- Email: [email protected]
Classical Biological Control ofPalaeococcus fuscipennis(Burmeister) (Homoptera: Margarodidae) in Israel
12, 151–157 (1998) BC980621
BIOLOGICAL CONTROL ARTICLE NO.
Classical Biological Control of Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) in Israel1 Zvi Mendel,* Fabienne Assael,* Suheil Zeidan,† and Amiram Zehavi† *Department of Entomology, ARO, The Volcani Center, Bet Dagan 50250, Israel; and †Forests Department, Keren Kayemet LeYisrael, Eshta’ol 99775, Israel Received August 18, 1997; accepted February 24, 1998
Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) is rarely observed in pine forests in Mediterranean and Central European countries. It was discovered in Israel in 1990 in a single pine stand in Nahal ‘Iron (northern Samaria). Between the time of its detection and the summer of 1996, the scale insect had spread to the NE and NW, infesting 1300 ha of forest of Pinus brutia ssp. brutia Tenore, P. halepensis Miller, P. pinea L., and P. canariensis C. Smith. Infested trees were covered with honeydew and with stems and crowns displaying thick layers of sooty mold. Association of the scale with several predacious arthropods, including large populations of the coccinellid Rodolia cardinalis Mulsant (Coleoptera: Coccinellidae), failed to reduce its population level and spread to new plantations. In 1994 and 1995 two specific natural enemies of P. fuscipennis, the coccinellid Novius cruentatus Mulsant and the parasitoid Cryptochetum jorgepastori Cadahia (Diptera: Cryptochetidae), were introduced from ‘‘Marismas del Dial Nature Reserve’’ SE of Huelva in southern Spain and released at a single site in ‘Iron forest in Nahal ‘Iron. In the summer of 1996, both enemies were detected over most of the range of the pest. A large decrease in the pest’s population density and in the sooty mold cover was observed at the site of release of its natural enemies. Our findings suggest that N. cruentatus is the major contributor so far to the population reduction of P. fuscipennis. r 1998 Academic Press Key Words: biological control; Palaeococcus fuscipennis; Homoptera; Margarodidae; Rodolia cardinalis; Coleoptera; Novius cruentatus; Coccinellidae; Cryptochetum jorgepastori; Diptera; Cryptochetidae; Pinus brutia ssp. brutia; Pinus halepensis.
INTRODUCTION
Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) has been recorded from the northern
1 Contribution from the Agriculture Research Organization, The Volcani Center, Bet Dagan, 50250 Israel, No. 2244-E, 1997 series.
Mediterranean region, Morocco, and southern and central Europe (Cadahia, 1982; Kosztarab and Kozar, 1988; and literature cited therein) (Fig. 1). P. fuscipennis is probably the only species of the genus; the attribution of Palaeococcus brasiliensis (Walker) to the genus is doubtful (Morrison, 1928). P. fuscipennis infests Pinus halepensis Miller, Pinus brutia ssp. brutia Tenore, P. pinea L, and P. pinaster Aiton as well as Cedrus atlantica Manetti (Cadahia, 1982). Since P. fuscipennis is known to develop only on Pinaceae, the report of its occurrence on the broadleaved genera Acer L. and Quercus L. (Kosztarab and Kozar, 1988) is probably erroneous. Like other monophlebids, P. fuscipennis feeds on phloem and secretes honeydew. In the Mediterranean area it has two generations per year (Schimischek, 1944; Cadahia, 1982). Until the 1970s, P. fuscipennis outbreaks were generally unknown (Escherich and Baer, 1913; Balachowsky, 1932; Schimischek, 1944; Kosztarab and Kozar, 1988) except for one outbreak on mature trees of P. pinea in a nature reserve near Huelva in southern Spain. The outbreak was attributed to aerial insecticide applications to surrounding salt marshes to control mosquitoes (Cadahia, 1982). Principal predators of monophlebids (e.g., the genera Icerya Signoret, Monophlebus Burmeister, Palaeococcus Cockerell) are coccinellids, viz. the genera Rodolia Mulsant and Novius Mulsant (Hodek, 1996), and the principal parasitoids are flies in the genus Cryptochetum Rondani (Diptera: Cryptochetidae) (Menon, 1949; Cadahia, 1984). P. fuscipennis is attacked by three specific natural enemies: Novius cruentatus Mulsant, which occurs throughout the scale’s natural range (Escherich and Baer, 1913; Schimischek, 1944); Cryptochetum buccatum Hendel, indigenous to western Europe; and Cryptochetum jorgepastori Cadahia from southern Spain (Cadahia, 1984). Since the early 1990s, P. fuscipennis has been found on planted pine in few plots in Nahal ‘Iron in northern Samaria, causing thick layers of sooty mold on stems and crowns. The present study describes the first
151
1049-9644/98 $25.00 Copyright r 1998 by Academic Press All rights of reproduction in any form reserved.
152
MENDEL ET AL.
FIG. 1. Natural range of Palaeococcus fuscipennis (the blacken area) until 1990 (after Balachowsky 1932; Schimischek, 1944; Kosztarab and Kozar, 1988).
record and spread in Israel of P. fuscipennis and the acclimatization of two principal natural enemies. MATERIALS AND METHODS
Survey of P. fuscipennis in Nahal ‘Iron The distribution of P. fuscipennis in northern Samaria was surveyed at 6-month intervals in the planted pine in ‘Iron, Megido, and Gal’ed forests on both sides of Nahal ‘Iron (a valley in northern Samaria). Its presence was determined as follows: trees with honeydewcontaminated bark with spots of sooty mold or with foraging honeybees were closely examined for the occurrence of any development stages of the pest. The suspected trees were examined by having the bark scale removed from at least 2500 cm2 of the mid-stem surface of a minimum of 20 randomly selected trees per plot. All four pine species planted in Nahal ‘Iron, P. halepensis, P. brutia ssp. brutia, P. pinea, and P. canariensis, were examined. Sampling of Arthropods Associated with P. fuscipennis in 1991 In May 1991, 10 randomly selected trees of P. halepensis and P. brutia ssp. brutia in an infested site (plot No. 07, in Yaar Katzir, planted in 1971) in ‘Iron Forest were cut and examined for natural enemies of P. fuscipennis. Both pine species were also infested by Matsucoccus josephi Bodenheimer and Harpaz (Homoptera: Matsucoccidae), but unlike P. halepensis the latter pine species did not display chronic injury by M. josephi (e.g., Mendel et al., 1994). From each tree, between 4
and 5 stem sections with approximately 2000-cm2 bark area were collected. These stem collections consisted (as far as possible) of two rough bark samples and three partly smooth bark samples. All insects on these stem sections, except for M. josephi, were removed and counted. The arthropods found were divided into three groups: (i) common species associated with P. halepensis infested with M. josephi, (ii) rare species on pine, infested or not infested by M. josephi and present in high numbers on trees infested by P. fuscipennis; and (iii) species occurring in small numbers and not related to the presence of P. fuscipennis. Collection of Natural Enemies of P. fuscipennis in Spain Natural enemies were collected in the La Cascatera woodland located on sand ridges forming part of the Spartina swamps of the Marismas del Dial Nature Reserve, SE of Huelva, where significant populations of P. fuscipennis existed. Collections were made in March 1994 and in April 1995. Collections included adult females of P. fuscipennis and larvae, pupae, and adult coccinellids occurring on a group of four trees of P. pinea infested with P. fuscipennis. The material was shipped to Israel. Release and Sampling to Assess Establishment of N. cruentatus and C. jorgepastori Releases of adult natural enemies were made in a single heavily infested plot in ‘Iron forest (Plot No. 08, planted in 1951). In 1994, from 25 April to 5 May, we
153
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis
released ca 270 N. cruentatus and ca 365 C. jorgepastori, and from 3 to 30 May 1995, 250 N. cruentatus and 285 C. jorgepastori. Sampling to detect the released flies was conducted in six mature stands (age of 22–45 years) each with an area of 4–7 ha. Stands consisted of two plots of P. halepensis, two plots of P. brutia ssp. brutia, a plot planted with both pine species, and a plot of P. canariensis. The plots were at a distance of 0.5–5 km from the release plot. Annual surveys were carried out during April and May 1994–1996. Since tree cutting was restricted, the sampling was conducted by several persons. A minimum of 150 gravid females of P. fuscipennis was collected. In the P. canariensis stand only 130 individuals could be found. The sample size of females per plot ranged between 150 and 280. The collected females were placed in petri dishes for 2 months at 25°C. Then the number of parasitized females was counted. Sampling of coccinellids in Nahal ‘Iron was conducted in four of the above-mentioned plots of P. halepensis and P. brutia ssp. brutia, located at a distance of 0.5–2 km from the release plot. Annual samplings were undertaken during April of 1993–1997. The samplings were conducted by three persons during 20 min (an hour’s walk), in each of the four study plots. Larvae, pupae, and adult beetles were collected. The development stages were segregated and kept in different rearing boxes. The larvae were fed with larvae and ovisacs of P. fuscipennis and most of them developed to adults.
Sampling of P. fuscipennis in the Release Plot The sampling of P. fuscipennis was conducted once a year during late April or early May between 1993 and 1996 in the release site (plot No. 08 in ‘Iron Forest). Since the plot was a recreation site, only five trees of P. halepensis or P. brutia ssp. brutia were cut each time. Adult females were collected from a 3–4 m length section of the mid stem, and their density per 1000 cm2 of the bark surface was calculated. RESULTS
Occurrence of P. fuscipennis in Israel Since the time of its discovery in Israel, P. fuscipennis has spread to the NE and NW in pine plantations on both sides of the Nahal ‘Iron valley, infesting 1300 has of pine (Fig. 2). Based on sooty mold coverage, mature P. brutia ssp. brutia and P. halepensis were more severely affected than P. pinea and P. canariensis. Twoto 5-year-old seedlings were not naturally infested by the scale, but were suitable host plants when artificially infested in a greenhouse. Observation in Nahal ‘Iron showed that adult males and ovisacs were present during October–September and April–May, indicating that there are two generations per year in Israel. Initial infestations of P. fuscipennis were on the mid-stem section of the tree on recently pealed bark partly covered by flakes. Heavily infested trees, from mid-stem sections to top, were covered with honeydew, and stems and part of the crown displayed thick layers
FIG. 2. Annual increase in forest area affected by Palaeococcus fuscipennis at Nahal ‘Iron, Israel.
154
MENDEL ET AL.
of sooty mold. It took 4–5 years for the scale population to cover most of the stem with sooty mold in two artificially infested 15-year-old trees. Damage Observations on heavily infested trees did not reveal direct injury to the plants by scale feeding. However, the thick layers of sooty mold caused forest rangers to suspect possible damage to the trees by increased heat absorption of the black bark. Visitors to the camping sites in ‘Iron forest were inconvenienced by honeybees and hornets that swarmed around honeydew-covered trees. Arthropods Associated with P. fuscipennis before the Release of Exotic Natural Enemies Arthropods found in 1991 on felled trees in heavily infested plot in ‘Iron forest consisted of M. josephi and its principal associates, Elatophilus hebraicus Pericart, Dufouriellus ater (Dufour) (both, Heteroptera: Anthocoridae), Ulrike syriaca (Steinmann) (Neuroptera: Raphidiidae), and Cryptolestes sp. (Coleoptera: Cucujidae). A second group of arthropods on infested pines was composed of Rodolia cardinalis (Mulsant), which was the most common associate of P. fuscipennis. On heavily infested trees hundreds of pupae of R. cardinalis were counted. The beetle population had been conspicuous already in 1990 on the first affected trees. Observations suggested that both larvae and adults of R. cardinalis fed mainly on the egg masses but not on mature larvae or adults of P. fuscipennis. Homalotylus flaminius (Dalman) (Hymenoptera: Encyrtidae) emerged from larvae of R. cardinalis and was very common on infested sites in Nahal ‘Iron. Adults of Erythraeus sp. (Acarina: Erythraeidae) were collected for the first time in Israel from trees infested with P. fuscipennis. The mites were carried by P. fuscipennis searching for ovipositing sites. Other common associates were larvae and adults of Dapsa inornata Gorhan (Coleoptera: Endomychidae) that fed on sooty mold and larvae of Dioryctria spp. (Lepidoptera: Phycitidae) boring in the cork and cortex of bark covered with honeydew. A third group on felled trees in heavily infested plots in ‘Iron forest consisted of Crysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Orius minutus (L.) (Heteroptera: Anthocoridae). These species have occurred in very small numbers and are not related to the presence of P. fuscipennis. The presence of these entomophagous arthropods failed to prevent the continuous expansion of the range of P. fuscipennis and damage was not prevented. None of P. fuscipennis’ important known natural enemies in the western Mediterranean region were found in Nahal ‘Iron.
Collection of Natural Enemies of P. fuscipennis in Spain The P. pinea trees in the Spartina swamps near Huelva were not conspicuously covered by sooty mold and, based on the time needed to collect the females, we estimated that the density of P. fuscipennis was much lower than that on heavily infested P. halepensis and P. brutia ssp. brutia trees in ‘Iron forest. In 1994 we collected in the Spartina swamps area from the group of P. pinea trees approximately 250 mature females of P. fuscipennis and several hundred larvae and pupae of N. cruentatus. In April 1995, ca 200 females of P. fuscipennis and ca 350 larvae and pupae of N. cruentatus were collected. About half of the females collected in 1994 and almost all of the females collected in 1995 were parasitized by C. jorgepastori. Larvae of N. cruentatus collected in Spain were reared to adult in the laboratory on P. fuscipennis collected in ‘Iron forest. Recoveries of N. cruentatus and C. jorgepastori at Release Locations The first recovery of N. cruentatus was as pupae collected in July 1995. From coccinellid pupae collected during 1992–1994 only R. cardinalis emerged. In October 1995, 17 months after the first release of N. cruentatus, among the ca 300 coccinellid pupae collected in the release plot, 17 (5.6%) consisted of pupae of N. cruentatus; the rest were R. cardinalis. Since 1996 partial displacement of R. cardinalis by N. cruentatus has occurred. In April 1996, collections of adult coccinellids showed significantly more individuals per sample of N. cruentatus (49.7 6 11.6) than R. cardinalis (26.5 6 4.9) (PT 5 t 5 0.009, df 5 3, two-tail t test). In April 1997, N. cruentatus was found in all infested plots and 91.2% of all coccinellids associated with P. fuscipennis were N. cruentatus (Fig. 3).
FIG. 3. Shift in occurrence between Rodolia cardinalis and Novius cruentatus (mean percentages 6 SD in composite samples) at a camping site in Nahal ‘Iron, Israel.
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis
C. jorgepastori was first recovered at release sites in Israel in October 1995, following its release in 1994. C. jorgepastori were recovered in October 1995 from four of six sampled plots in Nahal ‘Iron. In April 1996 it was found at Megido forest, at a distance of 5 km from the point of release at ‘Iron forest; parasitism in samples reached 3.4% of adult female scales. Occurrence of P. fuscipennis in 1996 Our observations suggest that the spread of P. fuscipennis stopped after 1996 (Fig. 2). As a result of the interaction between P. fuscipennis and the introduced predator and the parasitoid, the mean number of female P. fuscipennis per 1000 cm2 of bark in the release plot in ‘Iron forest has decreased from 115 6 58 in 1993 to 3 6 5 in 1996 (Fig. 4). Black bark has decreased steadily with the reduction in honeydew production and natural peeling of the sooty moldcovered flakes. The level of infestation revealed by the intensity of sooty mold at newly infested sites did not reach that of the initially infested plots. Hence, the occurrence of the scale at these sites was not detected by the forest rangers. DISCUSSION
Despite numerous insect surveys conducted in local pine forests P. fuscipennis was unrecorded in Israel before 1990. P. fuscipennis was accidentally discovered in Israel in 1990 on a few trees in a single pine stand in ‘Iron forest on the western slopes of Nahal ‘Iron (Mendel et al., 1991a). At that time, the scale population was not recognized as a new introduction because this scale occurs naturally on P. halepensis and P. brutia ssp. brutia in other areas of the Near East. Several other distinctive pests of pine in Israel ‘‘crossed’’ the observation threshold due to the increasing area covered with pine and the increasing age of potential hosts. For
FIG. 4. Mean density (6SD) of females of Palaeococcus fuscipennis per 1000 cm2 pine bark at a camping site in Nahal ‘Iron, Israel.
155
example, galleries of Tomicus destruens (Wollaston) (Coleoptera: Scolytidae) were found in Israel in the early 1960s, but the first outbreak did not occur until 1978 (Mendel et al., 1985). From the pattern and speed of dispersal of P. fuscipennis in Nahal ‘Iron (‘Iron forest and two adjacent forests) it is believed that the pest arrived in Israel in the late 1980s and was not accompanied by its principal enemies. How this scale reached Israel is unknown. Two potential methods, on nursery stock of pines or logs by camper traffic between Israel and its northern neighboring countries, can be excluded because of legal and political restrictions in these countries. This suggests that the appearance of P. fuscipennis in northern Samaria may be the result of its spread by migratory song birds. Samaria is within the seasonal migration route along the Afro-Syrian rift from Eastern Europe and Russia to Africa. It has been suggested that about 8% of the 5 billion birds that migrate from the Western Palearctic to Africa each autumn fly across Israel and the Jordan Valley (Frumkin et al., 1995). Birds are known to carry eggs and crawlers of small insects (McClure, 1990). Until the late 1980s, honeydew-producing Coccoidea on pine in Israel were represented by a single and rather rare species—Phenacoccus yerushalmi Ben-Dov (Pseudococcidae). The rapid buildup of the population of P. fuscipennis on P. halepensis and P. brutia spp. brutia in Nahal ‘Iron created a new type of injury to pine in Israel. Although the direct impact of sooty mold was not investigated, there is little doubt that the dirty appearance of the blackened trees and swarms of bees and hornets feeding on honeydew necessitated biological control of the scale. The high-density population of P. fuscipennis and intensive honeydew production led to a marked change in the arthropod complex on the pine stems. Due to the ample honeydew supply, the forest became an important foraging area for honeybees, especially during the winter and mid-summer when sources of nectar are limited. The unusually high densities of larvae of Dioryctria spp. may be explained by attraction of the adults to the honeydew, whereas the frequent occurrence of D. inornata is related to the fresh sooty mold. The occurrence of Erythraeus sp. for the first time in Israel in ‘Iron forest is also related to the appearance of P. fuscipennis in the area. Although the role of the mite is not yet clear, it is noteworthy that larvae of Erythraeidae usually parasitize arthropods, whereas their nymphs and adults are predators (Gerson and Smiley, 1990). The contribution of the predaceous mite Erythraeus sp. to the control of P. fuscipennis is limited. E. hebraicus Pericart, D. ater (Dufour), U. syriaca (Steinmann), and Cryptolestes sp. are common associates of M. josephi and occur on P. halepensis and P. brutia ssp. brutia in other areas of the eastern Mediterranean
156
MENDEL ET AL.
(Mendel, 1992). However, while E. hebraicus Pericart is a specific predator of M. josephi (Mendel et al., 1991b), the other species may feed also on P. fuscipennis. R. cardinalis was probably attracted from the adjacent citrus groves and gardens by the high density of P. fuscipennis and was the most common natural enemy in Nahal ‘Iron. Reproducing populations of this beetle were not expected to occur in pine forests in Israel because appropriate prey species did not occur on pine in Israel. R. cardinalis is the principal enemy of Icerya purchasi Maskell but may feed and develop on other Monophlebinae (Caltagirone and Doutt, 1989), although with a resulting lower reproductive capacity (Mendel et al., 1993). Prey used by Coccinellidae may be classified as essential, acceptable, alternative, or rejected (Hodek, 1996). It is accepted among coccinellid researchers that only an essential food is suitable for a beetle to complete its development. The level of prey specificity in the Coccinellidae is not always clear, with specialization becoming apparent within individual tribes. Limited information, however, is available regarding the tribe Noviini. For example, under controlled conditions Rodolia iceryae Jenson fed on Icerya aegyptiaca Douglas but laid no eggs. The beetle fed and laid eggs on plants infested with I. purchasi, but the larvae that developed on I. purchasi died during pupation (Mendel and Blumberg, 1991). Similarly, we suggest that P. fuscipennis is not an essential prey of R. cardinalis, although the beetle may complete its development on P. fuscipennis when scale egg masses are available. Egg masses are more appropriate food in such cases. For example, larvae of R. cardinalis died when they fed on larvae or adults of I. purchasi that infest plants with high levels of alkaloids, but could develop and reproduce to some extent on egg masses of I. purchasi produced on those plants (Mendel et al., 1993). Marginal suitability of P. fuscipennis as a food source may explain why R. cardinalis was unable to limit the increase and spread of the population of P. fuscipennis. The frequent occurrence of the larval parasitoid H. flaminius reflected the abundance of R. cardinalis larvae on the infested sites. Homalotylus spp. are principal parasitoids of Coccinellidae (Myartseva, 1981). H. flaminius is a common parasitoid of R. cardinalis (Bodenheimer, 1951), but has not been collected in citrus groves in Israel during the last decade (D. Blumberg and Z. Mendel, unpublished). In previous biological control projects of monophlebids, the introduction of a species of Cryptochetum was aimed at the control of I. purchasi and Icerya seychellarum (Westwood). Successful or partial control of other Icerya spp. was obtained by introduction of Rodolia spp. (Bartlett, 1978). The present case is the first successful trial of acclimatization of N. cruentatus and C. jorgepastori. The success of establishment of the
introductions was expected, since the species were introduced into a forest area which is very similar to their natural habitat and with no interference from insecticides. Present data suggest that N. cruentatus is the major contributor to the population reduction of P. fuscipennis in Israel. The biological control of I. purchasi in California, which was repeated in many areas, was achieved by the introduction from Australia of both R. cardinalis and Cryptochetum iceryae Williston (Caltagirone and Doutt, 1989). Several studies showed that the fly is more effective than the beetle in cool areas, although it occurs throughout most of the range of I. purchasi (Quezada and DeBach, 1973; Prasad, 1989). C. iceryae was introduced into Israel from California in 1988, ca 60 years after the introduction of R. cardinalis, to complete the biological control, and both enemies are required for efficient control of I. purchasi in citrus and ornamentals (Mendel and Blumberg, 1991). However, from the present experience of better recovery of the beetle it seems that N. cruentatus is relatively more effective than C. jorgepastori at high prey densities. However, as the scale population decreases to lower levels, C. jorgepastori may end up playing a more important role in regulating the pest at low population levels. ACKNOWLEDGMENTS We thank our colleague Leandro Gonzalez Tirado and Pedro Miguel Bernabe Ruiz from the Servicio de Proteccio´n de los Vegetales de la Junta de Andalucia, Huelva, our Israeli colleagues David Nestel and Rene Karschon, for their assistance in collecting the natural enemies in southern Spain, Nitza Saphir of the Forests Department of JNF, Israel, for her help in the sampling of P. fuscipennis and its natural enemies, Uri Gerson from the Faculty of Agriculture, the Hebrew University of Jerusalem, for the identification of Erythraeus, and two anonymous reviewers for their valuable comments to a previous version of the manuscript.
REFERENCES Balachowsky, A. 1932. ‘‘Etude biologique des coccides du bassin occidental de la Mediterrane´e. Encyclope´die Entomologique,’’ Vol. 15. P.LeChevalier, Paris. Bartlett, B. R. 1978. Margarodidae. In ‘‘Introduced Parasites and Predators of Arthropods and Weeds: A World Review’’ (C. P. Clausen, Ed.), pp. 132–137. USDA Agric. Handb. No. 480. Bodenheimer, F. S. 1951. ‘‘Citrus Entomology in the Middle East.’’ Junk, The Hague. Cadahia, D. 1982. Palaeococcus fuscipennis Burm. (Homoptera: Margarodidae), plaga de los pinares de la costa de Huelva. Bol. Serv. Plagas 8, 201–214. Cadahia, D. 1984. El intere´s biolo´gico del ge´nero Cryptochaetum Rond. Diptera: Cryptochaetidae y descripcio´n de una nueve espe´cie. Bol. Serv. Plagas 10, 159–184. Caltagirone, L. E., and Doutt, R. L. 1989. The history of the vedalia beetle importation to California and its impact on the development of biological control. Annu. Rev. Entomol. 34, 1–16.
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis Frumkin, R., Pinshow, B., and Kleinhaus, S. 1995. A review of bird migration over Israel. J. Ornithol. 136, 127–147. Escherich, K., and Baer, E. 1913. Tharandter zoologische Miszellen. Nat. Z. Forst. Landwirtschaft. 11, 98–129. Gerson, U., and Smiley, R. L. 1990. ‘‘Acarine Biocontrol Agents.’’ Chapman & Hall, London. Hodek, I. 1996. Food relationships. In ‘‘Ecology of Coccinellidae’’ (I. Hodek, and A. Honek, Eds.), pp. 143–238. Kluwer Academic, London. Kosztarab, M., and Kozar, F. 1988. ‘‘Scale Insects of Central Europe.’’ Akademiai Kiado, Budapest. McClure, M. S. 1990. Role of wind, deer, and humans in the dispersal of the hemlock woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 19, 36–43. Mendel, Z. 1992. The occurrence of Matsucoccus josephi in Cyprus and Turkey and its relation to decline of Aleppo pine. Entomol. Gen. 17, 299–306. Mendel, Z., and Blumberg, D. 1991. Colonization trials of Cryptochaetum iceryae and Rodolia iceryae for improved biological control of Icerya purchasi in Israel. Biol. Control 1, 68–74. Mendel, Z., Golan, Y., and Madar, Z. 1985. Comparison of the seasonal occurrence and behavior of seven pine bark beetles (Coleoptera: Scolytidae) in Israel. Phytoparasitica 13, 21–32. Mendel, Z., Zehavi, A., and Zeidan, S. 1991a. Palaeococcus fuscipennis Burm. (Homoptera: Margarodidae), a new pest of pine in Israel. Hassadeh 71, 759–760. [in Hebrew, with English summary]
157
Mendel, Z., Carmi, E., and Podoler, H. 1991b. The relations between the genera Matsucoccus Cockerell (Homoptera: Margarodidae) and Elatophilus Reuter (Hemiptera: Anthocoridae) and their significance. Ann. Entomol. Soc. Am. 84, 502–507. Mendel, Z., Blumberg, D., Zehavi, A., and Weisenberg, M. 1993. Some polyphagous Homoptera gain protection from their natural enemies by feeding on Spartium junceum and Erythrina corallodendrum (Leguminosae). Chemoecology 3, 118–124. Mendel, Z., Assael, F., Saphir, N., Zehavi, A., and Kfisheh, W. A. M. 1994. Matsucoccus josephi and Pineus pini (Homoptera) on pine trees in parts of the Near East. Phytoparasitica 22, 9–18. Morrison, H. 1928. ‘‘A Classification of Higher Groups and Genera of the Coccid Family Margarodidae. USDA Tech. Bull. No. 52. Myartseva, S. N. 1981. ‘‘Species of Homalotylus Mayer (Hymenoptera: Encyrtidae)—Coccinellid Parasites (Coleoptera: Coccinellidae) in Turkmenistan, pp. 35–41. Izv. Akad. Nauk. Turkm. SSR, Ser. Biol. Nauk. No. 6. [in Russian, with English summary] Prasad, Y. K. 1989. The role of natural enemies in controlling Icerya purchasi in South Australia. Entomophaga 34, 391–395. Quezada, J. R., and DeBach, P. 1973. Biological and population studies of the cottony cushion scale Icerya purchasi Mask, and its natural enemies, Rodolia cardinalis Mul. and Cryptochaetum iceryae Will. in southern California. Hilgardia 41, 631–688. Schimischek, E. 1944. ‘‘Forstinsekten der Turkei und ihre Umwelt.’’ Volk und Reich Verlag, Prague.
BIOLOGICAL CONTROL ARTICLE NO.
Classical Biological Control of Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) in Israel1 Zvi Mendel,* Fabienne Assael,* Suheil Zeidan,† and Amiram Zehavi† *Department of Entomology, ARO, The Volcani Center, Bet Dagan 50250, Israel; and †Forests Department, Keren Kayemet LeYisrael, Eshta’ol 99775, Israel Received August 18, 1997; accepted February 24, 1998
Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) is rarely observed in pine forests in Mediterranean and Central European countries. It was discovered in Israel in 1990 in a single pine stand in Nahal ‘Iron (northern Samaria). Between the time of its detection and the summer of 1996, the scale insect had spread to the NE and NW, infesting 1300 ha of forest of Pinus brutia ssp. brutia Tenore, P. halepensis Miller, P. pinea L., and P. canariensis C. Smith. Infested trees were covered with honeydew and with stems and crowns displaying thick layers of sooty mold. Association of the scale with several predacious arthropods, including large populations of the coccinellid Rodolia cardinalis Mulsant (Coleoptera: Coccinellidae), failed to reduce its population level and spread to new plantations. In 1994 and 1995 two specific natural enemies of P. fuscipennis, the coccinellid Novius cruentatus Mulsant and the parasitoid Cryptochetum jorgepastori Cadahia (Diptera: Cryptochetidae), were introduced from ‘‘Marismas del Dial Nature Reserve’’ SE of Huelva in southern Spain and released at a single site in ‘Iron forest in Nahal ‘Iron. In the summer of 1996, both enemies were detected over most of the range of the pest. A large decrease in the pest’s population density and in the sooty mold cover was observed at the site of release of its natural enemies. Our findings suggest that N. cruentatus is the major contributor so far to the population reduction of P. fuscipennis. r 1998 Academic Press Key Words: biological control; Palaeococcus fuscipennis; Homoptera; Margarodidae; Rodolia cardinalis; Coleoptera; Novius cruentatus; Coccinellidae; Cryptochetum jorgepastori; Diptera; Cryptochetidae; Pinus brutia ssp. brutia; Pinus halepensis.
INTRODUCTION
Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) has been recorded from the northern
1 Contribution from the Agriculture Research Organization, The Volcani Center, Bet Dagan, 50250 Israel, No. 2244-E, 1997 series.
Mediterranean region, Morocco, and southern and central Europe (Cadahia, 1982; Kosztarab and Kozar, 1988; and literature cited therein) (Fig. 1). P. fuscipennis is probably the only species of the genus; the attribution of Palaeococcus brasiliensis (Walker) to the genus is doubtful (Morrison, 1928). P. fuscipennis infests Pinus halepensis Miller, Pinus brutia ssp. brutia Tenore, P. pinea L, and P. pinaster Aiton as well as Cedrus atlantica Manetti (Cadahia, 1982). Since P. fuscipennis is known to develop only on Pinaceae, the report of its occurrence on the broadleaved genera Acer L. and Quercus L. (Kosztarab and Kozar, 1988) is probably erroneous. Like other monophlebids, P. fuscipennis feeds on phloem and secretes honeydew. In the Mediterranean area it has two generations per year (Schimischek, 1944; Cadahia, 1982). Until the 1970s, P. fuscipennis outbreaks were generally unknown (Escherich and Baer, 1913; Balachowsky, 1932; Schimischek, 1944; Kosztarab and Kozar, 1988) except for one outbreak on mature trees of P. pinea in a nature reserve near Huelva in southern Spain. The outbreak was attributed to aerial insecticide applications to surrounding salt marshes to control mosquitoes (Cadahia, 1982). Principal predators of monophlebids (e.g., the genera Icerya Signoret, Monophlebus Burmeister, Palaeococcus Cockerell) are coccinellids, viz. the genera Rodolia Mulsant and Novius Mulsant (Hodek, 1996), and the principal parasitoids are flies in the genus Cryptochetum Rondani (Diptera: Cryptochetidae) (Menon, 1949; Cadahia, 1984). P. fuscipennis is attacked by three specific natural enemies: Novius cruentatus Mulsant, which occurs throughout the scale’s natural range (Escherich and Baer, 1913; Schimischek, 1944); Cryptochetum buccatum Hendel, indigenous to western Europe; and Cryptochetum jorgepastori Cadahia from southern Spain (Cadahia, 1984). Since the early 1990s, P. fuscipennis has been found on planted pine in few plots in Nahal ‘Iron in northern Samaria, causing thick layers of sooty mold on stems and crowns. The present study describes the first
151
1049-9644/98 $25.00 Copyright r 1998 by Academic Press All rights of reproduction in any form reserved.
152
MENDEL ET AL.
FIG. 1. Natural range of Palaeococcus fuscipennis (the blacken area) until 1990 (after Balachowsky 1932; Schimischek, 1944; Kosztarab and Kozar, 1988).
record and spread in Israel of P. fuscipennis and the acclimatization of two principal natural enemies. MATERIALS AND METHODS
Survey of P. fuscipennis in Nahal ‘Iron The distribution of P. fuscipennis in northern Samaria was surveyed at 6-month intervals in the planted pine in ‘Iron, Megido, and Gal’ed forests on both sides of Nahal ‘Iron (a valley in northern Samaria). Its presence was determined as follows: trees with honeydewcontaminated bark with spots of sooty mold or with foraging honeybees were closely examined for the occurrence of any development stages of the pest. The suspected trees were examined by having the bark scale removed from at least 2500 cm2 of the mid-stem surface of a minimum of 20 randomly selected trees per plot. All four pine species planted in Nahal ‘Iron, P. halepensis, P. brutia ssp. brutia, P. pinea, and P. canariensis, were examined. Sampling of Arthropods Associated with P. fuscipennis in 1991 In May 1991, 10 randomly selected trees of P. halepensis and P. brutia ssp. brutia in an infested site (plot No. 07, in Yaar Katzir, planted in 1971) in ‘Iron Forest were cut and examined for natural enemies of P. fuscipennis. Both pine species were also infested by Matsucoccus josephi Bodenheimer and Harpaz (Homoptera: Matsucoccidae), but unlike P. halepensis the latter pine species did not display chronic injury by M. josephi (e.g., Mendel et al., 1994). From each tree, between 4
and 5 stem sections with approximately 2000-cm2 bark area were collected. These stem collections consisted (as far as possible) of two rough bark samples and three partly smooth bark samples. All insects on these stem sections, except for M. josephi, were removed and counted. The arthropods found were divided into three groups: (i) common species associated with P. halepensis infested with M. josephi, (ii) rare species on pine, infested or not infested by M. josephi and present in high numbers on trees infested by P. fuscipennis; and (iii) species occurring in small numbers and not related to the presence of P. fuscipennis. Collection of Natural Enemies of P. fuscipennis in Spain Natural enemies were collected in the La Cascatera woodland located on sand ridges forming part of the Spartina swamps of the Marismas del Dial Nature Reserve, SE of Huelva, where significant populations of P. fuscipennis existed. Collections were made in March 1994 and in April 1995. Collections included adult females of P. fuscipennis and larvae, pupae, and adult coccinellids occurring on a group of four trees of P. pinea infested with P. fuscipennis. The material was shipped to Israel. Release and Sampling to Assess Establishment of N. cruentatus and C. jorgepastori Releases of adult natural enemies were made in a single heavily infested plot in ‘Iron forest (Plot No. 08, planted in 1951). In 1994, from 25 April to 5 May, we
153
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis
released ca 270 N. cruentatus and ca 365 C. jorgepastori, and from 3 to 30 May 1995, 250 N. cruentatus and 285 C. jorgepastori. Sampling to detect the released flies was conducted in six mature stands (age of 22–45 years) each with an area of 4–7 ha. Stands consisted of two plots of P. halepensis, two plots of P. brutia ssp. brutia, a plot planted with both pine species, and a plot of P. canariensis. The plots were at a distance of 0.5–5 km from the release plot. Annual surveys were carried out during April and May 1994–1996. Since tree cutting was restricted, the sampling was conducted by several persons. A minimum of 150 gravid females of P. fuscipennis was collected. In the P. canariensis stand only 130 individuals could be found. The sample size of females per plot ranged between 150 and 280. The collected females were placed in petri dishes for 2 months at 25°C. Then the number of parasitized females was counted. Sampling of coccinellids in Nahal ‘Iron was conducted in four of the above-mentioned plots of P. halepensis and P. brutia ssp. brutia, located at a distance of 0.5–2 km from the release plot. Annual samplings were undertaken during April of 1993–1997. The samplings were conducted by three persons during 20 min (an hour’s walk), in each of the four study plots. Larvae, pupae, and adult beetles were collected. The development stages were segregated and kept in different rearing boxes. The larvae were fed with larvae and ovisacs of P. fuscipennis and most of them developed to adults.
Sampling of P. fuscipennis in the Release Plot The sampling of P. fuscipennis was conducted once a year during late April or early May between 1993 and 1996 in the release site (plot No. 08 in ‘Iron Forest). Since the plot was a recreation site, only five trees of P. halepensis or P. brutia ssp. brutia were cut each time. Adult females were collected from a 3–4 m length section of the mid stem, and their density per 1000 cm2 of the bark surface was calculated. RESULTS
Occurrence of P. fuscipennis in Israel Since the time of its discovery in Israel, P. fuscipennis has spread to the NE and NW in pine plantations on both sides of the Nahal ‘Iron valley, infesting 1300 has of pine (Fig. 2). Based on sooty mold coverage, mature P. brutia ssp. brutia and P. halepensis were more severely affected than P. pinea and P. canariensis. Twoto 5-year-old seedlings were not naturally infested by the scale, but were suitable host plants when artificially infested in a greenhouse. Observation in Nahal ‘Iron showed that adult males and ovisacs were present during October–September and April–May, indicating that there are two generations per year in Israel. Initial infestations of P. fuscipennis were on the mid-stem section of the tree on recently pealed bark partly covered by flakes. Heavily infested trees, from mid-stem sections to top, were covered with honeydew, and stems and part of the crown displayed thick layers
FIG. 2. Annual increase in forest area affected by Palaeococcus fuscipennis at Nahal ‘Iron, Israel.
154
MENDEL ET AL.
of sooty mold. It took 4–5 years for the scale population to cover most of the stem with sooty mold in two artificially infested 15-year-old trees. Damage Observations on heavily infested trees did not reveal direct injury to the plants by scale feeding. However, the thick layers of sooty mold caused forest rangers to suspect possible damage to the trees by increased heat absorption of the black bark. Visitors to the camping sites in ‘Iron forest were inconvenienced by honeybees and hornets that swarmed around honeydew-covered trees. Arthropods Associated with P. fuscipennis before the Release of Exotic Natural Enemies Arthropods found in 1991 on felled trees in heavily infested plot in ‘Iron forest consisted of M. josephi and its principal associates, Elatophilus hebraicus Pericart, Dufouriellus ater (Dufour) (both, Heteroptera: Anthocoridae), Ulrike syriaca (Steinmann) (Neuroptera: Raphidiidae), and Cryptolestes sp. (Coleoptera: Cucujidae). A second group of arthropods on infested pines was composed of Rodolia cardinalis (Mulsant), which was the most common associate of P. fuscipennis. On heavily infested trees hundreds of pupae of R. cardinalis were counted. The beetle population had been conspicuous already in 1990 on the first affected trees. Observations suggested that both larvae and adults of R. cardinalis fed mainly on the egg masses but not on mature larvae or adults of P. fuscipennis. Homalotylus flaminius (Dalman) (Hymenoptera: Encyrtidae) emerged from larvae of R. cardinalis and was very common on infested sites in Nahal ‘Iron. Adults of Erythraeus sp. (Acarina: Erythraeidae) were collected for the first time in Israel from trees infested with P. fuscipennis. The mites were carried by P. fuscipennis searching for ovipositing sites. Other common associates were larvae and adults of Dapsa inornata Gorhan (Coleoptera: Endomychidae) that fed on sooty mold and larvae of Dioryctria spp. (Lepidoptera: Phycitidae) boring in the cork and cortex of bark covered with honeydew. A third group on felled trees in heavily infested plots in ‘Iron forest consisted of Crysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Orius minutus (L.) (Heteroptera: Anthocoridae). These species have occurred in very small numbers and are not related to the presence of P. fuscipennis. The presence of these entomophagous arthropods failed to prevent the continuous expansion of the range of P. fuscipennis and damage was not prevented. None of P. fuscipennis’ important known natural enemies in the western Mediterranean region were found in Nahal ‘Iron.
Collection of Natural Enemies of P. fuscipennis in Spain The P. pinea trees in the Spartina swamps near Huelva were not conspicuously covered by sooty mold and, based on the time needed to collect the females, we estimated that the density of P. fuscipennis was much lower than that on heavily infested P. halepensis and P. brutia ssp. brutia trees in ‘Iron forest. In 1994 we collected in the Spartina swamps area from the group of P. pinea trees approximately 250 mature females of P. fuscipennis and several hundred larvae and pupae of N. cruentatus. In April 1995, ca 200 females of P. fuscipennis and ca 350 larvae and pupae of N. cruentatus were collected. About half of the females collected in 1994 and almost all of the females collected in 1995 were parasitized by C. jorgepastori. Larvae of N. cruentatus collected in Spain were reared to adult in the laboratory on P. fuscipennis collected in ‘Iron forest. Recoveries of N. cruentatus and C. jorgepastori at Release Locations The first recovery of N. cruentatus was as pupae collected in July 1995. From coccinellid pupae collected during 1992–1994 only R. cardinalis emerged. In October 1995, 17 months after the first release of N. cruentatus, among the ca 300 coccinellid pupae collected in the release plot, 17 (5.6%) consisted of pupae of N. cruentatus; the rest were R. cardinalis. Since 1996 partial displacement of R. cardinalis by N. cruentatus has occurred. In April 1996, collections of adult coccinellids showed significantly more individuals per sample of N. cruentatus (49.7 6 11.6) than R. cardinalis (26.5 6 4.9) (PT 5 t 5 0.009, df 5 3, two-tail t test). In April 1997, N. cruentatus was found in all infested plots and 91.2% of all coccinellids associated with P. fuscipennis were N. cruentatus (Fig. 3).
FIG. 3. Shift in occurrence between Rodolia cardinalis and Novius cruentatus (mean percentages 6 SD in composite samples) at a camping site in Nahal ‘Iron, Israel.
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis
C. jorgepastori was first recovered at release sites in Israel in October 1995, following its release in 1994. C. jorgepastori were recovered in October 1995 from four of six sampled plots in Nahal ‘Iron. In April 1996 it was found at Megido forest, at a distance of 5 km from the point of release at ‘Iron forest; parasitism in samples reached 3.4% of adult female scales. Occurrence of P. fuscipennis in 1996 Our observations suggest that the spread of P. fuscipennis stopped after 1996 (Fig. 2). As a result of the interaction between P. fuscipennis and the introduced predator and the parasitoid, the mean number of female P. fuscipennis per 1000 cm2 of bark in the release plot in ‘Iron forest has decreased from 115 6 58 in 1993 to 3 6 5 in 1996 (Fig. 4). Black bark has decreased steadily with the reduction in honeydew production and natural peeling of the sooty moldcovered flakes. The level of infestation revealed by the intensity of sooty mold at newly infested sites did not reach that of the initially infested plots. Hence, the occurrence of the scale at these sites was not detected by the forest rangers. DISCUSSION
Despite numerous insect surveys conducted in local pine forests P. fuscipennis was unrecorded in Israel before 1990. P. fuscipennis was accidentally discovered in Israel in 1990 on a few trees in a single pine stand in ‘Iron forest on the western slopes of Nahal ‘Iron (Mendel et al., 1991a). At that time, the scale population was not recognized as a new introduction because this scale occurs naturally on P. halepensis and P. brutia ssp. brutia in other areas of the Near East. Several other distinctive pests of pine in Israel ‘‘crossed’’ the observation threshold due to the increasing area covered with pine and the increasing age of potential hosts. For
FIG. 4. Mean density (6SD) of females of Palaeococcus fuscipennis per 1000 cm2 pine bark at a camping site in Nahal ‘Iron, Israel.
155
example, galleries of Tomicus destruens (Wollaston) (Coleoptera: Scolytidae) were found in Israel in the early 1960s, but the first outbreak did not occur until 1978 (Mendel et al., 1985). From the pattern and speed of dispersal of P. fuscipennis in Nahal ‘Iron (‘Iron forest and two adjacent forests) it is believed that the pest arrived in Israel in the late 1980s and was not accompanied by its principal enemies. How this scale reached Israel is unknown. Two potential methods, on nursery stock of pines or logs by camper traffic between Israel and its northern neighboring countries, can be excluded because of legal and political restrictions in these countries. This suggests that the appearance of P. fuscipennis in northern Samaria may be the result of its spread by migratory song birds. Samaria is within the seasonal migration route along the Afro-Syrian rift from Eastern Europe and Russia to Africa. It has been suggested that about 8% of the 5 billion birds that migrate from the Western Palearctic to Africa each autumn fly across Israel and the Jordan Valley (Frumkin et al., 1995). Birds are known to carry eggs and crawlers of small insects (McClure, 1990). Until the late 1980s, honeydew-producing Coccoidea on pine in Israel were represented by a single and rather rare species—Phenacoccus yerushalmi Ben-Dov (Pseudococcidae). The rapid buildup of the population of P. fuscipennis on P. halepensis and P. brutia spp. brutia in Nahal ‘Iron created a new type of injury to pine in Israel. Although the direct impact of sooty mold was not investigated, there is little doubt that the dirty appearance of the blackened trees and swarms of bees and hornets feeding on honeydew necessitated biological control of the scale. The high-density population of P. fuscipennis and intensive honeydew production led to a marked change in the arthropod complex on the pine stems. Due to the ample honeydew supply, the forest became an important foraging area for honeybees, especially during the winter and mid-summer when sources of nectar are limited. The unusually high densities of larvae of Dioryctria spp. may be explained by attraction of the adults to the honeydew, whereas the frequent occurrence of D. inornata is related to the fresh sooty mold. The occurrence of Erythraeus sp. for the first time in Israel in ‘Iron forest is also related to the appearance of P. fuscipennis in the area. Although the role of the mite is not yet clear, it is noteworthy that larvae of Erythraeidae usually parasitize arthropods, whereas their nymphs and adults are predators (Gerson and Smiley, 1990). The contribution of the predaceous mite Erythraeus sp. to the control of P. fuscipennis is limited. E. hebraicus Pericart, D. ater (Dufour), U. syriaca (Steinmann), and Cryptolestes sp. are common associates of M. josephi and occur on P. halepensis and P. brutia ssp. brutia in other areas of the eastern Mediterranean
156
MENDEL ET AL.
(Mendel, 1992). However, while E. hebraicus Pericart is a specific predator of M. josephi (Mendel et al., 1991b), the other species may feed also on P. fuscipennis. R. cardinalis was probably attracted from the adjacent citrus groves and gardens by the high density of P. fuscipennis and was the most common natural enemy in Nahal ‘Iron. Reproducing populations of this beetle were not expected to occur in pine forests in Israel because appropriate prey species did not occur on pine in Israel. R. cardinalis is the principal enemy of Icerya purchasi Maskell but may feed and develop on other Monophlebinae (Caltagirone and Doutt, 1989), although with a resulting lower reproductive capacity (Mendel et al., 1993). Prey used by Coccinellidae may be classified as essential, acceptable, alternative, or rejected (Hodek, 1996). It is accepted among coccinellid researchers that only an essential food is suitable for a beetle to complete its development. The level of prey specificity in the Coccinellidae is not always clear, with specialization becoming apparent within individual tribes. Limited information, however, is available regarding the tribe Noviini. For example, under controlled conditions Rodolia iceryae Jenson fed on Icerya aegyptiaca Douglas but laid no eggs. The beetle fed and laid eggs on plants infested with I. purchasi, but the larvae that developed on I. purchasi died during pupation (Mendel and Blumberg, 1991). Similarly, we suggest that P. fuscipennis is not an essential prey of R. cardinalis, although the beetle may complete its development on P. fuscipennis when scale egg masses are available. Egg masses are more appropriate food in such cases. For example, larvae of R. cardinalis died when they fed on larvae or adults of I. purchasi that infest plants with high levels of alkaloids, but could develop and reproduce to some extent on egg masses of I. purchasi produced on those plants (Mendel et al., 1993). Marginal suitability of P. fuscipennis as a food source may explain why R. cardinalis was unable to limit the increase and spread of the population of P. fuscipennis. The frequent occurrence of the larval parasitoid H. flaminius reflected the abundance of R. cardinalis larvae on the infested sites. Homalotylus spp. are principal parasitoids of Coccinellidae (Myartseva, 1981). H. flaminius is a common parasitoid of R. cardinalis (Bodenheimer, 1951), but has not been collected in citrus groves in Israel during the last decade (D. Blumberg and Z. Mendel, unpublished). In previous biological control projects of monophlebids, the introduction of a species of Cryptochetum was aimed at the control of I. purchasi and Icerya seychellarum (Westwood). Successful or partial control of other Icerya spp. was obtained by introduction of Rodolia spp. (Bartlett, 1978). The present case is the first successful trial of acclimatization of N. cruentatus and C. jorgepastori. The success of establishment of the
introductions was expected, since the species were introduced into a forest area which is very similar to their natural habitat and with no interference from insecticides. Present data suggest that N. cruentatus is the major contributor to the population reduction of P. fuscipennis in Israel. The biological control of I. purchasi in California, which was repeated in many areas, was achieved by the introduction from Australia of both R. cardinalis and Cryptochetum iceryae Williston (Caltagirone and Doutt, 1989). Several studies showed that the fly is more effective than the beetle in cool areas, although it occurs throughout most of the range of I. purchasi (Quezada and DeBach, 1973; Prasad, 1989). C. iceryae was introduced into Israel from California in 1988, ca 60 years after the introduction of R. cardinalis, to complete the biological control, and both enemies are required for efficient control of I. purchasi in citrus and ornamentals (Mendel and Blumberg, 1991). However, from the present experience of better recovery of the beetle it seems that N. cruentatus is relatively more effective than C. jorgepastori at high prey densities. However, as the scale population decreases to lower levels, C. jorgepastori may end up playing a more important role in regulating the pest at low population levels. ACKNOWLEDGMENTS We thank our colleague Leandro Gonzalez Tirado and Pedro Miguel Bernabe Ruiz from the Servicio de Proteccio´n de los Vegetales de la Junta de Andalucia, Huelva, our Israeli colleagues David Nestel and Rene Karschon, for their assistance in collecting the natural enemies in southern Spain, Nitza Saphir of the Forests Department of JNF, Israel, for her help in the sampling of P. fuscipennis and its natural enemies, Uri Gerson from the Faculty of Agriculture, the Hebrew University of Jerusalem, for the identification of Erythraeus, and two anonymous reviewers for their valuable comments to a previous version of the manuscript.
REFERENCES Balachowsky, A. 1932. ‘‘Etude biologique des coccides du bassin occidental de la Mediterrane´e. Encyclope´die Entomologique,’’ Vol. 15. P.LeChevalier, Paris. Bartlett, B. R. 1978. Margarodidae. In ‘‘Introduced Parasites and Predators of Arthropods and Weeds: A World Review’’ (C. P. Clausen, Ed.), pp. 132–137. USDA Agric. Handb. No. 480. Bodenheimer, F. S. 1951. ‘‘Citrus Entomology in the Middle East.’’ Junk, The Hague. Cadahia, D. 1982. Palaeococcus fuscipennis Burm. (Homoptera: Margarodidae), plaga de los pinares de la costa de Huelva. Bol. Serv. Plagas 8, 201–214. Cadahia, D. 1984. El intere´s biolo´gico del ge´nero Cryptochaetum Rond. Diptera: Cryptochaetidae y descripcio´n de una nueve espe´cie. Bol. Serv. Plagas 10, 159–184. Caltagirone, L. E., and Doutt, R. L. 1989. The history of the vedalia beetle importation to California and its impact on the development of biological control. Annu. Rev. Entomol. 34, 1–16.
BIOLOGICAL CONTROL OF Palaeococcus fuscipennis Frumkin, R., Pinshow, B., and Kleinhaus, S. 1995. A review of bird migration over Israel. J. Ornithol. 136, 127–147. Escherich, K., and Baer, E. 1913. Tharandter zoologische Miszellen. Nat. Z. Forst. Landwirtschaft. 11, 98–129. Gerson, U., and Smiley, R. L. 1990. ‘‘Acarine Biocontrol Agents.’’ Chapman & Hall, London. Hodek, I. 1996. Food relationships. In ‘‘Ecology of Coccinellidae’’ (I. Hodek, and A. Honek, Eds.), pp. 143–238. Kluwer Academic, London. Kosztarab, M., and Kozar, F. 1988. ‘‘Scale Insects of Central Europe.’’ Akademiai Kiado, Budapest. McClure, M. S. 1990. Role of wind, deer, and humans in the dispersal of the hemlock woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 19, 36–43. Mendel, Z. 1992. The occurrence of Matsucoccus josephi in Cyprus and Turkey and its relation to decline of Aleppo pine. Entomol. Gen. 17, 299–306. Mendel, Z., and Blumberg, D. 1991. Colonization trials of Cryptochaetum iceryae and Rodolia iceryae for improved biological control of Icerya purchasi in Israel. Biol. Control 1, 68–74. Mendel, Z., Golan, Y., and Madar, Z. 1985. Comparison of the seasonal occurrence and behavior of seven pine bark beetles (Coleoptera: Scolytidae) in Israel. Phytoparasitica 13, 21–32. Mendel, Z., Zehavi, A., and Zeidan, S. 1991a. Palaeococcus fuscipennis Burm. (Homoptera: Margarodidae), a new pest of pine in Israel. Hassadeh 71, 759–760. [in Hebrew, with English summary]
157
Mendel, Z., Carmi, E., and Podoler, H. 1991b. The relations between the genera Matsucoccus Cockerell (Homoptera: Margarodidae) and Elatophilus Reuter (Hemiptera: Anthocoridae) and their significance. Ann. Entomol. Soc. Am. 84, 502–507. Mendel, Z., Blumberg, D., Zehavi, A., and Weisenberg, M. 1993. Some polyphagous Homoptera gain protection from their natural enemies by feeding on Spartium junceum and Erythrina corallodendrum (Leguminosae). Chemoecology 3, 118–124. Mendel, Z., Assael, F., Saphir, N., Zehavi, A., and Kfisheh, W. A. M. 1994. Matsucoccus josephi and Pineus pini (Homoptera) on pine trees in parts of the Near East. Phytoparasitica 22, 9–18. Morrison, H. 1928. ‘‘A Classification of Higher Groups and Genera of the Coccid Family Margarodidae. USDA Tech. Bull. No. 52. Myartseva, S. N. 1981. ‘‘Species of Homalotylus Mayer (Hymenoptera: Encyrtidae)—Coccinellid Parasites (Coleoptera: Coccinellidae) in Turkmenistan, pp. 35–41. Izv. Akad. Nauk. Turkm. SSR, Ser. Biol. Nauk. No. 6. [in Russian, with English summary] Prasad, Y. K. 1989. The role of natural enemies in controlling Icerya purchasi in South Australia. Entomophaga 34, 391–395. Quezada, J. R., and DeBach, P. 1973. Biological and population studies of the cottony cushion scale Icerya purchasi Mask, and its natural enemies, Rodolia cardinalis Mul. and Cryptochaetum iceryae Will. in southern California. Hilgardia 41, 631–688. Schimischek, E. 1944. ‘‘Forstinsekten der Turkei und ihre Umwelt.’’ Volk und Reich Verlag, Prague.