Mr. Mahmut EROĞLU
Karadeniz Technical University, Faculty of Forestry, TRABZON
Turkey
Summary
Gall wasps belong to the family Cynipidae that is placed, with other families, in the super family Cynipoidea. Cynipoidea are parasitic Hymenoptera and all species except those in the subfamily Cynipinae behave as typical parasitoids or hyperparasitoids of other insects. The Cynipinae are the gall wasps and they alone induce gall formation and as larvae are phytophagus. In the Cynipinae, there are some gall wasps whose larvae have lost the ability to induce gall formation and these larvae live obligatorily as inquilines in the galls of gall-forming Cynipinae.
Over 90 percent of gall-inducing animals occur on dicotyledonous plants and most of these infest only three families, Rosaceae, Compositae, and Fagaceae. The fidelity of cynipids to oaks demonstrates the degree of monophagy among gall inducers. In North America and Europe, for instance, 87 and 76 percent of all cynipids attack species of Quercus and the host range of each wasp species is generally restricted to one or a few related oak species. Oak cynipids are notable for structural diversity of galls they induce. They also display a range of galling sites on the plant, host plant associations and life cycle. Many of them have two generations each year. The galls of the two generations are often radically different in structure.
The diversity of cynipid galls is the result of venation in gall tissues which develop outside the larval chamber, including surrounding layers of wood or spongy tissue, complex air spaces within the gall, and surface coats of sticky resins, hairs or spines.
The structure of galls peripheral to the nutritive zone is varied. One of the most specialized galls is that of Andicus kollari (Harting) ö in which eight concentric zones of different tissues have been described. Several galls, like in those Andricus gallaetinctoriae (Oliv.) have high tannin content which render them bitter-tasting. Because of their high tannin contents, galls of A.gallaetinctoriae and A.kollari have been utilized for thousands of years.
Agamic generation of A.gallaetinctoriae can be found most common on Quercus infectoria Oliv., however, they are also found on Quercus ithaburensis Decne. Ssp. macrolepis (Kotschy.) Hedge and Yalt., Q.cerris L., Q.conferta Kitt., Q.ilex L., Q.rubur L., Q.petraea (Mattuschka) Lieb. and Q.pubescens Willd. Q.infectoria is almost found in all woodlands of Turkey, however, it grows most commonly in the South Eastern Anatolia. In its large range, the two sub species, Q.infectoria ssp. biossieri (Reut) Gtirke is found West, Middle, East, and South Eastern parts of Anatolia and Q.Infectoria ssp. infectoria A. Camus is found in the North west and Marmara regions.
Adults of agamic generation are 5–8 mm in length, and mainly dull brown with yellowish white, fine, short, and thick hairs. The antenna coated with sparse hairs includes fourteen segments. Thorax is covered with dense light brown pubescense. Prothorax becomes narrow towards the front. There are two longitudinal stripes on mesothorax. Anteriorly the scutellum is provided with two pits, the form of which may be of taxonomic value.
A.gallaetinctoriae have a high reproductive potential (like many other gall wasps) and females may contain about 700 to 800 eggs. Eggs consist of a rather short body and a long pedicel which is 10 to 14 times as long the egg body. Egg laying is lasted until early June. After oviposition, the egg is more or less embedded in bud tissue. Larval stage is lasted about two months, from early June to late August or to the beginning of September. Gall formation period lasts about from mid June to beginning of July, so immature galls are found from mid-July to early September. Pupation generally begins in mid-August when the color of gall changes from light green to white, and lasts about 15 to 25 days.
Mature agamic galls of A.gallaetinctoriae are almost spherical, 13–24 mm in diameter, clothed with sharp, stiff spines about 1–4 mm in length, and 1.23 to 6 gram in weight. Maturing galls are bright in color, single-chambered and non-coalesced clusters. Walls of mature galls are 5–6 mm in thickness and can not be crushed without a stroke of a hammer. Perhaps, there is an interaction between the color of gall and the development of the gall wasps in it. The galls which are indigo-blue in color generally includes young larvae. The mature larvae can be found in the green or light green galls. White galls include pupae or adults gnawing an exit hole. In the following days, especially after a rain, color become reddish. Emergence of adults was not observed in the galls collected before late July. Adult exiting from galls collected in different years and places showed that the adult emerging period begins in early September and lasts until late October.
Adult emergency from the galls collected in late August and early September and stored in the room conditions occurred between 8 to 21 October. Early harvest of galls results in not only the loss of crop but also the reduction in the population of the gall wasps. In gall harvesting, the galls collected should be kept in the vicinity of the production area until wasps exit the galls.
Abstract
Gall formation is arguably the most intimate relationship between herbivorous insects and their host plants, and galls induced by cynipid gall wasps might well be the most sophisticated structures of induced plant growth. Each species of cynipid gall wasps induce the growth of unique galls which are both structurally distinct and anatomically novel structures to their host plant. Most species of cynipids are in tribe Cynipini, all of which gall oaks and allied Fageceae. In Europe approximately 76 percent of all cynipids attack species of Quercus and the host range of each wasp species is generally restricted to one or a few related oak species. European oaks are members of two different oak species groups within the genus Quercus, the ‘white’ oaks of the section Quercus, and the ‘black’ oaks of the section Cerris. In the cynipid gall wasps, a sexual spring generation develops on oaks in the section Cerris, particularly the Turkey oak, Quercus cerris, while a parthenenogenetic summer generation develops on oaks in section Quarcus, such as Q. petraea, Q.pubescens, and Q.robur. The two oak groups occur together naturally in southern Europe, the Mediterranean coast of north Africa, and Asia Minor, and these regions represent the natural, native distribution of gall wasps exhibiting the alternating life cycle. The majority of host altering Andricuc species are found in the eastern part of this region, where the Turkey oak, Q.cerris, is the host of sexual generation galls. In Turkey, where the Turkey oak, Q.cerris has a large natural range, approximately 20 species of cinipid wasps induce galls on the oaks of Turkey. The vast majority of oak galls are of no particular economic significance. Because of their high tannin contents, galls of A.gallaetinctoriae and A.kollari have been utilized for thousands of years in Asia Minor. Agamic generation galls of A.gallaetinctoriae can be found most common on Quercus infectoria Oliv., however, they are also found on Q.petraea (Mattuschka) Lieb. and Q.pubescens Willd. Q.infectoria is almost found all oak woodlands of Turkey, however, it grows most commonly in the Southern East Anatolia. A.kollari is found around the Sea of Marmara, along the Aegean cost, and some inner parts of Turkey. In gall developing areas, negative effects of human being and animal grazing have a great role on gall production. Early harvest of galls results in not only the loss of crop but also the reduction in the population of the gall wasps. This may also result in the increase in the population of other harmful species on the same host plants. In the last 10 years, the income portion of the gall exportation in Turkey's non-wood forest products has been 0.74% on average. This number indicates that, while it has the potential of providing the people living in rural areas and having low life standards with an important source of income, gall production in Turkey is still far from what is expected because of inefficient gall harvesting strategies.
Introduction
Gall wasps belong to the family Cynipidae which is placed, with other families, in the superfamily Cynipoidea. All species of this superfamily, except those in the subfamily Cynipinae behave as typical parasitoids or hyperparasitoids of other insects (Askew, 1984). The Cynipinae are the gall wasps and they alone induce gall formation and as larvae are phytophagus (Quinlan, 1979; Evenhuis, 1980). In the Cynipinae there are some gall wasps whose larvae have lost the ability to induce gall formation and these larvae live obligatorily as ‘inquilines’ in the galls of gall-forming Cynipinae (Krombein et al., 1979). All cynipid inquilines are phytophaqous and feed on specialized nutritive cells that they themselves induce from issues of the host gall. (Shorthouse, 1980; Washburn and Cornell, 1981).
Herbivory by gall-makers has the potential to result in number of negative impacts on host plants. The negative impacts of gall-makers infesting certain agricultural crops are well documented. But, the frequency and degree to which gall-makers injure their hosts in natural situation is still open to question (Abrahamson and McCreea, 1986; Price, 1987). Some workers have suggested that gall-maker impact is negligible (Wangberg, 1978; Gander, 1979), however, quantitative analyses have repeatedly shown that galls are metabolic sinks for carbon (Fourcroy and Braun, 1967; Jankiewicz et al., 1970; Hartnett and Abrahamson, 1979), and some mineral elements (Palct and Hassler, 1967).
Over 90 percent of gall-inducing animals occur on dicotyledonous plants and most of these infest only three families, Fagaceae, Rosaceae, and Compositae (Mani 1964). Cynipid gall inducers are divided into three (Kinsey, 1920; Askew, 1984) or five (Ronquist, 1994) tribes, based on morphological similarities and partly on host plant. Most species of cynipids are in tribe Cynipini, all of which gall oaks and allied Fageceae. The fidelity of cynipids to oaks demonstrates the degree of monophagy among gall inducers. In North America and Europe, for instance, 87 and 76 percent of all cynipids attack species of Quercus and the host range of each wasp species is generally restricted to one or a few related oak species (Krombein et al., 1979; Abrahamson and Weis 1987). Oak cynipids are notable for structural diversity of galls they induce (Askew 1984; Dreger-Jauffret and Shorthouse, 1992; Shorthouse and Rohfritsch 1992; Williams, 1994). They also display a range of galling sites on the plant, host plant associations and life cycle (Askew, 1961, 1984; Ambrus 1974; Cook et al. 1998). Oak cynipid gall structures are characteristic of the gall-inducer, rather than of the host plant (Ambrus, 1974; Rohfritsch, 1992), and result from cynipid traits expressed at two stages in the wasp's life cycle.
European oaks are members of two different oak species groups within the genus Quercus, the ‘white’ oaks of the section Quercus, and the ‘black’ oaks of the section Cerris (Nixon and Crepet, 1985). These two oak sections are, to some extent, associated with different cynipid genera (Amburs 1974; Csóka, 1997). An interesting feature of the genus Andricus is that the vast majority of galls found on section Cerris oaks belong to sexual generations, including 9 of the 10 sexual generation-only species, and 6 of the 20 species known to have a two generation life-cycle. The remainder of two-generation species have both generations on section Quercus oaks, and all of the asexual generation-only Andricus species attack oaks in this group (Cook et al., 1988). Hebert (1987) pointed out that all major groups of cyclic parthenogenes include obligately asexual members and Andricus is no exception with 35 asexual species in Europe.
Many species of oak cynipid gall wasps have two generations each year, one sexual and the other parhenogenetic. The most complex reproductive cycle is seen in most of the gall wasps that attack oak. Here, there is an alternation of generations, a sexual generation of males and females alternating with a so-called ‘agamic’ generation comprising only females. In Andricus and Neuroterus genera, it is usual to find not only that agamic generation of females is composed of strict androphores and gynephores, but also that one sexual generation female will produce in her progeny either agamic androphores or gynephores but not usually both (Folliot, 1964). Thus there is here even earlier determination of sex of the sexual generation; at the agamic generation one-and-a-half life cycles previously (Askew, 1984).
The galls of the two generations are often radically different in structure, and produce adults of very different size; where both generations are present in the life-cycle, sexual generation galls and adults are usually smaller than their asexual counterparts (Ambrus, 1974; Askew, 1984; Pujade, 1994, 1997). In Andricus, sexual generation galls usually develop more rapidly than associated asexual generations, and are often tiny, inconspicuous structures (Cook et al., 1998). The two galls are often induced on different plant organs. The majority of known sexual generation Andricus galls are induced on buds or catkins, with fewer species galling stems (Ambrus, 1974; Pujade, 1994). Leaves are very rarely galled by Andricus species (Askew, 1984).
In the cynipid gall wasps, a sexual spring generation develops on oaks in the section Cerris, particularly the Turkey oak, Quercus cerris L., while a parthenogenetic summer generation develops on oaks in the section Quercus, such as Q.petraea (Mattuschka) Lieb., Q.pubescens Wild., and Q.robur L: (Cook et al., 1988). The two oak groups occur together naturally in southern Europe, the Mediterranean coast of north Africa, and Asia Minor, and these regions represent the natural, native distribution of gall wasps exhibiting the alternating life cycle (Csóka et al., 1988). The majority of host altering Andricus species are found in the eastern part of this region, where the Turkey oak, Q.cerris, is the host of sexual generation galls (Amburus, 1974; Csóka 1997). The asexual generation may be highly host-specific, or attack a range of host species in this oak section (Amburus, 1974; Nieves-Aldry, 1987; Csóka, 1997). Within Andricus, a phylogenetically dispersed set of species have sexual generations on oaks in the section Cerris, either as a part of an alternating life cycle or in sexual-only life cycles (Cook et al., 1998).
Gall formation does not begin until after the gall wasp larva has emerged from its egg, and that gall development ceases upon death of the larvae (Askew, 1984). Larval secretions, as yet uncharacterized (Schönrogge, et al., 1998), are thought to control the type and structure of plant tissue forming the gall (Rohfritsch, 1992). Maternal egg-laying behavior determines how many larval cells develop within a single gall structure, and so whether the gall is unilocular or multiclocular. Gall structures, though constructed of plant tissues, thus represent the extended phenotypes of gall wasp genes (Dawkins, 1983; Stern 1995; Crespi et al., 1997).
The shapes and morphologies of cynipid galls vary widely not only between the species of gallformer, but also between generations, where the gall former has more than one generation per year (Dregger-Jauffret and Shorthouse, 1992). Mature cynipid galls can be as small as 2–3 millimeters or as large as 10 cm in diameter. Galls of some species house only a single larva whereas others are inhabited by several hundred. Cynipids induce galls on virtually all plant organs and many of them have impressive surface structures, such as spines of variable shapes or glands, which can secrete sugary or otherwise sticky compounds (Ambrus, 1974). Although the gross morphology of cynipid galls may vary, the inner organization of tissues is similar (Bronner, 1992; Rohfritsch, 1992). Tissues found in all cynipid galls include a layer of cytoplasmically dense nutritive cells which line the larval chamber, followed by a layer of vacuolate parenchyma, a layer of sclerenchyma, a layer of parenchymatous gall cortex and epidermis (Rohfritsch, 1992). Nutritive cells are unique to insect galls and serve the inducers as the sole source of food. Adjoining parenchyma are converted to nutritive cells as the inducer feeds (Bronner, 1976).
Cynipid wasps also control the physiology of gall tissues (Bagatto et al., 1996 ; Harris and Shorthouse, 1996). Not only do gall serve as physiological sinks for nutrients and assimilates, but tannins and phenolic compounds, thought to serve as feeding inhibitors for herbivorous insects, are concentrated in the peripheral parenchyma while inner gall tissue have non (Bronner, 1976).
There have been a number of invasions of new geographical areas by cynipid gall wasps, always associated with introduction to the area of their host plant. A.kollari, A.lignicola and A.quercuscalicis have expanded their ranges into northern and western Europe from natural distributions in southern Europe following human introduction of Turkey oak, Q.cerris., A.lignicola and A.quercuscaicis reached Britain through natural range expansion from Italy and the Balkans, while A.kollari was purposely introduced into Britain in large numbers in the first half of the 19th century from the eastern Mediterranean (Claridge, 1962; Williamson, 1996) to utilize its galls as raw material in the manufacture of ink (Askew, 1984).
In Turkey approximately 20 species of cynipid wasps induce galls on the oaks of Turkey. (Acatay, 1943; Schimitschek, 1944; Alkan, 1952; Karaca, 1956; Baş, 1973; Ekici, 1975; Eroğlu, 1977; Çanakçioğlu and Mol, 1998; Eroğlu, 2000). The vast majority of oak galls are of no particular economic significance. Because of their high tannin contents, galls of A.gallaetinctoriae and A.kollari have been utilized for thousands of years. A. gallaetinctoriae is found over much of Turkey where the two host oak groups occur together naturally in large areas. A.kollari is found around the Sea of Marmara, along the Aegean cost, and some inner parts of the country. In gall developing areas, negative effects of human being and grazing have a great role on gall production. Galls collected have not been kept in a close vicinity of woodlands. Early harvest of galls results in not only the loss of crop but also the reduction in the population of the gall wasps. This may also result in the increase in the population of other harmful species on the same host plants. The purpose of this study is to discuss the rural potentiality of gallings by these two important gall-maker species and the gall harvesting strategies that interfere with their life cycles.
Material and Method
Information on life cycle of the two important gall-makers, A. gallaetinctoriae and A.kollari came from some field collections of agamic galls on Quercus infectoria Oliv. in Adiyaman Forest District along with additional collections of galls on Q.pubescens in Kemalpaşa and Edremit in Turkey.
Collection of galls were made in the last August and early September and galls were placed in jars at room temperature and adults removed, counted and curated daily as they exited. The average longevity of agamics under laboratory conditions was observed. The emergency period of agamics and commercially gall production times were evaluated.
The gall production strategy that has been interfered with life cycles of these two important gallmaker species was discussed.
Results
Adults of agamic generation A. galleatinctoriae are mainly dull brown with yellowish white, fine, short, and thick hairs. The lengths of the adults were average 6.2 (5.0 to 7.6) millimeters (Baş, 1973; Ekici, 1975). The adults reared galls from Quercus infectoria Oliv. were average 39.4 (15.6 to 49.9) mg and from Q.pubescens were average 22.4 (12.5 to 32.3) mg in the weight (Ekici, 1975). This species has a high reproductive potential (like most of the other gall wasps) and females may contain about 700 to 800 eggs (Baş, 1973; Ekici, 1975). Egg laying is lasted until early June. Larval stage is lasted about two months, from early June to late August or to the beginning of September (Ekici, 1975). Each gall includes only one larva (Baş, 1973). Rarely, when two or more eggs are laid in a bud, the galls induced fuse with each other (Ekici, 1975).
Gall formation period lasts about from mid June to beginning of July, so immature galls are found from mid-July to early September. Pupation generally begins in mid-August when the color of gall changes from light green to white, and lasts about 15 to 25 days. Immature gall are found from mid-July to early September. Mature agamic galls of A.gallaetinctoriae are almost spherical, 13–24 (average 17.8) mm in diameter, clothed with sharp, stiff spines about 1 to 4 millimeters in length, and 1.23 to 6 (average 3.3) gram in weight. Walls of mature galls are 5–6 mm in thickness and can not be crushed without a stroke of a hammer. (Eroğlu, 2000). Maturing galls are bright in color, single-chambered and non-coalesced clusters.
Agamic generation galls of A.gallaetinctoriae can be found most common on Q.infectoria Oliv., however, they are also found on Q.ithaburensis Decne., Q.rubur L., Q.petraea (Mattuschka) Lieb. and Q.pubescens Willd. (Schimitschek, 1944; Alkan, 1952); Karaca, 1956; Baş, 1973; Ekici, 1975; Eroğlu, 1997). Q.pubescens and Q.petraea are two common hosts in the second group. Q.infectoria is almost found all woodlands of Turkey, however, it grows most commonly in the Southern East Anatolia. In its large range, the two sub species, Q.infectoria ssp. biossieri (Reut) Gürke is found west, middle, east, and southern east parts of Anatolia and Q.Infectoria ssp. infectoria A. Camus is found north west and Marmara regions (Kayacik, 1963). A.gallaetinctoriae is found over much of Turkey (Figure 1) where the two host oak groups occur together naturally in large areas.
Figure 1. Galling areas of Andricus gallaetinctoriae in Turkey
Emergence of adults was not observed in the galls collected before late July. The highest emergency occurred from the galls that were collected in the last week of August (Ekici, 1975). Adult exiting from galls collected in different years and places showed that the adult emerging period begins in early September and lasts until late October (Ekici, 1975; Eroglu, 1997). Adult emergency from the galls collected late August and early September and stored in the room conditions occured between 8 to 21 October (Eroglu, 2000).
Twenty five percent of the agamics of A. gallaetinctoriae emerged between the dates of 8 to 14 October and the rest 15 to 21 October. The large portion of emergence was occured in the second half of the October. Before winter, we reared about 50 adults of A. gallaetinctoriae from the 60 percent of the galls collected in Ad_yaman-Kuyucak. The average longevity of these adults under laboratory was 12.7 (4 to 16) days (Eroglu, 2000). This period for the adults reared galls from Edremit was 12 to 18 days. Ba_(1973) and Ekici (1975) were found the longevity 6 to 12 and 4 to 13 days.
Agamic galls of A. kollari are similar to galls of A. gallaetinctoriae but do not have stiff spines protruding through the surface. They are globular, woody marble galls, 14 to 23 (average 16.5) millimeter in diameter, and from 0.50 to 2.10 (average 1.32) grams in weight. Almost all adults exited the galls until late September from galls collected on Q.pubescens in Edremit and Kemalpa_. (Eroglu, 2000).
Sexual females of Andricus kollari (Hartig) (=circulans Mayr) oviposit in May to June in buds of Q.robur, and also Q.petraea and Q.pubescens. Agamic galls of A.kollari mature in August and agamic females mostly emerge in September although some larvae overwinter and do not emerge until the following May or June. Agamic females oviposit in buds of Q. cerris, depositing eggs between the embryonic leaves. Development during winter is slow and the sexual galls, which are small, thin-walled, ellipsoid structures, do not become visible among the buds scales until March or April (Beijerinck, 1902; Marsden-Jones, 1953; Folliot, 1964, Askew, 1984).
Discussion
A.gallaetinctoriae and A.kollari are oak galling cynipids requiring two different oak species groups for their development. They are found throughout the overlapping native ranges of the two oak groups. While A.gallaetinctoriae is found over much of Turkey (Figure 1), A.kollari is found only the areas around the Sea of Marmara, along the Aegean cost, Black Sea cost as far as Samsun, and some inner parts of Anatolia.
Only the agamic generation of A.gallaetinctoriae can be found most common on Q. robur, Q. petraea and Q.pubascens in the North Hungary and Transcarpathia (Melika and Csoka, 1993; Diakontshuk and Melika, 1993). Agamic generation of A.kollari is found on Q.robur, and most common on Q.petraea, in the North Hungary, Transcarpathia (Melika and Csóka, 1993), and in the rest of the Ukraine, it can be found on Q.suber and Q.ilex (Diakontshuk and Melika, 1993).
In agamic generation of A.gallaetinctoriae, adult emerging period begins in early September and lasts until late October. The average longevity of the adults under laboratory was 12.7 days on average. Adults from galls collected in Edermit lived 12 to 18 days. The longevity was also found 6 to 12 and 4 to 13 days (Baş, 1973; Ekici, 1975).
Observations on the sexual generations of A.kollari suggest that both males and females will prove shorter-live than the agamic generation. Without food, males of this species live for 2–3 days, females 4–5 days. Despite their smaller size, and thus a greater potential for wind dispersal, such short lifespan may effectively limit the dispersal potential of the sexual generation (Stone et al. 1995). In Andricus quercuscalicis (Burgsd.) a nested analysis of deviance showed that there was no difference in longevity between the no food treatment and water only, but the treatment with sugar-water produced a significant increase in longevity. The average longevity of agamics under laboratory conditions without sugar was 12.2 days and with sugar-water as food was 16.2 days. It is possible that with a diet including nutrients other than sugars, the agamics could live for more than three weeks (Stone et al. 1995).
Two species of inquiline gall wasps reared from the agamic galls of A.gallaetinctoriae collected from South Eastern and western Anatolia were S.umbraculus Olivier and Synergus gallaepomiformis Boyer de Fonsc. (Ekici, 1975) which was also reared from galls of Cynips insana Westw. in the western Anatolia (Schimitschek, 1944). The greatest number of individuals emerged from a single gall were 8 in S.gallaepomiformis and 4 in S.umbraculus. Inquilines reared from agamic galls of A.gallaetinctoriae were S.hayneanus Hart., S.pallidipennis Mayr, S.reinhardi Mayri, S.tristis Mayr, and S.umbraculus Ol. (Diakontshuk & Melika, 1993). Inquilines reared from agamic galls of A.kollari were Synergus albipes Hart., S.crassicornis (Curtis), S.hayneanus Hart., S.nervosus Hart., S.pallicornis Hart., S.pallidipennis Mayr, S.reinhardi Mayri, S.rotundiventris Mayr, and S.umbraculus Ol. (Diakontshuk & Melika, 1993).
Both types of inquiline larvae emphasized in Askew (1984) may be seen in galls of A. gallaetinctoriae and A.kollari in which S.reinhardi occludes the larval chamber and destroys the gall-making larva, and S.umbraculus and S.gallaepomiformis Boyer de Fonsc. occupy peripheral cells in the parenchyma. Galls inquilined by S.umbraculus and S.gallaepomiformis may also produce adults of both gall-makers and inquilines. As a conclusion the inquilines do not have an important negative impact on these two gall-makers in their galling areas in Turkey.
Perhaps, there is an interaction between the color of gall and the development of the gall wasps in it. The galls which are indigo-blue in color generally includes young larvae. The mature larvae can be found in green or light green galls. White galls include pupae or adults gnawing an exit hole. In the following days, especially after a rain, color becomes reddish.
Galls of A.gallaetinctoria are commonly harvested in July and August, when they are indigo-blue or light green. However emergence of adults was not observed in the galls collected before late July. Adult exiting from galls collected in different years and places showed that the adult emerging period begins in early September and lasts until late October (Ekici, 1975; Eroğlu, 1997).
Galls collected in an area are not usually kept or stored in a close vicinity of woodlands so as to give the adults a chance to go back to the woodlands for their next generation. Early harvest or early removal of galls results in not only the loss of crop but also the reduction in the population of gall wasps. This may also result in the increase in the population of other harmful species on the same host plants. Suporting this is the fact that about fifty percent of the agamics collected in Adiyaman-Kuyucak were galls of A.gallaetinctoriae and the rest were galls of Cynips insana Westwood (Eroğlu 2000). Gall inducers do not move from place to place seeking food as to other phytophagous insects (Strong et al., 1984), but remain stationary and create highly nutritious food at their feeding sites.
In gall developing areas, negative effects of human being and animal grazing have also a great role on gall production, whereas there has been no evidence as to whether the galls of A.gallaetinctoriae and A.kollari can cause severe injury and bring about the demise of host trees. On the contrary, if the oaks with galls are protected from the other agents (such as humans and animals), they can reach up to 15 to 20 m in height and 1.0 to 1.5 m in diameter.
Although the exportation income from gall production in Turkey, shows differences by the years, but the average income in a long period is more or less stable. For example, the yearly average exportation income of galls between the years of 1961 to 1970 was 395.000 USD and 1990 to 1999 was 495.000 USD. In the last 10 years, the income portion of the gall exportation in Turkey's non-wood forest products has been 0.74% on average. This number indicates that, while it has the potential of providing the people living in rural areas and having low life standards with an important source of income, gall production in Turkey is still far from what is expected because of inefficient gall harvesting strategies
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M. Mahmut EROGLU
Faculté de foresterie, Université technique de Karadeniz, TRABZON
Turquie
RÉSUMÉ
Les insectes galligènes appartiennent à la famille des cynipidés qui, avec d'autres familles, est dans la superfamille des cynipoidea. Ce sont des hyménoptères parasites et toutes les espèces, à l'exception des espèces de la sous-famille des cynipinae se comportent typiquement comme des parasites ou des hyperparasites d'autres insectes. Les cynipinae sont des galligènes; ce sont les seuls à produire des galles. À l'état larvaire, ils sont phytophages. Il y a des cynips dont les larves ont perdu la capacité de produire des galles, qui vivent donc obligatoirement comme espèces inquilines, dans les galles formées par d'autres cynips.
Plus de 90 % des insectes galligènes se développent sur des plantes dicotylédones et la plupart ne s'attaquent qu'à trois familles: les rosacées, les composacées et les fagacées. La fidélité des cynips aux chênes montre combien les agents galligènes sont monophages. En Amérique du Nord et en Europe par exemple, 87 et 76 % des cynips se développent sur le chêne (Quercus) et chaque agent ne se développe généralement que sur une espèce de chêne ou sur quelques espèces apparentées. Le cynips du chêne est remarquable par la diversité structurelle des galles qu'il provoque. Il se caractérise également par la diversité des parties de la plante qu'il peut attaquer, la diversité des associations végétales hôtes et de son cycle évolutif. Un grand nombre de cynips ont deux générations par an. D'une génération à l'autre, les galles ont souvent une structure radicalement différente.
La diversité des galles dues au cynips tient à la nervation des tissus qui se développent à l'intérieur de la logette larvaire, y compris des couches de tissu ligneux ou spongieux environnantes, des alvéoles complexes à l'intérieur de la galle et, en surface, des couches de résine collante, de poils ou d'épines.
La structure des galles qui se développent autour de la zone nutritive est diverse. L'une des galles les plus spécialisées est celle d'Andricus kollari (Harting), dans laquelle huit zones concentriques de tissus différents ont été trouvées. Plusieurs galles, comme celles d'Andricus gallaetinctoriae (Oliv.) sont très riches en tanin, ce qui leur donne un goût amer. Leur richesse en tanin fait que les galles d'Andricus gallaetinctoriae et d'Andricus kollari sont utilisées depuis des milliers d'années.
La génération agame d'Andricus gallaetinctoriae se retrouve le plus fréquemment sur le chêne à galles des teinturiers (Quercus infectoria Oliv.); mais on la trouve aussi sur Quercus ithaburensis Decne Ssp. macrolepis (Kotschy.) Hedge et Yalt., Quercus cerris L., Quercus conferta Kitt., Quercus ilex L., Quercus rubur L., Quercus petraea (Mattuschka) Lieb. et Quercus pubescens Willd. Le chêne des teinturiers (Quercus infectoria) est présent dans quasiment toutes les forêts de Turquie, mais c'est dans le sud-est, en Anatolie, qu'il est le plus commun. La sous-espèce Quercus infectoria ssp. biossieri (Reut) Gtirke est présente dans l'ouest. le centre, l'est et le sud-est de l'Anatolie, et Quercus infectoria ssp. infectoria A. Camus, l'autre sous-espèce, est courante dans le nord-ouest et dans la région de Marmara.
Les adultes nés de la parthénogénèse ont entre 5 et 8 mm de long et sont principalement de couleur brun foncé avec des poils blanc jaunâtre, fins, courts et épais. L'antenne, couverte de poils épars, comporte 14 articles. Le thorax est couvert d'un duvet brun clair, dense. Le prothorax se rétrécit vers l'avant. Le mésothorax porte deux rayures longitudinales. Le scutellum comporte deux cavités, dont la forme peut être intéressante du point de vue taxinomique.
Andricus gallaetinctoriae, comme de nombreux autres cynips, a une capacité de reproduction élevée et les femelles peuvent pondre de 700 à 800 œufs environ. Les œufs comportent un corps assez court et un long pédicelle qui est 10 à 14 fois plus long que le corps. La ponte dure jusqu'au début de juin. Une fois pondu, l'œuf est plus ou moins inclus dans le tissu du bourgeon. Le stade larvaire dure environ deux mois, du début de juin à la fin d'août ou au début de septembre. La période de formation de la galle dure environ du milieu du mois de juin au début du mois de juillet et l'on trouve des galles immatures de la mi-juillet au début du mois de septembre. Le nymphage commence généralement vers la mi-août, quand la couleur de la galle passe du vert pâle au blanc, et dure entre 15 et 25 jours.
Les galles agames adultes d'Andricus gallaetinctoriae sont presque parfaitement sphériques, ont un diamètre de 13 à 24 mm et sont recouvertes d'épines pointues et raides d'environ 1 à 4 mm de long, elles pèsent entre 1,23 et 6 grammes. Les galles en cours de maturation sont de couleur vive, ont une chambre unique et ne sont pas coalescentes. Les coques des galles, d'une épaisseur de 5 à 6 mm, ne peuvent être cassées qu'à l'aide d'un marteau. Il se peut qu'il y ait un rapport entre la couleur de la galle et le stade de développement de la larve. Les galles de couleur indigo hébergent généralement des jeunes larves. Les larves adultes se trouvent dans les galles vertes ou vert clair. Les galles blanches hébergent des nymphes ou des adultes qui commencent à percer un trou pour sortir. Dans les jours qui suivent, en particulier après la pluie, la galle devient rougeâtre. Les galles recueillies avant la fin du mois de juillet ne comportent pas d'adultes. Les observations faites en différentes années et en différents endroits montrent que la période de sortie des adultes va de début septembre à fin octobre.
La sortie des adultes des galles qui avaient été recueillies à la fin du mois d'août et au début du mois de septembre et conservées à température ambiante a eu lieu entre le 8 et le 21 octobre. Si l'on recueille les galles trop tôt, non seulement on perd la récolte mais on diminue en outre la population de cynips. Les galles recueillies doivent être conservées à proximité de la zone de production jusqu'à la sortie des insectes.
