florida citrus. Agistemus floridanus fed and reproduced on a combination diet of Phyllocoptruta oleivora, Panonychus citri (McGregor), Tydeus sp., and Tropacarus mumai Cunliffe and fed on all stages of T. mumai and Paraleyrodes perseae (Quaint.) but did not produce eggs on these two latter species (Muma and Selhime 1971). Agistemus floridanus fed on the eggs of Eotetranychus sexmaculatus (Riley), on Eutetranychus banksi (McGregor), on eggs and nymphs of Dialeurodes citrifolii (Morgan), on eggs of an unidentified tarsonemid species, on Typhlodromalus peregrinus and Brevipalpus phoenicis (Geijskes), and was frequently found under scale exuviae (Muma and Selhime 1971). The first author has repeatedly observed this mite under various scale insect or whitefly exuviae on citrus leaves. This behavior of hiding beneath various materials likely results in underestimating the numbers of A. floridanus using the alcohol wash technique reported in this paper. Muma (1975) reported that A. floridanus fed on Fungitarsonemus peregrinosus Attiah, Tydeus gloveri (Ashmead), and on crawlers of Chrysomphalus aonidium. Agistemus floridanus fed on all stages of P. oleivora, immature stages of Tetranychus urticae Koch, eggs and larvae of Eotetranychus sexmaculatus, eggs of Tropacarus mumai, and on all stages of an unidentified Tydeidae in laboratory studies (Abou-Setta and Childers, unpublished data). Agistemus floridanus accepted a wider array of acarine prey on rubber trees in Brazil compared with Euseius concordis (Chant) or Neoseiulus anonymus (Chant and Baker) (Ferla and de Moraes 2003). Acceptable foods for A. floridanus included: Calacarus heveae Feres, Oligonychus gossypii (Zacher), Polyphagotarsonemus latus (Banks), Tenuipalpus heveae Baker, Tetranychus mexicanus (McGregor), and cattail pollen, Typha angustifolia L. Agistemus floridanus was not able to complete its life cycle when provided with ice plant pollen, Malephora crocea (Jacquin), as the only food source in a controlled laboratory study and would only feed on Panonychus citri eggs and not on the motile stages of this species (Goldarazena et al. 2004). Two important key questions remain unanswered. Can A. floridanus feed and reproduce on a single or combination diet of citrus pollen and/or citrus rust mites? Population increases of A. floridanus, as well as several phytoseiid species, within the citrus orchards during the spring interval may be due, in part, to citrus flowering and the resulting availability of other pollens such as Quercus and Pinus species during February–March (Villanueva and Childers 2004). Full bloom occurred in these citrus orchards during March 1995.

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Numbers of Agistemus floridanus differed among the seven orchard sites. Differences in past and current management practices are likely major contributing factors. The three orchards with the highest numbers of A. floridanus were Mixon I, Mixon II, and Yarborough. All three had herbicide treatments in 1995. Trask had the fourth highest number of A. floridanus. However, no records were available to indicate what pesticides, especially herbicides, were applied in 1993 or earlier. Hart I had herbicide applications but ethion ? petroleum oil, and the acaricides fenbutatin-oxide and propargite were applied prior to 1995. Pollard and Hart II had the lowest numbers of A. floridanus and the highest numbers of the phytoseiid E. mesembrinus among the seven sampled orchard sites (Childers and Denmark 2011). Neither Pollard nor Hart II had a pesticide application after 1993. Eight A. terminalis were collected but only from inner and outer leaves between January and March from Pollard, Mixon I, and Mixon II. One A. terminalus was collected from a 20 fruit sample of ‘Hamlin’ oranges and two from leaves in Hardee County, Florida in October 1989. Muma and Selhime (1971) reported that this species occurred on leaves and was uncommon to rare in occurrence on Florida citrus with only three collections in 18 years of sampling. Agistemus terminalis feeds on eriophyid mites, Panonychus citri, and Unaspis yanonensis (Kuwana) (Ehara 1964). Adult females of A. terminalis preferred eggs of P. citri and seldom fed on the larvae or nymphal stages (Inoue and Tanaka 1983). They also reported that A. terminalis hibernated as adult females on the undersides of citrus leaves in Japan with high mortality resulting. Nineteen Eustigmaeus arcuata (Chaudhri) were collected from trunk scrapings during January in Pollard, Hart II, and Mixon I. Three E. arcuata were collected from fruit during January in Mixon I. This species has not been previously reported in Florida citrus. The genus Eustigmaeus consists of a large group of mites within the family Stigmaeidae. Specific feeding habits of this species and others that follow within this genus are unknown. However, four species of Eustigmaeus were found to parasitize phlebotomine flies (Diptera: Psychodidae) (Zhang and Gerson 1995), while other species of Eustigmaeus feed on mosses (Gerson 1972; Flechtmann 1984). A comprehensive revision of the genus has been suggested by Faraji et al. (2007). A total of 58 Eustigmaeus sp. near arcuata was collected from trunk scrapings in Trask, Pollard, Yarborough, and Mixon II during January through March. No data are available as to the feeding preferences of this species. Two Eustigmaeus segnis (Koch) were collected from inner leaves in the Trask orchard during July and September. Single specimens were collected from trunk scrapings in Hart II during January and from Pollard and Yarborough during March. Five E. segnis were collected from trunk samples in Mixon I during January, February, and March. Two specimens were collected from Bidens alba in January. Nothing is known about the feeding habits of this mite. Rakha and McCoy (1984) described Eryngiopus citri as a new species on citrus. This species forms part of a new genus, Mediostigmaeus, created by Fan and Walter (2005). One specimen of M. citri (Rakha and McCoy) was collected on inner leaves and three from inner twigs in Hart II during May (Table 2). Two other specimens were collected from trunk scrapings during March in Yarborough. From one to three M. citri were collected from 20 leaf samples in a ‘Hamlin’ orange block in Lake County, Florida between June and November 1998. Rakha and McCoy (1984) found M. citri feeding on the eggs of Tydeus mumai Baker and depositing spherical orange eggs on new leaves and bark. One specimen of Stigmaeus seminudus Wood was collected on inner leaves in January, one from a mature fruit in May, and four from 25 immature fruit samples collected during

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Table 7 The known species of Eupalopsellidae and Stigmaeidae that occur on citrus in Florida, 1975–2013 Mite family Genera and species

Habitat Leaves

Reference/status Twigs

Fruit

Trunk scrape

Ground or vines

Eupalopsellidae Eupalopsellus rostridius Summers Exothorhis caudata Summers

X X

X

Saniosulus harteni (vanDis and Ueckermann)

Rakha and McCoy (1985) X

X

X

X

Muma (1975) (on fruit and leaves) New record

Saniosulus nudus Summers

Muma (1975) (within tree locations not given)

Stigmaeidae Agistemus floridanus Gonzalez

X

Agistemus terminalis (Quayle)

X

X

X

X

X

Eustigmaeus arcuata (Chandhri)

X

Eustigmaeus sp. near arcuata

X

Muma (1975) Muma and Selhime (1971)

X

New record

X

New record

Eustigmaeus plumifer (Halbert)

X

Muma (1975)

Eustigmaeus segnis (Koch)

X

Muma (1975)

Mediostigmaeus citri (Rakha and McCoy)

X

Rakha and McCoy (1985)

Stigmaeus seminudus Wood

X

Zetzellia languida Gonzalez

X

Zetzellia sp. near silvicola

X

X

X

New record

X

Muma (1975) New record

January, March, April, and November in Mixon II. Nothing is known about the feeding habits of this species. Two Zetzellia languida Gonzalez were collected from inner leaves during March and April and one specimen from a 25 fruit sample collected in January, all from Mixon II. This species was described from an unidentified tree in the Democratic Republic of Congo and was previously reported by Gonzalez (1965) on citrus in Florida. One Z. languida was collected from a 50 leaf ‘Hamlin’ orange sample in DeSoto County, Florida in January 1999. From one to five Z. languida were collected from unsprayed leaves and twigs of orange or grapefruit in Hardee County, Florida during July 1998. One Z. languida each was collected from two 20 ‘Hamlin’ orange leaf samples in June and one in July 1999 in Lake County, Florida. Feeding preferences of this species are not known. However, Z. mali Ewing feeds on Panonychus ulmi Koch, Aculus schlectendali Nalepa, species of tarsonemid mites (Villanueva and Harmsen 1998), as well as eggs of a pyralid moth, eggs of Amblyseius fallacis (Garman), and apple pollen (Santos and Laing 1985).

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One female Zetzellia sp. near silvicola was collected from a 50 leaf sample of ‘Hamlin’ orange in DeSoto County, Florida in February 2002. This is a new state record for this mite.

Summary Four species of eupalopsellids including Eupalopsellus rostridius, Exothorhis caudata, Saniosulus harteni, and S. nudus are found in Florida citrus orchards with E. caudata being the most abundant species. Saniosulus nudus was collected by Muma (1975) but he failed to indicate where the species was collected within citrus tree canopies. Ten species of stigmaeid mites including Agistemus floridanus, A. terminalis, Eustigmaeus arcuata, E. sp. near arcuata, E. plumifer, E. segnis, Mediostigmaeus citri, Stigmaeus seminudus, Zetzellia languida, and Z. sp. near silvicola are found in Florida citrus orchards in one or more sample types (Table 7). Agistemus floridanus was the most abundant stigmaeid species found and it is a known predator of the citrus rust mites Phyllocoptruta oleivora and Aculops pelekassi. Reduced ground cover plants using herbicides resulted in higher numbers of A. floridanus occurring within citrus tree canopies compared with other citrus orchards not on herbicide spray programs in this study. Manipulation of ground cover plant species in Florida citrus orchards may offer one means of improving A. floridanus densities early in the year. This may have more significance in reducing the potential threat of A. pelekassi which can develop very high population densities on small immature fruit beginning in April in some orchard blocks in Florida (Childers and Achor 1999). Complete elimination of all weeds (= ground cover plants) from the citrus orchard floor is not recommended. However, the goal of weed management in Florida citrus orchards is to minimize the competitive effect of the weeds for nutrients and water (Futch and Singh 2012). This study documents the diversity and abundance of the eupalopsellid and stigmaeid species found in Florida citrus orchards under relatively stable conditions of low pesticide usage. This study began before the onset of intense insecticide use to control the Asian citrus psyllid (ACP), the vector of Huanglongbing (= citrus greening). Prior to the introduction of this devastating disease, arthropod pests and their natural enemy complex in Florida citrus were relatively stable. In recent years, Florida citrus growers have averaged 6–8 insecticide applications annually to control ACP in an attempt to slow the spread of Huanglongbing (Rogers et al. 2013). Most of the currently recommended insecticides for ACP control include an array of carbamates, organophosphates, and pyrethroid products. Most of these pesticides are slightly to non-toxic to Agistemus industani Gonzalez or to A. fleschneri Summers (Nelson et al. 1973; Childers et al. 2001). However, many of the current acaricides and fungicides recommended for phytophagous pest mite control and several fungal pathogens on Florida citrus are moderately to highly toxic to A. industani. We were unable to use A. floridanus in the above pesticide experiments as the laboratory culture of this mite was too low. Agistemus floridanus has the potential to increase early in the season, between late March through May, prior to or during a critical time for rust mite increase and resulting in feeding injury to fruit. The value of the research reported in this paper provides strong support for manipulating orchard management practices to optimize populations of this predacious mite. The presence of ground cover plants in citrus orchards neither increases the numbers of A. floridanus early in the year nor do these plants provide major cover or alternate food sources throughout the year.

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Low numbers of beneficial mites were found during infrequent qualitative surveys conducted in commercial citrus orchards between 1994 and 2010. Past research efforts identified a potentially successful integrated pest management program for processed citrus fruit in Florida that combined the use of horticultural mineral oils (HMOs) and optimized beneficial mite populations (Childers 2002, 2011; Childers and Denmark 2011). Substantially reducing or eliminating Huanglongbing as a threat to the Florida citrus industry is the major on-going focus of the University of Florida’s research centers involved with citrus. Dozens of researchers have channeled their efforts towards combating Huanglongbing. We must assume that on-going research efforts will lead to a significant reduction or elimination of the destructive effects of Huanglongbing on Florida citrus. The citrus industry has no alternative. Once research has identified successful reduced-pesticide control approaches, then the research reported in this paper will be of considerable value as a step towards establishing a viable integrated mite control program for processed citrus fruit. Interest in the mite fauna on citrus in Florida has not declined from an applied point of view. Prior to the spread of Huanglongbing, the citrus rust mite P. oleivora and the pink citrus rust mite Aculops pelekassi were the two most important mite pests on Florida citrus. Some may argue that the data reported in this paper come from a world that no longer exists. Actually, the predators reported in this paper do exist in abandoned citrus blocks that remain alive as well as dooryard citrus throughout the state. On-going surveys of mostly dooryard citrus and a few abandoned commercial blocks between 2009 and 2013 support this fact (Childers et al., unpublished data). Acknowledgments The authors wish to thank Kent Perkins, Collection Manager, The Herbarium, University of Florida, Gainesville, for identification of plant specimens. Appreciation is extended to Deanna Threlkeld, Eugenia White, David Dills, Karen Colston, Robert Hoobin, Michael K. Simms, Perceivia Mariner, and Paul Threlkeld for collection, processing, and slide-mounting of specimens. Voucher specimens were deposited in the Florida Department of Agriculture and Consumer Services, Division of Plant Industry Museum, Gainesville, Florida. Appreciation is extended to J. G. Morse, University of CaliforniaRiverside and M. Shepard, Clemson University and the journal referees for their constructive criticism of this manuscript and to Barbara Thompson for typing and formatting. This research was supported in part by grants from USDA CSREES Pest Management Alternatives Program (PMAP), two Florida Citrus Production Research Advisory Council grants during 1993–1995, and a grant from Sustainable Agriculture Research and Education (SARE).

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