Functional Response of Orius albidipennis (Hemiptera: Anthocoridae) to the Two-spotted Spider Mite Tetranychus urticae (Acari: Tetranychidae)
Nesrin A. El-Basha,
The objective of this study was to determine the functional response of the predator Orius albidipennis (Reuter) fed on egg of Tetranychus urticae Koch. We conducted a logistic regression of the proportion of prey consumed as a function of initial prey density to identify functional response types and used nonlinear least-squares regression and the random predator equation to estimate attack rates and handling times. Overall, all stages of O. albidipennis exhibited a type-I functional response to T. urticae. Whereas, attack rate (a) and handling time (Th) of O. albidipennis female and male recorded 1.267, 0.828, 0.0122 and 0.0141 when offering eggs of T. urticae, respectively.
Received: December 05, 2011;
Accepted: February 15, 2012;
Published: March 27, 2012
The two spotted spider mite Tetranychus urticae Koch. (Acari: Tetranychidae),
considers one of the most important pests around the world in various ornamental
and vegetable crops (Zaher, 1986; Childers,
1994; Takafuji et al., 2000; Zhang,
2003; Alatawi et al., 2005; Abd-Elhady
and Heikal, 2011). On other hand, Insect predators are most effective regulators
of pest populations (Cardoso and Lazzari, 2003; Padmalatha
et al., 2003), which has led their increasing use in insect pest
management programs (Wiedenmann and Smith, 1997; Riudavents
and Castane, 1998). Due to, the current concerns to reduce the excessive
use of chemicals insecticides for pest control, as well as to avoid increments
in doses or utilization of highly toxic compounds (Gravena,
1989) biological control stands as a profitable alternative to the use of
chemicals in the agroecosystem (Lester et al., 2000).
Predation is supposed to be one of the great biotic mortality factors reducing
insect pest populations and using them in insect pest management programs has
been receiving better consideration because of the recent need to reduce the
exclusive apply of insecticides for pest control (Sarmento
et al., 2007).
Members of the genus Orius (Heteroptera: Anthocoridae) are important
predators of certain arthropods like aphids, aleyrodids, eggs and larvae of
lepidopterous, thrips and mites (Pericart, 1972; Vacante
et al., 1997; Reitz et al., 2006;
Butler and ONeil, 2007; Fathi
and Nouri-Ganbalani, 2009). However, thrips and mites are believed to represent
imperative diets for Orius spp. (Wright, 1994).
Furthermore, several species of Orius have been received considerable
attention in biological control programs due to their efficiency in number of
agricultural ecosystems (Cocuzza et al., 1997).
Additionally the previous literatures stated that Orius spp. could effectively
suppress spider mite populations in the field (Oatman and
McMurthry, 1966; Du and Yan, 1995; Wittmann
and Leather, 1997; Sanderson et al., 2005;
Rosenheim, 2005; Xu and Enkegaard,
2009). Of them, Orius albidipennis (Reuter) (Heteroptera: Anthocoridae)
was found in the south Mediterranean basin, in the Canary Islands and East Africa
(Salim et al., 1987; Chyzik
et al., 1995; Fritsche and Tamo, 2000). In
Egypt, O. albidipennis is very common in cultivated areas, especially
in corn and cotton fields. It is generally establish in flowers of plants infested
with thrips, lepidopteran eggs or other small arthropods. O. albidipennis
does not occur in the field earlier than March, but its activity increases from
April until the end of November (Tawfik and Atta, 1974;
Zaki, 1989; Sobhi et al.,
Prior to the release of a natural enemy in a biological control program, it
is essential to evaluate its efficiency under laboratory conditions. One useful
method for evaluating the efficiency of a natural enemy is to assess of their
behavioral characteristics including functional response and searching rates
(Fathipour et al., 2006; Bayoumy
et al., 2009). The relationship among the number of prey consumed
per predator individual and prey density was defined as functional response
(Solomon, 1949; Holling, 1959a,
b). It plays a critical role in the perspective of prey-predator
interactions and their ecological and evolutionary consequences (Tully
et al., 2005). Holling (1959a) identified
three basic types of functional responses in general. The Type I response is
characterized by a linear rise with a constant attack rate over all prey densities
until satiation is reached. In the Type II response the attack rate decreases
as prey density increases. Type III is represented by a sigmoid curve, where
the attack rate increases with increasing prey density. Holling
(1961) divided the functional response into several basic and subsidiary
components. The attack rate (a) can be considered as a function of: (1) the
reaction distance of the predator, i.e., the maximum distance at which the predator
will react by attacking prey, (2) the speed movement of predator and prey and
(3) the proportion of attacks that are successful. The handling time (Th)
can be considered to be a function of: (1) the time spent pursuing an individual
prey, (2) the time spent investigating and probing each prey and (3) the time
spent drilling each prey. The time as prey and predator exposure (T) can be
considered to be a function of: (1) time in non-feeding activities and (2) time
in feeding-related activities (i.e., Th). The objective of this study
was to investigate the functional response of O. albidipennis stages
when preying on egg of T. urticae to improve our understanding of prey-predator
interaction and get a better strategy for the biological control of T. urticae
using O. albidipennis.
MATERIALS AND METHODS
Mite colony: The stock colony of Tetranychus urticae was collected
from eggplant at the experimental farm, Ismailia Agricultural Research Station.
T. urticae was collected from the same locations and host plants used
for the collection of Orius albidipennis. The colony of T. urticae
was kept on detached sweet potato branches kept with their upper part of the
stem in contact with water in glass vials at 25±1°C, 50-80% RH and
photoperiod was 14L/10D h.
Rearing of Orius albidipennis: A colony of O. albidipennis was established from nymphs and adults collected on eggplant plants (Solanum melongena L.) infested with T. urticae at the experimental farm, Ismailia Agricultural Research Station, Ismailia, Egypt. Adults and nymphs were maintained in plastic jars (10 cm diameterx20 cm height), which were covered with muslin that was held in place by rubber bands. Each jar was provided with sufficient quantities of T. urticae as a food supply, a piece of cotton that had been soaked in a 10% honey solution and bean pods (Phaseolus vulgaris L.) as an oviposition substrate. Bean pods with newly deposited eggs were removed and replaced daily, kept in previous jars. Jars were examined daily for hatching, after hatching nymphs were provided with T. urticae and small balls of foam to reduce cannibalism. Upon eclosion, adult males and females were sexed and placed in new plastic jars, provided with the same time of prey and oviposition substrates. Colonies were maintained at 26±1°C and 60±10% RH.
Functional response: The predator O. albidipennis larvae (4 h post molting) were collected from the colony and starved for 4 h in glass vials (7 cmx2 cm) containing small wet cotton with water without preys. Adult males and females 7 days old were collected in the same size of glass vials and starved 24 h before being used. Small discs 1.5 cm of sweet potato leaves harboring eggs of T. urticae was prepared and number of eggs was counted and put in Huffaker cells. Starved predators were singly transferred to modified Huffaker cells. T. urticae eggs were introduced as prey into modified Huffaker cell at six densities increased gradually to be synchronize with the developmental stage of the predators. Whereas, six prey densities of T. urticae were evaluated: 30, 40, 50, 60, 70 and 80 eggs for the fourth instar, fifth instar and adult males and females, respectively. Each predator individuals (larva and adult) was replicated ten times. After 24 h, numbers of consumed eggs of T. urticae were recorded.
Data analysis: The approach developed by Juliano
(2001) was used to analyze the predators functional response. Initially,
the type (shape) of response was determined by seeing if the data pit a type
I, II or III response, using a polynomial logistic regression of the proportion
of prey consumed (Na/No) versus the initial number of prey offered (No) as follows:
where, Na is the number of prey consumed, N0 is the initial
number of prey density and P0, P1, P2 and P3
are the intercept, linear, quadratic and cubic coefficients, respectively. These
parameters can be estimated using the CATMOD procedure in SAS (Juliano,
2001). The logistic regression was used to obtain the maximum likelihood
estimates of parameters P0 to P3. The functional response
type was determined by the sign of the linear coefficient from Eq.
1 and the significance of the parameters from the logistic model was evaluated
by log likelihood tests. For a type I, the curve of Na/No versus No has a linear
shape if the linear term from Eq. 1 was not significantly
different from 0, a type I functional response was indicated , whereas a significant
negative value indicated a type II response and a significant positive value
indicated a type III (Juliano, 2001). The second part
of the analyses used Holling disk equation (Holling 1959a)
to estimate the parameter values of type I as follows:
where, Ha defines the number of prey attacked by a predator per time unit, a is attack rate of a predator, H is the original number of prey items offered to each predator at the beginning of the experiment, T is the total time of exposure time (1 day in this experiment) and Th is handling time for each prey caught (proportion of the exposure time that a predator spends in identifying, pursuing, killing, consuming and digesting prey).
The parameters a (the rate of successful attack) and Th (the time
required to handle a prey item) were calculated using least-squares non-linear
regression. Whereas, Th values were used to calculate maximum attack
rate as T/Th (Hassell, 1978), this represent
the maximal number of prey individuals that could be consumed by O. albidipennis
during 24 h.
RESULTS AND DISCUSSION
Functional response, though an important tool, cannot only be attributed to
report success and failures in biocontrol programs. For instance, other factors,
such as intrinsic growth rates, host patchiness, predation and competition,
host traits and environmental complexities (abiotic and biotic factors) also
have a major influence on the efficiency of predator in managing the prey population
(Pervez and Omkar, 2005).
The average number of T. urticae attacked by O. albidipennis
increased with prey density during a 24 h period. Prey consumption by 4th, 5th,
male and female of O. albidipennis increased 20.4 to 33.4, 23 to 38.4,
18.2 to 32.4 and 26 to 43.4 individual with increase in density of eggs of T.
urticae, respectively. While, the proportion of killed preys by 4th, 5th,
male and female of O. albidipennis decreased from 0.68 to 0.41, 0.76
to 0.48, 0.6 to 0.4 and 0.86 to 0.54 with increase in density of eggs of T.
urticae, respectively (Fig. 1a, b).
Decreasing in proportion of prey consume with increasing prey density is common
for arthropods predator Holling (1961). Jalalizand
et al. (2011) showed that functional response of Orius niger niger
Take type II when fed on adult of T. urticae while it take type III when
fed on egg of T. urticae. Gitonga et al. (2002)
reported a functional Type I response curve of O. albidipennis preying
on Megalurothrips sjostedti Trybom second instar larvae and adults at
|Fig. 1 (a, b):
||Observed functional response of Orius albidipennis 4th,
5th, male and female to Tetranychus urticae egg densities
||Results of logistic regression analyses, indicating estimates
and standard errors of linear, quadratic and cubic coefficient for the proportion
of prey eaten by O. albidipennis against initial prey number offered
Data presented in Table 1 showed that the outcome of the
logistic regression 4th, 5th instars, male and female to densities of eggs of
Tetranychus urticae reflected a type I functional response, in all cases
the sign of the linear term was negative and p>0.05 (Table
1).Whereas, the type of functional response can be determined based on the
sign of the linear coefficient (Juliano, 1993). The type
of functional response and estimated parameters for a natural enemy could be
affected by some factors such as host plant. Temperature and type of prey or
host and prey stages (Wang and Ferro, 1998; De
Clercq et al., 2000; Mohaghegh et al.,
2001). Xu and Enkegaard (2009) noticed that female
of Orius sauteri (Poppius) reflected a type I functional response to
densities of deutonymph of T. urticae. Whereas, Zamani
et al. (2009) showed that the functional response of O. albidipennis
to densities of female of T. urticae take type II. Although, Jalalizand
et al. (2011) reported that O. niger female exhibited a type
II and III functional response in their predation of T. urticae female
and eggs, respectively.
The functional response data of O. albidipennis 4th, 5th, male and female
to densities of eggs of Tetranychus urticae were successfully fitted
to the Holling disk equation (Holling, 1959a) (Fig.
2, Table 2).
Attack rate and handling time were the parameters used to determine the magnitude
of functional responses Pervez and Omkar (2005). The
attack rate of O. albidipennis 4th and 5th was 1.613 and 1.148 whereas,
male and female of O. albidipennis attack rate was 0.828 and 1.267 (Table
Xu and Enkegaard (2009) showed that attack rate of
O. saurteri female on T. urticae was 0.042. Whereas, Jalalizand
et al. (2011) reported that attack rates of O. niger on both
cucumber and strawberry for T. urticae female was 0.021 and 0.045, respectively.
While, attack rates of O. niger on the same host for T. urticae
egg was 0.001 and 0.003, respectively. On other hand, handling time is a good
indicator of consumption rate and predator efficacy because it reflects the
cumulative effect of time taken during capturing, killing, subduing and digesting
the prey(Veeravel and Baskaran, 1997). Handling time
(Th) O. albidipennis 4th, 5th, male and female between 0.0122
||Consumption rate of Orius albidipennis ,4th, 5th, male
and female on eggs of Tetranychus urticae at 25±1°C, The
fitted lines are predictions of the Holling (1959a)
||Effect of Tetranychus urticae densities on the attack
rate (a), handling time (Th) and maximum number of consumption
(T/Th) on O. albidipennis derived from random predator
Whereas, The expected maximum consumption (T/Th) of O. albidipennis
4th, 5th, male and female between 44.44 and 81.96 eggs per day of T. urticae
(Table 2). Xu and Enkegaard (2009)
reported that handling time (Th) of O. saurteri female on
T. urticae deutonymph was 1.217. Whereas, Zamani
et al. (2009) showed that handling time (Th) for the O.
albidipennis when reared on T. urticae ranged between 0.005 to 0.012
days and the highest theoretical maximum predation rate was (80 adult).
In conclusion, the present study has improved our understanding of the O.
albidipennis behavior to T. urticae. However, functional responses
studies in small laboratory arenas have been criticized as being unrepresentative
of natural conditions (Kareiva, 1990) and should be interpreted
with care. We believe they may have some value as a first step in estimating
predatory capacity but recommend that additional studies be conduct.
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