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Morphometric Comparisons of Citrus Rust Mite,

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 Morphometric Comparisons of Citrus Rust Mite,
Phyllocoptruta oleivora (Ashmead)1, Populations in
Texas and Kenya
Authors: Steven M. Reyna, Sunday Ekesi, and Mamoudou
Sétamou
Source: Southwestern Entomologist, 44(3) : 607-616
Published By: Society of Southwestern Entomologists
URL: https://doi.org/10.3958/059.044.0306

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 VOL. 44, NO. 3 SOUTHWESTERN ENTOMOLOGIST SEP. 2019

Morphometric Comparisons of Citrus Rust Mite, Phyllocoptruta oleivora

(Ashmead)1, Populations in Texas and Kenya

Steven M. Reyna2,3*, Sunday Ekesi4, and Mamoudou Sétamou2

Abstract. The citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Acari:

Eriophyidae), is a serious pest of citrus worldwide, but is especially important in areas
where citrus is produced for fresh markets. Kenya and Texas produce fruit for fresh
markets; however, Texas fruit is marketed commercially and globally, while fruit in
Kenya is sold locally. Development of an effective pest management program to
control P. oleivora requires proper identification to species. However, diminutive size
and lack of taxonomic characteristics make proper identification of P. oleivora difficult
without the aid of a powerful microscope, and therefore cryptic species can occur.
Cryptic species might occur in a citrus tree, grove, or variety, or geographical area,
and different species might respond differently to insecticides that can severely
impede management strategies. The purpose of this study was to use morphological
characteristics to assess populations of P. oleivora in Texas and Kenya.
Morphometrics is statistical analysis of characteristics or a combination of
characteristics that can detect morphological variation. 300 P. oleivora individuals
were collected; 90 individuals were collected from oranges (Citrus sinensis
(Linnaeus)) and 60 from tangerines (Citrus tangerina (Tanaka)) in Kenya. In Texas,
90 individuals were collected from oranges and 60 individuals were collected from
grapefruit (Citrus x paradisi (MacFadanyen)). Ten morphological traits and four
biometric ratios were compared between each population using a pooled t-test.
Principal component analysis was used to analyze the morphometric measurements
and stepwise discriminant analysis was used to distinguish further any morphological
trait that determined population grouping. Morphological compairsons revealed all to
morphological traits and three out of 4 bioratios were significantly different from each
population. Principal component 1 and principal component 2 represented 86% of
morphological variation, and Kenyan and Texan populations were distinguished by
relation to principal component 1. Stepwise discriminant analysis revealed three
morphological traits that strongly contributed to differentiation between P. oleivora
from Kenya and Texas: width of prodorsal shield (F = 97.18, P < 0.0001), tail end (F
= 30.67, P < 0.0001), and body length (F = 29.64, P < 0.0001). Morphological
differences could be due to differences in geography or complete or partial genetic
separation.

________________________
1Acari:Eriophyidae
2Texas A&M University-Kingsville Citrus Center, 312 N. International Blvd., Weslaco, TX 78599
3Current address: Department of Entomology and Plant Pathology, North Carolina State University,

Raleigh, NC 27695
4International Centre of Insect Physiology and Ecology, Nairobi, Kenya.

*Corresponding author: Mamoudou.Setamou@tamuk.edu

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 Introduction

The citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Acari: Eriophyidae),

is one of the most economically damaging pests of citrus worldwide, particularly to
industries which fruit are destined for fresh market (Jeppson 1989, Vacante 2010).
P. oleivora is a global vagrant species of mites that live on leaves and fruit of all citrus
varieties year around (Yothers and Mason 1930, Jeppson 1989). P. oleivora
reproduces via arrhenotokous parthenogenesis, and in subtropical conditions in
which citrus are grown, abundance of mites can increase exponentially if not
controlled (McCoy and Albrigo 1975, Vacante 2010). Feeding by P. oleivora can
cause economic loss either by reducing the fruit size or load or by reducing cosmetic
value of the fruit (Yang et al. 1994). Two types of damage by P. oleivora generally
are recorded on citrus fruit. When infestation by P. oleivora occurs early in
development of the fruit, reduced fruit size can result, the rind becomes silver
eventually leading to “shark-skin,” and in extreme cases, fruit can be aborted from
the tree (Yang et al. 1994). If infestation by P. oleivora occurs during the middle or
late in fruit development, intense feeding by P. oleivora can cause “russet” or
“bronzing” that probably is caused by formation of lignin and oxidation of
cytoplasmatic substances released during probing for feeding (Vacante 2010).
Texas ranks third in citrus production in the United States, with most fruit
produced destined for fresh fruit markets (USDA 2016). Grapefruit (Citrus x paradisi
(MacFadanyen)) is the dominant citrus produced in Texas, comprising ~65% of the
total 30,000 acres of citrus in Texas. Grapefruit is also a preferred host of P. oleivora
in comparison to sweet oranges (Citrus sinensis (Linnaeus)) or tangerines (Citrus
tangerina (Tanaka)) (Yothers and Mason 1930, Sekula 2009). In 2009, P. oleivora
was recognized as an economically concerning pest among citrus growers in Texas.
Considering the absence of effective natural enemies, strategies to control P. oleivora
in Texas citrus are based on chemicals, with biweekly monitoring of fields (Sekula
2009) and three to four applications of miticides per year (French 2001). Use of
miticide provides only temporary suppression of P. oleivora. Use of non-specific
broad-spectrum pesticide especially negatively affects natural enemies (parasitoids
and predators) in the system, thus incapacitating biological control strategies.
However, despite heavy use of insecticide, P. oleivora continues to inflict severe
damage to citrus and has been the key pest of Texas citrus for more than 50 years
(French 2001, Sekula 2009).
Farmers in Kenya produce mostly citrus fruit destined for fresh market and
face the same challenges as farmers in the United States. In Kenya and Texas, P.
oleivora has not been well studied, and management programs rely on application of
miticide that can have adverse effects on human health and the environment (Kilalo
2009). In Kenya, citrus ranks third in production, after bananas and mangoes. Citrus
fruits are important sources of income for resource-poor farmers, employment in rural
areas, and human nourishment.
Monitoring, implementation, and assessment of pest management strategies
are essential to integrated pest management, but the critical first step is accurate
identification of pest species (Gotzek et al. 2012). By correctly identifying the pest
species, pest management programs can accurately identify effective chemical and
biological control agents without wasting valuable resources (Rosen 1986). Accurate
identification of Eriophyoidea is difficult because of the diminutive size of eriophyoid
species, their structural simplicity, and limited number of characteristic traits

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 (Lindquist et al. 1996, Skoracka et al. 2012). Besides P. oleivora, three other
eriophyoid species are found on US citrus, pink citrus rust mite, Aculops pelekassi
(Keifer); citrus bud mite, Aceria sheldoni (Ewing); and Diptilomiopus floridanus
Craemer and Amrine (Yang 1994, Villanueva et al. 2006, Craemer et al. 2017).
However, because of their minute size and similar body shape, distinguishing
between Eriophoidea species is challenging without the aid of specialized mounting
techniques and a powerful microscope.
A method to distinguish or identify cryptic species is based on statistical
analysis of morphological characteristics or a combination of characteristics, known
as morphometrics (Gotzek et al. 2012, Mehle and Trdan 2012). Morphometrics can
test historical phylogenetic hypotheses to detect variation in quantitative characters
and evaluate patterns of relationships (Navia et al. 2009). Morphometrics also can
provide insight on the variation of morphology caused by host preference and/or
geographical distances that might contribute to taxonomic knowledge of P. oleivora
(Skoracka et al. 2002). The pest status of P. oleivora and other Eriophoidea species
of citrus might be attributed to lack of biological, ecological, and taxonomic knowledge
and may result in misuse of insecticides followed by destruction of natural enemies
and development of resistance.
The goal of this study was to use morphometrics to compare P. oleivora in
citrus orchards in Texas and Kenya. Precise identification of species can improve
research efforts controlling the mite or developing biological control programs.
Results of this study will potentially be used to reassess management practices for
P. oleivora in citrus orchards in Texas and Kenya.

Materials and Methods

The study area encompasses citrus grown in Cameron, Hidalgo, and Willacy
counties in the Lower Rio Grande Valley of Texas. In the area, citrus varieties are
grown commercially and for ornamental use as backyard trees. Mites were sampled
from grapefruit and sweet orange groves during two growing seasons (Table 1). The
species of citrus were selected because of their prevalence throughout the region,
economic importance to the citrus industry, and use as ornamentals for homeowners
and municipalities throughout Texas. A 15x hand lens was used to aid in collection
of P. oleivora from fruit and foliage of citrus trees. Infested fruit was put into a brown
paper bag kept at 4°C at the Texas A&M University, Kingsville Citrus Center
(Weslaco, TX). Infested leaves were put into a 1-gallon clear Ziploc bag, labeled,
and stored at 4°C.
P. oleivora specimens were collected from either oranges or tangerines in
commercial orchards near the city of Wote in Makueni County, approximately 105 km
southeast of Nairobi, Kenya (Table 1). Sweet oranges and tangerines are the primary
citrus species grown at Wote, and most fruit is sold in non-commercial open markets.
A 15x hand lens was used to assist in collecting mites from fruit and foliage. Infested
fruit was put into a brown paper bag and kept at 4°C at the International Centre of
Insect Physiology and Ecology (icipe), Nairobi, Kenya. Infested leaves were put into
a 1-gallon clear Ziploc bag, labeled, and stored at 4°C.
P. oleivora were individually removed from the infested substrate by using a
SZX12 stereomicroscope (Olympus America, Central Valley, PA) and sterile 0.15-
mm pin (BioQuip Products, Rancho Dominguez, CA) attached to a 200-μl pipette tip
(Thermo Fisher Scientific, Waltham, MA). Approximately 30 P. oleivora were
removed from infested fruit or leaves at each collection site in Texas and placed on

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 Table 1. Phyllocoptruta oleivora Collection Information from Grapefruit, Orange, and Tangerine at Different

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Sites in Texas and Kenya
Coordinates Elevation above
Country State City Citrus N Latitude Longitude sea level (m)
USA Texas Bayview Grapefruit 30 26° 8’ 21” N 97° 23’ 50.3” W 8
Edinburg Grapefruit 30 26° 11’ 59” N 98° 2’ 39.6” W 29
Orange 30
La Feria Orange 30 26° 13’ 49” N 97°46’ 39” W 17

610
Weslaco Orange 30 26° 8’ 44.9” N 97° 58’ 14.4” W 24
Kenya Wote Simba J Orange 59 1° 48' 57.3” S 37° 36 ' 28.8” E 1,216
Maluvani Orange 30 1°47' 30.3” S 37° 35' 43.6” E 1,189
Tangerine 55

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 slides containing modified Berlese’s clearing medium (Amrine 1996). To view
characteristics, mites were placed ventral dorsally onto slides. Using forceps, #1
thickness 15-mm round cover glass was put gently on top of the mites. The slides
were put for 72 hours at 70°C in an oven to initiate clearing. Once mites were cleared,
clear fingernail polish was used to secure the cover glass to the slide. Female mites
were identified to genera by using dichotomous keys from Keys to the World Genera
of the Eriophyoidea (Acari: Prostigmata) (Amrine et al. 2003) and to species by using
Review of Phyllocoptruta (Xue et al. 2010). Voucher specimens are kept at the Texas
A&M University Kingsville Citrus Center in Weslaco, Texas, USA.
Approximately 30 females were randomly selected from each area of study
and examined using a ML2970 compound microscope (Meiji Techno America, San
Jose, CA) and a 1-mm stage micrometer. For comprehensive coverage of the body
of P. oleivora 10 traits were measured individually for each mite: (A) body length, (B)
length of prodorsal shield, (C) width of prodorsal shield, (D) width of scapular setae
apart, (E) length of tibia I, (F) length of tarsus I, (G) width of genital shield, (H) length
of genital shield, (I) width of the tail-end, and (J) width of the mid-section (Skoracka
et al. 2002). Ratios between body length/tail end, body length/mid-section, mid-
section/tail end, and width of the genital shield/length of the genital shield were
calculated.
Data for each morphological trait were tested for normality using the Wilks-
Shapiro test. Each morphological trait was distributed normally and considered
independent. A pooled t-test was used to compare means of each morphological trait
and the biometric ratio between populations. Principal component analysis was used
to analyze all the morphometric measurements. Stepwise discriminate analysis was
used to distinguish further any morphological trait that determines population
grouping. Morphological traits were selected based on a significance of 0.05. The
variables selected were used in canonical correlated analysis. Mahalanobis distances
were calculated and used to compare morphometric divergence among populations.
SAS 9.4 was used for all statistical analyses.

Results and Discussion

For the study, 300 P. oleivora individuals were collected; 90 individuals were
collected from oranges and 60 from tangerines in Kenya (Table 1). In Texas, 90
individuals were collected from oranges and 60 individuals were collected from
grapefruit. Of the 10 morphological traits measured in the study, all were significantly
different between the Texan and Kenyan populations of P. oleivora (Table 2).
Likewise, comparing means of biometric ratios between Kenyan and Texan
populations of P. oleivora showed that all ratios except the body length/mid-section
ratio were significantly different. Principal component 1 and principal component 2
represented 86% of morphological variation, and Kenyan and Texan populations
were distinguished by relation to principal component 1 (Fig. 1).
Stepwise discriminant analysis revealed three morphological traits that
strongly contributed to differentiation between P. oleivora from Kenya and Texas:
width of prodorsal shield (F = 97.18, P < 0.0001), tail end (F = 30.67, P < 0.0001),
and body length (F = 29.64, P < 0.0001) (Table 3). Using the three traits, canonical
discriminant analysis correctly assigned 87.50% of mites from Kenya to its group, and
74.03% of mites from Texas to its own group (Wilks’ lambda (F = 30.16, P < 0.0001)
(Fig. 2).

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 Table 2. Means and Standard Errors of 10 Morphological Traits and Four Biometric
Ratios of Phyllocoptruta oleivora Mites Collected from Texas and Kenya
Texas Kenya
Trait Mean SE Mean SE
A-Body length 0.00015160 0.00000130 0.00013528 0.00000105
B-Length of prodorsal shield 0.00004157 0.00000034 0.00003776 0.00000033
C-Width of prodorsal shield 0.00004852 0.00000039 0.00004189 0.00000037
D-Width of scapular seta apart 0.00002284 0.00000020 0.00002134 0.00000022
E-Tibia I 0.00000536 0.00000027 0.00000450 0.00000007
F-Length of tarsus I 0.00000660 0.00000014 0.00000620 0.00000013
G-Width of genital shield 0.00002099 0.00000028 0.00001928 0.00000027
H-Length of genital shield 0.00001802 0.00000034 0.00001462 0.00000024
I-Width of Tail end 0.00001501 0.00000013 0.00001679 0.00000021
J-Mid-section 0.00005489 0.00000045 0.00004821 0.00000046
Body length/tail end ratio 10.20 0.1155 8.2570 0.1306
aBody length/mid-section ratio 2.789 0.03189 2.8314 0.02756
Mid-section/tail end ratio 3.700 0.0447 2.9453 0.05029
Width of the genital shield/
1.20835 0.02114 1.3460 0.02022
length of genital shield
aCharacteristics were not significantly different.

0.3
Kenya
Texas
0.2
Principal Component 2

0.1

0.0

-0.1

-0.2

-0.3
-0.6 -0.4 -0.2 0.0 0.2 0.4 0.6

Fig. 1. Principal component analysis of Phyllocoptruta oleivora from Kenya and

Texas.

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 Table 3. Stepwise Discriminate Analysis in Canonical Analysis Found Three
Morphological Traits that Segregate Populations of Phyllocoptruta oleivora from
Kenya and Texas
Trait F-value P-value
C – width of prodorsal shield 97.18 <0.001
O – tail end 30.67 <0.001
A – body length 29.64 <0.001

4
Kenya
3 Texas

1
Canonical 2

-1

-2

-3

-4
-4 -3 -2 -1 0 1 2 3 4
Canonical 1
Fig. 2. Phyllocoptruta oleivora from Kenya and Texas can be segregated by
canonical function 1 (Wilks’ lambda F = 58.66, P < 0.0001). Discriminate functions
were calculated from morphological traits width of prodorsal shield, tail end, and body
length.

The study also showed that P. oleivora on oranges and grapefruits in Texas
were morphologically distinct from those on tangerines and oranges in Kenya.
Although the differences are significant, the taxonomical meaning of the differences
is still unclear. Specialist herbivores such as eriophyid mites show strong-host
dependent morphological variation in adaption to different host species and
environmental conditions (Skoracka et al. 2002). For example, Boczek et al. (1984)
found morphological differences in females of peach silver mite, Aculus fockeui
(Nalepa & Troussart), on different species of Prunus in controlled experiments. Apple
russet mite, Aculus schlechtendali (Nalepa), differed in body size and length of the
ventral seta, living on several varieties of apple trees (Kozlowski 1998). Skoracka et
al. (2002) also found host-dependent morphological variation in three populations of
Abacarus hystrix (Nalepa) on different grasses.

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 Geographical location also might influence morphological variation between
Kenyan and Texan populations of P. oleivora. P. oleivora was collected from Makueni
in the arid/semi-arid area of Kenya. Soil is rich in nutrients and annual rainfall ranges
from 150 to 650 mm. The elevation of the area where mites were collected in Kenya
was 1,157 m above sea level, and temperature averaged 10-26°C. The P. oleivora
from Texas were from the sub-tropical part of the state, where annual rainfall
averaged 150-630 mm; however, the Rio Grande Valley is only 24 m above sea level,
and average temperature ranged from 11-36°C. Insects from higher elevations and
colder temperatures often are smaller than those at lower elevation in warmer
climates (Guevara and Avilés 2007).
Morphological differences found in the study could be explained by partial or
complete genetic separation due to geography. P. oleivora is host specific and found
exclusively on citrus (Yothers and Mason 1930, Vacante 2010). Host-plant
specialization such as exhibited by P. oleivora could lead to genetic or phenotypic
differentiation because of the intimate relationship with the host if there is extreme
selection pressure (Via 1999). P. oleivora reproduces through arrhenotokous
parthenogenesis and reduces the recombination rate compared to obligate sex
organisms, so novel or mutant traits can be fixed more quickly when sex is limited
(Dickey and Medina 2010). However, without the use of molecular tools or analysis,
it is impossible to draw a concrete conclusion.
The study was the first morphological study of P. oleivora in the United States
and Kenya. Based on results of the study, scientists and pest managers now have
insight into morphological variation of P. oleivora populations in Texas and in Kenya.
Further molecular studies need to elucidate P. oleivora from Kenya is a different
species of mite than those in Texas. If a new species, it might influence compatibility
of a pest management program from a different geographical location.

Acknowledgment

We thank Peterson Wachira Mderitu, Samira Abuelgasim Mohamed, Daisy

Salifu, Dr. Bob Copeland, Valentina Migani, and Dr. Christian Borgemeister of ICIPE
for their hospitality and support in Kenya, and Robert Saldana and Jim Hearn of
Texas A&M University Kingsville Citrus Center for help collecting mites in Texas.
SMR also thanks all the instructors of the 2011 Ohio State Acarology Summer
program. This work was partially supported by a Borlaug Global Food Security
Graduate Student Grant and used as partial fulfillment of the requirements for the
M.S. degree of SMR at Texas A&M University, Kingsville.

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