Ricoseius loxocheles, a phytoseiid mite that feedson coffee leaf rust

Cleber M. Oliveira • Joao A. M. Ferreira • Rafael M. Oliveira •

Francisco O. Santos • Angelo Pallini

Received: 21 October 2013 / Accepted: 8 April 2014� Springer International Publishing Switzerland 2014

Abstract One of the most important diseases of coffee plants is the coffee leaf rust

fungus Hemileia vastatrix Berkeley and Broome (Uredinales). It can cause 30 % yield loss

in some varieties of Coffea arabica (L.). Besides fungus, the coffee plants are attacked by

phytophagous mites. The most common species is the coffee red mite, Oligonychus ilicis

McGregor (Acari: Tetranychidae). Predatory mites of the Phytoseiidae family are well-

known for their potential to control herbivorous mites and insects, but they can also

develop and reproduce on various other food sources, such as plant pathogenic fungi. In a

field survey, we found Ricoseius loxocheles (De Leon) (Acari: Phytoseiidae) on the

necrotic areas caused by the coffee leaf rust fungus during the reproductive phase of the

pathogen. We therefore assessed the development, survivorship and reproduction of

R. loxocheles feeding on coffee leaf rust fungus and measured predation and oviposition of

this phytoseiid having coffee red mite as prey under laboratory conditions. The mite fed,

survived, developed and reproduced successfully on this pathogen but it was not able to

prey on O. ilicis. Survival and oviposition with only prey were the same as without food.

This phytoseiid mite does not really use O. ilicis as food. It is suggested that R. loxocheles

is one phytoseiid that uses fungi as a main food source.

Keywords Mycophagy � Biological control � Feeding habits � Life table �Phytopathogenic fungi � Phytoseiidae � Generalist predatory mite � Coffee

red mite

Introduction

Biological control of plant pests and diseases with natural enemies is an alternative to

chemical control (Colfer et al. 2003; Onzo et al. 2012). The use of natural enemies prevents

C. M. Oliveira � J. A. M. Ferreira (&) � R. M. Oliveira � F. O. Santos � A. PalliniDepartment of Entomology, Federal University of Vicosa, Av. Peter Henry Rolfs, s/n,Campus Universitario, Vicosa, MG 36570-000, Brazile-mail: joao.marinho@ufv.br

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Exp Appl AcarolDOI 10.1007/s10493-014-9814-y

environmental risks associated with chemical pesticides, such as pesticide resistance,

environmental pollution, worker health impacts and the presence of residues in food (Hajek

2004). Several predatory mite species of the family Phytoseiidae have been reported and

used as biological control agents of phytophagous mites and small insects (e.g. trips)

(Chant 1985) in many differents crops. Phytoseiid mites are both generalist and specialists

and the generalists are predators that can persist on plants when prey is absent or scarce by

feeding on other food sources (McMurtry and Croft 1997). There are some reports that

demonstrate the relationship between mites and fungi, some demonstrated the effectiveness

of mites to control fungi (Duso et al. 2003; English-Loeb et al. 2005; Pozzebon et al. 2009).

Mycophagy can be considered a feeding behavior for some mite families, such as

Phytoseiidae and Tydeidae. Many studies have shown that tydeid mites are efficient in

biological control of fungi (Mendel and Gerson 1982; English-Loeb et al. 1999; Norton

et al. 2000). They are able to feed on the main prey that is also mites and during periods

with low prey densities the predator population can persist by feeding on alternative foods,

such as pollen and fungi causing plant diseases (Pozzebon et al. 2009; Duso et al. 2005).

Some authors suggest that the presence of plant pathogenic fungi on the leaves may

provide favorable condition, such as the ones inside the leaf domatia (Reding et al. 2001;

Zemek 2005). Coffee plants possess pit-shaped domatia that are located in the primary vein

axils on the underside of leaves (O’Dowd 1994) and they have been shown to have positive

effects on predatory mite population.

Studies on mite diversity on coffee in Brazil have mainly targeted phytophagous mites and

information on predatory and fungivorous mites is scarce. The most common species of phy-

tophagous mites on the coffee plant is the coffee red mite, Oligonychus ilicis McGregor (Acari:

Tetranychidae). Coffee red mite is considered an important coffee pest in many producing

countries and it is found on the upper leaf surface causing reduction of photosynthesis rate and

premature leaf drop as a consequence of the infestation (Reis 2005). Even this, there is a high

abundance of phytoseiid species in coffee crops (Spongoski et al. 2005) and Ricoseius

loxocheles (De Leon) is commonly found on coffee plants infected with the coffee leaf rust

Hemileia vastatrix Berkeley and Broome (Oliveira, CM, personal observation).

Ricoseius loxocheles is known from plant material collected in Brazil, Florida (USA),

Colombia, Costa Rica, Guadeloupe, Honduras, Martinique (Flechtmann 1967; Denmark and

Muma 1973; Flechtmann 1976; Moraes et al. 1991; Denmark et al. 1999; Moraes et al. 1999).

Despite this large distribution, little is known about this mite species. Flechtmann (1976)

suggested that it may feed on spores of coffee leaf rust and possibly spread the disease among

plants due to their habit of moving actively through the crop, but this has not been confirmed.

Moreover, there is no published research on the biology and behaviour of R. loxocheles on

coffee plants and its relationship with coffee leaf rust or any other pathogen. We therefore

assessed the development, survivorship and reproductive parameters of R. loxocheles feeding

on coffee leaf rust and measured predation and oviposition of this phytodeiid having coffee-

red-mite as prey under laboratory conditions. Knowledge of the biology of this phytoseiid is

essential to understand its role in coffee crops infected by pathogens.

Materials and methods

Rearing of Ricoseius loxocheles

Ricoseius loxocheles was collected from coffee plants infected with coffee leaf rust

(Hemileia vastatrix) in July 2010 in Vicosa (20�450 1400 S42�520 5500O), Minas Gerais State

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(Brazil). The colony was kept on the underside of coffee leaves infected with coffee leaf

rust and placed on top of a moist sponge inside a box (250 9 150 9 50 mm). The edges of

the leaves were surrounded with moistened cotton wool to prevent mites from escaping.

The leaves were replaced when their turgidity was severely reduced. Cultures were kept

inside a climate room at 25 ± 1 �C, 60 ± 10 % RH and at a 12:12 light: dark cycle.

Arenas were examined once per day. When over-population of the mites was observed,

phytoseiids were transferred to new arenas.

Immature development

In order to determine the development and survival of immature mites, eggs of similar age

were used. To obtain such a cohort, several adult females were allowed to lay eggs on a

detached infected leaf with urediniospores of coffee leaf rust on wet cotton wool and

placed inside a tray. The adults were removed after 24 h and the eggs were carefully

transferred to the experimental units. Each experimental unit consisted of a coffee leaf disc

(0.8 cm in diameter) infected with spores of coffee leaf rust and placed upon a small island

of agar (0.8 cm in diameter) in the middle of a Petri dish (2 cm in diameter, 1 cm high).

Water was added in the Petri dish to prevent the escape of mites and keep the disc turgid.

When the leaf discs were deteriorating, the mites were transferred to a new arena. The

presence of an exuvium was used as the criterion for successful molting to the next

developmental stage. The characteristics observed were incubation period of the egg stage,

duration of protonymphal and deutonymphal stages, and sex ratio. The duration and

survivorship of each stage was determined daily at 7 am, noon and 6 pm. The arenas were

incubated under the same conditions as above.

Reproduction and life table parameters

Newly emerged adults of R. loxocheles (around 9 days old) were taken from a cohort. They

were individually transferred to an experimental unit as described above, but these arenas

had a diameter of 3.2 cm and the Petri dish had a diameter of 3.5 cm and was 4.0 cm high.

The mites were observed at 12 h intervals to record the first oviposition. Subsequently, the

mites were observed at 24 h intervals. The number of eggs laid was counted daily until the

female died. The arenas were incubated under the same conditions as above.

The mean generation time (T), the doubling time (Dt), the net reproduction rate (Ro),

and the finite rate of increase (k), were calculated using the method recommend by Birch

(1948):

T ¼Xn

x¼0

mxlxx

mxlx

Dt ¼ ln 2ð Þ=rm

R0 ¼XT

x¼0

mxlx

k ¼ erm

The intrinsic rate of increase (rm) was calculated by Lotka’s equation (Carey 1993):

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XT

x¼0

lxmxe�rm xþ1ð Þ ¼ 1

Age-specific survival rates (lx) and number of female offspring per female (mx) for each

age interval (x) were used for the life table data. The Jackknife procedure was used to

estimate a standard error for the rm values (Meyer et al. 1986).

Oviposition, survival and predation

The predation, oviposition rate and survival of R. loxocheles were measured on a diet

consisting of: O. ilicis eggs (Rl ? EOi), O. ilicis eggs and H. vastatrix urediniospores

(Rl ? EOi ? Hv), O. ilicis juveniles (Rl ? JOI), O. ilicis juveniles and H. vastatrix

urediniospores (Rl ? JOi ? Hv), O. ilicis adult (Rl ? AOi) and O. ilicis adult and

H. vastatrix urediniospores (Rl ? AOi ? Hv). In order to obtain prey eggs, coffee leaf

discs (Ø = 2.8 cm) were infested with 20 adult females for 48 h. Subsequently, females

were removed and the eggs were counted. The other stages were collected from a rearing

unit and placed on clean coffee leaf discs with a fine brush 24 h after started the experiment.

A single gravid female of R. loxocheles with nine days old was added at the same time

in all treatments. Twelve replicates were done for each stage, and the densites of prey per

arena were 86.65 ± 2.57 eggs, 25.00 ± 0.00 juveniles and 19.97 ± 0.10 adult females. As

a control for natural prey mortality, 12 replicates per stage with the same mean number of

prey were incubated without predator and as a control to natural mortality of R. loxocheles

without food (Rl), 12 replicates were incubated without food (H. vastatrix urediniospores

nor prey). To assess the fecundity and survival of the R. loxocheles only with H. vastatrix

urediniospores, was done twelve replicates with this kind of food. The number of con-

sumed and alive prey as well as survival and oviposition of the predators was recorded

every day during four days. Kaplan–Meier survival curves on different diets were fitted and

compared using the Tukey test (Hosmer and Lemeshow 1999, library survival, R Devel-

opment Core Team, 2005). Predation rate was compared between days and treatment using

a generalized linear mixed effects model with Poisson errors and a random factor within

days to correct for pseudoreplication, using R (lmer, R Development Core Team 2005).

Oviposition rate was first analyzed with generalized linear model with binomial errors to

separated treatments with and without oviposition and after the treatments with oviposition

was analyzed with generalized linear model with Poisson erros, using R (glm, R Devel-

opment Core Team 2005). These two steps were done because we had problems with

oviposition rate. Half of the treatment does not have oviposition so we observed the zero

inflated problem.

Results

Immature development

The eggs are translucent and have an elongated shape, very common characteristics of

phytoseiids eggs. This mite usually oviposits near the vein among the H. vastatrix

urediniospores, and the eggs are covered with urediniospores of coffee leaf rust by females.

The duration of the egg period was the longest phase of the immature development

(Table 1).

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The stage with the shortest developmental period was the deutonymph. Survival varied

with development stage, with the highest survival in the larva stage. The highest mortality

was observed in protonymphs (Table 1).

Reproduction and life table parameters

Females had a much shorter period of pre-oviposition and post-oviposition compared with

the oviposition period. The daily oviposition rate and the total egg production by females

were 0.76 and 9.47, respectively (Table 2). The sex ratio [$/($ ? #)] was highly female-

biased (85.85 %).

The intrinsic rate of increase (rm) was 0.09 (0.091–0.092) females/female/day. The

average duration of each generation (T) was 18.90 days and net reproductive rate (R0) was

5.60 female/female/generation. The number of offspring produced per female (mx) reached

a peak on day 13 of adulthood (1.06) and decreased from this time to reach zero at 23rd day

(Fig. 1).

Oviposition, survival and predation rate

Ricoseius loxocheles oviposited only when fed on H. vastatrix urediniospores or on a

mixed of prey and urediniospores. Oviposition rate on treatment without urediniospores of

coffee leaf rust and on treatment with R. loxocheles without food was null and did not

differ (df = 3, p = 1) but these treatments differ from treatment with urediniospores of

coffee leaf rust (df = 7, p\ 0.0001) but the oviposition rate on all treatment with

urediniospores of coffee leaf rust or mixed with prey was not different (df = 3, p = 0.71)

(Fig. 2).

The survival of R. loxocheles was different among the treatments (Likelihood ratio

test = 79.7, df = 7, p \ 0.001), but there was no difference between the treatment with or

without urediniospores of coffee rust accordiling with Tukey test (Fig. 3).

Ricoseius loxocheles was not able to feed on any stages of O. ilicis (Fig. 4). The

phytoseiid species did not prey adults of O. ilicis (v2 = 7.995, df = 5, p = 0.16) (Fig. 4a).

The decrease in the amount of survival adults of the prey was similar between the treat-

ments with and without the phytoseiid, so we can suggest that this decrease was due the

natural mortality.

We found the same trend in the treatment with juvenile as food source, with no pre-

dation recorded (v2 = 0.7558, df = 5, p = 0.98) (Fig. 4B). We also evaluated the

potential of predation of R. loxocheles on eggs of the prey O. ilicis and it was not sig-

nificant the variation on eggs (v2 = 1.5097, df = 5, p = 0.91) (Fig. 4c).

Discussion

The predatory mite R. loxocheles could develop and reproduce successfully when feeding

only on H. vastatrix spores. To our knowledge, this is the first study that involves this mite

species and its food source. This phytoseiid species is the only one belonging to the genus

Ricoseius (Chant and McMurtry 2005) and the feeding behaviour of this mite was not clear

until now. Considering the definition of alternative food proposed by Overmeer (1985), the

coffee leaf rust can be considered as an alternative food to R. loxocheles because this mite

cannot only survive and develop, but also reproduce when feeding on its specific food

source.

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We observed that females of the predatory mite lay their eggs inside the spore patches

of the pathogen. Possibly, the spores provide favourable structures for predaceous mites

(Reding et al. 2001). Some plant features that are non-pest associated can provide struc-

tures and harbour mites, such as domatia (Walter 1996; Walter and O’Dowd 1992). Leaf

domatia have been shown to positively affect predatory and mycophagous mite populations

(Ferreira et al., 2008, 2011; Karban et al. 1995; Walter and Denmark 1991).

Table 1 Mean duration (in days) ± SE and survival (%) of the immature stages of Ricoseius loxochelesfeeding on urediniospores of coffee leaf rust, Hemileia vastatrix (25 ± 1 �C, 60 ± 10 % RH and 12:12 h)

Stage Duration (days) Survival (%)

Egg 2.96 ± 0.25 88.89

Larva 1.96 ± 0.14 95.83

Protonymph 2.09 ± 0.22 86.96

Deutonymph 1.80 ± 0.21 95.00

Egg to adult 8.88 ± 0.29 70.37

Table 2 Reproduction parame-ters (mean ± SE) of Ricoseiusloxocheles females feeding onurediniospores of coffee leaf rust,Hemileia vastatrix

Stage

Pre-oviposition in days 3.59 ± 0.60

Oviposition in days 12.95 ± 3.05

Post-oviposition in days 3.05 ± 0.59

Longevity in days 19.59 ± 0.84

Eggs per female per day 0.76 ± 0.07

Total eggs per female 9.47 ± 0.91

Fig. 1 Age-specific survival (solid line) and fecundity (dotted line) of Ricoseius loxocheles feeding onurediniospores of coffee leaf rust, Hemileia vastatrix

Exp Appl Acarol

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Within all immature stage, the longest stage is the egg, which holds for other phyto-

seiids as well (Broufas and Koveos 2001; Kasap and Sekeroglu 2004; Vantornhout et al.,

2004; Tsoukanas et al., 2006; Abad-Moyano et al. 2009; Da Silva Melo et al. 2009;

Pozzebon et al. 2009; Kasap 2009; Kolokytha et al. 2011). In this study, R. loxocheles

showed higher viability of egg-adult period than Amblyseius andersoni Chant and

Fig. 2 Mean (? SE) number of eggs produced per Ricoseius loxocheles in 4 days on diet of Hemileiavastatrix (Rl ? Hv), without food (Rl), Oligonychus ilicis females and H. vastatrix (Rl ? AOi ? Hv),O. ilicis females (Rl ? AOi), O. ilicis juveniles and H. vastatrix (Rl ? JOi ? Hv), O. ilicis juveniles(Rl ? JOi), O. ilicis eggs and H. vastatrix (Rl ? EOi ? Hv), O. ilicis eggs (Rl ? EOi) at laboratory(25 ± 1 �C, 60 ± 10 % RH and at a 12:12 light: dark cycle). Different characters above the bars indicatesignificant differences in oviposition (p \ 0.05, Tukey HSD test)

Fig. 3 Survival of Ricoseius loxocheles adult females on diet of Hemileia vastatrix (Rl ? Hv), withoutfood (Rl), Oligonychus ilicis females and H. vastatrix (Rl ? AOi ? Hv), O. ilicis females (Rl ? AOi),O. ilicis juveniles and H. vastatrix (Rl ? JOi ? Hv), O. ilicis juveniles (Rl ? JOi), O. ilicis eggs andH. vastatrix (Rl ? EOi ? Hv), O. ilicis eggs (Rl ? EOi) at laboratory (25 ± 1 �C, 60 ± 10 % RH and at a12:12 light: dark cycle)

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Typhlodromus pyri Scheuten reared on grape downy mildew (Plasmopara viticola)

(Pozzebon and Duso 2008; Pozzebon et al. 2009). Our results show that coffee leaf rust is

an appropriate food source for the development and reproduction of this phytoseiid. We

observed that this mite species occurs on coffee plants only during the reproductive phase

of H. vastatrix (February–August) (Oliveira, CM, personal observation) and it may migrate

to other plants to seek for other food sources when the pathogen is not present.

Our results are consistent with previous studies on other fungi-phytoseiid relationships,

which also demonstrated the ability of phytoseiid mites to develop and reproduce suc-

cessfully when feeding on fungi (Chant 1959; Kropczynska-Linkiewicz 1971; Bakker

1993; Zemek and Prenerova 1997; Pozzebon and Duso 2008). In this study, R. loxocheles

fed on urediniospores of coffee leaf rust showed the behaviour of carrying urediniospores

on their dorsum. Further studies are being conducted to evaluate the ability of this phy-

toseiid to disperse or to control this plant disease.

Adult females of R. loxocheles reached the peak of oviposition in the 13th day of

adulthood (around one eggs per day). Ricoseius loxocheles has a low reproductive rate

(0.09 females/female/day) when fed on coffee leaf rust compared with other phytoseiids

(Van Rijn and Tanigoshi 1999; Broufas and Koveos 2001; Steiner et al. 2003; Tsoukanas

et al. 2006).

Ricoseius loxocheles are not able to feed on any of the stages of the coffee red mite,

O. ilicis. These observations are contrary to our expectations because many others Phy-

toseiidae species can develop and reproduce or only survive feeding on prey. This species

does not use the prey neither as alternative food nor as supplementary food because it

cannot survive eating only this prey.

In the current study we proved that this phytoseiid is specialized to feed on fungi and the

coffe-red-mite is not an adequate food for it, however more studies using others phy-

tophagous mites and other food sources need be done to confirm the mite feeding habit.

Ricoseius loxocheles could survive and oviposit only on arenas with urediniospores of

coffee leaf rust or with urediniospores of coffee leaf rust and prey. Survival and oviposition

on arenas with only prey were the same as arenas without food, so coffee red mite was not

really used as food. Ramos and Rodrıguez (2006) hypothesized that this phytoseiid mite

can feed on Tetranychidae species on Citrus spp. However, they did not test this hypothesis

at all. So, new investigations should be conducted to test the predation capacity of its

phytoseiid mite and its reproductive success on different prey than O. ilicis. One possible

prey for this phytoseiid mite is the vector of the coffee ring spot virus, Brevipalpus

phoenicis (Geijskes 1939) (Acari: Tenuipalpidae).

So, more studies are being carried out and more investigations are necessary to clarify

the interaction between R. loxocheles and H. vastatrix on coffee plants. Some species of

mites are able to control fungi disease, is it possible R. loxocheles be considerate one

biological control of coffee leaf rust? More investigations are being done to answer this

question.

Acknowledgments We are grateful to Minas Gerais Research Support Foundation (FAPEMIG), Coor-dination for the Improvement of Higher Education Personnel (CAPES) and National Council of Scientificand Technological Development (CNPq) for the financial supports. Arne Janssen is thanked for commentson previous versions of this manuscript.

Fig. 4 Mean (± SE) numbers of Oligonychus ilicis females (a), juveniles (b), and eggs (c) as functionof time on leaf discs without Ricoseius loxochles (close triangles), with R. loxocheles (open circles) or withR. loxocheles mixed with urediniospores of coffee leaf rust (close circles). No significant differences werefound

b

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