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. 3.7k Downloads. Abstract The BIOCAT database of introductions of insect biological control agents for the control of insect pests was updated to the end of 2010 to include 6158 introductions, using 2384 different insect biological control agents against 588 pest species in 148 countries.
Of the introductions, 2007 (32.6%) led to establishment, and 620 (10.1%) resulted in satisfactory control being reported against 172 (29.3%) different pest species. The number of introductions has decreased each decade since the 1970s, but in the same period a higher proportion of introductions became established and contributed to successful control of target pests, and the number of countries implementing classical biological control increased. These positive trends reflect the greater research effort now made to optimize the chances of successful outcomes and increased confidence in classical biological control as a viable pest management strategy against a backdrop of a risk-averse culture that has developed in some key countries in recent years. Classical biological control (CBC, not to be confused with conservation biological control) of alien insect pests by the deliberate introduction of insect natural enemies continues to be a powerful pest management tool, especially now that invasive insect pests along with other pest species are on the increase through global trade and travel (Bebber et al. However, understanding the factors that lead to successful outcomes continues to challenge researchers and practitioners. There has been much previous effort to improve predictability.
In the case of insect parasitoids used as biological control agents (BCAs), significant strides have been made in the strengthening of the ecological basis of CBC, mainly through the identification of the broad negative relation between the extent of structural and behavioural defences of target hosts and total parasitism by coevolved parasitoids (Gross; Hawkins et al.; Hochberg and Hawkins ), which has provided practitioners with a strong tool to judge the likelihood of success of a CBC project. A parallel approach has been the identification of factors that underpin success derived from the biological control record.
There are inherent weaknesses in this approach (e.g. Hokkanen ) because CBC outcomes are closely tied to economic and political factors and not so much to the absolute impact of a CBC agent. As Cock et al. ( ) describe, implicitly or explicitly CBC is carried out to achieve specific societal goals, e.g.
Protecting livelihoods of smallholder farmers, reduce pesticide use, or protect biodiversity, whereas the outputs of CBC are often measured in terms to the reduction of the target pest population. Nonetheless, such analyses are useful as they complement the ecological approaches by providing useful insights into global trends in releases, establishments, outcomes and the broad factors that seem to influence success.
A collation of the historical record also provides a crucial source of information about past projects against specific pests that practitioners can use in the design of new efforts against those pests (van Driesche and Bellows ). BIOCAT is a database documenting all deliberate introductions of insects for the biological control of other insects since the 1890s. It was developed and compiled by the late David J. Greathead, former Director of the then International Institute of Biological Control (now integrated into CABI) with the help of his wife, Annette H. In 1992, they provided a description of the database and overview analysis of the data (Greathead and Greathead ).

After that, D. Greathead continued to update the database until his untimely death in 2006 (Murphy and Cock ). Thereafter, the database was neglected for some years until picked up by the present team. Unfortunately we do not have the definitive version of BIOCAT used for Greathead and Greathead ( ), only the updated live version that D.J. Greathead worked on. This prevents us from checking and recreating the numbers in Greathead and Greathead ( ) to confirm how they were derived.
There are no other published global collations and analyses of this type apart from those of introductions against weed targets (Winston et al. ) and nematodes and pathogens as BCAs (Hajek et al. The 1992 database has been used to assess benefits and risks of insect introductions (Greathead ), an updated but unpublished version—including records up to end 2001—was used in a historical overview of biological control in Africa (Greathead ), and the same or a different version was used to summarize the use of insect BCAs against insect pests in Hajek ( ). Unfortunately at the time of David Greathead’s death, none of these versions of BIOCAT had been archived in such a way that we can now identify them. The database has now been updated to include information from publications to the end of 2010, some fields have been restructured, and the nomenclature checked, especially for BCAs. In this, the first of a series of planned papers, an overview analysis is presented that compares our results of historical and country trends in introductions and outcomes with those of Greathead and Greathead ( ). In particular, the trends in these parameters post-1992 and new perspectives on the entire history that BIOCAT now covers are highlighted.
Hereafter the two versions of the database are referred to as BIOCAT1992 and BIOCAT2010, and the latter will be archived as such. CABI plans to convert BIOCAT back to a relational database and make an interrogatable version available open access via the Plantwise knowledge bank ( ) in 2016. Materials and methods. Overall summary statistics on introductions 1890–2010 were compiled to compare with those presented as Table 3 in Greathead and Greathead ( ). BIOCAT2010 was analysed in two ways: mode 1, treating each unique combination of BCA, target country and first year of introduction as one introduction (this was the approach in Greathead and Greathead ); and mode 2, treating each unique combination of BCA, source country, target country and first year of introduction as one introduction (the approach in Cock et al.
Introducing different strains of the same species from different countries is usually done in the expectation that one strain may have a better climatic or ecological match and hence more effective in the target country, but may be for other reasons including adding genetic diversity to a laboratory colony or practical reasons, e.g. Collections from several nearby populations in adjacent European countries, to obtain sufficient individuals for shipment. Interpreting the results of multiple strain introductions has been difficult in the past, but should be possible now using molecular methods.
Generally counts for mode 2 will be slightly higher, as only a small proportion of introductions comprise multiple country sources. Mode 2 is clearly the appropriate approach to take when access and benefits sharing issues are to be considered. The derivation of each summary statistic is as follows. The number of pest target species was obtained as a count of each unique combination of ‘Target genus’ and ‘Target species’. This will undercount those cases where releases were made against more than one target pest, and either a species listed as ‘Target other’ has not been a primary target, or a release was against a target identified as spp. Spodoptera spp.

Lepidoptera: Noctuidae which will only count as one target species). It will also undercount releases that were made against higher taxonomic groups, e.g. Aphids, mealybugs. We do not know how Greathead and Greathead ( ) handled these relatively small numbers of cases. Historical trends in introductions were analysed by dividing the records up into decades based on the date of first introduction (‘Date first year’). All records that had no date of introduction, or the information was too vague (e.g. ‘before 1920’), were omitted, accounting for 5.6% of all records.
The number of introductions per decade was plotted using both mode 1 and mode 2. Establishment and BCA success rates over time also used the data segregated by decades, and ignored all records with no date of introduction. For the analysis, each record was categorized as one of the following: not established (including ‘Not known’, ‘Not established’ and ‘Temporary establishment’); established but no significant control (‘Result unknown’, ‘Established but no control’ and ‘Partial control’); established and contributing to at least ‘Substantial control’.
Next, we considered the number of unique successes based on the date of first introduction of a BCA that contributed to a substantial or complete control. Each target only counts once, i.e. Repeat successes in other countries were not counted.
Establishment and success rates over time also used the data segregated by decade, and ignored all records with no date of introduction. All records with impact less than substantial were then discarded.
The remainder were sorted and the earliest for each combination of target genus and target species was kept and tabulated, i.e. 171 reported successes for which the year of first introduction is known. Trends in country effort and successes were then analysed.
For country effort, the number of introductions (mode 1) per decade was analysed for each country and grouped by decade of first introduction. As before, all records that had no date of introduction or the information was too vague were omitted. For country successes, as for the summary statistics, the number of successful BCAs is a count of those introductions where impact is rated substantial control or better.
Mode 2 was used for this as normally there was no way of showing which BCA source country populations contributed to control. After discarding all records which were not successes, the remainder were categorized by decade and country. The small number of successes that had no date of introduction or for which the date was too vague were omitted. For ease of comparison, the following results of the analysis of BIOCAT2010 reported here largely follow the format in Greathead and Greathead ( ). The summary of records in BIOCAT2010 compared to BIOCAT1992 is presented in Table. BIOCAT2010 contains information on 6158 introductions of BCAs, of which 2007 (32.6%) have become established, leading to 620 satisfactory biological controls (10.1% of introductions; 30.9% of established BCAs) against 172 different pests (29.3% of those targeted).
It can be seen that under mode 1, the number of introductions, the number of BCAs established, the number of pest target species, the number of BCAs and the number of successful biological controls (i.e. At least satisfactory control) have risen quite substantially due to the 18 years of literature since BIOCAT1992. Thus introductions have risen by nearly 20%, the number of targets by over 8%, the number of agents employed by nearly 19%, the number of establishments (excluding temporary) by over 27%, and the number of satisfactory controls by 20%. On the other hand, the total number of countries and areas implementing CBC has only risen marginally (just under 4%).
This table reveals one apparent difference in the results: Greathead and Greathead ( ) indicate from BIOCAT1992 that 421 different pest species were satisfactorily controlled, whereas we find from BIOCAT2010 that there are only 172. However, we count the number of successful programmes as 440, and so conclude that Greathead and Greathead ( )’s figure of 421 actually refers to the number of successful programmes, not the number of different pest species satisfactorily controlled. BIOCAT1992 BIOCAT2010 (Mode 1 a) BIOCAT2010 (Mode 2 b) 1 No. Of introductions (total records) 4769 5715 6158 2a No. Of establishments (excluding temporary) 1434 c 1823 2007 2b No. Of establishments (including temporary) 1445 1894 2084 3 No.
Of pest targets 543 588 4 No. Of agent species 2011 2384 5 No. Of countries and islands 196 203 6 No. Of countries 148 7 No. Of additional islands 55 8 No. Of successful biological control agents 517 620 9 No. Of successful programmes 440 10 No.
Of different pest species controlled 421 172. AMode 1 each agent/target country/year is a separate introduction/establishment, e.g.
An introduction of a biological control agent (BCA) from six countries counts as one introduction bMode 2 each source country/agent/target country/year is a separate introduction/establishment, e.g. An introduction of the same BCA from six countries counts as six introductions cGreathead and Greathead ( ) did not include this statistic. It was extrapolated from BIOCAT2010 by removing records of temporary establishment of introductions from 1989 onwards where the source of information was published after 1992 The statistics for mode 2 illustrate that post-1992 some CBC projects have used several source countries for a particular BCA and this has led to an increase in the number of establishments of BCAs overall (by 10%). Unfortunately no figures are available for BIOCAT1992 for comparison.
Some of the main features of the changes in the summary statistics from BIOCAT1992 to BIOCAT2010 are described in the following sections. Historical trends in introductions, establishments and successes. The total number of introductions (for modes 1 and 2) made globally for each decade period plateaued in the 1950s to the 1970s, and has since been declining (Fig.
Some of the main factors that have probably influenced this trend are discussed later. Greathead and Greathead ( ) presented a similar figure (their Fig. 2a—mode 1 only), and underestimated the introductions for the 1980s by about 20% due to the literature cut-off date. Similarly, since BIOCAT2010 is based on literature to the end of 2010, the number of introductions reported for the 2000s is likely to be underestimated, but we suggest this would be by no more than 25%, i.e. The total for the 2000s may prove to be fewer than 200. Fig. 2 Breakdown of introductions per decade to show the percentage that failed to become established ( triangles), that became established but have not been shown to contribute to control ( squares), and became established and contributed to successful biological control ( circles). To present these results, we focussed on those countries that made more than 40 CBC releases in total and our analysis was based on the date of introduction (when known) over the total period 1870–2010 (Table ). The results are consistent with Greathead and Greathead ( ) and show that to 2010, the USA was still the biggest user but Australia, Canada, the UK, New Zealand, Mauritius, Fiji, France, Israel and South Africa have also consistently invested considerable effort in BCA releases.
However, the number of introductions by these countries declined in the 1980s and/or 1990s, particularly strongly in New Zealand, Mauritius and Fiji. Otherwise, the emphasis on CBC has fluctuated around the world but the number of countries making CBC introductions each decade has generally increased over time reaching 80 in the 1990s, again not including the likely incomplete records for the 2000s (Fig. Similarly, the proportion of total releases each decade made by countries other than the ten countries that in total made the most releases has steadily increased, and these now account for more than half of all introductions (Fig. The trends in numbers of successful BCAs are fairly consistent between countries (Table ), peaking in the 1930s and then at a plateau from the 1960s to 1990s. This table includes the ‘top ten’ (i.e. The ten countries that have reported the highest numbers of successful BCAs) and other countries as categories but here the top ten includes Italy, Chile and Spain, which have had relatively more successes than Mauritius, Fiji and Israel, which are among the top ten for number of releases (Table ). Generally the number of countries reporting one or more successful biological control programmes each decade has been increasing (Fig.
At the moment it is not clear whether the 2000s represents a true drop, or a delay in evaluating and reporting successes. The proportion of all introductions of successful BCAs into countries other than the ten with the most introductions of successful BCAs has been generally increasing, and now more than half the introductions of successful BCAs are reported from these relatively less active countries (Fig. It is important to recognize that many of the limitations of BIOCAT1992 remain with BIOCAT2010. Greathead and Greathead ( ) listed these as: the very uneven reporting of introductions between countries, the fact that researchers are likely to publish successes rather than failures, and that subsequent observations have not supported initial assessments. These categories are, of course, not always mutually exclusive. Reporting remains uneven. One cause may be a lack of agreed reporting standards or peer-reviewed outlets for simple reports of the release or establishment of a BCA.
The fields used in the BIOCAT database offer insight into minimum reporting requirements: What was released? Where did it come from (immediately and originally if different)? Where was it released (preferably with information of numbers of releases and numbers of individuals)?
When was it released? Why was it released?
Where was the BCA recovered? At what level of incidence? How long after releases were last made? What other published or unpublished documentation is available relating to this release and recovery? A common cause for uneven reporting is that, in general, less information is available for nationally funded projects or parts of projects (usually the monitoring and evaluation phase) in developing countries largely because of either lack of human resources or lack of the necessary skills to record and process relevant data on results of impact of a BCA. For example, introductions of parasitoids for trial against the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae), have been made in several major coffee growing developing countries across the globe stretching over several decades (Baker et al.
) but the results of these are still unclear in several cases. In addition, we suggest that where the outcome is not clear-cut, e.g.
Control is partial or only effective in certain areas or under certain conditions, it is likely that these cases will not be fully investigated and documented, or will be simplified in reports. Greathead and Greathead ( ) also mention the lack of information from Latin American countries and this still remains probably because of the major language divide as most international outlets for biological control reporting lie in English language journals. The recent book by Bettiol et al. ( ) will help to address this, but was too recent to include in our update. There are no specific data to support the suggestion that successes are more likely to be published than failures but it seems a reasonable assumption, and it is known that in several biological projects the full outcomes are not known for all the agents released.
As one example of many for this last point, much effort has been made by some countries in the CBC of invasive Liriomyza spp. Leaf miners (Diptera: Agromyzidae) of vegetable crops and while complete control has been reported in several cases and a dominant parasitoid highlighted, the data in BIOCAT2010 suggest that the outcome of approximately 30% of the individual released agents is unknown. The tendency to overstate impact also persists. For example, in reviewing new data for BIOCAT2010, based on their personal field experience, the current authors found several examples of what were likely to be ‘overstated’ results. Initial results following a release may look spectacular in the short term and be reported as such, but in the longer term population dynamics or crop management practices may allow occasional pest outbreaks and damage to continue, for example due to pest resurgence following pesticide applications to control another pest.
In addition to the limitations in the nature of the available data on CBC introductions and outcomes, there have been difficulties in confirming the identity and taxonomic status of some BCA species. We have noted some of the most useful resources for name-checking in the methods section. Additional groups where an authoritative global checklist would have been especially useful include Coccinellidae, Tachinidae, Scoliidae and Tiphiidae. While the total number of introductions has been falling since the 1970s (Fig.
), comparing the overall statistics in BIOCAT2010 with BIOCAT1992 shows that the total introductions have risen by 20% in that 18 year period compared to the total for the 112 years 1880–1992. Much of this growth is attributable to projects in countries without a long history of biological control (Fig.
We believe this indicates that CBC has remained a core activity of pest management for many national programmes. Unfortunately, the number of different pests controlled in the period 1880–1992 given in Greathead and Greathead ( ) is in error and somewhat surprisingly, no one seems to have challenged this number in the interim, although the real figure (172) is well under half of that reported earlier (421). Our figure for the number of unique pests controlled also broadly agrees with the analysis of DeBach and Rosen ( ) where, using records up to 1991, they estimate the species of insect pests being permanently controlled by introduced natural enemies to be 164. Most of the pests controlled are major invasive species that have affected the agricultural economies of countries and in some cases wider regions. Thus to date the collective effort in CBC has stemmed the loss of millions of dollars in crop losses across the globe, protecting livelihoods and alleviating poverty (Cock et al.; DeBach; Greathead; Gurr and Wratten; Hill and Greathead; Lubulwa and McMeniman; Norgaard ). Our analysis shows that up to 2010, the ten countries that invested the most in BCA releases (Table ) remain the same as those highlighted in Greathead and Greathead ( ). The USA has been the largest user accounting for 32% of all introductions.
Over the last two decades, several of these ‘traditional big user countries’ have cut back, but in contrast there is a marked increase over time in the number of countries making one or more introductions (Figs., ), from fewer than ten in the 1890s to 90 in the 1990s with the only substantial drop in the 1940s which would have been due to the impact of World War II. The number of countries reporting successes has generally increased over time (Fig. ) and the current analysis shows that the top ten countries for successes (Table ) differs from the top ten users (Table ) with Italy, Chile and Spain replacing Mauritius, Fiji and Israel. In an analysis of BIOCAT data, Hajek ( ) shows that successful outcomes increase in relation to the number of agents introduced but reach a plateau at 9–14 agents.
Thus, over time, CBC has become a tool in use across the globe, and no longer concentrated in a few countries, although its development has progressed at different times and different rates between countries as noted earlier by Huffaker and Messenger ( ). For example, France has been continuously active since the 1950s. Mauritius and Fiji were most active from the 1920s to the 1970s but introductions have now dropped off to almost nothing. Activity in both countries reflects investment during the colonial period, followed by a period of strong partnership with CABI (Greathead; Rao ). India and Barbados were particularly active in the 1960s and 1970s, which reflects partnership with CABI for the former (Rao et al. ) and with CABI and the Caribbean Agricultural Research and Development Institute for the latter (Cock ).
Either CBC activity in the countries of the former USSR was poorly documented, at least with regard to dates, or we have failed to identify, access and interpret relevant literature. Interestingly countries other than the top ten users overall form an increasing proportion of the successes (Fig.
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