Directory UMM :Journals:Journal of Stored Products Research:Vol 36.Issue1.Jan2000:
Journal of Stored Products Research 36 (2000) 55±63
www.elsevier.com/locate/jspr
Potential of Acarophenax lacunatus (Prostigmata:
Acarophenacidae) as a biological control agent of
Rhyzopertha dominica (Coleoptera: Bostrichidae)
L.R.D'A. Faroni a, R.N.C. Guedes b,*, A.L. Matioli c
a
Departamento de Engenharia AgrõÂcola, Universidade Federal de Vic° osa, Vic° osa, MG 36571-000, Brazil
b
Departamento de Biologia Animal, Universidade Federal de Vic° osa, Vic° osa, MG 36571-000, Brazil
c
Departamento de Entomologia e Nematologia, Universidade Estadual de SaÄo Paulo, Jaboticabal, SP 14870-000,
Brazil
Accepted 9 June 1999
Abstract
A recent report of the parasitic mite species Acarophenax lacunatus (Cross and Krantz) (Prostigmata:
Acarophenacidae) attacking populations of Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) led to
the present investigation. Maximum female size and average number of progeny per female mite were
assessed at eight dierent temperatures (ranging from 20 to 418C) and 60% r.h. using R. dominica as the
host. The ability of the mite species to suppress eggs, ®rst instar larvae, and adults of R. dominica was
assessed at 308C and 60% r.h. The largest female sizes of the mite and progeny numbers were obtained
around 308C (259 mm and 17 ospring/female respectively) with minimum values obtained at the most
extreme temperatures used in this study. Mite densities of at least four individuals per 500 ml jar
containing 50 adults of R. dominica, resulted in almost complete suppression of eggs, ®rst instar larvae,
and adults of the host species after 45 days. This same range of mite densities led to reductions of wheat
weight losses of 15 and 25% after 45 and 60 days after infestation respectively. Acarophenax lacunatus
shows good potential as a biological control agent of R. dominica. # 2000 Elsevier Science Ltd. All
rights reserved.
Keywords: Mites; Stored products; Wheat; Grain borer
* Corresponding author Tel: +55-31-899-2006; telefax: +55-31-899-2537.
E-mail address: guedes@mail.ufv.br (R.N.C. Guedes)
0022-474X/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 2 - 4 7 4 X ( 9 9 ) 0 0 0 2 7 - 2
56
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
1. Introduction
Biological control of pests has received considerable attention throughout the world (e.g.,
Wood and Way, 1988; Debach and Rosen, 1991; Hoy, 1994) despite recent questions regarding
its environmental safety (Howarth, 1991; Simberlo and Stiling, 1996). In stored product
protection there is an increasing interest in biological control (Arbogast, 1984; Guedes, 1990;
Brower, 1991; Brower et al., 1996). However, research on the potential of biocontrol agents of
stored-product insects has been restricted to a small number of species (Guedes, 1990; Brower
et al., 1996).
There is little information available about some important groups of natural enemies of
stored-grain insects such as parasitic and predatory mites (Brower et al., 1996; Matioli, 1997).
Among these, only a few species, such as Pyemotes tritici (Lagreze-Fossat and Montane)
(Prostigmata: Pyemotidae), are reported as potential biological control agents of storedproduct insects (Bruce and LeCato, 1979; Bruce, 1983). Nonetheless, a recent report of a
parasitic mite species, Acarophenax lacunatus (Cross and Krantz) (Prostigmata:
Acarophenacidae), suppressing Spanish populations of the lesser grain borer, Rhyzopertha
dominica (F.) (Coleoptera: Bostrichidae) (Faroni, 1992), one of the most destructive storedgrain pests throughout the world, indicates a renewed interest in this group of natural enemies
(Faroni, 1992; Faroni and Garcia-Mari, 1992; Matioli, 1997).
The mite species A. lacunatus was ®rst reported in colonies of the rusty grain beetle,
Cryptolestes ferrugineus (Stephens) (Coleoptera: Cucujidae), by Cross and Krantz (1964). It
was initially placed within the family Pyemotidae and latter transferred to a new family Ð
Acarophenacidae (Steinkraus and Cross, 1993; Magowski, 1994). Acarophenax and related
genera are reported as insect egg parasites which usually exhibit two peculiar traits: (1) female
physogastry, characterized by development of progeny within the female body, which
subsequently emerge as sexually mature adults (Cross and Krantz, 1964; Rakha and Kandeel,
1983; Steinkraus and Cross, 1993); and (2) phoresy, which refers to the passive transport of an
arthropod by another for purposes other than direct parasitization (Clausen, 1976; Ro, 1991;
Steinkraus and Cross, 1993). The phoretic attachment of young adult female mites on adult
hosts may be the major mechanism for their dispersal into new host oviposition sites
(Steinkraus and Cross, 1993).
Although A. lacunatus seems to have potential as a biological control agent of R. dominica,
there are few studies providing biological data on this mite species or an assessment of its
possible importance as a mortality factor in lesser grain borer populations. The objective of the
present study was to assess the potential of A. lacunatus to suppress populations of R. dominica
in wheat.
2. Materials and methods
Acarophenax lacunatus was obtained from the Laboratory of the Department of
Entomology, Valencia Polytechnic University, Valencia, Spain, in 1992. It has subsequently
been maintained at the Federal University of Vic° osa on colonies of R. dominica reared on
whole hard wheat at 32 218C and 652 5% r.h.
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
57
The laboratory population of R. dominica used to sustain the parasitic mite population was
kept on whole hard wheat with 13% m.c. and 258C inside 500 ml glass jars. Host eggs were
collected using sieves with an aperture diameter of 1 mm and placed at the center of covered
Petri dishes (10 cm diameter). Newly-emerged mites were obtained from infested colonies of R.
dominica using sieves and the mites were transferred to Petri dishes containing R. dominica
eggs. After 24 h, sets of 40 female mites per treatment, attached to host eggs and already in
physogastry (i.e., attached to host egg but still without signi®cant increase in body volume),
were collected and individually placed in smaller Petri dishes (5 cm diameter) and covered until
progeny emergence. With this procedure, the eect of temperature on female size and progeny
production was studied at eight dierent temperatures (20, 25, 29, 30, 32, 35, 38, and 418C)
and 60% r.h., in eight climatic chambers. The female size was assessed by measuring the
Fig. 1. Eect of temperature on maximum size (A) and progeny (B) of physogastric females of Acarophenax
lacunatus feeding on eggs of Rhyzopertha dominica. Each symbol represents the mean from between 5 and 31
replicates (41 and 308C respectively). ( p < 0.0001, r 2=0.20 (A) and =0.48 (B), df =137, n = 141).
58
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
mesopodosomal area in its transversal section by using a micrometer coupled to a
stereomicroscope with 40 magni®cation.
The parasitism potential of A. lacunatus on R. dominica was assessed at 308C and 60% r.h.
Zero, 4, 6, 8, and 10 physogastric females of A. lacunatus were released in 500 ml glass jars
with whole wheat and 50 adults of R. dominica that were 3±7 days old. The jars, ®lled with
420 g of whole hard wheat (13% m.c.), were ringed with vaseline in their upper part and they
were covered with organza. After 45 and 60 days following infestation, the number of
surviving adults and ®rst instar larvae and the number of non-parasitized eggs of the lesser
grain borer were recorded by direct count after sieving the wheat. Eight replicates were used
for each treatment. The grain weight loss (%) during the period was also assessed by weighing
the grain before the infestation and 45 and 60 days afterwards, removing the ®ne material by
sieving prior to weighing the grain. The obtained data were subjected to correlation and
regression analysis. Correlation and linear regression analyses were done using the procedures
PROC CORR and PROC REG, respectively (SAS Institute, 1987). Non-linear regression
analyses were done using the curve ®tting procedure of SigmaPlot (Jandel Scienti®c, 1986).
3. Results
Temperature aected the size of physogastric female mites which reached maximum size
(1260 mm) at about 308C (Fig. 1A). The smallest physogastric mites (1195 mm) were observed
at the lowest and highest temperatures within the range studied (i.e., 20 and 418C).
Temperature also aected the number of ospring per physogastric female with larger number
of progeny (ca. 17/female) occurring at about 308C and decreasing at higher and lower
temperatures (Fig. 1B). At 418C, there was no production of ospring. There was a positive
correlation (r = 0.46, p < 0.0001) between maximum female size and fertility, where larger
females produced more progeny (Fig. 2).
Fig. 2. Correlation between maximum female size and progeny produced per female of Acarophenax lacunatus
feeding on eggs of Rhyzopertha dominica. ( p < 0.0001, r = 0.46, df =138, n = 141).
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
59
Fig. 3. Eect of the density of physogastric females of Acarophenax lacunatus on the suppression of eggs (A), ®rst
instar larvae (B), and adults (C) of Rhyzopertha dominica. Each symbol represents the average of eight replicates.
Evaluations were made after 45 (r) and 60 days (w) of the infestation. ( p < 0.01, r 2 > 0.80, df =38, n = 40).
60
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
Increasing densities of female mites increased egg parasitism (Fig. 3A) and reduced the
population size of ®rst instar larvae and adults of R. dominica (Fig. 3B and C). Densities as
low as two physogastric females per jar led to complete suppression of live ®rst instar larvae
and non-parasitized host eggs in 45 days. Full suppression of host adults took longer (i.e., 60 d)
and required higher mite densities (at least six physogastric females per jar). The increasing
densities of physogastric female mites also decreased the wheat weight loss due to damage by
the lesser grain borer (Fig. 4). Initial densities of ten female mites per jar decreased the grain
weight loss from 21 and 27% to 3 and 6% after 45 and 60 days respectively. Mite densities as
low as two per jar reduced the grain weight loss by over 50% compared to the control.
4. Discussion
The straw itch mite, Pyemotes tritici, is the best studied mite species with potential for
biological control of stored-product insects (Brower et al., 1996). This mite attacks all
developmental stages of Plodia interpunctella (HuÈbner) and Cadra cautella (Walker)
(Lepidoptera: Pyralidae), Oryzaephilus mercator (Fauvel) (Coleoptera: Cucujidae), and
Lasioderma serricorne (F.) (Coleoptera: Anobiidae) (Bruce and LeCato, 1979). However,
despite its great potential as a biological control agent, its commercial use has been limited
because it, like other members of the family Pyemotidae, can also bite humans (Moser, 1975;
Brower et al., 1996). Because the genus Acarophenax was initially described within this family,
there are questions regarding its safety or nuisance value to humans (Cross and Krantz, 1964;
Steinkraus and Cross, 1993; Matioli, 1997). However, the inspections of A. lacunatus while in
quarantine, in Brazil, by the SaÄo Paulo Vegetal Sanitation Service and the Brazilian Ministry
of Agriculture (Process 21.000.002807/95-82) did not provide any evidence of harmful eects
on man or mammals leading to its clearance for further studies. Steinkraus and Cross (1993)
Fig. 4. Eect of the density of physogastric females of Acarophenax lacunatus on grain weight loss (%) after 45 (r)
and 60 days (w) of the infestation. Each symbol represents the average of eight replicates. ( p < 0.05, r 2 > 0.75, df
=38, n = 40).
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
61
also observed no harmful eects of Acarophenax mahunkai (Steinkraus & Cross) on man or
higher animals.
Acarophenax spp leave the host during host oviposition, parasitize the host eggs, and feed on
the egg's contents. These mites kill the host egg and one host egg is usually sucient for
complete progeny development (Lindquist, 1983; Steinkraus and Cross, 1993). After mating,
mature female mites go into physogastry and numerous mites develop, reach adulthood, and
mate within the gravid females (Steinkraus and Cross, 1993). These same general life history
traits occur in A. lacunatus. This species also has the typical phoretic behavior not associated
with direct parasitization as described by Clausen (1976) and Ro (1991) which increases even
further the potential of this parasitic mite species as a biological control agent of R. dominica.
Acarophenax lacunatus is not a true parasite since it kills the host eggs, but it is not considered
a predator either, since the females feed in just one egg during their life time and this mite
species has a fast life cycle. Acarophenax lacunatus acts more like parasitoids according to
Lindquist (1983) although, like other species within the genus Acarophenax, it is usually
referred to as parasitic (Cross and Krantz, 1964; Faroni, 1992; Steinkraus and Cross, 1993;
Matioli, 1997). Adult males of Acarophenax spp are ephemeral and may not emerge from
physogastric females (Steinkraus and Cross, 1993), but single males of A. lacunatus do emerge
from physogastric females.
Temperature had a strong eect on female size and fertility. At temperatures around 308C,
physogastric females reach larger sizes and produce more progeny, probably maximizing the
suppression of its host population at this temperature range. Since R. dominica is an insect of
tropical origin (Potter, 1935) with a strong ability to ¯y (Dowdy, 1994; Guedes, Kambhampati
and Dover, 1997), the usefulness of A. lacunatus as a biological control agent of R. dominica
seems promising, especially where there is lack of alternative control methods to insecticides
(Guedes et al., 1996).
Parasitization by A. lacunatus was invariably fatal to eggs of lesser grain borer, as was also
reported for A. mahunkai attacking lesser mealworms, Alphitobius diaperinus (Panzer), by
Steinkraus and Cross (1993). This ability to reduce the population size of the lesser grain
borer, the short life cycle of A. lacunatus, its high fertility at temperatures around 308C, and
the lack of evidence of harmful eects on humans and higher animals, suggests that this mite
species may be a useful biological control agent of R. dominica, especially in tropical areas.
Acknowledgements
The authors would like to thank Drs. G.J. Moraes (Department of Zoology, University of
SaÄo Paulo, Piracicaba (SP), Brazil) and M.C. Picanc° o (Department of Animal Biology, Federal
University of Vic° osa, Vic° osa (MG), Brazil) for their helpful suggestions throughout this
investigation; and to Dr. F. Garcia-Mari (Department of Entomology, Valencia Polytechnic
University, Valencia, Spain) for providing the initial mite population used in our studies.
Financial support was provided by CAPES, CNPq and FAPEMIG and was greatly
appreciated.
62
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
References
Arbogast, R.T., 1984. Natural enemies as control agents for stored-product insects. In: Proceedings of the 3rd
International Working Conference on Stored-Product Protection, Manhattan, KS, pp. 360±374.
Brower, J.H., 1991. Replacing fumigants with bene®cial insects. California Agriculturist 2, 14±16.
Brower, J.H., Smith, L., Vail, P.V., Flinn, P.W., 1996. Biological control. In: Subramanyam, Bh, Hagstrum, D.W.
(Eds.), Integrated Management of Insects in Stored Products. Dekker, New York, pp. 223±286.
Bruce, W.A., 1983. Mites as biological control agents of stored product pests. In: Hoy, M.A., Cunningham, G.L.,
Knutson, L. (Eds.), Biological Control of Pests by Mites. University of California, Berkeley, pp. 74±78.
Bruce, W.A., LeCato, G.L., 1979. Pyemotes tritici: potential biological control agent of stored-product insects.
Recent Advances in Acarology 1, 213±220.
Clausen, C.P., 1976. Phoresy among entomophagous insects. Annual Review of Entomology 21, 343±367.
Cross, E.A., Krantz, G.W., 1964. Two new species of the genus Acarophenax Newstead and Duvall 1918
(Acarina:Pyemotidae). Acarologia 6, 287±295.
Debach, P., Rosen, D., 1991. Biological Control by Natural Enemies, 2nd ed. Cambridge University Press,
Cambridge, UK.
Dowdy, A.K., 1994. Flight initiation of lesser grain borer (Coleoptera:Bostrichidae) as in¯uenced by temperature,
humidity, and light. Journal of Economic Entomology 87, 1714±1717.
Faroni, L.R.D'A., 1992. Biologia y control del gorgojo de los granos Rhyzopertha dominica (F.). D.S. Thesis,
Universidad PoliteÂcnica de Valencia, Valencia, Spain.
Faroni, L.R.D'A., Garcia-Mari, F., 1992. In¯uencia de la temperatura sobre los paraÂmetros bioloÂgicos de
Rhyzopertha dominica (F.). Boletin de Sanidad Vegetal 18, 455±468.
Guedes, R.N.C., 1990. Manejo integrado para a protec° aÄo de graÄos armazenados contra insetos. Revista Brasileira
de Armazenamento 15, 3±48.
Guedes, R.N.C., Dover, B.A., Kambhampati, S., 1996. Resistance to chlorpyrifos-methyl, pirimiphos-methyl, and
malathion in Brazilian and U.S. populations of Rhyzopertha dominica (Coleoptera:Bostrichidae). Journal of
Economic Entomology 89, 27±32.
Guedes, R.N.C., Kambhampati, S., Dover, B.A., 1997. Allozyme variation among Brazilian and U.S. populations
of Rhyzopertha dominica resistant to insecticides. Entomologia Experimentalis et Applicata 84, 49±57.
Hoy, M.A., 1994. Parasitoids and predators in management of arthropod pests. In: Metcalf, R.L., Luckmann, W.H.
(Eds.), Introduction to Insect Pest Management, 3rd ed. Wiley, New York, pp. 129±198.
Howarth, F.G., 1991. Environmental impacts of classical biological control. Annual Review of Entomology 36,
485±509.
Jandel, Scienti®c, 1986. SigmaPlot Scienti®c Graphing Software Ð User's Manual. Jandel Scienti®c, San Rafael,
CA, USA.
Lindquist, E.E., 1983. Some thoughts on the potential for use of mites in biological control, including a modi®ed
concept of ``parasitoids''. In: Hoy, M.A., Cunningham, G.L., Knutson, L. (Eds.), Biological Control of Pests by
Mites. University of California, Berkeley, pp. 12±20.
Magowski, W.L., 1994. Discovery of the ®rst representative of the mite subcohort Heterostigmata (Arachnidae:
Acari) in the Mesozoic Siberian amber. Acarologia 35, 229±241.
Matioli, A.L. 1997. Biologia de Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) e seu
potencial de parasitismo sobre Rhyzopertha dominica (F.) (Coleoptera:Bostrichidae). M.S. Thesis, Universidade
Federal de Vic° osa, Vic° osa, MG, Brazil.
Moser, J.C., 1975. Biosystematics of the straw itch mite with special reference to nomenclature and dermatology.
Transactions of the Royal Entomological Society of London 122, 185±191.
Potter, C., 1935. The biology and distribution of Rhyzopertha dominica (Fab.). Transactions of the Royal
Entomological Society of London 83, 449±482.
Rakha, M.A., Kandeel, M.M.H., 1983. Acarophenax meropsi n. sp., from the European bee eater, Merops apiaster
in Egypt, (Acari:Tarsonemidae). Acarologia 24, 295±297.
Ro, D.A., 1991. Life history consequences of bioenergetic and biomechanical constraints on migration. American
Zoologist 31, 205±215.
SAS Institute, 1987. SAS/STAT User's Guide for Personal Computers, Version 6. SAS Institute, Cary, NC, USA.
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
63
Simberlo, D., Stiling, P., 1996. How risky is biological control? Ecology 77, 1965±1974.
Steinkraus, D.C., Cross, E.A., 1993. Description and life history of Acarophenax mahunkai, n. sp. (Acari,
Tarsonemina: Acarophenaciedae), an egg parasite of the lesser mealworm (Coleoptera:Tenebrionidae). Annals of
the Entomological Society of America 86, 239±249.
Wood, R.K.S., Way, M.J. (Eds.), 1988. Biological control of pests, pathogens, and weeds: developments and prospects. Philosophical Transactions of the Royal Society of London Series B 318, 109±376.
www.elsevier.com/locate/jspr
Potential of Acarophenax lacunatus (Prostigmata:
Acarophenacidae) as a biological control agent of
Rhyzopertha dominica (Coleoptera: Bostrichidae)
L.R.D'A. Faroni a, R.N.C. Guedes b,*, A.L. Matioli c
a
Departamento de Engenharia AgrõÂcola, Universidade Federal de Vic° osa, Vic° osa, MG 36571-000, Brazil
b
Departamento de Biologia Animal, Universidade Federal de Vic° osa, Vic° osa, MG 36571-000, Brazil
c
Departamento de Entomologia e Nematologia, Universidade Estadual de SaÄo Paulo, Jaboticabal, SP 14870-000,
Brazil
Accepted 9 June 1999
Abstract
A recent report of the parasitic mite species Acarophenax lacunatus (Cross and Krantz) (Prostigmata:
Acarophenacidae) attacking populations of Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) led to
the present investigation. Maximum female size and average number of progeny per female mite were
assessed at eight dierent temperatures (ranging from 20 to 418C) and 60% r.h. using R. dominica as the
host. The ability of the mite species to suppress eggs, ®rst instar larvae, and adults of R. dominica was
assessed at 308C and 60% r.h. The largest female sizes of the mite and progeny numbers were obtained
around 308C (259 mm and 17 ospring/female respectively) with minimum values obtained at the most
extreme temperatures used in this study. Mite densities of at least four individuals per 500 ml jar
containing 50 adults of R. dominica, resulted in almost complete suppression of eggs, ®rst instar larvae,
and adults of the host species after 45 days. This same range of mite densities led to reductions of wheat
weight losses of 15 and 25% after 45 and 60 days after infestation respectively. Acarophenax lacunatus
shows good potential as a biological control agent of R. dominica. # 2000 Elsevier Science Ltd. All
rights reserved.
Keywords: Mites; Stored products; Wheat; Grain borer
* Corresponding author Tel: +55-31-899-2006; telefax: +55-31-899-2537.
E-mail address: guedes@mail.ufv.br (R.N.C. Guedes)
0022-474X/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 2 - 4 7 4 X ( 9 9 ) 0 0 0 2 7 - 2
56
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
1. Introduction
Biological control of pests has received considerable attention throughout the world (e.g.,
Wood and Way, 1988; Debach and Rosen, 1991; Hoy, 1994) despite recent questions regarding
its environmental safety (Howarth, 1991; Simberlo and Stiling, 1996). In stored product
protection there is an increasing interest in biological control (Arbogast, 1984; Guedes, 1990;
Brower, 1991; Brower et al., 1996). However, research on the potential of biocontrol agents of
stored-product insects has been restricted to a small number of species (Guedes, 1990; Brower
et al., 1996).
There is little information available about some important groups of natural enemies of
stored-grain insects such as parasitic and predatory mites (Brower et al., 1996; Matioli, 1997).
Among these, only a few species, such as Pyemotes tritici (Lagreze-Fossat and Montane)
(Prostigmata: Pyemotidae), are reported as potential biological control agents of storedproduct insects (Bruce and LeCato, 1979; Bruce, 1983). Nonetheless, a recent report of a
parasitic mite species, Acarophenax lacunatus (Cross and Krantz) (Prostigmata:
Acarophenacidae), suppressing Spanish populations of the lesser grain borer, Rhyzopertha
dominica (F.) (Coleoptera: Bostrichidae) (Faroni, 1992), one of the most destructive storedgrain pests throughout the world, indicates a renewed interest in this group of natural enemies
(Faroni, 1992; Faroni and Garcia-Mari, 1992; Matioli, 1997).
The mite species A. lacunatus was ®rst reported in colonies of the rusty grain beetle,
Cryptolestes ferrugineus (Stephens) (Coleoptera: Cucujidae), by Cross and Krantz (1964). It
was initially placed within the family Pyemotidae and latter transferred to a new family Ð
Acarophenacidae (Steinkraus and Cross, 1993; Magowski, 1994). Acarophenax and related
genera are reported as insect egg parasites which usually exhibit two peculiar traits: (1) female
physogastry, characterized by development of progeny within the female body, which
subsequently emerge as sexually mature adults (Cross and Krantz, 1964; Rakha and Kandeel,
1983; Steinkraus and Cross, 1993); and (2) phoresy, which refers to the passive transport of an
arthropod by another for purposes other than direct parasitization (Clausen, 1976; Ro, 1991;
Steinkraus and Cross, 1993). The phoretic attachment of young adult female mites on adult
hosts may be the major mechanism for their dispersal into new host oviposition sites
(Steinkraus and Cross, 1993).
Although A. lacunatus seems to have potential as a biological control agent of R. dominica,
there are few studies providing biological data on this mite species or an assessment of its
possible importance as a mortality factor in lesser grain borer populations. The objective of the
present study was to assess the potential of A. lacunatus to suppress populations of R. dominica
in wheat.
2. Materials and methods
Acarophenax lacunatus was obtained from the Laboratory of the Department of
Entomology, Valencia Polytechnic University, Valencia, Spain, in 1992. It has subsequently
been maintained at the Federal University of Vic° osa on colonies of R. dominica reared on
whole hard wheat at 32 218C and 652 5% r.h.
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
57
The laboratory population of R. dominica used to sustain the parasitic mite population was
kept on whole hard wheat with 13% m.c. and 258C inside 500 ml glass jars. Host eggs were
collected using sieves with an aperture diameter of 1 mm and placed at the center of covered
Petri dishes (10 cm diameter). Newly-emerged mites were obtained from infested colonies of R.
dominica using sieves and the mites were transferred to Petri dishes containing R. dominica
eggs. After 24 h, sets of 40 female mites per treatment, attached to host eggs and already in
physogastry (i.e., attached to host egg but still without signi®cant increase in body volume),
were collected and individually placed in smaller Petri dishes (5 cm diameter) and covered until
progeny emergence. With this procedure, the eect of temperature on female size and progeny
production was studied at eight dierent temperatures (20, 25, 29, 30, 32, 35, 38, and 418C)
and 60% r.h., in eight climatic chambers. The female size was assessed by measuring the
Fig. 1. Eect of temperature on maximum size (A) and progeny (B) of physogastric females of Acarophenax
lacunatus feeding on eggs of Rhyzopertha dominica. Each symbol represents the mean from between 5 and 31
replicates (41 and 308C respectively). ( p < 0.0001, r 2=0.20 (A) and =0.48 (B), df =137, n = 141).
58
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
mesopodosomal area in its transversal section by using a micrometer coupled to a
stereomicroscope with 40 magni®cation.
The parasitism potential of A. lacunatus on R. dominica was assessed at 308C and 60% r.h.
Zero, 4, 6, 8, and 10 physogastric females of A. lacunatus were released in 500 ml glass jars
with whole wheat and 50 adults of R. dominica that were 3±7 days old. The jars, ®lled with
420 g of whole hard wheat (13% m.c.), were ringed with vaseline in their upper part and they
were covered with organza. After 45 and 60 days following infestation, the number of
surviving adults and ®rst instar larvae and the number of non-parasitized eggs of the lesser
grain borer were recorded by direct count after sieving the wheat. Eight replicates were used
for each treatment. The grain weight loss (%) during the period was also assessed by weighing
the grain before the infestation and 45 and 60 days afterwards, removing the ®ne material by
sieving prior to weighing the grain. The obtained data were subjected to correlation and
regression analysis. Correlation and linear regression analyses were done using the procedures
PROC CORR and PROC REG, respectively (SAS Institute, 1987). Non-linear regression
analyses were done using the curve ®tting procedure of SigmaPlot (Jandel Scienti®c, 1986).
3. Results
Temperature aected the size of physogastric female mites which reached maximum size
(1260 mm) at about 308C (Fig. 1A). The smallest physogastric mites (1195 mm) were observed
at the lowest and highest temperatures within the range studied (i.e., 20 and 418C).
Temperature also aected the number of ospring per physogastric female with larger number
of progeny (ca. 17/female) occurring at about 308C and decreasing at higher and lower
temperatures (Fig. 1B). At 418C, there was no production of ospring. There was a positive
correlation (r = 0.46, p < 0.0001) between maximum female size and fertility, where larger
females produced more progeny (Fig. 2).
Fig. 2. Correlation between maximum female size and progeny produced per female of Acarophenax lacunatus
feeding on eggs of Rhyzopertha dominica. ( p < 0.0001, r = 0.46, df =138, n = 141).
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
59
Fig. 3. Eect of the density of physogastric females of Acarophenax lacunatus on the suppression of eggs (A), ®rst
instar larvae (B), and adults (C) of Rhyzopertha dominica. Each symbol represents the average of eight replicates.
Evaluations were made after 45 (r) and 60 days (w) of the infestation. ( p < 0.01, r 2 > 0.80, df =38, n = 40).
60
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
Increasing densities of female mites increased egg parasitism (Fig. 3A) and reduced the
population size of ®rst instar larvae and adults of R. dominica (Fig. 3B and C). Densities as
low as two physogastric females per jar led to complete suppression of live ®rst instar larvae
and non-parasitized host eggs in 45 days. Full suppression of host adults took longer (i.e., 60 d)
and required higher mite densities (at least six physogastric females per jar). The increasing
densities of physogastric female mites also decreased the wheat weight loss due to damage by
the lesser grain borer (Fig. 4). Initial densities of ten female mites per jar decreased the grain
weight loss from 21 and 27% to 3 and 6% after 45 and 60 days respectively. Mite densities as
low as two per jar reduced the grain weight loss by over 50% compared to the control.
4. Discussion
The straw itch mite, Pyemotes tritici, is the best studied mite species with potential for
biological control of stored-product insects (Brower et al., 1996). This mite attacks all
developmental stages of Plodia interpunctella (HuÈbner) and Cadra cautella (Walker)
(Lepidoptera: Pyralidae), Oryzaephilus mercator (Fauvel) (Coleoptera: Cucujidae), and
Lasioderma serricorne (F.) (Coleoptera: Anobiidae) (Bruce and LeCato, 1979). However,
despite its great potential as a biological control agent, its commercial use has been limited
because it, like other members of the family Pyemotidae, can also bite humans (Moser, 1975;
Brower et al., 1996). Because the genus Acarophenax was initially described within this family,
there are questions regarding its safety or nuisance value to humans (Cross and Krantz, 1964;
Steinkraus and Cross, 1993; Matioli, 1997). However, the inspections of A. lacunatus while in
quarantine, in Brazil, by the SaÄo Paulo Vegetal Sanitation Service and the Brazilian Ministry
of Agriculture (Process 21.000.002807/95-82) did not provide any evidence of harmful eects
on man or mammals leading to its clearance for further studies. Steinkraus and Cross (1993)
Fig. 4. Eect of the density of physogastric females of Acarophenax lacunatus on grain weight loss (%) after 45 (r)
and 60 days (w) of the infestation. Each symbol represents the average of eight replicates. ( p < 0.05, r 2 > 0.75, df
=38, n = 40).
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
61
also observed no harmful eects of Acarophenax mahunkai (Steinkraus & Cross) on man or
higher animals.
Acarophenax spp leave the host during host oviposition, parasitize the host eggs, and feed on
the egg's contents. These mites kill the host egg and one host egg is usually sucient for
complete progeny development (Lindquist, 1983; Steinkraus and Cross, 1993). After mating,
mature female mites go into physogastry and numerous mites develop, reach adulthood, and
mate within the gravid females (Steinkraus and Cross, 1993). These same general life history
traits occur in A. lacunatus. This species also has the typical phoretic behavior not associated
with direct parasitization as described by Clausen (1976) and Ro (1991) which increases even
further the potential of this parasitic mite species as a biological control agent of R. dominica.
Acarophenax lacunatus is not a true parasite since it kills the host eggs, but it is not considered
a predator either, since the females feed in just one egg during their life time and this mite
species has a fast life cycle. Acarophenax lacunatus acts more like parasitoids according to
Lindquist (1983) although, like other species within the genus Acarophenax, it is usually
referred to as parasitic (Cross and Krantz, 1964; Faroni, 1992; Steinkraus and Cross, 1993;
Matioli, 1997). Adult males of Acarophenax spp are ephemeral and may not emerge from
physogastric females (Steinkraus and Cross, 1993), but single males of A. lacunatus do emerge
from physogastric females.
Temperature had a strong eect on female size and fertility. At temperatures around 308C,
physogastric females reach larger sizes and produce more progeny, probably maximizing the
suppression of its host population at this temperature range. Since R. dominica is an insect of
tropical origin (Potter, 1935) with a strong ability to ¯y (Dowdy, 1994; Guedes, Kambhampati
and Dover, 1997), the usefulness of A. lacunatus as a biological control agent of R. dominica
seems promising, especially where there is lack of alternative control methods to insecticides
(Guedes et al., 1996).
Parasitization by A. lacunatus was invariably fatal to eggs of lesser grain borer, as was also
reported for A. mahunkai attacking lesser mealworms, Alphitobius diaperinus (Panzer), by
Steinkraus and Cross (1993). This ability to reduce the population size of the lesser grain
borer, the short life cycle of A. lacunatus, its high fertility at temperatures around 308C, and
the lack of evidence of harmful eects on humans and higher animals, suggests that this mite
species may be a useful biological control agent of R. dominica, especially in tropical areas.
Acknowledgements
The authors would like to thank Drs. G.J. Moraes (Department of Zoology, University of
SaÄo Paulo, Piracicaba (SP), Brazil) and M.C. Picanc° o (Department of Animal Biology, Federal
University of Vic° osa, Vic° osa (MG), Brazil) for their helpful suggestions throughout this
investigation; and to Dr. F. Garcia-Mari (Department of Entomology, Valencia Polytechnic
University, Valencia, Spain) for providing the initial mite population used in our studies.
Financial support was provided by CAPES, CNPq and FAPEMIG and was greatly
appreciated.
62
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
References
Arbogast, R.T., 1984. Natural enemies as control agents for stored-product insects. In: Proceedings of the 3rd
International Working Conference on Stored-Product Protection, Manhattan, KS, pp. 360±374.
Brower, J.H., 1991. Replacing fumigants with bene®cial insects. California Agriculturist 2, 14±16.
Brower, J.H., Smith, L., Vail, P.V., Flinn, P.W., 1996. Biological control. In: Subramanyam, Bh, Hagstrum, D.W.
(Eds.), Integrated Management of Insects in Stored Products. Dekker, New York, pp. 223±286.
Bruce, W.A., 1983. Mites as biological control agents of stored product pests. In: Hoy, M.A., Cunningham, G.L.,
Knutson, L. (Eds.), Biological Control of Pests by Mites. University of California, Berkeley, pp. 74±78.
Bruce, W.A., LeCato, G.L., 1979. Pyemotes tritici: potential biological control agent of stored-product insects.
Recent Advances in Acarology 1, 213±220.
Clausen, C.P., 1976. Phoresy among entomophagous insects. Annual Review of Entomology 21, 343±367.
Cross, E.A., Krantz, G.W., 1964. Two new species of the genus Acarophenax Newstead and Duvall 1918
(Acarina:Pyemotidae). Acarologia 6, 287±295.
Debach, P., Rosen, D., 1991. Biological Control by Natural Enemies, 2nd ed. Cambridge University Press,
Cambridge, UK.
Dowdy, A.K., 1994. Flight initiation of lesser grain borer (Coleoptera:Bostrichidae) as in¯uenced by temperature,
humidity, and light. Journal of Economic Entomology 87, 1714±1717.
Faroni, L.R.D'A., 1992. Biologia y control del gorgojo de los granos Rhyzopertha dominica (F.). D.S. Thesis,
Universidad PoliteÂcnica de Valencia, Valencia, Spain.
Faroni, L.R.D'A., Garcia-Mari, F., 1992. In¯uencia de la temperatura sobre los paraÂmetros bioloÂgicos de
Rhyzopertha dominica (F.). Boletin de Sanidad Vegetal 18, 455±468.
Guedes, R.N.C., 1990. Manejo integrado para a protec° aÄo de graÄos armazenados contra insetos. Revista Brasileira
de Armazenamento 15, 3±48.
Guedes, R.N.C., Dover, B.A., Kambhampati, S., 1996. Resistance to chlorpyrifos-methyl, pirimiphos-methyl, and
malathion in Brazilian and U.S. populations of Rhyzopertha dominica (Coleoptera:Bostrichidae). Journal of
Economic Entomology 89, 27±32.
Guedes, R.N.C., Kambhampati, S., Dover, B.A., 1997. Allozyme variation among Brazilian and U.S. populations
of Rhyzopertha dominica resistant to insecticides. Entomologia Experimentalis et Applicata 84, 49±57.
Hoy, M.A., 1994. Parasitoids and predators in management of arthropod pests. In: Metcalf, R.L., Luckmann, W.H.
(Eds.), Introduction to Insect Pest Management, 3rd ed. Wiley, New York, pp. 129±198.
Howarth, F.G., 1991. Environmental impacts of classical biological control. Annual Review of Entomology 36,
485±509.
Jandel, Scienti®c, 1986. SigmaPlot Scienti®c Graphing Software Ð User's Manual. Jandel Scienti®c, San Rafael,
CA, USA.
Lindquist, E.E., 1983. Some thoughts on the potential for use of mites in biological control, including a modi®ed
concept of ``parasitoids''. In: Hoy, M.A., Cunningham, G.L., Knutson, L. (Eds.), Biological Control of Pests by
Mites. University of California, Berkeley, pp. 12±20.
Magowski, W.L., 1994. Discovery of the ®rst representative of the mite subcohort Heterostigmata (Arachnidae:
Acari) in the Mesozoic Siberian amber. Acarologia 35, 229±241.
Matioli, A.L. 1997. Biologia de Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) e seu
potencial de parasitismo sobre Rhyzopertha dominica (F.) (Coleoptera:Bostrichidae). M.S. Thesis, Universidade
Federal de Vic° osa, Vic° osa, MG, Brazil.
Moser, J.C., 1975. Biosystematics of the straw itch mite with special reference to nomenclature and dermatology.
Transactions of the Royal Entomological Society of London 122, 185±191.
Potter, C., 1935. The biology and distribution of Rhyzopertha dominica (Fab.). Transactions of the Royal
Entomological Society of London 83, 449±482.
Rakha, M.A., Kandeel, M.M.H., 1983. Acarophenax meropsi n. sp., from the European bee eater, Merops apiaster
in Egypt, (Acari:Tarsonemidae). Acarologia 24, 295±297.
Ro, D.A., 1991. Life history consequences of bioenergetic and biomechanical constraints on migration. American
Zoologist 31, 205±215.
SAS Institute, 1987. SAS/STAT User's Guide for Personal Computers, Version 6. SAS Institute, Cary, NC, USA.
L.R.D'A. Faroni et al. / Journal of Stored Products Research 36 (2000) 55±63
63
Simberlo, D., Stiling, P., 1996. How risky is biological control? Ecology 77, 1965±1974.
Steinkraus, D.C., Cross, E.A., 1993. Description and life history of Acarophenax mahunkai, n. sp. (Acari,
Tarsonemina: Acarophenaciedae), an egg parasite of the lesser mealworm (Coleoptera:Tenebrionidae). Annals of
the Entomological Society of America 86, 239±249.
Wood, R.K.S., Way, M.J. (Eds.), 1988. Biological control of pests, pathogens, and weeds: developments and prospects. Philosophical Transactions of the Royal Society of London Series B 318, 109±376.