Introduction
Scale insects (Hemiptera: Sternorrhyncha: Coccoidea) are sap-sucking plant pests that cause huge agricultural and horticultural losses (Erler & Tunc, Reference Erler and Tunc2001; Ouvrard & Kondo, Reference Ouvrard and Kondo2013). Generally, they infest cultivated plants, fruit trees, ornamental shrubs, forest trees, greenhouse, and indoor plantings (Kaydan et al., Reference Kaydan, Atlihan, Uygun and Enal2012). Their eco-biological traits coupled with growing international trade of plants and plant products explain outbreaks of these insects observed on crops worldwide (Ouvrard & Kondo, Reference Ouvrard and Kondo2013). The Diaspididae is one of the major scale insect families that includes many species of severs pests. They attack several economic important crops such as citrus, apple, pear, walnut, and ornamental trees all over the world (Navea & Vargas, Reference Navea and Vargas2012). The oleander scale, Aspidiotus nerii Bouche (Hemiptera, Diaspididae), is a cosmopolitan pest, known from tropical and subtropical parts of the world, particularly in the Mediterranean region. It is a polyphagous pest that has been reported associated with more than 100 plant families (Einhorn et al., Reference Einhorn, Guerrero, Ducrot, Boyer, Gieselmann and Roelofs1998). Severe damage is caused on lemon and olive trees and ornamental and landscaping plants, such as oleander and acacia. Due to the occupation of niche on trees and armored nature, insecticides are largely ineffective (Uygun & Elekciouglu, Reference Uygun and Elekciouglu1998); therefore, parasitoids and predators are likely to be relatively more effective in controlling and managing such insect pests (Erler & Tunc, Reference Erler and Tunc2001). The predaceous coccinellids are more effective biological control agents than other organisms (Obrycki & Kring, Reference Obrycki and Kring1998). Coccidophagous coccinellids are reported as one of the most important predator groups of diaspidid insects in the world (Smith & Cave, Reference Smith and Cave2006). The predominately Australian Coccinellid predator Rhyzobius lophanthae is known as an effective natural enemy of armored scale insects. It has been introduced, inundatively released, and is commercially available in several parts of the world (Smith & Cave, Reference Smith and Cave2006; Branco et al., Reference Branco, Dalmau, Borges and Soares2017). It has some of the characteristic features such as specificity of prey, high fecundity and long adult longevity, no-diapause, heat resistance, good mobility, rapid population development (5–7 generations per year), and lack of parasitism and is observed to be the most important natural enemy of most armored scale species (Stathas, Reference Stathas2000a). Additionally, R. lophanthae was reported as a carnivore of soft scale insects. In Jordan, it was listed in the first list of Jordanian coccinellidae ‘as a coccidophagous’ (Allawi, Reference Allawi1989). However, there is a lack of biological studies about this species in the MENA region and this study was designed and aimed to fill this gap and to assess the potential of the Jordanian R. lophanthae population as a native predator of armored A. nerii based on the developmental duration and consumption rate of the immature stages at two different temperature regimes 25 ± 1 and 30 ± 1°C. This pest is attacking many major economic crops such as citrus and olive trees in the whole country causing a significant loss.
Material and methods
The scale insect, A. nerii was collected from acacia (Acacia cyanophylla Lindley) trees in the Swaileh area 113.5 Km north of Amman (32.036969N, 35.833347E, and elev. 844 m above the sea level), and reared under controlled conditions at 27 ± 2°C, 65–70% RH, and 16L:8D (light:dark). Three host plants were used for the scale insect stock culture: butternut squash, potato tubers, and sprouts and potted 1–2 years old acacia seedlings. Crawlers of A. nerii were transferred by tailed hairbrush onto the first two hosts and placed in wooden cage of 54 × 40 × 33 cm. Parts of infested potato tubers and acacia leaves were laid on the new acacia seedlings. The coccinellid, R. lophanthae was collected from acacia trees infested with scale insects. It was reared on leaves of acacia infested with A. nerii and butternut squash placed in plastic cages (20 × 12 × 9 cm) in an incubator at 25 ± 1°C, 50–65% RH, and 16L:8D for three generations.
Developmental duration and mortality rate
To calculate the incubation period of eggs, two groups of eggs (50 per each) were incubated at 25 ± 1 and 30 ± 1°C, 50–65% RH, and 16L:8D. Newly hatched larvae (>1 h age) of coccinellid predator were placed individually onto leaves infested with adults of A. nerii that were placed on moist petri dishes (5 cm) under two temperature regimes 25 ± 1 and 30 ± 1°C, 50–65% RH, and 16 L:8D. The development threshold and thermal constant of the R. lophanthae immature stages were calculated based on the formula K = D (T − t), where D = days for development at temperature T and t = the developmental threshold (Stathas, Reference Stathas2000b). Both groups of larvae were provided with fresh infested leaves daily until the pupation. The mortality rate and the developmental duration were recorded. The newly emerged adults were distinguished based on the last abdominal segments (fig. 1) (Stathas, Reference Stathas2001), and the sex ratio was calculated. Ten pairs of male and female were potted as couples into petri-dishes (9 cm) and provided with fresh infested leaves daily until they laid the first eggs and based on that the pre-oviposition of the adults was calculated.
Venter of abdomen of male (a) and female (b) of Rhyzobius lophanthae. fl, femoral line (Stathas, Reference Stathas2000c).
Consumption rate
The daily and total prey consumption rates were calculated for each larval instar. Each individual was separately reared in Petridish (9 cm) and was fed only on A. nerii.
Statistical analysis
A complete randomized design with one factor (two temperature regimes) was used. The analysis of variance and the least significant deference test (P = 0.05) in SAS (Version 9.4 for Windows; SAS Institute, Cary, NC, USA) were used to identify differences between temperature regimes.
Results
Developmental duration
The results indicated that the incubation period and developmental duration of R. lophanthae were significantly affected by the temperatures. The incubation period of eggs decreased significantly from 6.01 days at 30°C to 4.76 days at 25°C (table 1). The developmental time of pre- and post-embryonic stages and pre-oviposition period was longer at 25°C (27.5 days) and decreased significantly at 30°C (21.3 days). There were no significant differences between the first larval instar at 30°C (2.2 days) and third larval instar at 25°C (2.3 days). The development time of pupal stage was significantly shorter (3.5 days) at highest temperatures 30°C than this at 25°C (4.01 days). The pre-oviposition period significantly reduced from 4.71 days at 25°C to 3.23 days at 30°C. The development threshold and thermal constant of immature stages were 7.823°C and 472.379 degree-days, respectively.
Mean duration of pre-, post-embryogenic, and pre-oviposition stages of Rhyzobius lophanthae reared at (25 ± 1 and 30 ± 1°C, 50–65% RH, and 16 L: 8D). Duration of developmental stages (days) (mean ± SE).
*n number of replicates.
Means in rows followed by different letters are significantly different using LSD test at P < 0.05.
Mortality rate
Survival of eggs and immature stages was very high. There was no mortality during the incubation period (table 2). The total mortality rates between the immature stages were 3.33 and 6.77% at 25 and 30°C, respectively. At the lowest temperature (25°C), the mortality was recorded during the first larval instar with 3.33%. Whereas, the mortality at the highest temperature (30°C) was recorded during the first and third larval instars with 3.33 and 3.44%, respectively.
Mortality rate of immaturity stages of Rhyzobius lophanthae reared at (25 ± 1 and 30 ± 1°C, 50–65% RH, and 16L: 8D).
*n number of replicates.
Consumption rate
Consumption rate (numbers of consumed scale insect/different predator larval instars) for each larval instar of R. lophanthae at two temperatures is presented in table 3. All larval instars successfully penetrated the armored scale of the A. nerii adult at both temperatures and predated the whole adult. The total number A. nerii consumed by the coccinellid predator from the first larval instar to the end of fourth larval instar ranging from 24.3 at 25°C and 33.5 at 30°C. Mean number of consumed A. nerii increased evidently from the first larval instar to the last instar. At the two temperatures studied, the fourth larval instar was more voracious and significantly different from the other instars. Mean number consumed by fourth instar exceeded 60% of the total consumption.
Consumption rate (mean numbers of scale ±SE/day) by larval instars of Rhyzobius lophanthae at 25 ± 1 and 30 ± 1°C, 50–65% RH, and 16 L: 8D.
*n number of replicates.
Means in rows followed by different letters are significantly different using LSD test at P < 0.05.
Discussion
The Cooccinellid R. lophanthea has been introduced, released and proven as bio-control agent for wide spectrum of armored scale insects worldwide (Thorson, Reference Thorson2009). Many studies (Stathas, Reference Stathas2000a, Reference Stathas2000b, Reference Stathas2000c, Reference Stathas2001; Stathas et al., Reference Stathas, Elioul, Kontodimas and Siamos2002; Thorson, Reference Thorson2009) provided eco-biological information about this predator under laboratory and open field conditions. All these studies concluded that this predator reduced the population of all studied diaspidids, such as A. nerii, Chrysomphalus aonidum and Aonidiella aurantii. The current study aimed to test the ability of local R. lophanthae to consume and develop on the adult of A. nerii. It successfully developed and survived and the study confirmed the effect of temperatures on the predation capacity and all biological parameters of immature stages. The development threshold and thermal constant reported in this study were 7.823°C and 472.379 degree-days, respectively. Stathas (Reference Stathas2000b) reported that the development threshold of R. lophanthae immature stages range from 7.6 to 9.3 and the thermal constant was 443.5 degree-days. The temperature appears to alter biotic potential of the predators, which corroborates with earlier work (Stathas, Reference Stathas2000b). Hodek (Reference Hodek1973) and Hodek & Honek (Reference Hodek and Honek1996) confirmed that the quality of prey influences significantly the duration of the developmental period and consumption rate of the instars of coccinellid, and other factors (i.e., host plant and its stage) affect the biological characteristics, such as prey consumption, adult longevity, and fecundity. Şimşek et al. (Reference Şimşek, Karaca and Kayahan2016) reported the effects of armored species on the developmental times of immature stages of R. lophanthae. It seems that the developmental duration of coccidophagous coccinelllids is highly associated with the prey species. Such finding is confirmed by Uygun & Elekciouglu (Reference Uygun and Elekciouglu1998), where the developmental duration performed of coccinellid predator Chilocorus bipustulatus significantly varied with three studied armored scale insects: A. nerii, A. aurantii, and Pseudaulacapsis pentagona. The survival of R. lophanthea was very high at low temperatures (25 and 30°C) and low mortalities have been reported. Stathas (Reference Stathas2001) reported the same results with A. nerii but the mortality rates have been increased with other coccid species. The mortality rate obtained in this study and in previous study shows that the oleander scale is more preferable or a more suitable prey for R. lophanthae. The voracity and the effectiveness of coccinellids varied greatly in relation to species and developmental stage of coccinellid (Isikber & Copland, Reference Isikber and Copland2001). Branco et al. (Reference Branco, Dalmau, Borges and Soares2017) pointed that the disapidid Chrysomphalus dictyospermi is an essential prey for R. lophanthae and give better performance comparing with the other prey species that have been used in previous studies. In the present study, all larval stages showed good voracity capacity and it was very clear that the temperatures and the age of larvae influenced the consumption rate. It was significantly increased with the increasing temperatures as well as with aging. The highest consumption rate was recorded by the fourth larval instars, which appeared in the largest size and performed fastest mobility compared with the first three larval instars. Low number of preys consumed by first and second instars compared with other more developed predatory stages may be due to their small size, slow movement, and longer prey handling time (Barbar et al., Reference Barbar, Kerhili and Aslan2016). This study provides good information on the performance of R. lophanthae fed A. nerii. We believe the results and real observations from the field will be fruitful to consider the use of these common and widespread coccinellid as a biological control agent and the efficient breeding of these predator rearing programs. However, further research on their life table parameters, and functional and numerical responses, optimal release strategies, as well as the efficiency with other kinds of preys under various environment, i.e., fruit trees, open crops fields, plastic houses, nurseries, are needed for a better understanding of the role of these predators in the suppression of scale insects.
Acknowledgement
The author warmly thank the reviewer/s for their efforts, fruitful comments and improvements. Special thanks for the Bulletin of Entomological Research and willingness to publish this work.
