Environmental Entomology Advance Access published January 30, 2015

POPULATION ECOLOGY

Temperature-Dependent Development and Reproductive Traits

of Tyrophagus putrescentiae (Sarcoptiformes: Acaridae)
Reared on Different Edible Mushrooms
S. X. QU, H. P. LI, L. MA, J. D. SONG,1 L. J. HOU, AND J. S. LIN
Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, 50 Zhongling Street, Nanjing 210014, China.

Environ. Entomol. 1–8 (2015); DOI: 10.1093/ee/nvu064

ABSTRACT China is the largest producer, consumer, and exporter of mushrooms in the world.
The storage mite, Tyrophagus putrescentiae Schrank, is one of the most important arthropod pests in
mushroom cultivation. This study investigated the development and reproductive traits of this mite
reared on four mushroom species: Agaricus bisporus Lange, Pleurotus ostreatus Kumm, Auricularia pol-
ytricha (Mont.) Sacc., and Flammulina velutipes (Fr.) Sing., at seven constant temperatures ranging
from 16 to 34 C at 80% relative humidity. Development time for the immature stages decreased with in-
creasing temperature, and was also significantly affected by mushroom species. The shortest immature
developmental period (7.0 6 0.2 d) was observed at 31 C when reared on F. velutipes, while the longest
development was at 16 C (36.0 6 0.3 d) reared on P. ostreatus. The effects of temperature and mush-
room hosts on the development, female longevity, and reproduction were also significant. The lower
threshold temperatures from egg-to-adult for the four mushroom species were 11.97, 12.02, 10.80, and
11.57 C, for A. bisporus, P. ostreatus, Au. polytricha, and F. velutipes, and the thermal constants were
133.3, 136.8, 165.2, and 135.9 degree days ( C d), for the same mushroom species, respectively. Life ta-
ble parameters at 25 C were estimated as follows: net reproductive rates (R0), 59.16, 28.94, 42.62, and
62.93, and intrinsic rate of natural increase (rm), 0.24, 0.13, 0.17, and 0.24, respectively. These results
suggest that these mushrooms are suitable hosts for T. putrescentiae, and the storage mite may be able to
adapt to higher temperatures.

KEY WORDS mushroom pest, trophic level, storage mite, flour mite

Introduction humid environments, and enter dormancy under dry

Mushrooms are the sixth largest crop in China, follow-
ing cereal, cotton, oil, vegetables, and fruit. Total mush-
room production reached 21 million tons in 2010, with
a value of US$21.1 billion (Li 2011). Mushrooms can
convert agricultural and forestry wastes such as cotton-
seed hulls, wheat bran, sawdust, bagasse, manure,
straw, and bark into food. Different species, varieties,
and strains of mushrooms require different substrate
resources and physical environments, and differ in their
physiology (Dong and Wang 2008, Qin and Qin 2010).
Approximately 100 arthropod species, including 43
mite species, are found in China that cause direct or in-
direct damage to mushrooms by feeding on mycelia
and mushroom fruit bodies. In particular, mites in the
families Acaridae, Aeroglyphidae, Glycyphagidae, Pyg-
mephoridae, Tarsonemidae, and Histiostomatidae have
been identified as economically important pests (Zou
and Gao 1987; Zou and Wang 1989; Zou et al. 1992,
1994; Jiang and Li 2005; Lan et al. 2012). Mites are
typically present in both facilities for production of
mushroom spawn and in spawning rooms (Wu and Yu
1996). Mushroom mites develop best in warm and
1
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C The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America.
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conditions (Wu and Yu 1996). While mites may be scat-
tered and difficult to observe in the early stages of their
population growth, large aggregates form as densities
increase, causing noticeable damage, and even destroy-
ing whole crops (Wu and Lu 1996, Lan et al. 2012).
Tyrophagus putrescentiae Schrank is a common,
worldwide pest of stored grain (Zhang and Jin 1960,
Hughes 1976, Chmielewski 1978, Eraky 1995) that also
feeds on many different fungi, including species of
Fusarium, Trichoderma, and various edible fungi.
(Smrz and Catska 1989; Zhang et al. 1992; Eraky 1995;
Hubert et al. 2004, 2012; Nesvorná et al. 2012). It can
vector pathogens, such as Aspergillus flavus Link and
Fusarium poae (Peck) Wollenw to sterile grain and
mushroom beds, and can also promote nonbeneficial
fungal growth, increasing aflatoxin and deoxynivalenol
production (Franzolin et al. 1999, Hubert et al. 2013b).
T. putrescentiae infests the mycelia and fruiting bodies
of edible mushrooms, decreasing production and caus-
ing mildews on dried mushrooms, human allergic der-
matitis, pulmonary acariasis, and intestinal acariasis (Li
et al. 2003, Jeong et al. 2007). The mite seriously af-
fects both the economic efficiency of mushroom pro-
duction and the health of mushroom growers (Zhang
et al. 1992). Previous studies have found its mushroom
hosts to include Lentinula edodes Berk, Agaricus
2 ENVIRONMENTAL ENTOMOLOGY
bisporus Lange, Pleurotus ostreatus Kumm, Gano-
derma lucidum (Leyss. ex Fr.) Karst, and Pleurotus pul-
monarius Fr. (Zou and Gao 1987, Zhang et al. 1992).
In China, A. bisporus, Flammulina velutipes (Fr.)
Sing., P. ostreatus, Auricularia spp., and L. edodes are
the most popular commercially cultivated mushrooms
(Li 2011). In 2010, the output of each of these species
was more than one million tons (Li 2011). However,
the damage to mushrooms caused by pests can be con-
siderable. One study reported finding 539 adult T.
putrescentiae mites feeding on a single fruit body (3 cm
in diameter) of P. ostreatus (Zhang et al. 1992). So far,
only one study (Kheradmand et al. 2007) has reported
the effects of temperature and species of edible fungi
on the development, life table parameters, and thermal
requirements of T. putrescentiae. Their results showed
that the net reproductive rate (R0) and the intrinsic
rate of increase (rm) of this mite were significantly dif-
ferent between A. bisporus and P. ostreatus at 25 C
and 70% relative humidity (RH; Kheradmand et al.
2007). Because of its importance, more information is
needed on the biology of T. putrescentiae in major
mushroom species and varieties to better guide its pest
management. The aim of this study is to determine the
effects of temperature and mushroom host (using the
four major commercial species produced in China) on
the development, reproduction, temperature thresh-
olds, and thermal constants of this mite at seven con-
stant temperatures from 16 to 34 C at 80% RH,
reflecting production conditions.
Materials and Methods
Mite and Mushroom Culture. The storage mites
used in this study were supplied from stock cultures
originating from a population collected in 2012 on
wood ear mushroom, Auricularia polytricha (Mont.)
Sacc., in Feng County (Jiangsu, China), which reared
on nine different mushroom species (Au. polytricha,
Lentinula edodes Berk, Agaricus bisporus Lange, Pleu-
rotus ostreatus Kumm, Flammulina velutipes (Fr.)
Sing., P. pulmonarius Fr., P. eryngii var. tuoliensis Mou,
Ganoderma lucidum (Leyss. ex Fr.) Karst, and Agro-
cybe cylindracea (Dc. ex Fr.) Maire in the laboratory at
25 C and approximately 85% RH.
One week before the start of our experiments,
the mycelia of the four mushroom species to be used
(Table 1: A. bisporus, P. ostreatus, Au. polytricha, and F.
velutipes) were inoculated onto potato dextrose agar
plates in 50-mm-diameter Petri dishes. The strains were
obtained from Agricultural Culture Collection of China.
The dishes were covered with lids and held in a growth
chamber at 25 C and 80% RH in complete darkness.
Table 1. The edible mushroom species used in this study
No. Species Strain no.
1 Agaricus bisporus AS2796
2 Pleurotus ostreatus heiping
3 Auricularia polytricha Fengmao No. 3
4 Flammulina velutipes Danbaijin
Development Times of Immature Mites. When
the mycelia covered the surface of inoculated Petri
dishes (50 mm in diameter), mated female mites were
transferred into the dishes (each female was isolated in
a dish), which were held in groups of ten at each of
seven different temperatures (16, 19, 22, 25, 28, 31,
and 34 6 1 C) at 80 6 5% RH in the dark. Newly laid
(1 d old) eggs were separated with a hair brush onto 10
new 50-mm Petri dishes containing the corresponding
host mushroom mycelia using an S8APO dissection
microscope (Leica, Wetzlar, Germany). Each Petri dish
received 7–10 eggs of the same age. The Petri dishes
were covered with Parafilm (Bemis, Neenah, WI) wrap
and placed in an SPX-2501C type growth chamber
(Suzhou Jiangdong Precision Instrument Co., Ltd.,
China). The developmental stage of each individual
was then recorded every 12 h until all mites either died
or became adults.
The relationship between temperature and develop-
mental rate was estimated by the line-fitting method
proposed by Ikemoto and Takai (2000):
DT ¼ k þ tD ½For T > t
where D is the development time (d), T is environmen-
tal temperature ( C), t is the lower threshold tempera-
ture, and k is the thermal constant.
Mite Reproduction and Female
Longevity. Newly molted adult female mites were
transferred individually into new 50-mm Petri dishes
containing the corresponding host mushroom mycelia,
together with one adult male that was obtained from
stock cultures and introduced for mating. Males were
removed from dishes after 24 h. Thirty replicates (one
female þ pair per dish) per mushroom species were
created to measure reproduction and female longevity.
The Petri dishes were observed every day at 9:00 am
and 3:00 pm, and the preoviposition, oviposition, and
postoviposition periods were recorded, along with adult
female longevity.
Egg Hatch, Mite Survival, and Sex Ratio. Newly
laid eggs were removed from female mites daily with
an artist paint brush, and the eggs held to determine
egg hatch, the survival of immature stages, and the pro-
portion of female offspring at 25 6 1 C. Those data
were recorded and used to calculate the age-specific
survival rate (lx) and the age-specific fecundity rate
(mx). The number of eggs laid by each female was
recorded daily throughout her lifetime to determine
fecundity.
Life-Table Parameters. Life tables were con-
structed from the observed survival and fecundity rates
of individuals. Parameters at 25 6 1 C were calculated
Family and genus Origin
Agaricales, Agaricaceae, Agaricus China, Fujiang
Agaricales, Pleurotaceae, Pleurotus China, Jiangsu
Auriculariales, Auriculariaceace, Auricularia China, Jiangsu
Agaricales, Tricholomataceae, Flammulina China, Jiangsu
2015 QU ET AL.: EFFECTS OF TEMPERATURE AND HOSTS ON T. putrescentiae
using Andrewartha and Birch’s method (1954). The rm
was estimated by nonlinear regression according to:
X degree-days (Table 3). Among life stages, the lower
ðexp ðrm xÞlx mx Þ ¼ 1
where x is the female age in days, lx is the fraction of
females surviving to age x (age-specific survival rate),
and mx is the expected number of daughters produced
per female alive at age x (age-specific fecundity rate),
obtained by multiplying the number of eggs by the
age-specific sex ratio, which is defined as the propor-
tion of females in the progeny (Roy et X al. 2002). Net
reproductive rate (R0) is given by R0 ¼ lx mx, mean
generation time (t) in days by t ¼ In R0 =rm, finite rate
of increase (k) by k ¼ erm , and doubling time (DT) by
DT ¼ In 2=rm .
Data Analysis. The effects of temperature on the
different immature survival, along with adult reproduc-
tive and longevity parameters were analyzed by analysis
of variance (ANOVA) followed by an SNK test
(P ¼ 0.05) using IBM SPSS Statistics 20.0 (Ma et al.
2005, SPSS Inc 2012). Before analysis, data were
checked for heterogeneity of variances.
The effect of mushroom host on the life table param-
eters at 25 6 1 C, and 80 6 5% RH were calculated
using Andrewartha and Birch’s method by nonlinear
regression (1954). Because both temperature and
mushroom host affected these parameters, two-way
ANOVA was used to evaluate their effects. Means were
compared using the SNK test (P ¼ 0.05) using IBM
SPSS Statistics 20.0.
Results
Effect of Temperature. Development times
of immature stages reared on all mushroom hosts dif-
fered significantly between temperatures (165.369 <
F6, 623 < 1770.113, P < 0.0001), expect for the larval
stage when reared on Au. polytricha (F6, 623 ¼ 777.415,
P ¼ 0.407; Table 2). The mean developmental time of
each stage decreased linearly with temperature from 16
to 31 C, but then increased at 34 C.
Egg had the longest stage duration among the
immature life stages on all mushrooms at 19 to 25 C
and the shortest stage at 16 C, while the larvae
stage was the longest at 28 to 34 C. The protonymph
and tritonymph stages were the shortest on all
tested mushrooms at 19 to 34 C except for the trito-
nymph at 19 C and the protonymph at 22 C reared on
Au. polytricha. The effect of temperature on proto-
nymph and tritonymph stages was greater than on
other stages. For example, the protonymph and trito-
nymph stages lasted 2 d at 31 C when reared on P.
ostreatus, but were 5 and 7 times longer at 16 C,
respectively.
The correlation coefficient for all immature develop-
mental stages was high, which suggested that the linear
model accurately described the effect of temperature
on T. putrescentiae’s developmental rate. The lower
threshold temperatures for the summed egg-to-adult
period varied among mushroom species from
3
10.80 6 1.49 C to 12.02 6 1.46 C, while the thermal
constant for the same life period ranged, among mush-
room species, from 133.31 6 26.64 to 165.21 6 24.61
threshold temperatures for egg, larva, protonymph, and
tritonymph varied from 7.41 6 2.30 to 13.99 6 1.10 C
(Au. polytricha), 9.95 6 2.06 to 13.21 6 1.66 C (A. bis-
porus), 10.10 6 3.34 to 13.16 6 0.87 C (P. ostreatus),
and 12.46 6 1.22 to 14.05 6 0.86 C (F. velutipes),
respectively.
The duration of preoviposition, ovipositional, and
postovipositional periods and female longevity were
all significantly influenced by temperature (36.334 <
F6, 203 < 398.540, P < 0.0001). The preoviposition peri-
ods for all mushroom varieties decreased with increas-
ing temperatures up to 31 C and then increased at
34 C (Table 4). Female longevity also decreased as the
temperature increased. On A. bisporus, the shortest
preoviposition duration occurred at 31 C, while on
other mushrooms, it occurred at 28 C and varied from
2.5 6 0.1 to 13.3 6 0.1 d (Table 4). The oviposition
period was the longest stage of the reproductive period
on all hosts.
Effect of Mushroom Hosts on Mite Life
History. Significant differences were observed in
immature development among different mushroom
hosts at the same temperature (4.050 < F6, 356
< 226.082, P < 0.013), except for the tritonymph stage
at 34 C (F6, 356 ¼ 0.297, P ¼ 0.828; Table 2). The lon-
gest total developmental time occurred when the mite
was reared on P. ostreatus, followed by those raised on
A. bisporus, Au. polytricha, and F. velutipes, in
descending order at 16 and 19 C; from 22 to 34 C, the
longest development was observed on Au. polytricha
and the shortest was on A. bisporus and F. velutipes.
Means of each stage were not significantly different
among P. ostreatus, A. bisporus, and Au. polytricha at
22 and 25 C, and no differences were observed
between 28 and 31 C when the mite was reared on
P. ostreatus.
Mushroom hosts had a significant effect on female
longevity (20.210 < F3, 116 < 26.724, P < 0.0001) and
reproductive periods (1.488 < F3, 116 < 25.407,
P < 0.043) at 16, 22, and 34 C, but less effect at 19 C
(1.488 < F3, 116 < 4.562, 0.045 < P < 0.222). Moreover,
no significant differences were observed among
mushroom hosts in the preoviposition stage at 28 C,
the ovipositional stage at 25 C, and female longevity
at 31 C when reared on the four mushroom hosts
(Table 4).
Meanwhile, the age-specific survival (lx) and fecund-
ity (mx) rates were affected by mushroom species
(Figs. 1 and 2). The first death of adult females
occurred after 13 d at 25 C when T. putrescentiae fed
on the three Agaricales species, but was at 15 d when
they fed on the Auriculariales species Au. polytricha.
The immature survival rate was 100% for all four
mushroom hosts at 25 C and 80% RH. Female fecund-
ity (egg per female per day) peaked on day 15 at about
14 eggs per female per day when reared on A. bisporus
and F. velutipes. However, when reared on P. ostreatus
and Au. polytricha, fecundity fluctuated during the
4 ENVIRONMENTAL ENTOMOLOGY

Table 2. Mean ( 6 SEM) of the development durations (d) for T. putrescentiae reared on different mushroom diets at seven different
temperatures (80% RH)

Host (n ¼ 90) Temp ( C) Stage

Egg Larvae Protonymph Tritonymph Total

A. bisporus 16 6.5 6 0.1aB 9.6 6 0.1aA 9.2 6 0.1aB 9.5 6 0.2aB 34.8 6 0.3aB
19 5.6 6 0.1bB 3.2 6 0.1bB 3.2 6 0.1bB 2.7 6 0.1bBC 14.7 6 0.1bB
22 3.1 6 0.1cC 2.4 6 0.1cB 2.0 6 0.1dC 1.9 6 0.1cA 9.4 6 0.1cB
25 3.0 6 0.1cB 2.4 6 0.1cB 1.8 6 0.1dC 1.6 6 0.1dAB 8.8 6 0.1cdB
28 2.4 6 0.1dA 2.6 6 0.1cB 1.3 6 0.1eC 2.1 6 0.0cA 8.4 6 0.1dB
31 1.7 6 0.1eB 2.1 6 0.0dC 0.9 6 0.0fC 2.5 6 0.1bA 7.2 6 0.1eC
34 2.5 6 0.1dA 2.8 6 0.1bcB 2.5 6 0.1cC 1.6 6 0.1d 9.4 6 0.1cAB
P. ostreatus 16 7.8 6 0.2aA 7.6 6 0.2aC 9.2 6 0.1aB 11.4 6 0.1aA 36.0 6 0.3aA
19 6.3 6 0.1bA 4.5 6 0.2bA 3.4 6 0.1bA 2.8 6 0.1bB 17.0 6 0.3bA
22 3.0 6 0.1cC 2.5 6 0.1dB 2.2 6 0.1cB 1.8 6 0.1cAB 9.5 6 0.1cB
25 2.8 6 0.1cB 2.5 6 0.1dB 2.1 6 0.1cB 1.5 6 0.1cB 8.9 6 0.1cB
28 1.8 6 0.1dC 3.2 6 0.1cA 1.7 6 0.1dB 1.6 6 0.1cB 8.3 6 0.2dB
31 1.6 6 0.1dB 3.3 6 0.1cA 1.6 6 0.1dB 1.5 6 0.1cB 8.0 6 0.1dB
34 2.0 6 0.1dB 2.1 6 0.1eC 3.3 6 0.1bA 1.6 6 0.1c 9.0 6 0.0cB
Au. polytricha 16 5.7 6 0.2aC 9.4 6 0.2aA 9.6 6 0.0aA 9.5 6 0.1aB 34.2 6 0.2aB
19 4.7 6 0.1bC 3.1 6 0.0bB 2.7 6 0.1cC 3.7 6 0.1bA 14.2 6 0.1bC
22 4.2 6 0.1cA 2.9 6 0.1bA 3.1 6 0.1bA 2.0 6 0.1cA 12.2 6 0.1cA
25 4.3 6 0.1cA 2.8 6 0.1bA 3.1 6 0.1bA 1.9 6 0.1cA 12.1 6 0.1cA
28 2.0 6 0.1eB 2.9 6 0.1bA 2.4 6 0.1dA 2.2 6 0.0cA 9.5 6 0.1dA
31 1.8 6 0.1eB 3.2 6 0.1bA 3.2 6 0.1bA 1.5 6 0.1dB 9.7 6 0.1dA
34 2.6 6 0.1dA 3.1 6 0.1bC 2.9 6 0.1cB 1.7 6 0.1dC 9.3 6 0.1dA
F. velutipes 16 6.0 6 0.1aC 8.5 6 0.1aB 8.1 6 0.1aC 9.1 6 0.1aC 31.7 6 0.2aC
19 4.9 6 0.1bC 3.6 6 0.1bB 2.4 6 0.0bD 2.6 6 0.0bC 13.5 6 0.1bD
22 3.6 6 0.1cB 3.2 6 0.1cA 1.3 6 0.1dD 1.6 6 0.1cB 9.7 6 0.1cB
25 3.0 6 0.1dB 2.7 6 0.1eAB 1.7 6 0.1cC 1.7 6 0.1cAB 9.1 6 0.2dB
28 2.3 6 0.1eAB 3.2 6 0.1cA 1.1 6 0.0dD 1.0 6 0.0dC 7.6 6 0.1eC
31 2.1 6 0.1eA 2.8 6 0.2dB 1.1 6 0.1dC 1.0 6 0.1dC 7.0 6 0.2fC
34 2.4 6 0.1eAB 3.1 6 0.1cA 1.4 6 0.1cD 1.6 6 0.1c 8.5 6 0.1dC
n, number of mites tested.
Means followed by different small letters within the same column indicated that the development durations are significantly different for the
same host at different temperature (SNK test: P < 0.05).
Means followed by different capital letters within the same column indicated that the development durations are significantly different for dif-
ferent hosts at the same temperature (SNK test: P < 0.05).

Table 3. Mean ( 6 SEM) for lower thermal thresholds (T), thermal constants (K), and estimates for the linear regression analyses of
T. putrescentiae growth stages on different mushroom hosts

Host Stage T ( C) K(degree-days) Equation R2

A. bisporus Egg 9.95 6 2.06 44.58 6 8.05 R ¼ 0.223 þ 0.022T 0.908
Larva 12.21 6 2.15 36.05 6 9.38 R ¼ 0.339 þ 0.028T 0.931
Protonymph 13.76 6 1.93 22.80 6 7.69 R ¼ 0.604 þ 0.044T 0.954
Tritonymph 13.21 6 1.66 26.75 6 6.76 R ¼ 0.494 6 0.037T 0.963
Total 11.97 6 1.66 133.31 6 26.64 R ¼ 0.090 þ 0.008T 0.955
Au. polytricha Egg 7.41 6 2.30 53.97 6 8.60 R ¼ 0.137 þ 0.019T 0.821
Larva 10.18 6 2.26 46.86 6 9.54 R ¼ 0.217 þ 0.021T 0.896
Protonymph 14.34 6 2.99 20.18 6 10.51 R ¼ 0.710 þ 0.050T 0.907
Tritonymph 13.99 6 1.10 18.19 6 4.14 R ¼ 0.769 þ 0.050T 0.985
Total 10.80 6 1.49 165.21 6 24.61 R ¼ 0.065 þ 0.006T 0.956
F. velutipes Egg 12.46 6 1.22 33.41 6 5.20 R ¼ 0.370 þ 0.030T 0.977
Larva 10.09 6 3.00 46.71 6 12.20 R ¼ 0.216 þ 0.021T 0.833
Protonymph 13.27 6 2.95 30.26 6 12.32 R ¼ 0.438 þ 0.033T 0.896
Tritonymph 14.05 6 0.86 21.23 6 3.98 R ¼ 0.662 þ 0.047T 0.991
Total 11.57 6 2.15 135.86 6 32.10 R ¼ 0.085 þ 0.007T 0.924
P. ostreatus Egg 10.10 6 3.34 45.62 6 12.82 R ¼ 0.221 þ 0.022T 0.804
Larva 11.18 6 3.01 46.24 6 13.82 R ¼ 0.242 þ 0.022T 0.853
Protonymph 12.65 6 2.08 34.24 6 9.12 R ¼ 0.370 þ 0.029T 0.939
Tritonymph 13.16 6 0.87 25.89 6 3.64 R ¼ 0.508 þ 0.039T 0.978
Total 12.02 6 1.46 136.82 6 24.47 R ¼ 0.088 þ 0.007T 0.965

ovipositional period. Overall, mite fecundity was
affected by diet and was higher on A. bisporus and
F. velutipes.
The rm and k parameters reached their maximum
reared on F. velutipes and A. bisporus, followed by P.
ostreatus and Au. polytricha (Table 5). The rm value
varied from 0.13 to 0.24 and k from 1.14 to 1.27. The
mean generation time (t) was 19.88, 19.52, 27.16, and
28.61 d, for F. velutipes, A. bisporus, P. ostreatus, and
Au. polytricha, respectively. These results indicated
that all the demographic parameters were affected by
diet.
2015 QU ET AL.: EFFECTS OF TEMPERATURE AND HOSTS ON T. putrescentiae 5

Table 4. Mean ( 6 SEM) of preovipositional, ovipositional, postovipositional periods, and female longevity values for T. putrescentiae
reared on different mushroom hosts

Host (n ¼ 30) Temp. ( C) Stage

Preoviposition Oviposition Postoviposition Female longevity

A. bisporus 16 6.6 6 0.2aB 23.4 6 0.3aB 11.2 6 0.2bB 41.2 6 0.3aC
19 4.3 6 0.2cA 23.4 6 0.3a 11.2 6 0.2b 38.9 6 0.4a
22 5.8 6 0.2bB 22.4 6 0.3bC 11.9 6 0.4a 40.1 6 0.3aB
25 4.2 6 0.2cAB 22.3 6 0.2b 11.8 6 0.1aC 38.5 6 0.3aB
28 2.7 6 0.1e 23.6 6 0.3aA 10.0 6 0.1cB 32.0 6 2.1bB
31 2.1 6 0.2fC 20.8 6 0.2cAB 9.4 6 0.1dA 31.5 6 0.3b
34 3.2 6 0.2dA 18.7 6 0.1dA 2.9 6 0.1eAB 24.8 6 0.2cA
P. ostreatus 16 7.6 6 0.2aA 23.8 6 0.3aAB 12.9 6 0.1aA 44.3 6 0.4aA
19 3.7 6 0.2cB 23.3 6 0.ab 11.9 6 0.3b 38.9 6 0.4c
22 6.4 6 0.2bA 24.0 6 0.3aA 12.7 6 0.2a 43.1 6 0.5bA
25 3.7 6 0.2cB 22.7 6 0.3b 13.3 6 0.1aA 39.5 6 0.4cA
28 2.3 6 0.1e 21.8 6 0.2cB 11.3 6 0.3cA 35.4 6 0.2dA
31 2.7 6 0.2deA 20.3 6 0.3dBC 8.3 6 0.1dB 31.4 6 0.4e
34 3.1 6 0.1dA 17.6 6 0.2eB 3.2 6 0.2eA 23.8 6 0.2fB
Au. polytricha 16 6.8 6 0.1aB 24.4 6 0.2aA 11.4 6 0.2bB 42.6 6 0.3aB
19 4.4 6 0.1bcA 24.4 6 0.2a 11.2 6 0.3b 40.0 6 0.3bB
22 4.7 6 0.1bC 23.5 6 0.3bAB 11.7 6 0.2b 39.9 6 0.4bB
25 4.1 6 0.1cAB 22.7 6 0.1b 12.8 6 0.1aB 39.7 6 0.2bA
28 2.1 6 0.2d 23.5 6 0.3bA 11.1 6 0.4bA 36.7 6 0.3cA
31 2.4 6 0.2dAB 21.2 6 0.3cA 7.0 6 0.3cC 30.2 6 0.4d
34 2.1 6 0.1dB 16.6 6 0.3dC 3.4 6 0.2dA 22.1 6 0.4eC
F. velutipes 16 5.2 6 0.2aC 24.2 6 0.3aAB 11.8 6 0.3bB 41.2 6 0.3aC
19 3.8 6 0.2dB 23.5 6 0.4ab 11.8 6 0.3b 39.1 6 0.6b
22 4.9 6 0.2bcC 22.9 6 0.3bcBC 11.7 6 0.2b 39.5 6 0.2bB
25 4.4 6 0.2cA 22.4 6 0.3c 13.3 6 0.1aA 39.7 6 0.3bA
28 2.5 6 0.1f 23.6 6 0.1abA 10.4 6 0.3cAB 36.5 6 0.3cA
31 3.0 6 0.1eA 20.0 6 0.1dC 8.0 6 0.3dB 30.9 6 0.5d
34 3.1 6 0.1eA 19.4 6 0.4dA 2.5 6 0.1eB 25.0 6 0.3eA
n, number of mites tested.
Means followed by different small letters within the same column indicated that the development durations are significantly different for the
same host at different temperature (SNK test: P < 0.05).
Means followed by different capital letters within the same column indicated that the development durations are significantly different for dif-
ferent hosts at the same temperature (SNK test: P < 0.05).

Fig. 1. Age-specific survival rate (lx) curves for T. putrescentiae reared on four mushroom hosts at 25 C and 80% RH.
6 ENVIRONMENTAL ENTOMOLOGY

Fig. 2. Age-specific fecundity rate (mx) curves for T. putrescentiae reared on four mushroom hosts at 25 C.

Table 5. Parameters of population increase for T. putrescen- time for each immature stage decreased linearly with
tiae reared on four mushrooms at 25 C and 80% RH temperature from 16 to 31 C, but increased at 34 C.
Hubert et al. (2013a) found that the optimum tempera-
Hosts rm R0 t DT k
ture for T. putrescentiae development to be 30 C,
A. bisporus 0.24 59.16 19.52 2.14 1.27 which corresponds with this study’s findings. The pro-
P. ostreatus 0.17 42.62 27.16 2.49 1.18 tonymph, tritonymph, and post-ovipositional stages
Au. polytricha 0.13 28.94 28.61 2.73 1.14
F. velutipes 0.24 62.94 19.88 2.12 1.27 were more variable at different temperatures when
reared on the same diet.
Mushroom species strongly affected population
Interactions of Temperature and Mushroom dynamics, in agreement with Kheradmand et al.
Hosts. Two-way ANOVA showed that both (2007). In our study, the four mushroom species tested
temperature and mushroom species significantly all significantly affected the development, reproduc-
affected immature development times (27.744 < tion, and female longevity at 16 to 34 C and 80% RH.
F18, 1919 < 61.219, P < 0.0001), female longevity The duration of immature development was shortest
(F6, 839 ¼ 6.234, P < 0.0001), and reproductive periods (about 7 d) when reared on F. velutipes at 31 C, and
(7.038 < F6, 839 < 11.842, P < 0.0001). In addition, the longest (about 36 d) when reared on P. ostreatus at
interaction between temperature and different mush- 16 C. Other researchers have observed the influence
room hosts was significant (Table 6). of food types on the immature development and repro-
ductive characteristics of T. putrescentiae (Eraky 1995;
Hubert et al. 2012, 2013a). The comparison of previous
Discussion studies for lower temperature threshold was compli-
Our study examined the interaction between four cated by the tested strains of fungi and humidity. In
species of edible fungi and T. putrescentiae mites. The our study, the lower temperature threshold of the mite
two-way ANOVA results revealed that with the excep- was 11.97 C when reared on A. bisporus, which was
tion of the egg stage, the development, reproduction, higher than 8.74 C, as reported by Kheradmand et al.
and female longevity of T. putrescentiae were all signifi- (2007), and different from those reared on other mush-
cantly affected by both mushroom host and tempera- room species in previous studies. Kheradmand et al.
ture. Thus, a predictive model of T. putrescentiae (2007) also reported that the rm values were 0.20 and
development rate should take both the temperature 0.12 on A. bisporus and P. ostreatus, respectively, which
and host into consideration (Hubert et al. 2013b). were lower than those reared on our mushroom vari-
As for most ectothermic animals, temperature signifi- eties, AS 2796 and heiping. Edible fungi are rich in
cantly affected the development, female longevity, and proteins and essential amino acids, with protein content
reproduction of T. putrescentiae. The development accounting for 10–50% of dry weight. In addition, they
2015 QU ET AL.: EFFECTS OF TEMPERATURE AND HOSTS ON T. putrescentiae
Table 6. ANOVA statistics for main effects and interactions of temperature (Temp) and mushroom diet (Food)
Stage Temp Food
(df ¼ 6, 1919 and 839, respectively) (df ¼ 3, 1919 and 839, respectively)
F P F P
Egg 905.178 <0.0001
Larvae 1918.272 <0.0001
Protonymph 5592.741 <0.0001 201.697
Tritonymph 5352.953 <0.0001
Egg to adult 13172.672 <0.0001 126.615
Preovipositional 341.677 <0.0001
Ovipositional 265.740 <0.0001
Postovipositional 962.114 <0.0001
Female longevity 597.271 <0.0001
contain carbohydrates, lipids, vitamins, minerals, and
other nutrients. Au. polytricha is composed of 7.9% pro-
tein and 64.8% carbohydrates, while P. ostreatus con-
tains 15.8 and 52.1%, F. velutipes contains 14.8 and
43.3%, and A. bisporus contains 25.0 and 44.0%, respec-
tively, on a dry weight basis (Liu et al. 1997, Zhu et al.
2003). Our results suggest that F. velutipes and A. bispo-
rus are favorable foods, having the highest rate of popu-
lation increase for T. putrescentiae. A previous study
determined that a T. putrescentiae population increased
by 318.5 times, 316.7 times, and 179.9 times over 6 wks
when yeast powder, glucose, and sugar was added to the
basic wheat bran diet, respectively (Huang et al. 2013).
Hubert et al. (2012) compared the mite development
rates on 14 strains of seven Fusarium species and dis-
covered that the rates were significantly different among
strains, even when the same strain was inoculated onto
different culture mediums. Similar results were reported
by Franzolin et al. (1999), who demonstrated that T.
putrescentiae grew better in grain inoculated with Asper-
gillus flavus than on un-inoculated grain. These studies
have shown that different cultivars or strains of fungi
hosts (differing in nutritional content) affect the devel-
opment of mites, making these cultivars or strains varia-
bles of a predictive model.
The results of this study were consistent with the
view that hosts strongly influence the population
increase of pests. We found that T. putrescentiae pre-
fers to feed on F. velutipes and A. bisporus, and in
addition prefers higher temperatures. These insights
will help develop a mite phenology model that can be
used to predict population dynamics for pest manage-
ment under field conditions.
Acknowledgments
This work was financially supported by the earmarked
fund for Modern Agro-industry Technology Research System
of China (No: CARS-24). We also thank for the English edit-
ing provided by Van Driesche Scientific Editing.
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Received 29 August 2014; accepted 5 December 2014.