Abstract: The predatory effect of female adults of four Coccinellid species on two aphid species was examined under laboratory conditions in controlled environmental chambers. This study was conducted on single rose leaves in transparent small plastic cages at varying proportions of predator/total number of aphids. The predators used proved to be effective for the biological control of aphids under controlled conditions. It is proposed to use C. septempunctata in biological control programs in greenhouses and fully controlled conditions, only under high pest densities (at proportions over 1:30 predator/aphids). It is also proposed to use M. picta in biological control programs in greenhouses, as a specialized predator of A. spiraecola at proportions close to 1:30 predator/aphids. A. bipunctata can be used as a predator for T. aurantii at the same proportions. H. variegata can be used as a predator of both aphid species with satisfying effectiveness at proportions close to 1:30 predator/aphids.
INTRODUCTION
Biological pest management programs may involve (a) habitat modification, (b) use of resistance in plants (proper varieties) and (c) enhancement of naturally occurring biological control agents (Bottrell, 1979). Especially interactions of phytophagous species and their natural enemies are considered of great importance for biological control programs (Evans and England, 1996). The complexity of this relationship is based mainly on the predator effectiveness leading to a successful biological control program. Predator effectiveness is a presumption for the selection of a specific species (Deligeorgidis, 2002; Deligeorgidis et al., 2005a, b). Predaceous species in the families Anthocoridae, Coccinellidae, Chrysopidae, Hemerobiidae, are usually capable to maintain pest numbers below damaging levels (Onillon, 1990). Coccinellidae is a family of very capable predators that have been used for many years in biological control programs. Coccinellids are used in the biological control of aphids, thrips and whiteflies (Gerling, 1990; Holmer et al., 1993; Mari et al., 2005; Solangi and Lohar, 2005) in greenhouses and also in integrated control of field pests.
Seven-spotted ladybird Coccinella septempunctata L. (Coleoptera: Coccinelidae) is considered one of the most important species of coccinellids (Gordon, 1985), that have been used throughout Europe to control pests in glasshouse crops such as tomato, sweet peppers and cucumbers. C. septempunctata is also one of the most numerous coccinellid beetles in Greece (Deligeorgidis et al., 2005a,b). It is predaceous usually on aphids and additionally on thrips, whiteflies, mites and lepidoptera (Gordon, 1985). After hybernation in the adult stage, they spread to fields in early April or even March. Aphids can cause great damages to many plant species, but natural enemies such as C. septempunctata are very capable to control aphids’ population. The adults of C. septempunctata prefer aphids to feed and are reported as common aphid predators and thus they can be used in biological control programs (Sundby, 1966). In general, adult stages of C. septempunctata are more predaceous than larval stages (Sethi and Atwal, 1964; Agrawala and Saha, 1986; Singh et al., 1994; Kumari and Singh, 2000). The Two-spotted ladybird Adalia bipunctata L., is also a coccinellid beetle with similar appearance, shape and behavior to C. septempunctata. The Pine lady beetle Mulsantina picta Randall, also of the same family can be found in backyards or parks with small trees. It is carnivorous, eating preferably aphids or little insects found on apple or other trees. Adults also eat nectar or pollen. The Spotted amber ladybird Hippodamia variegata (Goeze) can be found also in backyards or parks or field margins of wild plants (Burgio et al., 2006), eating aphids, or little spiders, whiteflies or eggs of other insects, or even nectar and pollen. It is 4-5 mm long (Gordon, 1987), similar in shape to C. septempunctata and it is considered a very effective predator especially in mixed prey invasions in Greece (Bioinsecta prospectus, 2008). The Harlequin ladybird Harmonia axyridis (Pallas) is an Asian coccinellid species lately imported that pushes all other lady beetles out of the ecosystems. Competition is common among coccinellids and newly imported species like H. axyridis are usually better competitors (Kajita et al., 2000; Van Rijn et al., 2005). M. picta and H. variegata do not suffer yet from strong competition. H. axyridis is a typical coccinellid beetle that occurs in three main color forms: red or orange with black spots (known as form succinea); black with four red spots (form spectabilis) and black with two red spots (form conspicua). However, numerous intermediate and divergent forms have also been recorded (Koch, 2003). This species is also effective in mixed prey, especially the females (Soares et al., 2003).
Predatory effect estimations were based on various models (Holling, 1959a, b; Foglar et al., 1990; Deligeorgidis et al., 2005a, b). Prey density is correlated to individual predator consumption of prey. If natural deaths (or other sources of mortality) of prey are ignored, this may lead to approximate measurements (Wiedenmann and O’Neil, 1990). For a fast and simple estimation of effective predation and prey preference, the method proposed by Deligeorgidis et al. (2005a, b) was found to be satisfactory (Deligeorgidis et al., 2005b, c). In this study, a laboratory estimation of the predatory effect under controlled conditions of two-day old female adults of four coccinellid species on two aphid species was conducted. The aim was to propose an estimation index for effective predation based on survivorship rate of prey (Deligeorgidis et al., 2005a, b). This index was based on theoretical mathematical models for fast and easy estimation of predation efficiency under controlled conditions.
MATERIALS AND METHODS
The predatory effect of four coccinellid species Coccinella septempunctata L., Adalia bipunctata L., Mulsantina picta Randall and Hippodamia variegata (Goeze) was studied in 2007 on two common aphid species, green aphid Aphis spiraecola Patch and black aphid Toxoptera aurantii (Boyer) (Homoptera: Aphididae) using a series of experiments in small cages. The basic experimental unit was a single rose leaf (approximately 45 cm2) in a 7x7x7 cm clear plastic cage (a little smaller in comparison to the cages used by Deligeorgidis et al., 2005a, b). The cages had one hole of 6x5 cm covered with muslin cloth (0.06 mm opening) for airing and a wet piece of cotton for moisturizing air. Each rose leaf in the cage was held away from the upper internal part of the cage with sticky tape. One 2-day old female of each of the four coccinellid species were introduced separately into each cage containing 10, 20, 30 or 40 aphids. Each treatment was replicated 8 times. Four more cages for each aphid species were used as control (check). In these cages there were 10, 20, 30 or 40 aphids per cage but in absence of predators and aphid mortality was measured after 24 h. The four different pest densities used in this study were considered satisfactory for data analyses and suitable for second-degree models (Snedecor and Cochran, 1980). An estimation of H. axyridis predatory effect on A. spiraecola was made, but based only on four replications (results are not presented).
The predators were starved for 24 h before use (Kumar et al., 2002; Deligeorgidis et al., 2005a, b). The predators and aphids used for the experiment were obtained from laboratory colonies that were maintained for nine months at 25±1°C. After introduction of the aphids and the predator, cages were held in controlled environment chambers at a temperature of 23±1°C, 67±2% relative humidity (RH), with a 16 h light : 8 h dark photoperiod and intensity of light 9000 Lux and survivorship of aphids was measured after 24 h (Deligeorgidis et al., 2005a, b). Estimations of the predation effect of the four predators were based on the percentage of aphids consumed by the predator. Statistical analysis was based on both the original data and transformed data according to the formulas below, but original data presented in tables:
(adaptation from Snedecor and Cochran, 1980)
RESULTS
Analysis of variance on the original and transformed data revealed statistically significant differences on the efficiency of predators (Table 1). The number of aphids consumed by the individual predators ranged between 8 and 30 aphids and increased as the number of aphids in the cage increased. At the highest prey density of 40 aphids per cage, M. picta and A. bipunctata consumed the greatest number of A. spiraecola while H. variegata consumed the greatest number of T. aurantii. More A. spiraecola was consumed by predators than T. aurantii (Table 1). The total number of prey consumed for both aphid species was lower for C. septempunctata than the other predators. Predatory efficiency was the highest for A. bipunctata and H. variegata.
| Table 1: | Mean number of aphids (1: A. spiraecola, 2: T. aurantii) consumed by the 4 Coccinellidae (C. septempunctata, A. bipunctata, H. variegata, M. picta) at the 4 levels of prey density |
| |
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| SE = 0.75, F = 71.155, p<0.001 | |
The predatory efficiency of the four predators on A. spiraecola are shown in Fig. 1. The predatory effect of C. septempunctata was described by the relation y = -0.038x2+2.289x-8.412 (R2 = 0.65) while that for A. bipunctata was y = 0.033x2-1.472x+29.219 (R2 = 0.75). Similarly, the effect of H. variegata on A. spiraecola was described by the equation y = 0.014x2-0.056x+4.896 (R2 = 0.75) and predatory effect of M. picta was y = 0.007x2 + 0.866x - 1.823 (R2 = 1).
| Fig. 1: | Second-degree model describing the relation between the total number of green aphids A. spiraecola (Total number of aphids) and the percentage (%) of insects that may survive (Aphids escaped%) |
| Fig. 2: | Second-degree model describing the relation between the total number of black aphids T. aurantii (Total number of aphids) and the percentage (%) of insects that may survive (Aphids escaped%) |
Similar relations were observed for the predators on T. aurantii as for A. bipunctata as shown in Fig. 2. Finally, the equation describing predatory effect of H. axyridis on A. spiraecola was estimated as y = -0.042x2+2.271x-6.411.
DISCUSSION
The female adults coccinellids used in this study proved to be very capable predators. Coccinellid adults or late-instars larvae are considered more capable predators (Hagen, 1962; Sethi and Atwal, 1964; Singh and Malhotra, 1979; Mahmood and Mahmood, 1986; Agrawala and Saha, 1986; Singh et al., 1994; Kumari and Singh, 2000). For these attributes coccinellids are commercially used as biological control agents against whiteflies, thrips and aphids (Lenteren and Woets, 1988). Kumar et al. (2002) and Deligeorgidis (2002) used their findings as indicative parameters for biological control programs. Kumar et al. (2002) also consider C. septempunctata as a capable predator of L. erysimi.
In our study, all the coccinellid species exhibited almost the same predatory efficiencies except M. picta on T. aurantii. M. picta was rather effective at low densities of T aurantii than at high densities. Based on the total number of aphids preyed, A. bipuntata, H. variegata and M. picta were the more effective predators for the two aphid species than C. septempuntata.
The behavior of predators described by the second-degree models (Deligeorgidis et al., 2005a, b), involving number of individuals of prey that are consumed or the percentage of individuals of prey that escaped, revealed more than one factor for reducing efficiency of predation: (a) the predator’s failure because of aphids escape due to low rate of handling prey or low ability to find prey and (b) the hunger satiation of the predator.
Among aphid species, Macrosiphum euphorbiae (Thomas) is preferred to Myzus persicae (Sulzer) by the predator C. septempunctata (Shands and Simpson, 1972). Deligeorgidis et al. (2005b), reported that C. septempunctata adults prefer aphids (M. euphorbiae) than thrips (Thrips tabaci Lindeman) or whiteflies (Trialeurodes vaporariorum Westwood). Deligeorgidis et al. (2005a, b) used a derivation on second-degree models to define effective predation rate and subsequently the proportion of predators/aphids for effective predation. They proposed that intercept (a-value) defines the prey preference and slope (b-value) the proportion for effective predation. They also concluded that effective predation is correlated with predator/prey ratio rather than to prey preference. In our study there was not any apparent preference for the aphid T. aurantii among the four coccinellid species. Contrarily, there was a preference for green aphid A. spiraecola from H. variegata and M. picta.
When initial number of aphids is high, C. septempunctata was found to be less effective (Deligeorgidis et al., 2005a, b). They considered that a proportion close to 1:30-1:35 predator/aphids was satisfactory for biological control under controlled conditions. The authors explained that, at these proportions (1:30-1:35), only 20-25% of individuals of the aphid M. euphorbiae escaped, while 40-50% of thrips and 60-70% of whiteflies escaped. Triltsch and Roßberg (1997) reported that predation rate of C. septempunctata on cereal aphids was higher when aphid density was higher and was depended on temperature conditions without determining upper limit. In caged field experiments, hunger of the predators declined with decreasing aphid availability (Frazer and Gill, 1981). In this study, only M. picta on the black aphid T. aurantii in high prey densities (a proportion over 1:30 predator/aphids) was found to be relatively ineffective, may be because of
early hanger satiation and thus it cannot be proposed for biological control of T. aurantii. According to our findings, A. bipunctata and H. variegata are considered better predators of T. aurantii. At low prey densities (10 aphids), A. bipunctata seems not to prefer A. spiraecola, revealing possible difficulties on finding A. spiraecola, M. picta showed a more stable behavior and thus it can be proposed for biological control of A. spiraecola. C. septempunctata showed an unstable behavior at the relatively low proportion of 1:20 predator/aphids, resulting in negative curves, indicating that this species may be more effective at higher prey densities. Furthermore, this kind of behavior may reveal slower hanger satiation of this species. It is possible that a few predators did not reach hanger satiation at these populations of prey. In general, data from all coccinellid species showed that at proportions 1:40 (predator/aphids) only 20-25% of aphid individuals could escape, except for M. picta on T. aurantii (35% escaped).
As a conclusion, according to the results of this research, the four coccinellid species have been proved effective predators for biological control programs under controlled conditions (no renewing of prey populations). It is proposed to use C. septempunctata in biological control programs in greenhouses, only under high pest densities (especially at proportions 1:40 predator/aphids or even higher). It is also proposed to use M. picta in biological control programs in greenhouses, as a specialized predator of A. spiraecola at proportions near 1:30 predator/aphids. A. bipunctata can be used as a predator for T. aurantii at the same proportions. H. variegata can be used as a predator of both aphid species with satisfying effectiveness at proportions near 1:30 predator/aphids and this might be the reason for being effective also in mixed prey. Combination of predator releases may be ineffective due to competition between coccinellidae species (Kajita et al., 2000; Van Rijn et al., 2005).
The predators’ behavior in open agrosystems may be different according to the literature, because hunger and predatory effect are influenced by many factors (Van Lenteren, 2000; Deligeorgidis et al., 2005a, b). Additionally, competition among various predator species may affect predators’ effectiveness (Kajita et al., 2000; Deligeorgidis et al., 2006). Wiedenmann and O’Neil (1990) tried to relate laboratory experiments to open field trials and stated that this could be done but only for specific stages of the insects and under controlled conditions. Van Lenteren (2000) stated that greenhouses are isolated units and this isolation prevents massive immigration of pest organisms. Furthermore, a limited number of pest species occurs in greenhouses and this makes biological control easier because natural enemies of only a few pest species have to be introduced.