Acta Hortic. 1164. ISHS 2017. DOI 10.17660/ActaHortic.2017.1164.55, 425-430 Proc. III International Symposium on Organic Greenhouse Horticulture,Izmir, Turkey
Predatory efficacy of Dicyphus errans on different
prey
B.L. Ingegno1, N. Bodino1, A. Leman2, G.J. Messelink2, and L. Tavella1,a
1DISAFA, ULF Entomologia Generale e Applicata, University of Torino, Grugliasco (TO), Italy; 2Wageningen UR, Greenhouse Horticulture, Bleiswijk, The Netherlands.
aE-mail: luciana.tavella@unito.it
Abstract
The Palaearctic predator Dicyphus errans (Hemiptera: Miridae) lives omnivorously on various host plants, preying on a wide range of small arthropods, including some new invasive alien species. These characteristics make it a promising biological control agent (BCA) in organic greenhouses. The capacity of a BCA to find, kill and consume prey plays a fundamental role in trophic interactions and population dynamics in a predator-prey system. The functional response of a predator, which describes how the individual rate of prey consumption changes in response to prey density, is a key component to assess its effectiveness in pest control and the stability of its own populations. Therefore, the functional response of D. errans on different prey was studied to improve our knowledge on the potential of this mirid, which is naturally widespread in European organic greenhouses. Laboratory experiments were carried out on three exotic pests: the poinsettia thrips Echinothrips americanus (Thysanoptera: Thripidae), the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), and the tomato borer Tuta absoluta (Lepidoptera: Gelechiidae), to build functional response curves. Prey was offered at different densities to single females of D. errans for 24 h. The predation behaviour of D. errans on all the prey species was defined by Type II functional response curves. The female could daily prey about 62 adults of E. americanus, 114 pupae of T. vaporariorum, and 236 eggs of T. absoluta. The high voracity of this generalist predator on different prey confirmed its suitability as a BCA. For effective and stable pest control strategies, a prior to pest establishment of D. errans in organic greenhouses may prevent pest escaping in case of high infestation rates, even if the type II functional response reaches saturation at very high prey densities.
Keywords: functional response, Echinothrips americanus, Trialeurodes vaporariorum, Tuta absoluta, biological control agent (BCA)
INTRODUCTION
Mirid generalist predators (Hemiptera: Miridae) belonging to dicyphine tribe have been successfully used in augmentative control programmes on several pests. Besides the commercialized species Macrolophus pygmaeus and Nesidiocoris tenuis, attention has been recently focused on another promising mirid species, Dicyphus errans. It can prey upon several pests (e.g., whiteflies, spider mites, thrips, tomato borer) and live omnivorously on various host plants (over 150 species) (Voigt et al., 2007; Ingegno et al., 2008, 2013; Arvaniti et al., 2014; Messelink et al., 2015). Moreover, it naturally occurs in IPM and organic tomato crop [Solanum lycopersicum (Solanaceae)], especially in NW Italy where it is the most abundant dicyphine (Ingegno et al., 2009).
The capacity of a biological control agent (BCA) to find, kill and consume prey plays a crucial role in trophic interactions and population dynamics of a predator-prey system. The functional response of a predator, which describes how the individual rate of prey consumption changes in response to prey density, is a key component to assess its effectiveness in pest control and the stability of its own populations (Holling, 1959). Three types of Holling’s functional responses are generally used to investigate how a predator’s rate of prey capture is related to prey density (i.e., Type I: independence; Type II: inverse density dependence; Type III: density dependence) (Juliano, 2001). In previous studies on functional response on different prey, some dicyphine species, such as Dicyphus tamaninii, M.
pygmaeus and N. tenuis, showed a Type II functional response, typical of insect predators (Alvarado et
as a type III functional response, in general belonging to vertebrates (Enkegaard et al., 2001; Hamdan, 2006).
For a deeper knowledge on its efficacy as a BCA, the predation rate of D. errans on the following three exotic pests was here investigated: 1) adults of the poinsettia thrips Echinothrips americanus
(Thysanoptera: Thripidae); 2) pupae of the greenhouse whitefly Trialeurodes vaporariorum
(Homoptera: Aleyrodidae); 3) eggs of the tomato borer Tuta absoluta (Lepidoptera: Gelechiidae). The
poinsettia thrips is a Nearctic species that moved from its native distribution area to the eastern part of the US over the majority of North America. It was first introduced into Europe, in the UK in 1989, and spread rapidly across at least 22 European countries (Li et al., 2012). This pest is characterized by a rapid reproduction and a broad host plant range (46 plant taxa from 25 families) (Varga et al., 2010), which make it a major threat on various ornamentals and greenhouse crops. By now, the greenhouse whitefly has become successfully established in glasshouses in Europe. Even if it prefers tropical environments (high temperature and humidity), in temperate zones this pest is emerging as a serious threat to ornamental, vegetable and fruit production during summer and in the field as well (Wintermantel, 2004). Native from South America, the tomato borer is a multivoltine pest that has rapidly invaded Europe from its introduction in 2006, causing severe yield losses on tomato crop (Desneux et al., 2010; Tropea Garzia et al., 2012). Given its resistance to many insecticides, an ecologically based holistic approach is needed for an effective pest control (Ponti et al., 2015).
MATERIALS AND METHODS
All the plants used for both experiments and insect mass rearing were cultivated in an experimental heated greenhouse, at 27±3°C and 55±23% RH. Seeds were sown in plastic containers (∅ 14 cm), watered daily and fertilized. Colonies of D. errans were started from individuals collected on European black nightshade [Solanum nigrum (Solanaceae)] in Piedmont (NW Italy), and reared inside insect cubic cages (47.5 cm edge) (MegaView, Talchung, Taiwan) on tobacco [Nicotiana tabacum
(Solanaceae)], European black nightshade or ‘Marmande’ tomato at 24±1°C, 55±5% RH, with a L 16:D
8 photoperiod. Individuals were fed with eggs of Ephestia kuehniella (Lepidoptera: Pyralidae) (Bioplanet s.c.a., Cesena, Italy) and dehydrated and decapsuled cysts of Artemia salina (Anostraca:
Artemiidae) (La Mangrovia, Ostuni, Italy).
Colonies of E. americanus were started from individuals collected on ornamentals in greenhouses of South Holland region, and reared on ‘Bison’ gerbera. Definite densities of adults of E.
americanus were gently transferred with a tiny brush on a ‘Kimsey’ gerbera leaf disk on an absorbent
wet cotton in a 280-mL plastic box (∅ 80 mm) (Paardekooper Verpakkingen B.V., Oud-Beijerland, The Netherlands) with the drilled lid covered with a fine net mesh.
Pupae of T. vaporariorum coming from tobacco plants were provided by a commercial producer (Koppert B.V., Berkel en Rodenrijs, The Netherlands). Definite densities of pupae were gently transferred on gerbera leaf disk with the same procedure followed for E. americanus. Colonies of T.
absoluta were started from individuals provided by a commercial producer (Bioplanet s.c.a., Cesena,
Italy) and reared on tomato plants in net cages (150 W × 150 L × 110 H cm, mesh 0.23×0.23 mm) in an experimental heated greenhouse at 27±3°Cand 55±23% RH. Eggs were obtained by placing clean plants of tomato in the cage containing adults for 48 h. Definite densities of eggs were isolated on three tomato leaflets in a Petri dish (∅ 130 mm) with stalks plunged in water in a 2-mL Eppendorf® tube sealed with Parafilm®.
One-week-old females of D. errans were used to assess the functional response on the three pests. After a starvation of 16 h, single females were exposed to definite prey densities for 24 h. To fit the functional response curve for each prey, the following treatments, consisting in different densities of items offered as prey, were set: six for E. americanus (from 5 to 200 adults); 10 for T. vaporariorum
(from 5 to 250 pupae); 16 for T. absoluta (from 5 to 350 eggs). After predator removal, leaves were accurately inspected under a stereomicroscope to count predated items. Five repetitions were done for each treatment. Experiments were carried out in climatic chambers at 24±1°C, 65±5% RH, and L 16:D 8.
Data of functional response assays were analysed using the two-step technique (Juliano, 2001). To determine the type of functional response of D. errans on the three prey species a logistic regression analysis (LRA) of proportion of consumed items on the number of total items offered (Ne/N0) was
exp
(
P
0+
P
1N
0+
P
2N
02+
P
3N
03❑)
¿
¿
N
eN
0=
Prob
{
Y =1
}
=
¿
Eq. 1where Ne is the number of consumed items, N0 is the initial number of offered items and P0, P1, P2 and
P3 are the intercept, linear, quadratic and cubic coefficients, respectively. The value of the linear coefficient P1 is one criterion for separating Type II (P1<0) and III (P1>0) functional responses. Analyses were limited to cubic or lower order expressions, and Akaike information criterion (AIC) test was used to evaluate the goodness of fit of the different order equations.
Since the LRA suggested a Type II functional response (see Results), further analyses were restricted to type II functional response model, specifically Holling’s disc equation (Holling, 1959):
N
a=
a N
01+a T
hN
0Eq. 2
The parameters of functional response (a = attack rate; Th = handling time) were estimated using a non-linear least square regression based on Levenberg-Marquardt method (Elzhov et al., 2013) on Equation 2. The asymptotic 95% confidence interval of a and Th estimates should not include zero to consider the estimates of functional response parameters significantly different from zero. The best functional response model between Holling’s disc equation and random predator equation was selected using AIC test. Values of Th were used to calculate maximum attack rate as T/Th (Hassell, 2000), that represents the maximal number of prey that can be consumed by D. errans during the considered time interval (i.e., T = 1 day). Functional response analyses were performed using R (R Core Team, 2013).
RESULTS AND DISCUSSION
The predation behaviour of D. errans on all three prey species was defined by Type II functional response curves (Figure 1), since the linear term (P1) of Equation 1 was negative for all the tested prey. This type of decelerating curve is consistent with the results reported in most studies involving dicyphine species (Alvarado et al., 1997; Foglar et al., 1990; Montserrat et al., 2000; Fantinou et al., 2008; Maselou et al., 2014). Holling’s disc equation (Equation 2) parameter estimates were significant, and the attack rate was accounted to predict theoretical maximum daily predation rate of D. errans to the tested prey, obtaining an estimate of 62 adults of E. americanus, 114 pupae of T. vaporariorum and 236 eggs of T. absoluta consumed per female predator per day. In this study, the overkilling behaviour was not investigated, but since it was previously reported for both M. pygmaeus and N. tenuis, it probably also occurred (Valderrama et al., 2007; Fantinou et al., 2008). The estimates of instantaneous attack rate and handling time for each prey (E. americanus: a = 0.055±0.034 h-1; Th = 0.38±0.130 h; T.
vaporariorum: a = 0.037±0.009 h-1, Th = 0.21±0.048 h; T. absoluta: a = 0.041±0.002 h-1, Th =
0.102±0.007 h) underline the high voracity of this generalist predator. The handling time is proportional to the size of the prey since the predator takes longer time to eat larger prey as reported for other dicyphine species (Foglar et al., 1990; Peérez-Hedo and Urbaneja, 2015).
Furthermore, the prey mobility influences its consumption by the predator. In fact, the handling time for E. americanus adults was higher compared to the one for T. vaporariorum unless its similar size. The maximum daily predation rate of two other dicyphine species D. tamaninii and M. pygmaeus
on the greenhouse whitefly assessed in a previous study was of 63 and 20 pupae, respectively (Montserrat et al., 2000), which is much lower than that found here. In the same study, these two mirids were able to consume 112 and 70 second-instar larvae of the thrips Frankliniella occidentalis, respectively (Montserrat et al., 2000), which is higher than the maximum consumption of 62 adults of the poinsettia thrips observed in the current study. This result still suggests a strong influence of prey mobility on handling time.
The results we reported here are a part of a wider research aimed at identifying the most suitable mirid predator to control different pests in crops characterized by different environmental conditions. These preliminary results suggest that D. errans can be an important predator of several pests. Its high efficiency on different prey confirmed its suitability as BCA. The Type II functional response typically shows saturation effects at very high prey densities, thus high infestation rates may give prey an opportunity to escape from predation. However, a prior to pest establishment of D. errans
in cropping systems may prevent this possibility and contribute to effective and stable pest control strategies in organic greenhouses. Moreover, since functional and numerical assays on single predator– single prey systems in simplified laboratory environments do not allow predictions of the growth of mixed populations in realistic habitats (Lester and Harmsen, 2002), future research on the real efficacy as BCA of D. errans in field conditions and on mixed prey should be performed. Moreover, generalist predators often switch to the most abundant prey in the case of mixed prey populations (Murdoch, 1969). This prey switching may also transform the Type II response into a Type III response, because the consumption rate of the target prey will then be lower at low densities.
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Figu re 1. Mean (±SE) percentage (on the left) and number (on the right) of consumed prey (Echinothrips americanus, Trialeurodes vaporariorum, Tuta absoluta) on prey density offered to females of Dicyphus errans.
