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Article

Considering the Geographic Diversity of Natural Enemy Traits in Biological Control: A Quantitative Approach Using Orius Predators as an Example

by
Tarryn Schuldiner-Harpaz
† and
Moshe Coll
*
Department of Entomology, R.H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
*
Author to whom correspondence should be addressed.
†
Present address: Department of Zoology, University of Cambridge, Downing St., Cambridge CB2 3EJ, UK.
Diversity 2022, 14(11), 963; https://doi.org/10.3390/d14110963
Submission received: 7 October 2022 / Revised: 1 November 2022 / Accepted: 5 November 2022 / Published: 10 November 2022
(This article belongs to the Special Issue Heteroptera: Biodiversity, Evolution, Taxonomy and Conservation)
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Abstract

:
The desirable characteristics of effective natural enemies and the causes for failure of biological control efforts have been discussed extensively in the literature, yet predicting which collection site may yield efficient natural enemies remains a challenge. Insect characteristics, such as morphology, physiology, life history and behavior, often vary across geographic cline and location. These variations may reflect phenotypic plasticity across environments, or genetically based local (demic) adaptation. Parameters such as body size, photoperiod response, thermal tolerance and genetic diversity may greatly influence the outcome of biological control efforts. Therefore, geographic variation in such characteristics may be used to optimize the collection site of efficient enemies to be employed in biological control programs. The first step towards this goal is compilation of data on the trait diversity of promising natural enemies across their geographic distribution range. For example, we used published information to compile a database on the geographic distribution of various traits of 92 Orius species (Heteroptera: Anthocoridae), a genus known for its potential contribution to biological control in IPM systems. We discuss how the widespread distribution of this genus in different ecozones should enable the collection of species and populations that differ in various geographically dependent traits relevant to biological control. Finally, we suggest a quantitative method to optimize collection efforts of natural enemies. This approach balances the effects of several natural enemy traits that vary geographically. Lastly, we demonstrate the use of this method by evaluating the potential employment of two geographically distinct populations of O. albidipennis.

1. Introduction

It has been estimated that only one of every twenty attempts to find a successful natural enemy results in successful biological control of a target pest [1]. Even this value may overestimate the success rate of biological control, since failed efforts are likely to remain unpublished. Causes for the failure of biological control efforts, and desirable characteristics of effective natural enemies, have been discussed extensively in the literature [1,2,3,4,5,6]. Nonetheless, it is often difficult to predict which collection sites will yield efficient natural enemy populations with desirable characteristics.
Local climate may influence natural enemy survival, reproduction and efficiency as biological control agents in both classical and augmentative biological control. For example, in the 1920s and 1930s the parasitoid Aphelinus mali Haldeman (Hymenoptera: Aphelinidae) was used to control the woolly aphid Eriosoma lanigerum Hausmann (Hemiptera: Aphididae) in UK apple orchards. This biological control effort failed because the parasitoid was unable to overwinter under conditions found at the target site [1]. In addition, enemy efficiency is often temperature-dependant. For example, Cocuzza et al. [7] showed that at 15 °C and 25 °C, Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) consumed more Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) than Orius albidipennis Reuter (Hemiptera: Anthocoridae). Yet, the latter species, which is better adapted to hot and dry conditions, consumed more prey at 35 °C. It is clear, therefore, that imported natural enemies must be adapted to climatic conditions at the release site [3,8,9]. This could be achieved either by selecting natural enemies from regions with climates similar to that of the release site [3,9], or by selecting populations with a wide range of thermal tolerance and genetic variability, which will enable them to adapt to various climatic conditions.
Another factor that often retards biological control efforts is the mismatch between the phenology of an introduced biological control agent and that of the target pest. For example, a predator may enter diapause under the temperature and photoperiod conditions found at the release site, rendering it ineffective in suppressing pests that continue to develop under those same conditions [1,10,11,12]. Collecting natural enemies with a low tendency to diapause may increase the chance of success in such cases.
Genetic diversity of natural enemy populations is crucial for both classical (i.e., introduction) and augmentative biological control programs. Low genetic diversity often reduces the ability of introduced biological control agents to adapt to new conditions and become established in new surroundings [9,13]. In augmentative programs, genetically homogeneous mass-reared populations often accumulate undesirable genetic traits, thereby reducing the efficiency of natural enemies in the field [2]. Low genetic diversity may result when a cultured population originates from a small number of genetically homogeneous founding individuals [14,15]. Therefore, genetic diversity may be enhanced by collecting a founding population from geographic regions known to harbor genetically diverse populations.
To date, no attempt has been made to quantitatively assess the combined effects of several geographic properties of various enemy traits. As a result, the collection of promising biological control agents remains an art, rather than a scientifically based process in biological control programs. Furthermore, no attempt has been made to integrate eco-geographic rules into biological control practices.
Eco-geographic rules which identify physiological, morphological and life history traits that are correlated with geographic factors, have been studied and reviewed extensively in the literature [16,17,18,19]. Some of these rules are relevant for biological control and may directly or indirectly affect its success. We propose here, for the first time, a way to integrate the two fields, ecological zoogeography and biological control, in order to improve collection strategies of beneficial natural enemies. We propose a zoogeographic approach to classical and augmentative biological control efforts which would (i) promote the collection of geographically dependent information about the genetic structure and ecological, behavioral and life history traits of natural enemies, and (ii) allow judicious collection of natural enemies at selected sites in classical and augmentative biological control programs.
We begin by discussing variation in animal traits, and particularly insect traits, across geographic ranges. We discuss the way in which geographically linked information on enemy traits may promote biological control success rates. We then suggest a quantitative approach for balancing the effects of various geographic properties on enemy traits and thus facilitating the choice of appropriate collection sites. We exemplify our zoogeographic approach by first compiling data on the geographic distribution of all described predatory species of the genus Orius (Heteroptera: Anthocoridae). We then use these data to demonstrate how the suggested quantitative method could be used to assess the relative suitability of two geographically distinct populations of the species O. albidipennis.

1.1. Variation across Geographic Range

It has long been recognized that animal traits may vary across geographic distribution ranges [18]. Gradual variation in animal characteristics is particularly noticeable along clines such as latitude, longitude, altitude and depth [17,18]. For example, homoeothermic animals found at high latitudes and altitudes, where temperatures are relatively low, tend to have larger body mass than closely related animals found at lower altitudes or latitudes. This correlation is known as ‘Bergmann’s rule’ [20] and has also been reported in poikilothermic animals [21], specifically among several intra- and inter-specific insect taxa [16,17], including Orius spp. [22]. Some insect species, however, exhibit an opposite trend, with a decrease in body size at higher latitudes. This phenomenon supports the converse Bergmann’s rule and has been reported mainly for species with longer development times, indicating a possible effect of season length limitations at different latitudes. [23,24]. Other examples of morphological variation along geographic clines include wing morphology and body coloration [19,22,25].
In addition to morphological changes across geographic clines, other insect traits may also vary along geographic gradients (see summary and references in [18,19]). Physiological variation, for instance, is described by Rapoport’s rule, which predicts a wider range of thermal tolerance at higher latitudes; animals at higher latitudes may be well adapted to withstand thermal variance, and their populations may therefore be distributed over a wider geographical range [26]. Population size may also be correlated with geographic clines, as demonstrated by Hodkinson [19], who surveyed the relations between altitude and the abundance of various insect species. In addition, life history may change along geographic clines. This may be due to factors such as the need of non-migrating organisms to adjust their life cycles to the length of the growing season [27]. Consequently, in temperate zones, insects of different latitudinal origin experience different seasonal cycles and therefore vary in phenology. Finally, behavior may also vary along geographic gradients, as demonstrated in Colias butterflies (Lepidoptera: Pieridae), which change their thermoregulatory behavior along altitudinal gradients in order to adjust to local conditions [28].
Differences in insect traits may also vary independently of conditions associated with geographic clines. For example, in some cases, insect characteristics are affected by the position of the animal relative to the species distributional range; certain characteristics may differ between animals in the center versus those at the margins of their species’ range [18]. In addition, populations situated at the margins of the species range were found to display less genetic variation than populations at the center of the range [29].

1.2. Phenotypic Plasticity or Local Adaptation?

Variation in insect characteristics across geographic ranges may reflect phenotypic plasticity or local (demic) adaptation. Phenotypic plasticity is the ability of an organism to change its phenotype in response to changes in the environment, whereas local adaptation is a genetic, and thus heritable, change that takes place in response to local selection pressure [27]. In some cases, it may be difficult to conclude, based on field observations alone, whether geographic variation is a consequence of phenotypic plasticity or a reflection of adaptive processes in genetically distinct populations. For example, latitudinal or altitudinal gradients in body size (i.e., Bergmann’s rule or converse Bergmann’s rule) are sometimes thought to reflect phenotypic plasticity caused by different temperature conditions during arthropods’ development [30]. Others, however, claim that genetically based variation in body size along geographic clines is prevalent in many insect species, including the honeybee Apis mellifera Linnaeus (Hymenoptera: Apidae), the water strider Aquarius remiges (Say) (Heteroptera: Gerridae), several Drosophila species (Diptera: Drosophilidae) (see reviews by [17,23,31]). Such genetic-based adaptation would be less influenced by temperature experienced during immature development.
Nevertheless, phenotypic plasticity may be distinguished from local adaptation by conducting common garden experiments in which insects originating from different geographic populations are studied under identical conditions, or by reciprocal transfer of insects between geographic regions [17]. For example, Blanckenhorn and Fairbairn [27] collected water striders, A. remiges, from field populations at three different latitudes and exposed them to similar temperatures and photoperiod. Their results showed a genetic basis to life history differences found among the studied populations. Similarly, Orius species from different latitudes were shown to have both inter- and intra-specific genetic variation in their response to change in photoperiod; individuals from higher latitudes entered reproductive diapause earlier in response to shortened light hours than individuals from lower latitudes [10,32,33]. Genetic variation in diapause induction was also recorded along altitudinal gradients [12,34].
Understanding whether geographic variation in traits relevant to biological control is genetically based or the result of phenotypic plasticity is critical for the selection of promising natural enemy populations; traits that are not genetically based may be lost after the enemy is transferred into the new environment, be it agricultural field or a mass-production facility. Nevertheless, phenotypic plasticity may allow enemy populations to respond to changing environments and operate under various conditions, thereby promoting the establishment of enemies employed in classical biological control.

1.3. Integrating Zoogeography and Biological Control

Geographically variable parameters such as photoperiod response, thermal tolerance and body size may greatly influence the outcome of biological control efforts. To select enemies that will not enter diapause under release conditions for instance, detailed understanding of the response of natural enemies to changes in photoperiod at different latitudes and altitudes is needed. Havelka and Zemek [35] found that different geographic populations of the aphidophagous gall midge Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) differ in the critical photophase that induces their diapause; critical photophase was shorter in populations from lower latitudes under the same temperature conditions. Nechols et al. [36] and Ruberson et al. [37] found similar latitudinal variation in diapause induction between geographic populations of Chrysopa oculata Say (Neuroptera: Chrysopidae) and Geocoris punctipes Say (Hemiptera: Lygaeidae), respectively. Thus, the tendency of insects from higher latitudes to exhibit a wider thermal tolerance [26,38] may be used to locate natural enemy populations more likely to adapt to new climatic conditions and become established in the release habitat. Finally, variation in body size across latitudinal gradient has been shown to affect longevity, fecundity, mating success and competitive ability in various arthropod species [39,40]. These traits, which are influenced by body size, may affect the ability of natural enemies to rapidly build populations and suppress pest outbreaks. Therefore, change in body size along geographic clines may have important implications for the success of biological control.
Understanding the zoogeography of natural enemy traits may be important not only at the individual level but also on a population scale. High genetic diversity of imported natural enemy populations may increase the rate of establishment in classical biological control and decrease the accumulation of deleterious alleles in mass rearing for augmentative purposes [2,9,13]. Since populations are likely to be more genetically diverse in the center than at the margins of their natural range [29], it may be suggested that natural enemies intended for importation should be collected at the center of their distribution.
Flight capacity is another trait that often varies across geographic gradients and may affect biological control on the population scale. Dingle [41] showed that temperate and tropical populations of milkweed bugs of the genus Oncopeltus (Hemiptera: Lygaeidae) differ in flight duration. He predicted that temperate species may survive winter conditions by migrating to warmer areas and have therefore evolved better flight capacity. This prediction was supported by his finding that milkweed bugs from temperate populations flew longer than those from tropical regions. In addition, morphological and functional characteristics of insect wings, such as wing load and wing aspect ratio and length (with respect to body size), have been shown to vary with latitude and altitude. These variations are often genetically based and may allow insects to disperse at high latitudes and altitudes by compensating for the reduction in wing muscle efficiency at low temperatures [17,25,42,43,44,45]. Properties such as wing morphology, wing load and flight duration greatly affect the ability of natural enemies to disperse by flight. Therefore, if a quick and effective dispersal of an introduced agent is needed in classical biological control, it may be advisable to collect enemies from more temperate populations. However, in augmentative biological control, where enemies should restrict their activity to a limited area, it may be advisable to collect natural enemies from more tropical regions. It is important to note, however, that a trade-off may exist between flight capacity and fecundity (the flight-oogenesis syndrome, [46,47]). This was reported also for a heteropteran bug [48]. The geographic distribution of pests targeted for biological control should also be considered. For instance, lower parasitism and predation rates occur at higher altitude in some herbivorous insect populations [19]. This may result from either lower abundance of a specific parasitoid or predator, or reduced efficiency of natural enemies at higher altitudes. Either way, this information implies that the search for natural enemies of these pests should be conducted at lower altitudes.
Biological control practitioners have until now selected enemy collection sites based on their own experience and judgment. Yet, several eco-geographic rules discussed earlier could be used to help select collection sites of more promising natural enemy populations. While these rules may often operate in concert in terms of benefit for biological control, they may also occasionally contradict each other. Tendency for winter diapause, for instance, may increase with latitude, thereby shortening the period in which natural enemies from higher latitudes can suppress pest populations. Conversely, the tendency for a wider range of thermal tolerance at high latitudes, may suggest that it would benefit biological control to collect natural enemies from these areas. Furthermore, the relative importance of each of the geographically dependent traits may vary according to the intended use of the biological control agent. A wide range of thermal tolerance, for example, may be more important when targeting pests in temperate than in tropical regions.
In conclusion, an in-depth understanding of the manner in which natural enemy traits vary across geographic ranges, and knowledge of the geographic distribution of a given biological control agent, would allow for effective collection of individuals at a particular location. These individuals will then have a better chance of becoming established in classical biological control programs, or of being effectively reared for augmentative release.
In this paper, we propose a heuristic quantitative framework to assist practitioners with the challenge of collecting effective natural enemies at various geographic locations. This tool must be used only after the general region for exploration is matched climatically with the targeted release area.

2. A Quantitative Approach for Evaluating Collection Sites of Natural Enemies

Our approach balances the importance of various geographically dependent enemy traits for different biological control uses (i.e., classical, inundative or inoculative biocontrol; Table 1). Each potential collection site is ranked based on the assumed effect of its geographic location (latitude, altitude and distance from the center of species distribution) on several enemy traits, and the relative importance of each trait to the intended biological control programs. This allows the assessment of the relative suitability of two or more natural enemy collection sites. This could be conducted to compare several populations (collection sites) of a single natural enemy species, or the use of the same enemy population (a single collection site) in different biological control programs.
Table 1 should be used in two steps. First, the relative influence of geographic properties of a potential collection site is calculated for each enemy trait important for biological control (left part of the table). Then, the obtained values are multiplied by a factor (weight) derived from the relative importance of each enemy trait for classical, inundative and inoculative biological control programs in tropical and temperate regions. The values obtained for all enemy traits are then added to obtain a single rank for that collection site.
The influence of all three geographic gradients on trait values (X, Y and Z for latitude, altitude and distance from the center of species distribution, respectively) is standardized; the influence of latitude is equal to the measured geographic latitude, while the influence of the altitude is calculated by dividing the measured altitude (in meters) by 139, which is the altitudinal equivalent of one degree of latitude in terms of change in temperature [50]. The influence of the distance from the center of distribution range is calculated by dividing the measured distance (in kilometers) by 111, which is the equivalent of one degree of latitude in terms of distance. Lack of correlation between a trait and a geographic gradient is indicated by an influence value of 0. The over-all geographic influence on each trait is expressed by the sum of the influence magnitudes given for all three geographic criteria.
The nature of the biological control program in which the collected natural enemies are to be employed will determine how each of the considered enemy traits may influence the outcome of the biological control project. First, one must classify the method of biological control as either ‘classical’ or ‘augmentative’, the latter being further classified as ‘inoculative releases’ or ‘inundative releases’. The next classification is based on the climate at the target site, which can be either ‘tropical’ or ‘temperate’. Weights may range from −9 to 9; positive weights indicate that high values of the trait may increase the chance for successful control of the target pest, while negative weights indicate the opposite. Weights above the value of 5 or below the value of −5 indicate a trait which may have an immediate strong effect on the outcome of the biological control program and may determine its success or failure. Weights between the values of −5 and 5 indicate traits which may reduce or induce control of the target pest, respectively, but will have less influence on the final outcome of the project.
The final over-all rank describes how effective it would be to collect a natural enemy population at a specific geographic location, in order to employ it in a specific biological control program. Please note that (i) this tool is to be used after an initial climatic matching between release and collection regions, and (ii) final ranks should be treated as relative values which reflect the comparative suitability of different collection sites; negative values do not necessarily mean that collecting natural enemies from this site would have a negative effect on the success of the biological control effort.

3. Applying the Approach to Orius Bugs

The genus Orius, of the family Anthocoridae, has a wide geographic distribution and is taxonomically well resolved [23,51,52]. Most species of Orius are generalist predators that are known to feed primarily on thrips, aphids, mites, whiteflies, lepidopteran eggs and neonates of additional insects [53,54,55]. Despite their wide range of prey, Orius species have been shown to prefer larvae and adult thrips, including important agricultural pest species [56,57]. In addition, many Orius species supplement their prey diet with pollen and plant sap, and are able to sustain themselves in this way during periods of prey scarcity [51,58,59,60]. For these reasons, this genus has received much attention for its potential contribution to biological control in IPM systems. Species such as O. insidiosus Say, O. laevigatus, O. Sauteri Poppius and O. majusculus (Reuter) are considered effective natural enemies and are therefore being used successfully both in open fields and greenhouse cropping systems throughout the world [51,61,62].
To exemplify how zoogeographic information of natural enemy traits could be employed in biological control, we used published information to compile a database of the geographic distribution of described Orius species. The database encompasses 91 species from all continents except Antarctica (Table 2), which expands the previously estimated number of described Orius species [52] by about 20. We believe compilation of such databases would promote effective biological control efforts by (1) identifying exploration sites with climate similar to that of the target site, (2) facilitating the collection of various genotypes from different ecozones, and (3) indicating the availability of various potential enemy species within a region.
Geographic variation in the tendency to enter diapause was reported in O. laevigatus. This species is used commercially to suppress Thrips tabaci Lindeman (Thysanoptera: Thripidae) and F. occidentalis populations in greenhouses [90] and is naturally distributed across a wide range of latitudes in the Palaearctic region [53,65]. Tommasini and Van Lenteren [91] noticed that northern populations in Italy undergo a weak reproductive diapause, while southern populations do not. It may be advisable therefore to collect O. laevigatus for mass-rearing and field-release purposes at the southernmost parts of its range. Similarly, other Orius species, such as O. sauteri, O. nagaii Yasunaga, O. minutus (Linnaeus), O. strigicollis (Poppius) and O. tantillus (Motschulsky) from Japan [32,33], and O. tristicolor (White) from North America [10], show variation in the critical daylength for reproductive diapause, depending on their latitude of origin. Should any of these predators be employed as biological control agents, collecting southern populations and transferring them to northern areas could lengthen the reproductive period and reduce the number of diapausing individuals in those regions [10,11].
Body size may also vary geographically among and within Orius species. Orius laevigatus, O. niger Wolff and O. albidipennis have been found to vary in body size along a climatic cline in Israel, following Bergmann’s rule [22]. That geographic variation in Orius body size may be genetically based is supported by findings in other Hemipterans [23]. It seems therefore that since larger bugs are likely to be superior dispersers and foragers, more competitive, and more fecund, exploiting the geographic gradient in Orius body size could greatly benefit biological pest control by these predators.
Some species of Orius, such as O. retame (Noualhier) and O. limbatus Wagner, are restricted to relatively small geographic regions, while others, such as O. albidipennis and O. tristicolor, are distributed throughout entire ecozones. Brown [92] suggested that distribution range correlates with niche breadth, implying that specialized species often have more restricted ranges of distribution. Therefore, if specialist natural enemies are less likely to adversely affect non-target species, it would be advisable to collect species of more restricted geographic distribution. On the other hand, species that are not able to persist in a wide range of niches may not be able to adapt when released into new target sites. Species with limited ranges can be easily distinguished from those with a wide distribution range by examining the geographic distribution information presented in Table 2.

4. Orius albidipennis as a Case Study

We chose to use the species O. albidipennis to demonstrate the use of the quantitative method presented in Table 1 by comparing the suitability of two potential collection sites. O. albidipennis has several qualities which make it a promising biological control agent in general, and a suitable species for this case study, specifically. First, it feeds on a wide range of prey, including thrips, aphids, mites, leafhoppers and Lepidoptera eggs and neonates (reviewed by [52,93]). It may therefore serve as a biological control agent against a variety of pest species. In addition, its feeding habits may allow it to consume alternative prey and persist in the field when target pest populations are scarce [94]. Second, this species is widely distributed from East Africa in the south, through North Africa and the Mediterranean region in the north, from western India in the east to the Atlantic Ocean in the west (Figure 1) [53,63,65,66,67]. It is thus possible to collect several geographically distinct populations, which may vary in traits relevant to biological control. Thirdly, extensive research has been conducted to evaluate the predation capacity of O. albidipennis on various pest species and the effects of temperature and humidity on its oviposition, fecundity and longevity [7,94,95,96,97]. Available information may promote the adoption of this predator for appropriate biological control programs and the development of cost-effective mass rearing procedures. Finally, O. albidipennis adults are observed in the field year-round and no diapause induction has been recorded to date in this species [53,98]. As a result, O. albidipennis has frequently been proposed a candidate for biological control efforts against pests such as F. occidentalis and Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in countries such as Israel, Egypt, Kenya and Spain [67,94,96,99,100,101].
The use of the quantitative method presented in Table 1 is demonstrated here by evaluating the suitability of two collection sites, Albacete in South-eastern Spain and Giza in Egypt, for possible sources for O. albidipennis to be employed in an augmentative biological control programs using inoculative releases in a temperate climate; Orius albidipennis collections were reported in these regions, respectively, by Sanchez and Lacasa [96] and by Tawfik and Ata [97] (Figure 1).
The predator’s center of distribution was estimated to be on the border between Libya and Egypt, at approximately 24°30′00″ N, 24°60′00″ E (Figure 1, asterisk). The distance of the Albacete and the Giza collection sites from this area is about 3000 and 870 km, respectively. Accordingly, the values for the standardized influence of geographic location on enemy trait values are as follows: X = 38; Y = 740/139 = 5.3; Z = 3000/111 = 27 for the Albacete site; and X = 30; Y = 30/139 = 0.2; Z = 870/111 = 7.8 for the Giza site. Calculation results indicate that the Giza site received a higher rank (Table 3) and therefore may be more suitable for the collection of O. albidipennis for the tested biological control program.
Table
Table 3. Evaluation of the relative suitability of Orius albidipennis collected in Albacete, Spain and in Giza, Egypt for an inoculative biological control program in a temperate region (based on the quantitative method presented in Table 1).
Table 3. Evaluation of the relative suitability of Orius albidipennis collected in Albacete, Spain and in Giza, Egypt for an inoculative biological control program in a temperate region (based on the quantitative method presented in Table 1).
Geographically Variable TraitStandardized Influence of Geographic Location on Trait Values *Sum of Geographic Location InfluenceTrait Relative Weights Weighted Influence Values
Lat.Alt.D.
AlGiAlGiAlGiAlGiAlGi
Tendency for winter diapause-----------
Range of thermal tolerance3830000038307266210
Body size38305.30.20043.330.2313090.6
Genetic variability0000−27−7.8−27−7.88−216.2−62.7
Flight capacity38305.30.20043.330.2−4−173.3−120.9
Total rank 6.5117.1
* Lat.—latitude; Alt.—altitude; D.—distance from species center of distribution. Al—Albacete collection site; Gi—Giza collection site.

5. Future Directions

Predators of the genus Orius, and specifically O. albidipennis, illustrate the potential benefits of adopting a zoogeographic approach to biological control. Further research is needed in order to compile detailed geographic information about other promising natural enemies. Such information includes geographic distribution and genetic makeup and variability across the range of distribution. This information can then be applied to the proposed quantitative method in order to select the most promising enemy collection sites. The proposed heuristic method should merely serve as a basis for further fine-tuning and modifications. The influence of geographic properties on additional biological traits of the natural enemy and the relative correction values should both be tested. Finally, greater accuracy could be obtained by including additional climatic zones, such as desert and Mediterranean, to the table. We hope that the outlined method will be used to promote more scientifically based biological control practices, by optimizing the collection of natural enemies for classical and augmentative biological control programs.

Author Contributions

Conceptualization, T.S.-H. and M.C.; methodology, T.S.-H. and M.C.; writing—original draft preparation, T.S.-H.; writing—review and editing, M.C.; visualization, T.S.-H.; project administration, M.C.; funding acquisition, M.C. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported in part by the Israel Science Foundation, founded by the Academy of Science and Humanities (ISF grant 574/07 to MC).

Institutional Review Board Statement

Not applicable.

Acknowledgments

We thank Ruthann Yonah for help with manuscript development and the Israel Institute for Advance Studies for hosting MC during manuscript preparation.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Tendency for winter diapause:
₋
Trait values correlate positively with latitude and altitude, but not with distance from the center of species distribution.
₋
In the case of application of augmentative programs in annual summer crops, a tendency for winter diapause is of no consequence and should therefore be disregarded.
₋
Relative weights were determined as follows:
Within the category of classical biological control, temperate climate received a positive intermediate value, because the natural enemy must be able to overwinter successfully in order to establish itself. In a tropical climate, winter conditions are a less limiting factor and diapause may therefore hinder pest suppression, hence the negative value.
In augmentative biological control, the natural enemy does not become established; diapause is thus not necessary and may only hinder pest suppression. Negative values are therefore assigned for both inundative and inoculative releases. However, diapause is less of a problem in the inundative method, as it can be overcome by repeated releases; therefore, this method receives a less negative weight than the inoculative method. In both approaches, like in the classical method, a temperate climate receives a larger weight than a tropical one.
Range of thermal tolerance:
₋
Trait values correlate positively only with latitude.
₋
Relative weights were determined as follows:
In temperate climates, a large range of thermal tolerance is more important than in tropical climates.
The ability of the natural enemy to adapt to local conditions and withstand temperature fluctuations is more important in the classical approach, since the population must establish itself. In the inoculative method, the weight of this trait is higher than in the inundative one, because in the latter, the population does not need to sustain itself for long periods.
Body size:
₋
Applies only if the species follows Bergmann’s rule. If converse Bergmann’s rule applies, weight values should be multiplied by (−1). If no correlation has been found between body mass and latitude/altitude in this species, this trait should be disregarded.
₋
Trait values correlate positively with latitude and altitude, but not with distance from species center of distribution.
₋
Relative weights were determined as follows:
Body size affects both fecundity and enemy efficacy and therefore is equally important in all methods and climates, yet it is not critical for the success of biological control and receives a value lower than 5.
Genetic variability:
₋
Trait values correlate negatively only with distance from center of species distribution.
₋
Relative weights were determined as follows:
This trait is critical for the success of biological control and therefore receives high weights in all cases. In temperate climates, there are larger fluctuations in environmental conditions and therefore genetic variability is slightly more important than in tropical climates. The difference between the importance of the trait in the two climates is greater in the classical method because establishment is assumed to be more difficult in fluctuating conditions.
Flight capacity:
₋
Trait values correlate positively with latitude and altitude, but not with distance from center of species distribution.
₋
Relative weights were determined as follows: Ability to disperse is determined by flight capacity. In the classical approach, dispersal of the natural enemies is essential (positive values), while in the other methods it is undesirable (negative values). In temperate climates, resources are highly scattered and their availability is more variable. Therefore, in classical biological control, the ability to disperse is of a greater importance in temperate than tropical regions. The greater importance of fight ability in temperate augmentative programs is attributed to lower efficiency of flight muscles at lower temperatures.

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Diversity 14 00963 g001 550
Figure 1. Geographic distribution of Orius albidipennis (Heteroptera: Anthocoridae). Countries and areas in which O. albidipennis was reported are marked with black circles (•) [53,63,65,66,67]. The two sites evaluated for suitability for O. albidipennis collection (see Table 1 and Table 3) are marked with open circles (ο) and indicated with arrows: Albacete, Spain (latitude: 38°59′44″ N, altitude: ~740 m) and Giza, Egypt (latitude: 30°35′0″ N, altitude: ~30 m). The estimated center of distribution is marked by an asterisk (*).
Figure 1. Geographic distribution of Orius albidipennis (Heteroptera: Anthocoridae). Countries and areas in which O. albidipennis was reported are marked with black circles (•) [53,63,65,66,67]. The two sites evaluated for suitability for O. albidipennis collection (see Table 1 and Table 3) are marked with open circles (ο) and indicated with arrows: Albacete, Spain (latitude: 38°59′44″ N, altitude: ~740 m) and Giza, Egypt (latitude: 30°35′0″ N, altitude: ~30 m). The estimated center of distribution is marked by an asterisk (*).
Diversity 14 00963 g001
Table
Table 1. Quantitative heuristic framework for evaluating the suitability of natural enemy collection sites. See text and Appendix A for details.
Table 1. Quantitative heuristic framework for evaluating the suitability of natural enemy collection sites. See text and Appendix A for details.
Geographically Variable TraitStandardized Influence of Geographic Location on Trait ValueTrait Weight
(Based on Biological Control Approach)		Ref.
LatitudeAltitudeDistance from
Center of Species Distribution		ClassicalAugmentative
Inoculative ReleasesInundative Releases
Climate at Release Site:
Tropic (Tr) or Temperate (Te)
TrTeTrTeTrTe
Tendency for winter diapauseX *Y *0−15−4−7−3−6[10,12,27,32,33,34,35,36,37]
Range of thermal toleranceX00583726[26,38]
Body sizeXY0333333[16,17,20,23,26,27]
Genetic variability00−Z *797878[29,49]
Flight capacityXY023−3−4−2−3[41]
* X = latitude (deg.); Y = altitude (m)/139; Z = distance from center of species distribution (km)/111.
Table
Table 2. Zoogeographic distribution of Orius species (Heteroptera: Anthocoridae).
Table 2. Zoogeographic distribution of Orius species (Heteroptera: Anthocoridae).
AfrotropicPalaearcticIndo-MalayaAustral-AsiaNearcticNeotropical
Species Western AfricaSouthern AfricaEastern AfricaArabian desertNorthern AfricaMediterranean BasinWestern EuropeCentral EuropeWestern and Central AsiaEastern Asia CanadaEastern North AmericaCentral North AmericaWestern North AmericaCentral AmericaNorthern South AmericaCentral South AmericaSouthern South AmericaRef.
O. agilis (Flor) +++ [53,63,64,65]
O. albidipennis (Reuter) + +++++ + + [53,63,65,66,67]
O. alcides Herring + [68]
O. allaudi (Poppius) + [67]
O. alpina (Poppius) + [67]
O. amnesius Ghauri + [69]
O. armatus Gross + [70]
O. atratus Yasunaga ++ [71]
O. bifilarus Ghauri +++ [64,65,72]
O. brunnescens (Poppius) + [73]
O. bulgaconus Ghauri + [72]
O. camerunensis (Poppius) + ^ #
O. canariensis Wagner ++ [53,65]
O. candiope Herring + [68]
O. cardiostethoides (Poppius) + [67]
O. chadwicki Woodward & Postle + [70]
O. championi Herring ++ [68]
O. cocciphagus (Hesse) + [73]
O. conchaconus Ghauri + [72]
O. dendrophilus Postle, Steiner & Goodwin + [74]
O. diespeter Herring + [68]
O. dravidiensis Muraleedharan + [75] ^
O. elegans (Blanchard) +[76]
O. euryale Herring + [68]
O. flagellum Linnavuori + [65,77]
O. flaviceps (Poppius) + [68]
O. florentiae Herring ++ [68]
O. fogoensis Wagner + ^
O. fuscus (Reuter) ^+ [68]
O. gardinieri (Distant) + ^
O. gladiatus Zheng ++ [64,65]
O. gracilis Postle, Steiner & Goodwin + [74]
O. harpocrates Herring + [68]
O. heterorioides Woodward & Postle + [70]
O. heynei (Reuter) + [67]
O. horvathi (Reuter) ++++++ [53,63,64,65]
O. ianthe Distant + ^ #
O. indicus (Reuter) + [78]
O. insidiosus (say) ++++++++[68,76,79]
O. ixionides Herring + [68]
O. jasiones Herring + [68]
O. jeanneli (Poppius) + [67]
O. laevigatus (Fieber) +++++I+ [53,63,65,80]
O. lanatus Carayon + [73]
O. latibasis Ghauri + [72]
O. laticollis (Reuter) ++++++ [53,63,65]
O. lesliae Herring + [68]
O. limbatus Wagner + [53,65]
O. lindbergi Wagner ++++ [53,65]
O. lobeliae (Poppius) + [67]
O. luridoides Ghauri + [72]
O. luridus Wagner syn. O. laevigatus laevigatus (Fieber) [65]
O. maderensis (Reuter) syn. O. laevigatus maderensis (Reuter) [65]
O. majusculus (Reuter) ++++++ + [53,63,65,81]
O. maura (Poppius) + [67]
O. maxidentex (Ghauri) + + [72,78]
O. minutus (Linnaeus) +R+++++ I * I * [53,63,64,65,68,82]
O. miyamotoi Yasunaga + [71]
O. nagaii Yasunaga + [65,82]
O. naivashae (Poppius) + [67]
O. niger Wolff +++++++ [53,63,64,65,72]
O. niobe Herring syn. O. tantillus [65]
O. oblonga (Reuter) ^
O. pallidicornis (Reuter) +++++ [53,63,65]
O. pallidus (Poppius) ++[68]
O. parvulus (Blanchard) +^
O. pele Herring + [68]
O. pellucidus Garbiglietti + ^
O. peri Carayon + [83]
O. perpunctatus (Reuter) + + [68]
O. persequens (White) ^ + [84]
O. piceicollis (Lindberg) + [53,65]
O. pluto (Distant) + ^ #
O. proximbus (Poppius) + ^
O. pumilio (Champion) ++ + [68]
O. punctaticollis (Reuter)+ ^
O. puncticollis (Poppius) + ^ #
O. reedi (White) +[76]
O. retamae (Noualhier) + [53,65]
O. sauteri (Poppius) + [64,65,82]
O. shakebi Ghauri + [67]
O. shyamavarna Muraleedharan & Ananthakrishnan + [85] ^ #
O. sibiricus Wagner ++ [53,63,65]
O. similis Zheng syn. O. strigicollis [82]
O. sjöstedti (Poppius) + [67]
O. strigicollis (Poppius) ++ [65,82]
O. sublaevis (Poppius) ++ [65]
O. takaii Yasunaga + [77]
O. tantillus (Motschulsky) + +++ [64,65,67,70,80,86]
O. thripoborus (Hesse) ++ [67,73]
O. thyestes Herring ++ [68,79]
O. tristicolor (White) ++++++++[68,76]
O. trivandrensis Muraleedharan & Ananthakrishnan + [85] ^ #
O. ugandensis Hernandez & Stonedahl+ [67]
O. vicinus (Ribaut) +++++ + I [53,63,64,87,88]
I—introduced and established. R—rare. ^ Cited by Ford [89] without reference. # Cited by Yasunaga [80] without a reference. * May have been O. vicinus see ([88]).
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Schuldiner-Harpaz, T.; Coll, M. Considering the Geographic Diversity of Natural Enemy Traits in Biological Control: A Quantitative Approach Using Orius Predators as an Example. Diversity 2022, 14, 963. https://doi.org/10.3390/d14110963

AMA Style

Schuldiner-Harpaz T, Coll M. Considering the Geographic Diversity of Natural Enemy Traits in Biological Control: A Quantitative Approach Using Orius Predators as an Example. Diversity. 2022; 14(11):963. https://doi.org/10.3390/d14110963

Chicago/Turabian Style

Schuldiner-Harpaz, Tarryn, and Moshe Coll. 2022. "Considering the Geographic Diversity of Natural Enemy Traits in Biological Control: A Quantitative Approach Using Orius Predators as an Example" Diversity 14, no. 11: 963. https://doi.org/10.3390/d14110963

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