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249
Journal of Entomological
Society of Iran
2017, 36(4): 249-257
Comparative life table of Aphis craccivora (Hem.: Aphididae) on host plant, Robinia
pseudoacacia under natural and laboratory conditions
R. Jalalipour, A. Sahragard*, Kh. Madahi andA. Karimi-Malati
Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran.
*Corresponding author, E-mail: sahragard@guilan.ac.ir, ahad.sahragard@gmail.com
Abstract
The cowpea aphid, Aphis craccivora Koch, is an important pest of Robinia pseudoacacia Frisia. The life table
parameters of A. craccivora were determined under natural (16- 33ºC and 32-89% RH) and laboratory (25 ± 1ºC, 70 ±
5% RH and a photoperiod of 16:8 h (L: D) conditions. The data were analyzed using the age-stage, two-sex life table
theory. Each experiment was replicated 45 times for each condition. There were significant differences between the
survivorship, fecundity and longevity of the A. craccivora in laboratory and natural conditions. Under natural
conditions, A. craccivora had a significantly shorter nymphal developmental time, adult longevity and life span than
those reared under laboratory condition. However, the intrinsic rate of increase (r), net reproductive rate (R0), the finite
rate of increase (λ) and gross reproductive rate (GRR) in laboratory were higher than those obtained in the field except
for higher mean generation time (T) resulted from field experiment. The results provide better understanding of the
population dynamics of A. craccivora under field condition to effectively control the pest through integrated pest
management (IPM) programs.
Keywords: Aphis craccivora, generation time, intrinsic rate of increase, life table parameters, natural condition
هﺪﯿﮑﭼ
ﻪﺴﯾﺎﻘﻣ ﯽﮔﺪﻧز لوﺪﺟ ياAphis craccivora (Hem: : Aphididae) ﯽﻫﺎﯿﮔ نﺎﺑﺰﯿﻣ يورRobinia pseudoacacia هﺎﮕﺸﯾﺎﻣزآ و ﻪﻋرﺰﻣ ﻂﯾاﺮﺷ رد
ﯽﻤﯾﺮﮐ هدازآ و ﯽﺣاﺪﻣ ﻪﺠﯾﺪﺧ ،دﺮﮔاﺮﺤﺻ ﺪﺣا ،رﻮﭘ ﯽﻟﻼﺟ ﺎﺿر
-
ﯽﻃﻼﻣ
،ﺎﯿﻗﺎﻗا ﻪﺘﺷAphis craccivora Koch،ﺎﯿﻗﺎﻗا ﻢﻬﻣ ﺖﻓآFrisiaRobinia pseudoacaciaﺖﺳا.ﯽﮔﮋﯾوﯽﮔﺪﻧز لوﺪﺟ يﺎﻫ
A. craccivoraﯽﻌﯿﺒﻃ ﻂﯾاﺮﺷ رد) يﺎﻣد16
-
33 ﯽﺒﺴﻧ ﺖﺑﻮﻃر و سﻮﯿﺴﻠﺳ ﻪﺟرد32
-
89ﺪﺻرد ( ﯽﻫﺎﮕﺸﯾﺎﻣزآ و) يﺎﻣد1±25 ﻪﺟرد
،سﻮﯿﺴﻠﺳ5±70 يرﻮﻧ هرود و ﺪﺻرد16 و ﯽﯾﺎﻨﺷور ﺖﻋﺎﺳ8ﯽﮑﯾرﺎﺗ ﺖﻋﺎﺳ (ﺪﻧﺪﺷ ﻦﯿﯿﻌﺗ.هدادﺮﻈﻧ زا هدﺎﻔﺘﺳا ﺎﺑ ﺎﻫ ﻪﯾﻦﺳ
-
لوﺪﺟ ﻪﻠﺣﺮﻣ
ﺪﻧﺪﺷ ﻞﯿﻠﺤﺗ و ﻪﯾﺰﺠﺗ ﯽﺴﻨﺟود ﯽﮔﺪﻧز .ﺶﯾﺎﻣزآ ﺎﻫ ﺮﻫ رد زا ماﺪﮐ ﻂﯾاﺮﺷ45ﺪﺷ راﺮﮑﺗ رﺎﺑﺪﻧ .ﯽﻨﻌﻣ توﺎﻔﺗ ﺮﻤﻋ لﻮﻃ و يرورﺎﺑ ،ﺎﻘﺑ ﻦﯿﺑ يراد
A. craccivora و ﯽﻫﺎﮕﺸﯾﺎﻣزآ ﻂﯾاﺮﺷ ردﺖﺷاد دﻮﺟو ﯽﻌﯿﺒﻃ.ﯽﻌﯿﺒﻃ ﻂﯾاﺮﺷ رد،A. craccivoraﯽﻨﻌﻣ رﻮﻃ ﻪﺑ يرادﯽﮔرﻮﭘ هرود لﻮﻃ لﻮﻃ ،
ﻞﻣﺎﮐ تاﺮﺸﺣ ﺮﻤﻋو ﯽﮔﺪﻧز ﻪﺧﺮﭼهﺎﺗﻮﮐﺖﺷاد ﯽﻫﺎﮕﺸﯾﺎﻣزآ ﻂﯾاﺮﺷ ﻪﺑ ﺖﺒﺴﻧ يﺮﺗ . ﺶﯾاﺰﻓا ﯽﺗاذ خﺮﻧ ،لﺎﺣﺮﻫ ﻪﺑ(r)ﻞﺜﻣ ﺪﯿﻟﻮﺗ ﺺﻟﺎﺧ خﺮﻧ ،
(R0)، ﺖﯿﻌﻤﺟ ﺶﯾاﺰﻓآ ﯽﻫﺎﻨﺘﻣ خﺮﻧ(λ) ﻞﺜﻣ ﺪﯿﻟﻮﺗ ﺺﻟﺎﺧﺎﻧ خﺮﻧ و(GRR)د هﺪﻣآ ﺖﺳد ﻪﺑ ﺮﯾدﺎﻘﻣ زا ﺮﺗﻻﺎﺑ ﯽﻫﺎﮕﺸﯾﺎﻣزآ ﻂﯾاﺮﺷ ر ﻂﯾاﺮﺷ رد
ﻧدﻮﺑ ﯽﻌﯿﺒﻃﺪ.تﺪﻣ ،لﺎﺣ ﺮﻫ ردﯽﻧﻻﻮﻃ ﯽﻌﯿﺒﻃ ﻂﯾاﺮﺷ رد ﻞﺴﻧ نﺎﻣز ﯽﻫﺎﮕﺸﯾﺎﻣزآ ﻂﯾاﺮﺷ زا ﺮﺗدﻮﺑ . ﻪﮐ داد نﺎﺸﻧ ﻪﻌﻟﺎﻄﻣ ﻦﯾا ﺞﯾﺎﺘﻧ ،ﯽﻠﮐرﻮﻃ ﻪﺑ
توﺎﻔﺘﻣ ﻂﯾاﺮﺷ)هﺎﮕﺸﯾﺎﻣزآ و ﻪﻋرﺰﻣ (ﯽﻨﻌﻣ ﺮﯿﺛﺎﺗهرود يور يرادﯽﮔﮋﯾو و ﺪﺷر يﺎﻫ ﯽﮔﺪﻧز لوﺪﺟ يﺎﻫA. craccivora ﺪﻨﺘﺷاد زا ﺰﯾﺮﮔ و
ﻪﺠﯿﺘﻧ رﺎﮑﺷآ يﺮﯿﮔﺒﻣﺮﺑ ﯽﻨزا ﺪﯾﺎﺑ ﻪﮐ ﻦﯾاﺑ هﺎﮕﺸﯾﺎﻣزآ ﺞﯾﺎﺘﻧ ﺐﺳﺎﻨﻣﺎﻧ ﻢﯿﻤﻌﺗرد دﺮﺑرﺎﮐ ياﺮ ﯽﻌﯿﺒﻃ ﻂﯾاﺮﺷ ،ﻢﯿﻨﮐ يﺮﯿﮔﻮﻠﺟﺖﺳا ﺖﺨﺳ . ﻪﺑ ﺞﯾﺎﺘﻧ
ﯽﻣ ﺎﺠﻨﯾا رد هﺪﻣآ ﺖﺳد ﺖﯿﻌﻤﺟ ﯽﯾﺎﯾﻮﭘ كرد رد ﺪﻧاﻮﺗA. craccivora ﮏﻤﮐ ﺎﻣ ﻪﺑ ﺰﯿﻧ ﺮﺛﻮﻣ ﯽﻘﯿﻔﻠﺗ ﺖﯾﺮﯾﺪﻣ ﻪﻣﺎﻧﺮﺑ ﻪﻌﺳﻮﺗ و ﻪﻋرﺰﻣ ﻂﯾاﺮﺷ رد
ﺪﻨﮐ .
يﺪﯿﻠﮐ نﺎﮔژاو:Aphis craccivoraلوﺪﺟ يﺎﻫ ﯽﮔﮋﯾو ،ﺶﯾاﺰﻓا ﯽﺗاذ خﺮﻧ ،ﻞﺴﻧ نﺎﻣز تﺪﻣ ،،ﯽﮔﺪﻧزﯽﻌﯿﺒﻃ ﻂﯾاﺮﺷ
Introduction
Black locust, Robinia pseudoacacia Frisia,is a
nitrogen-fixing leguminous tree that is widely planted in
the temperate regions of North America, Europe and Asia
for its resistance to many environmental stresses such as
drought, low and high temperature, air pollutants and low
fertility (Surles et al., 1989; Dini-Papanastasi & Panetsos,
2000). Therefore, R. pseudoacacia is an economically
and ecologically important tree species in the world.
One of the most important pests of black locust is
Aphis craacivora Koch (Hemiptera: Aphididae). The
cowpea aphid, A. craccivora, is considered as a major
pest of important economic crops like alfalfa, beans and
250 Jalalipour et al. : Comparative life table of Aphis craccivora …
cowpea in Asia, Africa and Latin America (Singh &
Jackai, 1985; Pettersson et al., 1998). It can transmit
plant pathogenic viruses (Coceano & Peressini, 1989;
Chen et al., 1999). The early season injuries caused by
this pest on R.pseudoacacia induce severe malformation
of the newly established leaves (Rakhshani et al., 2005).
Understanding the factors affecting the aphid’s
development and implementing this information into
forecast models, may increase the efficacy and success of
control methods (Kührt et al., 2006). Understanding the
ecology of a pest and estimating the growth parameters
and reproduction potential of insect population is an
important issue for successful theoretical and applied
population ecology and pest management programs
(Soroushmehr et al., 2008). The life table provides an
integrated and comprehensive description in details of
development times, survival rates of each growth stage,
fecundity and life expectancy of a population, and is
often used by scientists as a method of projecting the
growth of populations and predicting their sizes (Chi,
1990; Carey, 1993; Medeiros et al., 2000; Southwood &
Henderson, 2000).
Population growth rate is a basic ecological
characteristic that usually described as the intrinsic rate
of increase (r), an estimate of population growth potential
introduced by Birch (1948). Southwood (1966)
demonstrated that the intrinsic rate of increase is the most
practical life table parameter to compare the population
growth potential of different species under specific
climatic and nutritional conditions (Roy et al., 2003). The
intrinsic rate of increase has been widely used as a
bioclimatic index (Hulting et al., 1990).
Numerous studies have been intended to evaluate
the effect of crop density on the population dynamics of
A. craccivora (Farrell, 1976), relationship between A.
craccivora and host plant odors and pheromones
(Pettersson et al., 1998), its parasitoids (Johnson, 1959;
Rakhshani et al., 2005), different species of ants
(Katayama & Suzuki, 2002; 2003), and clover stunt virus
(Gutierrez et al., 1971; 1974) and presence of different
endosymbiont on A. craccivora (Brady & White, 2013).
The only study on life table and population parameters of
A. craccivora was done on five cowpea varieties in
laboratory condition by Obopile & Ositile (2010).
R. pseudoacacia is an important ornamental tree
in Iran. The main purpose of this study was to determine
the impact of two different rearing conditions (natural
and laboratory conditions) on the life table parameters of
A. craccivora on black locust to construct precise
predictions of the dynamics of its populations in the field.
Materials and methods
Insect culture
Leaves bearing apterous adults and different
instars of A. craccivora were collected from R.
pseudoacacia bushes on the campus of Faculty of
Agricultural Sciences at the University of Guilan
(Northern Iran) in 2013 and placed in a growth chamber
at 25±1ºC, 65±5% relative humidity (RH) and
photoperiod of 16:8h (L:D).
Life table study
The colony of A. craccivora was maintained for
two generations on R. pseudoacacia. Some adults of
A. craccivora were released on R. pseudoacacia leaves
for 24 h. This procedure allowed standardizing the age of
newly born nymphs. Then, newly born nymphs of
A. craccivora were placed separately on a R.
pseudoacacia leaf in plastic Petri dishes (10 cm in
diameter) with a hole in the center of the lid covered with
fine nylon mesh for aeration. A layer of wet cotton
padding, 0.5 cm-thick, lined the Petri dish, and the leaf
was on the bottom of the Petri dish according to Madahi
& Sahragard (2012) and Hosseini-Tabesh et al. (2015).
Once leaves appeared to be discolored, they were
replaced with fresh ones (usually daily). The aphid
nymphs were placed in their natural position on the
undersurface of the leaves in laboratory condition
(25±1ºC, 65±5% RH) (Liu & Meng, 1999). Nymphal
development was recorded daily. After adult appearance,
longevity and the number of produced nymphs by
females were recorded daily.
A similar methodology was used to study the life
table of A. craccivora in leaf cages in the field. Each
Petri-dish had a hole in the center of the lid, and was
covered with muslin for aeration. A hole was made
through both the lid and the body of the Petri dish. The
leaf cage was placed over the leaf with the stem of the
plant passing through the side hole of the cage. The
aphids’ development was checked every 24 h, from the
first instars to the death of the adults (Fig. 1). A magnifier
55x was used to monitor the insects. Daily temperature
Journal of Entomological Society of Iran,2017, 36(4)
251
and humidity were measured with Digital hygro-
thermometer. The temperature ranged from 16–32°C, and
the relative humidity was 27–95%. Each experiment was
replicated 45 times for each condition.
Data analysis
Data were analyzed using age-stage, two-sex life
table theory (Chi & Liu, 1985) and the method described
by Chi (1988). To facilitate the tedious procedure, data
analysis and population parameters were calculated using
the TWOSEX-MSChart program designed in visual
BASIC for the Windows operation system
(Chi, 2015). The TWOSEX-MSChart is available at
http://140.120.197.173/Ecology/prod02.htm (Chung sing
University) and http://nhsbig.inhs.uiuc.edu/wes/chi.html
(Illinois Natural History Survey).
The age-stage specific survival rate (Sxj) (where
x= age and j= stage), the age-stage specific fecundity (fxj),
the age-specific survival rate (lx), the age-specific
fecundity (mx), and the population parameters (r, the
intrinsic rate of increase; λ, the finite rate of increase; R0,
the net reproductive rate, and T, the mean generation
time) were calculated accordingly.
The means and standard errors of the life table
parameters were estimated with the bootstrap (m=10.000)
method (Erfon & Tibshirani, 1993). Differences between
treatments were then compared by using the paired
bootstrap test (Efron and Tibshirani, 1993, Polat-
Akköprü et al. 2015).
Fig. 1. Leaf cage used to study life table of Aphis craacivora under field condition.
Results
The developmental times for each stage are listed in
Table 1. The first, second and fourth instar nymphs of A.
craccivora showed significantly slower development
under natural condition (Table 1). However, no
significant differences were found in third instar nymph
of A. craccivora reared in both natural and laboratory
conditions. The adult longevity and total life span of A.
craccivora was significantly shorter under natural
condition.
The parameters lx,mx, and age-specific maternity
(lxmx) are plotted in fig. 2. The survival rate (lx) in the
laboratory condition was higher. The trend of age-
specific fecundity (mx) showed that reproduction began at
the age of 7 days in both laboratory and field. The highest
fecundity occurred at the ages of 13 and 12 days in
laboratory and natural conditions, respectively. Based on
the age-stage, two-sex life table, the age-stage-specific
life expectancy (exj) gives the expected life span of an
individual of age xand stage jcan live after age x(fig. 3).
The trends of life expectancy in both conditions were
almost equal but life expectancy of A. craccivora in
laboratory was higher. The age-stage specific survival
rates (sxj) showed the probability of a newborn surviving
252 Jalalipour et al. : Comparative life table of Aphis craccivora …
to age xand stage j. The age-stage specific survival rates
of A.craccivora under field and laboratory conditions are
shown in fig. 4. The survival rate of A. craccivora in
laboratory condition was higher. The reproductive value
(vxj) is the contribution of individuals of age xand stage
jto the future population (fig. 5). The results revealed
that female with ages of 8 and 7 days made the highest
contribution to the population when reared in laboratory
and natural conditions, respectively.
Table 2 presents significant differences of
population parameters of A.craccivora between
laboratory and natural conditions. The intrinsic rate of
increase (r), the finite rate of increase (λ), net
reproductive rate (R0) and gross reproductive rate (GRR)
were significantly higher under laboratory condition.
Mean generation time (T) was significantly lower under
laboratory condition.
Fig. 2. Age-specific survival rate (lx), age-specific fecundity (mx) and age-specific maternity (lxmx) of Aphis craccivora
under laboratory and field conditions.
Fig. 3. Age-stage specific life expectancy of Aphis craccivora under laboratory and field conditions.
Journal of Entomological Society of Iran,2017, 36(4)
253
Table 1. Mean developmental times in days (mean ± SE), longevity and fecundity of Aphis craccivora in laboratory at 25 ±
1ºC, 70% ± 5% RH, photoperiod 16:8h (L: D) and in natural condition (range of temperature 16ºC -33ºC and 32-89% of
RH).
Mean in the same row followed by the same letter are not significantly different (Paired bootstrap test, P<0.05).
Table 2. Life table parameters (Means ± SE) of Aphis craccivora in laboratory at 25 ± 1ºC, 70±5 % RH, photoperiod 16:8h
(L: D) and in natural condition (temperature ranged 16ºC - 33 C and 32-89% RH.
Population parameters
Laboratory
Field
Intrinsic rate of increase (r) (day-1)
0.2339 ± 0.0037a
0.1906 ± 0.0055b
Finite rate of increase (λ) (day-1)
1.2635 ± 0.00462a
1.2100 ± 0.0066b
Net reproductive rate (R0) (offspring)
21.033 ± 0.71303a
13.689 ± 0.9573b
Mean generation time (T) (day)
13.023 ± 0.148b
13.73 ± 0.228a
Gross reproductive rate (GRR) (offspring)
23.439 ± 0.855a
18.164 ± 0.893b
Means in the same row followed by the same letter are not significantly different (Paired bootstrap test, P<0.05).
Fig. 4. Age-stage specific survival rate of Aphis craccivora under laboratory and field conditions.
Stages
Laboratory
Field
First instar nymph
2.02 ± 0.04b
2.18 ± 0.06a
Second instar nymph
1.89 ± 0.07b
2.36 ± 0.08a
Third instar nymph
1.98 ± 0.07a
2.09 ± 0.05a
Fourth instar nymph
1.98 ± 0.04b
2.13 ± 0.05a
Immature
7.87 ± 0.088b
8.76 ± 0.106a
Adult longevity
16.42 ± 0.374a
12.69 ± 0.807b
Life span
24.29 ± 0.376a
21.44 ± 0.784b
254 Jalalipour et al. : Comparative life table of Aphis craccivora …
Fig. 5. Age-stage-specific reproductive value of Aphis craccivora under laboratory and field conditions.
Discussion
Our study showed that immature development times
of A. craccivora under field conditions were higher,
except for the third instar nymphs with no significant
difference. The prolonged immature developmental times
in the field may reflect the unsuitability of the
environmental conditions. Our result were consistent with
those of Zanuncio et al. (2006) who stated that longevity
of the predatory pentatomid, Brontocoris tabidus
(Signoret), was longer under field conditions. Afshari et
al. (2007) mentioned that the fluctuating climatic and
natural conditions of cotton fields could increase
immature development time and decrease adult
development times and reproduction of A. gossypii.
Similar results were found for nymphal developmental
stage of Bactericera cockerelli (Sulc) on tomato (Yang et
al., 2013) and Aphis gossypii Glover on Hibiscus
syriacus L. (Hosseini-Tabesh et al., 2015) except for the
fifth and first instar nymphs, respectively.
The adult longevity and life span of A. gossypii in
field conditions were found to be shorter due to the
fluctuating temperature and humidity of field conditions.
Yang et al. (2013) reported that female longevity of B.
cockerelli reared on tomato were shorter under field
conditions (16.2±0.9 days) comparing to laboratory
conditions (60.5±8.4 days). According to Hosseini-
Tabesh et al. (2015), shorter adult longevity of A.
gossypii occurred in field, which is consistent with our
finding. These results corroborate studies on reverse
relationship between temperature and adult longevity of
Hyalopterus pruni (Geoffroy) (Latham & Mills, 2011),
mean developmental times of Bemisia argentifolii
(Bellows & Perring) (Yang & Chi, 2006), Brachycaudus
schwartzi (Börner) (Satar & Yokomi, 2002) and Aphis
spiraecola Patch (Wang & Tsai, 2000). Zamani et al.
(2006) also reported that temperature had negative impact
on the developmental time of A. gossypii reared on
Cucumis sativus L. under laboratory conditions.
In the past, the response of aphids to environmental
conditions has been used to develop phenological models
to forecast aphid outbreaks (Collier et al., 1994; Ro et al.,
1998). Dixon (1987) showed that the length of time
required for an aphid from birth to adult is variable and
dependent on two intrinsic factors, birth weight, whether
the morph is winged or unwinged, and two extrinsic
factors, food quality and weather conditions (especially
temperature). Environmental conditions, such as
temperature and relative humidity determine the
physiological state of insects that are the key variables
regulating their survival, fecundity, and population
growth. Different temperature and relative humidity were
important factors in significant differences (25 ± 1ºC,
70±5% RH and 16–32°C, and 27–95% RH, respectively).
Similar studies found that aphid population dynamics was
affected by the abiotic factors such as environmental
factors (Ruggle & Gutierrez, 1995; Diaz & Fereres, 2005;
Arbab et al., 2006; Hosseini-Tabesh et al., 2015).
In this study, the life table parameters of A. gossypii
showed significant differences between field and
laboratory conditions. Since intrinsic rate of increase (r)
is the reflection of several factors such as fecundity,
survival and generation time and physiological qualities
Journal of Entomological Society of Iran,2017, 36(4)
255
of an animal in relation to its capacity to increase, it
would be an appropriate index to evaluate the
performance of an insect in different situations
(Kocourek et al., 1994; Southwood & Henderson, 2000).
The rvalue is more useful to compare the population
growth potential of different species than R0(Price,
1997). The Intrinsic rate of increase (r) was 0.2339 and
0.1906 d–1under laboratory and natural conditions,
respectively. According to Obopile & Ositile (2010), the
rvalue of A. craccivora on five cowpea Vigna
unguiculala (L.) varieties under laboratory condition
ranged from 0.32+0.01 to 0.36+0.01 d–1, that was higher
than our results (0.1906 ±0.0055 and 0.2339 ±0.0037 d–1
in natural and laboratory conditions, respectively). These
differences may be due to discrepancy in host plants and
environmental conditions such as temperature and
relative humidity. The rof B. cockerelli fed on potato
was also significantly higher in the laboratory
(0.1966 d–1) than in field conditions (0.1015 d–1) (Yang et
al., 2010). Hosseini-Tabesh et al. (2015) reported higher
intrinsic rate of increase of A. gossypii in laboratory
condition. The higher rvalue in laboratory condition
indicated that A. craccivora had a greater reproductive
potential and more suitability. The R0was also
significantly higher under laboratory conditions. Similar
results was found for melon flies (Huang & Chi, 2013)
and A. gossypii (Hosseini-Tabesh et al., 2015), as the net
reproductive rate was calculated higher under laboratory
conditions. The mean generation time (T) for A.
craccivora in laboratory condition was significantly
higher, suggesting that laboratory condition is more
suitable for A. craccivora.
It is concluded that life table of insect pests in field
conditions could be a useful tool for making accurate
management decisions and selecting proper measures to
control insect pests of economically important crops. The
differences reported here between the laboratory and field
studies, together with the life table analysis, provide
valuable information leading to establish a successful
control program.
Acknowledgments
We thank the Faculty of Agricultural Sciences,
University of Guilan for providing us research facilities
and financial support.
References
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Received: 14 September 2016
Accepted: 1 January 2017