TAXONOMY OF NATURAL ENEMIES
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The importance of various aspects of taxonomy relative to biological control was summarized by Gordh & Beardsley (1999). Taxonomy was defined as that branch of biology, which involves the naming, identifying, and classifying of organisms. Previous emphasis had been placed on the importance of taxonomy to biological control by other researchers (Clausen 1942, Sabrosky 1955, Schlinger & Doutt 1964, Delucchi 1966, Compere 1969, Gordh 1977, 1982). For applied biological control workers, there is a need for names for the natural enemies and hosts that are being deployed. Such names provide an important mechanism for the dissemination of information. In theory taxonomy is important to biological control researchers because classification are developed which are intended to reflect evolutionary relationships. Such classifications are helpful because they are intended to predict details of biology and distribution.
The desire to arrange, organize, describe, name and classify is fundamental in human activity. Such an urge operates at all levels of social organization. In ancient civilizations names were applied to organisms, and the common names of many organisms are in widespread usage today. There are however several problems inherent in common names. Most serious is synonymy. Frequently more than one common name is applied to a single organism (synonyms), or the same common name is used for different organisms (homonyms). Synonymy creates confusion and misunderstanding because the biological characteristics and habits of similar organisms can differ greatly. In its earliest form, the scientific name given to an organism was often impractical. Scientific names during the lifetime of John Ray (Wray) (1628-1705) consisted of a series of Latin adjectives catenated in such a way as to describe the animal. The system was less ambiguous than the common name system, but it was cumbersome because the name of an animal frequently was several lines or a paragraph long.
A major contribution in the naming of organisms was made by the natural historian and physician Carl Linnaeus (1707-1778), who is credited with developing the current binomial system of naming organisms. The start of zoological nomenclature is taken as the 10th Edition of Linnaeus' monumental work, Systema Naturae. The notable exception is the nomenclature of spiders which originates with the work of Karl Alexander Clerck (1710-1765), Aranei svecici. The accepted date of publication of these contributions 1 Jan 1758, and this date is the official starting point of zoological nomenclature.
During the following century taxonomic zoologists followed the lead of Linnaeus and prepared descriptions of species for publication but named the animal with a binomen. The binomen consists of two parts, the generic name and the specific epithet. With the accumulation of taxonomic descriptions, problems developed with synonymy, homonymy, the inconsistent application of bionomens, and related nomenclatural difficulties. The first attempt to address these problems was the "Strickland Code," prepared in 1846. A panel of taxonomists, including Charles Darwin who was a noted taxonomist of barnacles, developed this code. Subsequently, an International Code of Zoological Nomenclature was developed in 1906. This code has been altered slightly, but continues to represent the basic guidelines for the formation and validation of zoological names for taxa. The most recent revision was published in 1985. Complicated problems of nomenclature, or matters requiring the fixation of names in the interest of stability, are referred to the International Commission of Zoological Nomenclature which serves as a kind of taxonomic supreme court.
Danks (1988) reviewed the importance of taxonomy to entomology. Its importance for biological control was emphasized by Clausen (1942), and subsequently by Sabrosky (1955), Schlinger & Doutt (1964), Gordh (1977) and Knutson (1981).
The Scientific Name
The scientific name of an organism is of utmost importance (Gordh 1977). It provides a key to the published literature regarding any zoological taxon and without the correct name the researcher has no access to knowledge published about an animal of interest.
The scientific name is a kind of shorthand method for conveying an enormous amount of information about an organism which is available in published literature. All the information which has been developed about any organism important in biological control is stored under the scientific name for that organism. Because of this, the correctness of the name needs to be emphasized.
The need for identification is great in biological control, but the importance of accurate identification is greater. Two species, which are very similar morphologically, are not always similar biologically. Subtle differences in morphology or biology of closely related species can be profound. Distinguishing between variation in taxonomic characters within a species and difference in character states between species (individual versus interspecific variation) is frequently difficult. Understanding the functional significance of the observed anatomical features which serve to distinguish between species is an area of research which has lagged behind orthodox taxonomic studies. Apparent slight anatomical differences may reflect significant differences in the biology of two organisms. So called minor structural differences can mean the difference between pest and nonpest status for species which are potential threats to agriculture, or between establishment and failure to establish in the case of natural enemies. Some examples follow:
Pink Bollworm, Pectinophora gossypiella (Saunders).--The gelechiid genus Pectinophora contains three described species: P. scutigera, P. endema and P. gossypiella. Pectinophora scutigera occurs in Australia, Papua New Guinea, Micronesia and Hawaii; P. endema is restricted to eastern Australia (Common 1958), while P. gossypiella occurs only in Western Australia and other world sites. All species consume the flowers, seeds and seed capsules of Malvaceae. Pectinophora endema consumes only native Hibiscus in Australia, and is not an agricultural pest. The remaining species consume other Malvaceae, including Gossypium spp. (cotton). Pectinophora gossypiella is one of the most serious cotton pests, and larvae of this species can diapause within the seeds of the host plant, which accounts for its widespread distribution. By contrast, P. scutigera does not diapause within seeds, is limited in distribution and is not considered a major pest of cotton.
Holdaway (1926) gave the name of P. scutigera based on larval differences. Later Holdaway (1929) described the structural characters of the adult genitalia to separate the species. The validity of P. scutigera as a species was originally challenged, but is now accepted (Zimmerman 1979).
The importance of correct identification of the bollworms focuses on the pest status of these insects and quarantine enforcement. In Australia P. scutigera is not a significant pest of cotton and its distribution is limited by intrinsic biological characteristics. It does not play a significant role in quarantine efforts. In contrast, P. gossypiella is very pestiferous in cotton. It occurs in the Northern Territory and Western Australia but not in Queensland. Quarantine serves as an important barrier restricting movement of this species. Quarantine is expensive to the state and the commercial enterprise.
Coffee Mealybug, Planococcus kenyae (LePelly).--This insect of Kenya presents an interesting example of early failure and delayed success in biological control caused by misidentification of the pest species. The pest first appeared during the 1930's and caused serious losses to coffee in Kenya. First it was identified as the common, widespread, citrus mealybug, Planococcus citri (Risso). Later it was determined as a related Philippine species, P. lilacinus (Cockerell). Finally both of these identifications were shown to be incorrect, but unfortunately, on the basis of these names, a great amount of effort and expense was devoted to searching for and shipping natural enemies of Planococcus in the Asiatic tropics. Parasitoids, which appeared promising when collected, could not be established in Kenya. The problem was resolved when the taxonomist LePelley examined specimens of the pest. He found relatively inconspicuous but consistent morphological differences which indicated the that coffee mealybug was an undescribed species, which he then named (LePelley 1935, 1943). It was then found that this mealybug also occurred in Uganda and Tanzania where it was under natural biological control. Parasitoids imported into Kenya from those areas produced complete biological control.
California Red Scale, Aonidiella aurantii (Maskell).--The California red scale gives an excellent example of the potential costs of incomplete taxonomic and biogeographic knowledge of a pest species. This scale is a member of a complex of species native to the tropics and subtropics of the Old World (Africa through southeast Asia and the Orient) (McKenzie 1937). It became a pest of citrus when introduced into the New World without its associated natural enemies (Compere 1961). Many parasitoids associated with closely related Aonidiella species would not attack, or were not effective against A. aurantii. The failure of early attempts at biological control were due, at least in part, to the inability to differentiate this species from such closely related species as A. citrina. Some parasitoids in the Orient appeared promising to entomologists, but these species failed when introduced into California because their preferred hosts were other species of Aonidiella. This was apparent after Howard McKenzie made a careful revision of the genus Aonidiella and showed that the species could be separated on the basis of microscopic differences.
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Of equal importance to accurate determination of pest species in biological control is the correct identification of the entomophagous organisms which are found in association with target pests and which are being considered for utilization in biological control. Sometimes such natural enemies belong to groups of small to minute insects, the species of which often resemble one another. Taxonomic knowledge needed to differentiate species level taxa in such groups has accumulated slowly and with great effort. In many groups knowledge remains incomplete. Some examples of the problems involving natural enemy taxa important to biological control are as follows:
Among the Aphelinidae, an important family of entomophagous Chalcidoidea, the genera Aphytis and Marietta appear closely related on the basis of morphology. Superficially it is difficult to place some species in the correct genus. Biologically the differences between the genera are profound. Aphytis species are primary parasitoids of armored scale insects while Marietta species are hyperparasitoids, usually associated with armored scale insects or other Coccoidea. Since hyperparasitoids are viewed as deleterious to biological control, importation or deliberate movement of Marietta could adversely affect biological control.
The family Encyrtidae, another large group within the Chalcidoidea, contains a vast array of genera whose species are primary parasitoids of phytophagous insects. However the same family also contains genera whose species are mostly secondary parasitoids (e.g., Cheiloneurus, Quaylea). Recognition of these hyperparasitoids and their elimination requires a taxonomic knowledge of the Encyrtidae. Failure to do so could result in the introduction and establishment of undesirable species, which is thought to have occurred in a few cases. A few genera of encyrtids (e.g., Psyllaephagus) contain both primary and secondary parasitoid species, which demands careful biological and taxonomic study to separate the beneficial primary and undesirable hyperparasitoids prior to releases.
In the case of the California red scale, not only did difficulty in distinguishing the pest from related species retard biological control, but this such was also encumbered by a lack of knowledge about a very important group of armored scale parasitoids, the genus Aphytis. DeBach et al. (1971) showed that this lack of knowledge delayed achievement of biological control of California red scale by 50 years. Early explorations for natural enemies revealed the presence of Aphytis parasitoids at several localities in the Orient. Specimens from these collections were determined as Aphytis chrysomphali Mercet, a species already present in California that was not especially effective. Therefore, no effort was made to propagate and release new oriental Aphytis until after World War II (Compere 1961). The two most effective natural enemies of red scale, Aphytis lingnanensis Compere and A. melinus DeBach, were not recognized as distinct species until 1948 and 1956, respectively. These species might have been introduced into California many years earlier had a proper understanding of the taxonomy of Aphytis existed.. Similarly, Aphytis holoxanthus DeBach, the most effective parasitoid of Florida red scale, Chrysomphalus aonidum (L.), apparently was first collected around 1900, but was ignored because it was confused with another species. Aphytis holoxanthus was made available for biological control in 1960 when DeBach recognized it as a distinct species (DeBach et al. 1971).
Trichogramma is a cosmopolitan genus of tiny parasitoids which occur as more than 120 species. All species for which the biology is known develop as primary internal parasitoids of eggs. Trichogramma has been used extensively against lepidopterous pests in classical biological control or inundative release programs. Some programs have produced contradictory results, with some workers claiming success and others admitting failure. Poor taxonomic knowledge has contributed to conflicting assessments. Early researchers rarely deposited voucher specimens for their research and without material to compare it was difficult or in some instances impossible to determine what species of Trichogramma was used in a release program. In one example, most references to Trichogramma minutum Riley, T. evanescens Westwood and T. semifumatum (Perkins) made prior to 1980 probably are in error. It is now known that Trichogramma contains many anatomically similar species which can be distinguished only by microscopic differences on antennae and genitalia. Traditional reliance on body coloration is if limited utility and has been shown to depend on environmentally induced variation. Many species display dark coloration at the base of the forewings, and the name T. semifumatum was often applied to such forms. The latter species is now recognized as endemic to the Hawaiian Islands based on one collection (Pinto et al. 1978).
There exists an element of reciprocity between the biological control worker and taxonomist which must be fully developed to maximize the usefulness of taxonomy as an adjunct to biological control. Biological control workers can offer taxonomists important data necessary to complete taxonomic identifications. The kinds of important information include zoogeographical, biological, behavioral ecological and hybridizational data.
Zoogeographical Data.--Biological control researchers frequently engage in time consuming and expensive foreign exploration. Often the results of this work are not published and the imported material is not studied. Such material can provide potentially important data for taxonomic studies in terms of understanding geographical variation and expanding known limits of distribution.
Biological Data.--Because it is believed that there are trends toward habitat specialization and host specificity in many groups of parasitic Hymenoptera, data on host range and host preference can be obtained in the field and in the insectary. Taxonomists to refine their taxonomic analyses f groups can use this information. Also, information on pest species, such as host plant preferences, can be shared with specialists.
Behavioral Data.--Subtle differences in behavior between populations of what appears to be one species may point to taxonomic differences between two or more closely related species. The taxonomist who must rely on preserved specimens, yet they must be made aware of such differences, cannot easily obtain behavioral differences between populations. Once behavioral differences are known, the taxonomist may find encouragement to search more for minor anatomical differences which can be used to distinguish between closely related taxa.
The kinds of important behavioral differences are many. For example, courtship behavior in Aphytis appears to be controlled primarily by species specific sex pheromones released by virgin females. Males are attracted to the pheromone released by conspecific females. Also, males produce a pheromone that appears to calm the virgin female and render her sexually receptive. Males and females do not normally respond to members of the opposite sex belonging to other, even closely related species (Rosen & DeBach 1979). Additionally, other kinds of behavior, such as host finding, may also be indicative of taxonomic difference between populations which show no readily apparent anatomical differences.
Ecological Data.--Closely related species often differ substantially in their ecological requirements. Important data must be kept on the ecological associations of entomophagous arthropods collected for biological control purposes. Factors such as elevations and season are important, but less apparent ecological data, such as the type of plant community in which the species occurs, can also provide valuable clues to the taxonomist who is attempting to differentiate similar forms. Host specificity among related species of parasitic Hymenoptera is often reflected in their association with specific plants which harbor their insect hosts. Thus, information on the plant hosts on which parasitoids are collected may prove useful to taxonomists.
Hybridization Studies.--Most classical taxonomists do not have access to insect rearing facilities, and as a consequence these taxonomists are restricted in their ability to test reproductive compatibility and to make judgements involving the biological species concepts. While most museum taxonomists would acknowledge reproductive compatibility as a viable approach to the study of species limits, in reality they are limited to conceptual acknowledgment only. Biological control researchers with access to laboratory and insectary facilities are able to provide detailed information regarding reproductive compatibility and reproductive isolation. This kind of information is important as is illustrated in such groups as Trichogramma (Pinto et al. 1986).
It is often difficult to find specialists sufficiently expert in the taxonomy of pests and natural enemies who are willing to provide biological control workers with the unequivocal identifications required. This has been especially true for groups of minute parasitoids that are of major importance. Dwindling public support for natural history museums and for taxonomic research in general has intensified this problem since the 1960's. Many biological control specialists have been required to undertake systematic research in an effort to solve taxonomic problems associated with their own research. Thus, scientists whose taxonomic interests originated with their involvement in applied biological control have conducted a considerable amount of basic research, particularly with entomophagous forms. An example is the detailed study of the aphelinid genus Aphytis by Rosen & DeBach (1979). As a result, Aphytis now is recognized as among the best-understood genera of Hymenoptera used in biological control. Similarly biosystematic studies by Dr. E. R. Oatman and colleagues have elucidated Trichogramma in the 1980's, and work with Muscidifurax by E. F. Legner has shown great diversity in a group that was previously regarded as monotypic. [ Please refer to Research ]
Directories of taxonomic specialists are published periodically (e.g., Blackwelder & Blackwelder 1961), and although helpful, they are quickly outdated. An effective method of locating taxonomic expertise is by consulting the most recent -volumes of the Zoological Record. Word of mouth approach is very effective also.
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