The greater the capacity of a species to produce propagules which is closely associated with body size , the greater is its capacity to increase its population density and extend its geographic range Davis, In ladybird species, body size seems to be a good surrogate of invasiveness once it is positively associated with potential reproductive rate and dispersal ability Hemptinne et al.
These factors seem to explain why the larger aphidophagous H. In Europe, three aphidophagous species were released extensively for the biological control of aphid populations; Hippodamia convergens Guerin, Harmonia conformis Boisduval and H. However, H. To what extent can the success of H. Taxonomy is a fundamental determinant of body size and the differences connected with phylogenetic constraints should be taken into account when evaluating the importance of characteristics determining invasiveness.
The invasive coccinellid species have a wide range of sizes.
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Aphidophagous species i. It is therefore appropriate to consider the characteristics of each group separately. The development times of exotherms depend on temperature and food resources quantity and quality. Species with lower thermal requirements may potentially complete development earlier and eventually produce more generations per year. In that case, potential invasive ladybirds are expected to be in an advantageous position in comparison with native species due to their lower thermal requirements and the consequent increase in their net reproductive rate and intrinsic rate of population increase.
In this paper we: i review the current status of alien ladybird species in Europe, highlighting the circumstances of their introductions, geographic origins and food relationships; ii establish some of the reasons why some species succeeded in entering new geographic areas, using the case studies of Europe and the USA; iii assess the characteristics that do not differ between native and alien aphidophagous species. With respect to the latter point we test the extent to which, a size of the geographic area occupied by aphidophagous ladybird species in their native regions and b some biological traits usually referred to as being the bases of successful invasions body size, fecundity, and developmental time , differ between native and alien species.
To do this we test four predictions: i native species occupying larger native areas will more likely become invasive when moved to new areas than species occupying smaller native geographic areas; ii larger invasive aphidophagous species will exhibit higher reproductive potential compared to smaller species; iii successful invasive aphidophagous ladybirds will have faster developmental rates than native species; iv the rate of spread of H. The review of non-native ladybird species in Europe to was provided by Roy and Migeon and updated to include the data of the period — The first prediction was tested with aphidophagous species of the subfamily Coccinellinae originating in the Palearctic that spread to the Nearctic.
This is because of the availability of information of species distribution in the source area and presence in the recipient area. Seven species that became established in the Nearctic were selected for analysis: C.
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Hemptinne et al. This catalog divides the Palearctic, mainly according to political boundaries, to 51 districts of Europe and 85 districts of Asia. The size of area occupied by a species was classed as the total number of districts occupied in Europe and Asia. This area size was determined for the above species that invaded the Nearctic and for each of their non-invasive congener species that occur only in the Palearctic. The differences in the number of ovarioles were tested using the Mann-Whitney test.
To test the third prediction, we focused on aphidophagous species that invaded from the Palearctic to the Nearctic, and that are widely distributed in the new area Hemptinne et al. Thermal constants, lower development threshold LDT and sum of effective temperatures SET , were established for a number of coccinellid species. Differences in either characteristic were not useful for comparison. For each stage and temperature the differences between invasive and native species were compared using the Mann-Whitney test. Regarding the fourth prediction, native and exotic species were characterized in terms of their dry body mass.
The potential reproductive rate was expressed as half the number of ovarioles, with data retrieved from the literature e.
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Predicted dispersal abilities of native and alien aphidophagous ladybirds were estimated from the values of dry body mass raised to the power of 0. The value of the power of dispersal ability takes into account the maximum rate of oxygen consumption, which increases with body mass raised to the power 0.
Finally, we tested the significance of the values of potential dispersal ability of the aphidophagous alien species H. A total of 24 new alien species-country records were found i. Harmonia axyridis is the most widespread ladybird species Figure 1. From the early s the number of countries where this species was found increased steadily, seemingly reaching a plateau in Figure 2. Harmonia axyridis was the species that invaded the most countries, followed by Cryptolaemus montrouzieri Mulsant with only a third of the newly reported records Table 2.
The alien ladybird species present in Europe 12 introduced to control coccids, aphids, psyllids and whitefly, are summarized in Table 3. Table 1. Numbers of newly reported i. Figure 1. Number of European countries with specified alien ladybird species recorded as present. Data combined from Roy and Migeon and — literature searches. Figure 2. Cumulative number of European countries with H. Island territories included with their country, e. Table 2. Number of European countries with specified alien ladybird species newly reported i.
Table 3. First introduction attempts of ladybirds species as biocontrol agents in Europe. The regions of origin of the alien coccinellid species to Europe are as follows: Australian 5 species: C. Figure 3. The standardized areas of species of the genera Coccinella, Harmonia, Hippodamia , and Propylea that remained limited to their native areas in the Palearctic non-invasive species and seven species of these genera that spread after they invaded the Nearctic invasive species.
We found that the number of ovarioles increased with body size; both in species feeding on aphids as well as non-aphidophagous species Figure 4. Figure 4. Dark symbols: species that invaded the Nearctic from the Palearctic. The potential dispersal ability of H. The rate of spread of H. Table 4. Table 5. The duration of egg, pupa and total development measured in days at seven constant temperatures in species invasive to the Nearctic C. Table 6. Thermal constants at seven constant temperatures in species invasive to the Nearctic C. Table 7. The 12 alien ladybird species recorded in Europe were introduced to control coccids, aphids, psyllids and whitefly, with the majority of the species being coccidophagous.
In two cases the source of the alien ladybirds is unknown.
These figures include species-country records in which the ladybird did not establish, and non-target effects are not evident in many further cases. Hence, only in a relatively small proportion of cases did the alien coccinellid have widespread non-target effects and these mostly involve H.
For example, in Great Britain some H. Additionally, the source populations were not restricted to Europe: some H.
The examples for which the exact pathway is known are rare: in most cases the mechanisms by which a particular insect or group of insects arrived to a particular place is unknown. Perhaps as would be expected, food relationship seems to be a good indirect predictor of a successful coccinellid introduction: worldwide, from the total attempts to control aphids and coccids using classical biological control approaches, only one case 0. On the contrary, the control of coccids has been considered complete in 23 cases 3. According to our initial prediction, invasive ladybirds tend to be more dispersed geographically in their native areas.
An ideal picture of coccinellid distributions would be via high resolution digital maps in which each pixel represents a small area of the Palearctic marked by the presence or absence of the species. However, reaching this goal seems impossible in the near future because of the difficulties associated with recording species presence in most parts of the world.
In this study, we have chosen a compromise solution of dividing the Palearctic into political districts and using data on species presence within these districts. This approach has some pitfalls, particularly since the districts are of unequal landscape diversity and size. Small districts with e. Consequently a species living in a small district with a diversified landscape may be adapted to a wider range of environmental conditions than a species living in an extensive area with uniform landscape conditions.
However, the correlation between landscape diversity and range of species adaptation to environmental conditions is not as important as it may seem. A consequence of this habitat specialization is a limited choice of utilizable sites, even in areas of high landscape diversity. However, some variation in environment cannot be eliminated even by a strong individual habitat choice: this is the variation associated with climatic differences among districts that fill a large geographic area.
Thus a species distributed in a large geographic area, despite its narrow habitat selection, is likely to meet, cope with and be adapted to a greater range of environmental conditions than a species distributed in a small geographic area and this adaptation may be, in our opinion, a basis of its success in colonization of new geographic areas. Our results thus confirm that invasive species are, in their native areas, more prone to adapt to a wide range of conditions compared to non-invasive species in their native ranges.
For generalist predators, flexibility and breadth of habitat use and diet are direct underlying factors of a successful invasion. In general, successful invaders in their new ranges tend to occupy the same habitats as in their native ranges. This is the case with C. However, despite occurring in many semi-natural and natural habitats in their invaded ranges, C. In the USA, H. In Europe, H. Coccinella septempunctata, H.
However, the mechanism by which integration of a new prey species into the diet of a generalist predator is able to drive adaptation to a new geographic range, is unclear. To explore this, it is important to evaluate whether life-history traits of organisms are responsive to selection, and what constraints and trade-offs may limit the overall possible set of traits. However, there are only three studies addressing prey adaptation, two using the generalist H. Over the course of several generations the aphidophagous species were able to improve their fitness when fed on a single diet of lower prey quality.
However, the genetic and epigenetic mechanisms that promote this difference remain to be studied. The absence of significant differences between developmental rates among aphidophagous ladybirds agrees with previous results from laboratory experiments. For instance, in some studies the overall pre-imaginal development time of H. An expected consequence of faster developmental rate is the possibility of the invasive species achieving more generations per year. However, this does not occur even with successful ladybirds spreading into novel ranges, partly because of lower average temperatures.
For instance, within much of the invaded range, H. In conclusion, our results do not corroborate our initial prediction because the invasive species may not have an advantage against natives in using the thermal environment. Although fecundity is influenced by abiotic e. The scatter of data for large aphidophagous species was greater than for small non-aphidophagous species. This may lead to invasive species having higher potential fecundity than non-invasive species. In fact, whilst large invasive species have, in some cases, more ovarioles than predicted by the overall relationship, this was not strongly evident in our results.
In the case of H. For instance, Italian specimens of H.
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Additionally, fewer eggs were laid by H. Soares et al. Michaud and Olsen , using psyllids as a food source, showed that H. Despite these similarities in fecundity, the differences in ovariole number do not always mirror clutch size or fecundity. This is because daily and lifetime egg production are influenced by other environmental factors. However, we predicted that H. To test this prediction, we compared the potential rate of spread of the three species based on their potential reproductive rates and adult body sizes.
However, data of species that have been introduced from the same region but have not become established in the new region would be important in order to better understand invasion processes. All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
Biodivers Data J. Published online Nov Author information Article notes Copyright and License information Disclaimer. Corresponding author. Xiaosheng Chen: moc. Corresponding author: Xiaosheng Chen moc. Received Sep 17; Accepted Nov This is an open access article distributed under the terms of the Creative Commons Attribution License 4.
Abstract Background Nephaspis indus Gordon, was imported into Taiwan from Hawaii in as a biological control agent for the spiralling whitefly, Aleurodicus dispersus Russell, Hemiptera : Aleyrodidae. New information Nephaspis indus Gordon, , a natural enemy of Aleurodicus dispersus Russell Hemiptera : Aleyrodidae native to the Neotropical region, is recorded as established in Taiwan for the first time. Keywords: Coccinelloidea , taxonomy, morphology, spiralling whitefly predator, biological control. Open in a separate window. Diagnosis Nephaspis Casey is similar to the Old World genus Clitostethus Weise, in general appearance and shares the following characters with the latter: body small, length less than 2 mm; antennae composed of 11 antennomeres Fig.
Distribution This genus is apparently endemic to Neotropical region with a natural geographic range extending from southern United States Florida, Louisiana and Texas and Mexico to Argentina Gordon Description TL: 1. Distribution Taiwan, Hawaii, Trinidad, Honduras. Notes There was some confusion about the taxonomy and nomenclature of N. Acknowledgements We are grateful to Dr. Notes Author contributions X. References Blackwelder R. Part 3. United States National Museum Bulletin. A revision of the American Coccinellidae. Journal of the New York Entomological Society. A new Carabus and Cychrus , with miscellaneous notes on Coleoptera.
The Canadian Entomologist. Occurrence and biological control of Aleurodicus dispersus. Formosan Entomologist Special Publication ; 3 — Chinese with English summary. West Indian Coccinellidae Coleoptera : some scale predators with keys to genera and species. The Coleopterists Bulletin. Proceedings of the Entomological Society of Washington. The Coccinellidae Coleoptera of America north of Mexico. South American Coccinellidae Coleoptera. Part V: A taxonomic revision of the genus Nephaspis Casey.
Frustula Entomologica. Coleopterorum Catologus. Pars Junk; Berlin: Efficacy of Nephaspis amnicola and Encarsia? Proceedings of the Hawaiian Entomological Society. Management of invasive alien species in Thailand. Australian ladybird beetles Coleoptera:Coccinellidae : their biology and classification. ABRS; Canberra: Coccinellidae Latreille, In: Leschen R. Handbook of Zoology, Vol. Biological control: Pacific prospects—Supplement 1.
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