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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>Tuta absoluta</italic> (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for Integrated Management Initiatives</title><author><name sortKey="Tarusikirwa, Vimbai L" sort="Tarusikirwa, Vimbai L" uniqKey="Tarusikirwa V" first="Vimbai L." last="Tarusikirwa">Vimbai L. Tarusikirwa</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author><author><name sortKey="Machekano, Honest" sort="Machekano, Honest" uniqKey="Machekano H" first="Honest" last="Machekano">Honest Machekano</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author><author><name sortKey="Mutamiswa, Reyard" sort="Mutamiswa, Reyard" uniqKey="Mutamiswa R" first="Reyard" last="Mutamiswa">Reyard Mutamiswa</name><affiliation><nlm:aff id="af2-insects-11-00764">Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa;<email>2018066841@ufs4life.ac.za</email> (R.M.);<email>ChidawanyikaF@ufs.ac.za</email> (F.C.)</nlm:aff></affiliation></author><author><name sortKey="Chidawanyika, Frank" sort="Chidawanyika, Frank" uniqKey="Chidawanyika F" first="Frank" last="Chidawanyika">Frank Chidawanyika</name><affiliation><nlm:aff id="af2-insects-11-00764">Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa;<email>2018066841@ufs4life.ac.za</email> (R.M.);<email>ChidawanyikaF@ufs.ac.za</email> (F.C.)</nlm:aff></affiliation></author><author><name sortKey="Nyamukondiwa, Casper" sort="Nyamukondiwa, Casper" uniqKey="Nyamukondiwa C" first="Casper" last="Nyamukondiwa">Casper Nyamukondiwa</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">33171892</idno><idno type="pmc">7694550</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7694550</idno><idno type="RBID">PMC:7694550</idno><idno type="doi">10.3390/insects11110764</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000302</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000302</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>Tuta absoluta</italic> (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for Integrated Management Initiatives</title><author><name sortKey="Tarusikirwa, Vimbai L" sort="Tarusikirwa, Vimbai L" uniqKey="Tarusikirwa V" first="Vimbai L." last="Tarusikirwa">Vimbai L. Tarusikirwa</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author><author><name sortKey="Machekano, Honest" sort="Machekano, Honest" uniqKey="Machekano H" first="Honest" last="Machekano">Honest Machekano</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author><author><name sortKey="Mutamiswa, Reyard" sort="Mutamiswa, Reyard" uniqKey="Mutamiswa R" first="Reyard" last="Mutamiswa">Reyard Mutamiswa</name><affiliation><nlm:aff id="af2-insects-11-00764">Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa;<email>2018066841@ufs4life.ac.za</email> (R.M.);<email>ChidawanyikaF@ufs.ac.za</email> (F.C.)</nlm:aff></affiliation></author><author><name sortKey="Chidawanyika, Frank" sort="Chidawanyika, Frank" uniqKey="Chidawanyika F" first="Frank" last="Chidawanyika">Frank Chidawanyika</name><affiliation><nlm:aff id="af2-insects-11-00764">Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa;<email>2018066841@ufs4life.ac.za</email> (R.M.);<email>ChidawanyikaF@ufs.ac.za</email> (F.C.)</nlm:aff></affiliation></author><author><name sortKey="Nyamukondiwa, Casper" sort="Nyamukondiwa, Casper" uniqKey="Nyamukondiwa C" first="Casper" last="Nyamukondiwa">Casper Nyamukondiwa</name><affiliation><nlm:aff id="af1-insects-11-00764">Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</nlm:aff></affiliation></author></analytic><series><title level="j">Insects</title><idno type="eISSN">2075-4450</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Simple Summary</title><p>The past decade has seen Africa being invaded by an invasive and destructive insect pest of tomato, the South American tomato pinworm. To date, the pest insect has since spread to almost the entire continent at lightning speed. Farmers have responded to this pest pressure through the sole injudicious use of chemical pesticides. However, this method of control is expensive, not effective (owing to reported insecticide resistance) and has potential adverse effects on the environment (including humans). To mitigate this, more environmentally friendly, bio-based and sustainable alternatives need to be put in place. Natural substances (NSs), for example, the use of pesticidal plant extracts, naturally occurring antagonists and related substances, can be used in this regard. A literature review was conducted explaining various factors that contributed to successful invasion by the pinworm. The review also explored various control mechanisms (e.g., biological control agents) that can be used in combination with natural and other low risk substances in a holistic way for successful pest control. Focus was also taken on the enabling and limiting factors that influence farmers in embracing the use of these NSs in an integrated approach.</p></sec><sec><title>Abstract</title><p>The South American tomato pinworm <italic>Tuta absoluta</italic> (Meyrick) has aggressively invaded the African continent. Since its first detection in North Africa in Morocco and Tunisia in 2008, it has successfully invaded the entire southern, eastern and western Africa, where it has been on the offensive, causing significant damage to Solanaceous food crops. While control of this prolific invader is primarily based on conventional synthetic pesticides, this form of control is consistently losing societal approval owing to (1) pesticide resistance development and consequential loss of field efficacy; (2) growing public health concerns; (3) environmental contamination and loss of biological diversity and its associated ecological services; and (4) unsustainable costs, particularly for resource-poor African farmers. As such, more ecologically sound pest management strategies, e.g., the use of natural substances (NSs), may offer a more sustainable approach to tackling this offensive. A systematic literature search through digital libraries and online databases (JSTOR, PubMed, Web of Science, SCOPUS and Google Scholar) was conducted using predetermined keywords on <italic>T. absoluta</italic>, e.g., South American tomato pinworm. We use this to explain the invasion of <italic>T. absoluta</italic> in Africa, citing mechanisms facilitating African invasion and exploring the potential of its control using diverse biological control agents, natural and low-risk substances. Specifically, we explore how botanicals, entomopathogens, semiochemicals, predators, parasitoids, host plant resistance, sterile insect technique and others have been spatially employed to control <italic>T. absoluta</italic> and discuss the potential of these control agents in African landscapes using more integrated approaches. We discuss the use of NSs as assets to general insect pest control, some potential associated liabilities and explain the potential use and barriers to adoption in African systems from a legislative, economic, ecological and social standpoint.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Olson, L J" uniqKey="Olson L">L.J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Insects</journal-id><journal-id journal-id-type="iso-abbrev">Insects</journal-id><journal-id journal-id-type="publisher-id">insects</journal-id><journal-title-group><journal-title>Insects</journal-title></journal-title-group><issn pub-type="epub">2075-4450</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">33171892</article-id><article-id pub-id-type="pmc">7694550</article-id><article-id pub-id-type="doi">10.3390/insects11110764</article-id><article-id pub-id-type="publisher-id">insects-11-00764</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title><italic>Tuta absoluta</italic> (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for Integrated Management Initiatives</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-9960-9945</contrib-id><name><surname>Tarusikirwa</surname><given-names>Vimbai L.</given-names></name><xref ref-type="aff" rid="af1-insects-11-00764">1</xref></contrib><contrib contrib-type="author"><name><surname>Machekano</surname><given-names>Honest</given-names></name><xref ref-type="aff" rid="af1-insects-11-00764">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-3978-8643</contrib-id><name><surname>Mutamiswa</surname><given-names>Reyard</given-names></name><xref ref-type="aff" rid="af2-insects-11-00764">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-4601-768X</contrib-id><name><surname>Chidawanyika</surname><given-names>Frank</given-names></name><xref ref-type="aff" rid="af2-insects-11-00764">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-0395-4980</contrib-id><name><surname>Nyamukondiwa</surname><given-names>Casper</given-names></name><xref ref-type="aff" rid="af1-insects-11-00764">1</xref><xref rid="c1-insects-11-00764" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-insects-11-00764"><label>1</label>Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana;<email>vimbai.tarusikirwa@studentmail.biust.ac.bw</email> (V.L.T.);<email>machekanoh@biust.ac.bw</email> (H.M.)</aff><aff id="af2-insects-11-00764"><label>2</label>Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa;<email>2018066841@ufs4life.ac.za</email> (R.M.);<email>ChidawanyikaF@ufs.ac.za</email> (F.C.)</aff><author-notes><corresp id="c1-insects-11-00764"><label>*</label>Correspondence: <email>nyamukondiwac@biust.ac.bw</email></corresp></author-notes><pub-date pub-type="epub"><day>06</day><month>11</month><year>2020</year></pub-date><pub-date pub-type="collection"><month>11</month><year>2020</year></pub-date><volume>11</volume><issue>11</issue><elocation-id>764</elocation-id><history><date date-type="received"><day>13</day><month>8</month><year>2020</year></date><date date-type="accepted"><day>16</day><month>9</month><year>2020</year></date></history><permissions><copyright-statement>© 2020 by the authors.</copyright-statement><copyright-year>2020</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><sec><title>Simple Summary</title><p>The past decade has seen Africa being invaded by an invasive and destructive insect pest of tomato, the South American tomato pinworm. To date, the pest insect has since spread to almost the entire continent at lightning speed. Farmers have responded to this pest pressure through the sole injudicious use of chemical pesticides. However, this method of control is expensive, not effective (owing to reported insecticide resistance) and has potential adverse effects on the environment (including humans). To mitigate this, more environmentally friendly, bio-based and sustainable alternatives need to be put in place. Natural substances (NSs), for example, the use of pesticidal plant extracts, naturally occurring antagonists and related substances, can be used in this regard. A literature review was conducted explaining various factors that contributed to successful invasion by the pinworm. The review also explored various control mechanisms (e.g., biological control agents) that can be used in combination with natural and other low risk substances in a holistic way for successful pest control. Focus was also taken on the enabling and limiting factors that influence farmers in embracing the use of these NSs in an integrated approach.</p></sec><sec><title>Abstract</title><p>The South American tomato pinworm <italic>Tuta absoluta</italic> (Meyrick) has aggressively invaded the African continent. Since its first detection in North Africa in Morocco and Tunisia in 2008, it has successfully invaded the entire southern, eastern and western Africa, where it has been on the offensive, causing significant damage to Solanaceous food crops. While control of this prolific invader is primarily based on conventional synthetic pesticides, this form of control is consistently losing societal approval owing to (1) pesticide resistance development and consequential loss of field efficacy; (2) growing public health concerns; (3) environmental contamination and loss of biological diversity and its associated ecological services; and (4) unsustainable costs, particularly for resource-poor African farmers. As such, more ecologically sound pest management strategies, e.g., the use of natural substances (NSs), may offer a more sustainable approach to tackling this offensive. A systematic literature search through digital libraries and online databases (JSTOR, PubMed, Web of Science, SCOPUS and Google Scholar) was conducted using predetermined keywords on <italic>T. absoluta</italic>, e.g., South American tomato pinworm. We use this to explain the invasion of <italic>T. absoluta</italic> in Africa, citing mechanisms facilitating African invasion and exploring the potential of its control using diverse biological control agents, natural and low-risk substances. Specifically, we explore how botanicals, entomopathogens, semiochemicals, predators, parasitoids, host plant resistance, sterile insect technique and others have been spatially employed to control <italic>T. absoluta</italic> and discuss the potential of these control agents in African landscapes using more integrated approaches. We discuss the use of NSs as assets to general insect pest control, some potential associated liabilities and explain the potential use and barriers to adoption in African systems from a legislative, economic, ecological and social standpoint.</p></sec></abstract><kwd-group><kwd>botanicals</kwd><kwd>invasive species</kwd><kwd>liabilities</kwd><kwd>pest management</kwd><kwd>tomato pinworm</kwd><kwd>natural substances</kwd></kwd-group></article-meta></front><body><sec sec-type="intro" id="sec1-insects-11-00764"><title>1. Introduction</title><p>Invasive insect pests are widely recognised as major threats to agricultural production, biodiversity conservation and the maintenance of ecological integrity [<xref rid="B1-insects-11-00764" ref-type="bibr">1</xref>,<xref rid="B2-insects-11-00764" ref-type="bibr">2</xref>,<xref rid="B3-insects-11-00764" ref-type="bibr">3</xref>]. Increased trade, human travel and globalisation have made crop production vulnerable to invasive alien insect pests [<xref rid="B4-insects-11-00764" ref-type="bibr">4</xref>,<xref rid="B5-insects-11-00764" ref-type="bibr">5</xref>,<xref rid="B6-insects-11-00764" ref-type="bibr">6</xref>]. In Africa, the rate of alien species invasion has dramatically increased in the past decades [<xref rid="B7-insects-11-00764" ref-type="bibr">7</xref>]. For example, “recent” invasive insect pest arrivals include <italic>Chilo partellus</italic> (Swinhoe) (Lepidoptera: Crambidae) [<xref rid="B8-insects-11-00764" ref-type="bibr">8</xref>], <italic>Prostephanus truncatus</italic> (Horn) (Coleoptera: Bostrichidae) [<xref rid="B9-insects-11-00764" ref-type="bibr">9</xref>], <italic>Phenacoccus manihoti</italic> Matile-Ferrero (Hemiptera: Pseudococcidae) [<xref rid="B10-insects-11-00764" ref-type="bibr">10</xref>], <italic>Bactrocera dorsalis</italic> (Hendel) (Diptera: Tephritidae) [<xref rid="B11-insects-11-00764" ref-type="bibr">11</xref>], <italic>Spodoptera frugiperda</italic> (JE Smith) (Lepidoptera: Noctuidae) [<xref rid="B12-insects-11-00764" ref-type="bibr">12</xref>] and indeed <italic>Tuta absoluta</italic> (Meyrick) (Lepidoptera: Gelechiidae) [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. Given that ~70–80% of African livelihoods depend on agriculture [<xref rid="B14-insects-11-00764" ref-type="bibr">14</xref>], these invasions represent a significant biosecurity as well as food and nutrition security threat.</p><p><italic>Tuta absoluta</italic>, commonly known as the South American tomato pinworm, is one of the most invasive destructive insect pests of tomato (<italic>Solanum lycopersicum</italic> (Solanaceae)) globally [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>,<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. It is thought to have originated from the Andes region in Peru before spreading to Latin American countries during the 1960s [<xref rid="B17-insects-11-00764" ref-type="bibr">17</xref>,<xref rid="B18-insects-11-00764" ref-type="bibr">18</xref>]. Although it is an endemic Neotropical insect pest whose initial distribution was restricted to its native range in South America, it has successfully extended its geographical range following an unintentional introduction in the Mediterranean basin [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B19-insects-11-00764" ref-type="bibr">19</xref>,<xref rid="B20-insects-11-00764" ref-type="bibr">20</xref>]. It acquired global pest status after detection in eastern Spain in late 2006 [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B21-insects-11-00764" ref-type="bibr">21</xref>], following introduction as a single initial Chilean population in the early 2000s [<xref rid="B22-insects-11-00764" ref-type="bibr">22</xref>]. Thereafter, it rapidly spread throughout Europe [<xref rid="B23-insects-11-00764" ref-type="bibr">23</xref>,<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>]. Since then, the pest has rapidly spread east- and southward, tracking favourable biophysical environments [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. During the last 10 years, <italic>T. absoluta</italic> has also spread in the Middle East and Asia at lightning speed, resulting in extensive naturalised populations in India, Iran, Israel, Syria, Turkey and Nepal [<xref rid="B25-insects-11-00764" ref-type="bibr">25</xref>,<xref rid="B26-insects-11-00764" ref-type="bibr">26</xref>,<xref rid="B27-insects-11-00764" ref-type="bibr">27</xref>,<xref rid="B28-insects-11-00764" ref-type="bibr">28</xref>,<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>]. Following its invasion in most European countries, <italic>T. absoluta</italic> successfully invaded the Afrotropics, reportedly via the Mediterranean Sea, with first detections reported in Tunisia, Algeria and Morocco in 2008–2009 [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B25-insects-11-00764" ref-type="bibr">25</xref>,<xref rid="B30-insects-11-00764" ref-type="bibr">30</xref>,<xref rid="B31-insects-11-00764" ref-type="bibr">31</xref>]. Since then, further detections have been reported in Niger, Nigeria (2010), Senegal (2012) [<xref rid="B32-insects-11-00764" ref-type="bibr">32</xref>], Sudan, Ethiopia (2011) [<xref rid="B32-insects-11-00764" ref-type="bibr">32</xref>], Kenya (2013) [<xref rid="B33-insects-11-00764" ref-type="bibr">33</xref>], Tanzania (2014) [<xref rid="B34-insects-11-00764" ref-type="bibr">34</xref>], Uganda (2015) [<xref rid="B33-insects-11-00764" ref-type="bibr">33</xref>], Zambia, Botswana, Mozambique, South Africa, Malawi (2016) [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>,<xref rid="B35-insects-11-00764" ref-type="bibr">35</xref>,<xref rid="B36-insects-11-00764" ref-type="bibr">36</xref>,<xref rid="B37-insects-11-00764" ref-type="bibr">37</xref>] and Angola (2017) [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>], thereby elevating its continental pest status. This rapid north–south and downward incursion between 2008 and 2017 poses a biosecurity threat to natural and agroecosystems in pest-free countries. On a global scale, this pest is believed to have increased from primarily infesting only 3% of the worldwide tomato cultivated areas to 60% within 10 years [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>], with the most recent in China, a major tomato growing country [<xref rid="B38-insects-11-00764" ref-type="bibr">38</xref>].</p><p>Underlying the invasion success of <italic>T. absoluta</italic> is its superior climate adaptation [<xref rid="B39-insects-11-00764" ref-type="bibr">39</xref>], polyphagous nature [<xref rid="B40-insects-11-00764" ref-type="bibr">40</xref>,<xref rid="B41-insects-11-00764" ref-type="bibr">41</xref>,<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>] and high biotic potential [<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>,<xref rid="B44-insects-11-00764" ref-type="bibr">44</xref>]. In response to <italic>T. absoluta</italic> infestations, chemical control is often used as the first line of defence [<xref rid="B18-insects-11-00764" ref-type="bibr">18</xref>,<xref rid="B45-insects-11-00764" ref-type="bibr">45</xref>], providing a quick fix to pest pressure. It is relatively easy to apply, readily available and may be cost effective when applied at a large scale. However, synthetic insecticides are expensive to many resource-constrained sub-Saharan African (SSA) farmers. The endophytic behavioural feeding and cryptic nature of <italic>T. absoluta</italic> larvae render the widely used contact insecticides ineffective [<xref rid="B46-insects-11-00764" ref-type="bibr">46</xref>,<xref rid="B47-insects-11-00764" ref-type="bibr">47</xref>,<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]. Moreover, synthetic insecticides also affect (i) non-target biological diversity and their related ecosystem services, e.g., natural enemies and pollinators, thus disrupting desirable trophic interactions; (ii) development of pest resurgence; (iii) insecticide resistance development; and (iv) public health, owing to residual insecticide contamination [<xref rid="B3-insects-11-00764" ref-type="bibr">3</xref>,<xref rid="B49-insects-11-00764" ref-type="bibr">49</xref>,<xref rid="B50-insects-11-00764" ref-type="bibr">50</xref>,<xref rid="B51-insects-11-00764" ref-type="bibr">51</xref>,<xref rid="B52-insects-11-00764" ref-type="bibr">52</xref>]. Some of these vices have already been observed in <italic>T. absoluta</italic> chemical control, e.g., insecticide resistance [<xref rid="B53-insects-11-00764" ref-type="bibr">53</xref>,<xref rid="B54-insects-11-00764" ref-type="bibr">54</xref>] and non-target effects on beneficial fauna [<xref rid="B55-insects-11-00764" ref-type="bibr">55</xref>]. The practical implications of the European Union Directive 2009/128/EC on the sustainable use of synthetic pesticides and the future prospects that residue restrictions may become more stringent also necessitate the exploration of novel, sustainable non-chemical alternatives for the management of <italic>T. absoluta</italic> [<xref rid="B56-insects-11-00764" ref-type="bibr">56</xref>]. As such, efficacious, ecologically sound and safer biologically based or natural alternatives are required for sustainable management of <italic>T. absoluta</italic> for use in an integrated approach. Natural insecticides/substances (NSs) are thus compatible as they are cost-effective and eco-friendly owing to their rapid environmental degradation [<xref rid="B57-insects-11-00764" ref-type="bibr">57</xref>,<xref rid="B58-insects-11-00764" ref-type="bibr">58</xref>]. However, studies on the NSs that are effective on <italic>T. absoluta</italic> are scattered in literature, warranting an in-depth comprehensive review of the current methods. This study, therefore, provides a comprehensive, gleaned compendium of potentially effective NSs on this invasive quarantine insect pest. The understanding of the role and potential of NSs in limiting <italic>T. absoluta</italic> economic damage is important in establishing a baseline for sustainable management options. NSs widely used in pest management include microbial (e.g., entomopathogens and entomopathogenic nematodes), botanical (e.g., insecticidal plants or their derivatives) and semiochemical agents [<xref rid="B59-insects-11-00764" ref-type="bibr">59</xref>,<xref rid="B60-insects-11-00764" ref-type="bibr">60</xref>,<xref rid="B61-insects-11-00764" ref-type="bibr">61</xref>,<xref rid="B62-insects-11-00764" ref-type="bibr">62</xref>,<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>]. Despite availability of multiple potential options, current organic tomato production systems mostly rely on <italic>Saccharopolyspora spinosa</italic> (spinosad), <italic>Azadirachta indica</italic> (neem) and <italic>Bacillus thuringiensis</italic> toxins [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B64-insects-11-00764" ref-type="bibr">64</xref>], signifying underutilisation of NSs. Moreover, identification and screening of effective locally available NSs remain scant in Africa [<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>,<xref rid="B65-insects-11-00764" ref-type="bibr">65</xref>,<xref rid="B66-insects-11-00764" ref-type="bibr">66</xref>]. Although NSs are environmentally friendly and have shown to be very effective in pest control, they have not been widely adopted by African farmers. Thus, this review also discusses <italic>T. absoluta</italic> invasion in Africa, possible mechanisms of invasion and the prospects of incorporating natural and low risk substances as assets in an integrated management approach. We also discuss barriers to the adoption and use of NSs in African agricultural systems from a legislative, economic, ecological and social standpoint.</p></sec><sec id="sec2-insects-11-00764"><title>2. Economic Impact of <italic>Tuta absoluta</italic> in Africa</title><p>Tomatoes are an important component of horticulture and a major pillar of sustainable development, with significant contribution to household and national food and nutritional security [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B67-insects-11-00764" ref-type="bibr">67</xref>]. They are a cash crop grown for home consumption in the backyards of the majority homesteads across SSA and are an important source of vitamins [<xref rid="B68-insects-11-00764" ref-type="bibr">68</xref>]. Tomato production also significantly contributes to economic development ascribed to its high economic returns and ability to create employment (~60% of total labour force) and along the value chain [<xref rid="B69-insects-11-00764" ref-type="bibr">69</xref>,<xref rid="B70-insects-11-00764" ref-type="bibr">70</xref>]. About 170 million tonnes of tomatoes are produced worldwide [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B71-insects-11-00764" ref-type="bibr">71</xref>]. Of this figure, Africa accounts for ~37.8 million tonnes annually. However, this figure is threatened by increased <italic>T. absoluta</italic> damage [<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>], with downstream consequences on African socio-economic value chains and household livelihoods [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>].</p><p><italic>Tuta absoluta</italic> larvae attack almost all aerial parts of tomato plants, resulting in ~80–100% yield losses if left uncontrolled [<xref rid="B73-insects-11-00764" ref-type="bibr">73</xref>]. Larval feeding also reduces fruit quality through creating pin holes prone to secondary attack by pathogens, rendering them unmarketable [<xref rid="B74-insects-11-00764" ref-type="bibr">74</xref>]. Increased cost of production has been reportedly experienced by small- and large-scale farmers in Africa due to increased costs for pesticides [<xref rid="B62-insects-11-00764" ref-type="bibr">62</xref>]. For example, recent evidence suggests decreased tomato yields and increased production costs [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>]. Highest losses are mostly experienced during early invasion owing to inadequate mitigation measures related to lack of preparedness [<xref rid="B18-insects-11-00764" ref-type="bibr">18</xref>]. Nigeria experienced up to 80% losses in tomato produce in 2016 due to unfamiliarity with the pest and management strategies [<xref rid="B70-insects-11-00764" ref-type="bibr">70</xref>]. This reduced supply and catapulted an estimated 10-fold increase in tomato prices due to the laws of demand and supply [<xref rid="B75-insects-11-00764" ref-type="bibr">75</xref>]. Similarly, following <italic>T. absoluta</italic> invasion in South Africa (2016), pest-free countries banned importation of tomato and other Solanaceae crops from that country [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>], resulting in significant economic losses. Similar losses have also been reported in Southwestern Angola [<xref rid="B76-insects-11-00764" ref-type="bibr">76</xref>]. Thus, <italic>T. absoluta</italic> pest pressure has negatively affected agricultural enterprises in Africa through direct losses and increased costs in pest management [<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>]. <italic>Tuta absoluta</italic> remains a pest of quarantine importance in countries under the Inter-African Phytosanitary Council (IAPSC) and has been reported on the European and Mediterranean Plant Protection Organization’s (EPPO’s) A2 list as a regulated insect pest [<xref rid="B77-insects-11-00764" ref-type="bibr">77</xref>].</p></sec><sec id="sec3-insects-11-00764"><title>3. <italic>Tuta absoluta</italic> Invasion Pathways and Distribution in Africa</title><p>Long-distance transmission and short-distance dispersal are the key drivers of <italic>T. absoluta</italic> invasion [<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>]. International agricultural trade is a key long-distance transmission mode that may have contributed to a larger extent in the introduction of <italic>T. absoluta</italic> into Africa, e.g., importation of fruits (e.g., tomatoes and egg plants) from pest-infested areas [<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>,<xref rid="B79-insects-11-00764" ref-type="bibr">79</xref>]. Other possible pathways for long-distance dissemination include production facilities and packaging materials (e.g., boxes, crates and pallets) from infested countries [<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>,<xref rid="B80-insects-11-00764" ref-type="bibr">80</xref>]. Hence, production facilities repack and distribute infested fruits, resulting in long-distance dissemination, reviewed in [<xref rid="B81-insects-11-00764" ref-type="bibr">81</xref>]. In addition, propagule material (e.g., seedlings), farm equipment and transportation vehicles from pest-infested areas are also possible pathways for long-distance transmission [<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>,<xref rid="B79-insects-11-00764" ref-type="bibr">79</xref>,<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]. From the foregoing, the rapid spread across Africa may have been exacerbated by porous port of entries, weak phytosanitary regulations and ineffective early surveillance in the region [<xref rid="B18-insects-11-00764" ref-type="bibr">18</xref>]. Furthermore, natural factors (e.g., wind and water), larval crawling and adult flight are possible key short-distance dispersal pathways [<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>]. To date, <italic>T. absoluta</italic> has been reported in 41 of the 54 African countries (see [<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>]). The pest has not yet been officially reported in a few central and southwestern African countries [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. However, cognisance of the widespread presence in Africa, this absence may be a consequence of lack of surveillance and pest detection mechanisms.</p></sec><sec id="sec4-insects-11-00764"><title>4. Factors Supporting <italic>T. absoluta</italic> Invasion in Africa</title><sec id="sec4dot1-insects-11-00764"><title>4.1. African Environments and Tuta absoluta Niche</title><p>Interactions between the invader and the recipient agro-ecological regions influence pest establishment and spread, with the prevailing biophysical environment contributing to the invasion process [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>,<xref rid="B83-insects-11-00764" ref-type="bibr">83</xref>,<xref rid="B84-insects-11-00764" ref-type="bibr">84</xref>]. Tropical regions, such as the majority of Africa, are highly vulnerable to insect pest invasions [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>,<xref rid="B85-insects-11-00764" ref-type="bibr">85</xref>,<xref rid="B86-insects-11-00764" ref-type="bibr">86</xref>]. Among the key determinants of invasion success are climatic suitability, propagule pressure and the availability of suitable hosts [<xref rid="B87-insects-11-00764" ref-type="bibr">87</xref>,<xref rid="B88-insects-11-00764" ref-type="bibr">88</xref>]. Environmental matches between native and novel invasion areas play a pivotal role in invasion success [<xref rid="B89-insects-11-00764" ref-type="bibr">89</xref>]. Modelling studies have shown that temperature, relative humidity (RH) and hosts are critical determinants of <italic>T. absoluta</italic> successful invasion [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>,<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>,<xref rid="B90-insects-11-00764" ref-type="bibr">90</xref>]. Research shows that Africa is a suitable biophysical niche for the pest [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>,<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>]. Various models have been constructed to predict environmental suitability, potential and timing of <italic>T. absoluta</italic> spread in Africa [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>,<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>,<xref rid="B90-insects-11-00764" ref-type="bibr">90</xref>]. Indeed, these models suggest temperature and RH environments for Africa are ideal for <italic>T. absoluta</italic> invasion and population establishment. However, it appears RH seems to have the strongest influence in <italic>T. absoluta</italic> invasion [<xref rid="B24-insects-11-00764" ref-type="bibr">24</xref>]. A comparison of temperature and precipitation between its native range and invaded African region shows a similarity in temperature ranges. However, the native range experiences higher precipitation as compared to the areas invaded in Africa (<xref ref-type="fig" rid="insects-11-00764-f001">Figure 1</xref>). Nevertheless, reports suggest <italic>T. absoluta</italic> can thrive in high temperature and low precipitation environments as long as host plants are available [<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>]. The optimal temperature for its development is 30 °C, with egg, larval and pupal lower developmental thresholds at 6.9, 7.6 and 9.2 °C, respectively [<xref rid="B91-insects-11-00764" ref-type="bibr">91</xref>,<xref rid="B92-insects-11-00764" ref-type="bibr">92</xref>]. In addition, the upper developmental threshold from the egg to adult cycle is 37.3 °C [<xref rid="B93-insects-11-00764" ref-type="bibr">93</xref>]. Low temperature and high altitudes (>1000 m) are limiting factors for its survival, and a high RH is suitable for its development and life span [<xref rid="B43-insects-11-00764" ref-type="bibr">43</xref>,<xref rid="B94-insects-11-00764" ref-type="bibr">94</xref>,<xref rid="B95-insects-11-00764" ref-type="bibr">95</xref>]. The negative impact of rainfall on population abundance of <italic>T. absoluta</italic> has been reported [<xref rid="B96-insects-11-00764" ref-type="bibr">96</xref>]. Based on these ecological requirements and evidence presented in Machekano et al. [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>], warm and humid conditions prevalent in Africa potentially elucidate its invasion success.</p></sec><sec id="sec4dot2-insects-11-00764"><title>4.2. Physiological Tolerance</title><p>Environmental adaptations enable invasive species to overcome variable stressful barriers along the invasion continuum and significantly contribute to alien species propensity [<xref rid="B97-insects-11-00764" ref-type="bibr">97</xref>,<xref rid="B98-insects-11-00764" ref-type="bibr">98</xref>,<xref rid="B99-insects-11-00764" ref-type="bibr">99</xref>]. Overcoming different stressful environmental barriers is the first of several potential factors determining whether a species may become established, naturalised and ultimately invasive [<xref rid="B83-insects-11-00764" ref-type="bibr">83</xref>]. Temperature is the key abiotic “ecological filter” [<xref rid="B100-insects-11-00764" ref-type="bibr">100</xref>] for successful invasion in novel habitats [<xref rid="B101-insects-11-00764" ref-type="bibr">101</xref>]. As such, failure to mount any compensatory physiological resistance mechanisms against environmental barriers may offset invasion success [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B102-insects-11-00764" ref-type="bibr">102</xref>]. Physiologically, some insect pests often increase invasion success through employing either increased phenotypic plasticity or basal stress tolerance [<xref rid="B39-insects-11-00764" ref-type="bibr">39</xref>,<xref rid="B98-insects-11-00764" ref-type="bibr">98</xref>,<xref rid="B99-insects-11-00764" ref-type="bibr">99</xref>,<xref rid="B103-insects-11-00764" ref-type="bibr">103</xref>]. A previous study has shown that <italic>T. absoluta</italic> larvae are more thermally plastic than adults and can shift their thermal tolerance in short and long timescales [<xref rid="B39-insects-11-00764" ref-type="bibr">39</xref>]. In addition, larvae showed a higher basal heat tolerance than adults, whereas adults recorded superior basal cold tolerance relative to larvae [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B104-insects-11-00764" ref-type="bibr">104</xref>]. This physiological tolerance may help elucidate the notion that ecophysiology may have aided the current invasion by <italic>T. absoluta</italic>.</p></sec><sec id="sec4dot3-insects-11-00764"><title>4.3. Increased Number of Generations</title><p><italic>Tuta absoluta</italic> is an r-selected, multivoltine species [<xref rid="B105-insects-11-00764" ref-type="bibr">105</xref>] that remains active in Mediterranean and African winter climates [<xref rid="B104-insects-11-00764" ref-type="bibr">104</xref>,<xref rid="B106-insects-11-00764" ref-type="bibr">106</xref>,<xref rid="B107-insects-11-00764" ref-type="bibr">107</xref>]. Its pest status is largely associated with a high rate of reproduction, with each female producing up to 260 eggs during its lifetime [<xref rid="B108-insects-11-00764" ref-type="bibr">108</xref>]. Under the projected warming in Africa [<xref rid="B109-insects-11-00764" ref-type="bibr">109</xref>], this promotes an even shorter developmental time and higher voltinism. The life cycle of <italic>T. absoluta</italic> takes ~24–38 days at 27 °C, resulting in ~10 to 13 generations per year [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B91-insects-11-00764" ref-type="bibr">91</xref>,<xref rid="B106-insects-11-00764" ref-type="bibr">106</xref>]. This rapid development may give <italic>T. absoluta</italic> a numerical advantage and propagule material that facilitates species proliferation.</p></sec><sec id="sec4dot4-insects-11-00764"><title>4.4. New Niche with Limited Natural Enemies</title><p>The enemy release hypothesis postulates that invasive species likely have reduced biotic pressure (e.g., natural enemies) than their native counterparts [<xref rid="B110-insects-11-00764" ref-type="bibr">110</xref>]. It also follows that parasitoids and predators (see [<xref rid="B111-insects-11-00764" ref-type="bibr">111</xref>,<xref rid="B112-insects-11-00764" ref-type="bibr">112</xref>]) specific to the invasive species may be absent in the novel areas, resulting in the pest not being suppressed [<xref rid="B113-insects-11-00764" ref-type="bibr">113</xref>] owing to a lack of co-evolved biological control agents following invasion [<xref rid="B114-insects-11-00764" ref-type="bibr">114</xref>]. This is likely the reason behind the limited natural biotic pressure on <italic>T. absoluta</italic> in Africa, consequently contributing to its quick establishment [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>]. The enemy-free hypothesis also states that invading species often perform better and experience rapid population growth in new areas [<xref rid="B115-insects-11-00764" ref-type="bibr">115</xref>,<xref rid="B116-insects-11-00764" ref-type="bibr">116</xref>,<xref rid="B117-insects-11-00764" ref-type="bibr">117</xref>]. This is because in the new habitats, invading species may at most encounter opportunistic generalist natural enemies in their new range, but not more efficacious coevolved specialists [<xref rid="B113-insects-11-00764" ref-type="bibr">113</xref>,<xref rid="B116-insects-11-00764" ref-type="bibr">116</xref>,<xref rid="B117-insects-11-00764" ref-type="bibr">117</xref>,<xref rid="B118-insects-11-00764" ref-type="bibr">118</xref>]. Indeed, various indigenous generalist predators and parasitoids have been recorded as potential biological agents of <italic>T. absoluta</italic> in some parts of Africa, albeit with low efficacy [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. However, these studies remain scant and constrained in space [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>]. Various authors have reviewed the natural enemy complex of <italic>T. absoluta</italic> [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>,<xref rid="B120-insects-11-00764" ref-type="bibr">120</xref>]. Amongst these species, a few have been recorded in Africa. The few documented in the continent are mostly prevalent in North Africa [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. The generalist mirid predator <italic>Nesidiocoris tenuis</italic> (Reuter) (Hemiptera: Miridae) has been the most reported, albeit also confined to North Africa [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>,<xref rid="B121-insects-11-00764" ref-type="bibr">121</xref>]. Other predators recorded include <italic>Macrolophus pygmaeus</italic>, (Rambur) (Hemiptera: Miridae), <italic>Macrolophus caliginosus</italic> (Wagner) (Heteroptera: Miridae), <italic>Dicyphus tamaninii</italic> (Wagner) (Heteroptera: Miridae), <italic>Rhynocoris segmentarius</italic> (Germar) (Hemiptera: Reduvidae) and <italic>Dicyphus errans</italic> (Wolff) (Hemiptera: Miridae) [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. In Africa, the parasitoid complex that has so far been recorded through field monitoring and surveys include larval braconid parasitoids of the genus <italic>Apanteles</italic> and <italic>Bracon</italic> in Nigeria; egg parasitoids of the genus <italic>Trichogramma</italic> in Nigeria, Tunisia, Algeria and Morocco [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>,<xref rid="B122-insects-11-00764" ref-type="bibr">122</xref>]; and several hymenopterous parasitoid species belonging to different families (Kenya), including <italic>B. nigricans</italic>, <italic>B. hebetor</italic>, <italic>Dolichogenidea appellatory</italic> (Telenga) (Hymenoptera: Braconidae), <italic>Ecdamua cadenat</italic> (Risbec) (Hymenoptera: Torymidae) and <italic>Neochrysocharis formosa</italic> (Westwood) (Hymenoptera: Eulophidae) in Sudan [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. However, reports suggest these parasitoids cannot solely provide effective <italic>T. absoluta</italic> control [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. Thus, use of other complementary NSs combined in an integrated approach may improve efficacy and sustainability in <italic>T. absoluta</italic> management (<xref ref-type="fig" rid="insects-11-00764-f002">Figure 2</xref>). To our knowledge, no egg parasitoids have been recorded in southern Africa. Thus, the inefficiency by current spatially isolated indigenous natural enemies coupled with total absence in some regions [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>] has provided an enemy-free platform for <italic>T. absoluta</italic> successful invasion and establishment.</p></sec><sec id="sec4dot5-insects-11-00764"><title>4.5. Wide Host Range</title><p><italic>Tuta absoluta</italic> is polyphagous, exploiting a wide range of alternate hosts [<xref rid="B123-insects-11-00764" ref-type="bibr">123</xref>,<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]. This behaviour allows the continuous and spatial omnipresence of the pest. Although Özgökçe et al. [<xref rid="B41-insects-11-00764" ref-type="bibr">41</xref>] reported 26 different host plant species for <italic>T. absoluta</italic>, it has a strong preference for solanaceous species, with tomato, potato (<italic>Solanum tuberosum</italic>) and European black nightshade (<italic>Solanum nigrum</italic>) being the most preferred [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B125-insects-11-00764" ref-type="bibr">125</xref>]. In addition, it can also oviposit and develop on several plants belonging to the Amaranthaceae, Convolvulaceae, Fabaceae and Malvaceae [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. Since <italic>T. absoluta</italic> is rapidly and continually evolving, evidence suggest it is also expanding its host range [<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]. For example, in Sudan, <italic>T. absoluta</italic> was recorded on watermelon (<italic>Citrullus lanatus</italic>) and alfalfa (<italic>Medigo sativa</italic>) [<xref rid="B40-insects-11-00764" ref-type="bibr">40</xref>] and on weeds such as thorn apple <italic>Datura stramonium</italic> [<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]. In Algeria, Drouai et al. [<xref rid="B126-insects-11-00764" ref-type="bibr">126</xref>] found <italic>T. absoluta</italic> on beet (<italic>Beta vulgaris</italic>), spinach (<italic>Spinacia oleracea</italic>) as well as the weed species <italic>Chenopodium bonushenricus</italic> and <italic>C. rubrum</italic>. In South Sudan up to 50% of the <italic>T. absoluta</italic> damage was observed on potato foliage [<xref rid="B30-insects-11-00764" ref-type="bibr">30</xref>]. In Botswana, <italic>T. absoluta</italic> was spotted on some wild hosts, <italic>Solanum aculeatissimum</italic> (Jacq.), <italic>Solanum coccineum</italic> (Jacq.) and <italic>Solanum supinum</italic> [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>]. Apart from the main solanaceous plant hosts, <italic>T. absoluta</italic> affects other crops of economic importance (<xref rid="insects-11-00764-t001" ref-type="table">Table 1</xref>). The availability of alternative host plants is an important factor that allows the sustainability of the pest in the absence of the primary tomato host [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B127-insects-11-00764" ref-type="bibr">127</xref>]. Therefore, the presence of a wide range of both cultivated and wild host plants in African landscapes creates a refuge opportunity for host switching and consequent pest success.</p></sec><sec id="sec4dot6-insects-11-00764"><title>4.6. Pesticide Resistance</title><p>Synthetic insecticides are employed as the primary method of control against insect pest infestation [<xref rid="B2-insects-11-00764" ref-type="bibr">2</xref>,<xref rid="B137-insects-11-00764" ref-type="bibr">137</xref>]. For example, Tunisia registered 18 new insecticides during 2009–2011 following <italic>T. absoluta</italic> invasion although they all turned out ineffective [<xref rid="B25-insects-11-00764" ref-type="bibr">25</xref>,<xref rid="B138-insects-11-00764" ref-type="bibr">138</xref>]. Intensive use of synthetic insecticides for <italic>T. absoluta</italic> management coupled with insect biological traits, such as a high reproductive potential and multivoltinism, endophytic larval feeding behaviour and mining habit as well as polyphagy, has increased <italic>T. absoluta</italic> selection pressure for insecticide resistance [<xref rid="B53-insects-11-00764" ref-type="bibr">53</xref>,<xref rid="B139-insects-11-00764" ref-type="bibr">139</xref>,<xref rid="B140-insects-11-00764" ref-type="bibr">140</xref>]. In South America and Europe, resistance has been reported against conventional insecticides such as organophosphates (OPs), pyrethroids, cartap, diamides and avermectins [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B46-insects-11-00764" ref-type="bibr">46</xref>,<xref rid="B139-insects-11-00764" ref-type="bibr">139</xref>,<xref rid="B141-insects-11-00764" ref-type="bibr">141</xref>,<xref rid="B142-insects-11-00764" ref-type="bibr">142</xref>]. The main resistance mechanisms evolved through altered target-site sensitivity and/or enhanced detoxification, depending on the chemical class [<xref rid="B64-insects-11-00764" ref-type="bibr">64</xref>]. In northern Nigeria, resistance was reported in cyhalothrin (a Type II pyrethroid), propoxur and chlorpyrifos-methyl via enzyme mutation, underlying the challenges in managing this invasive pest using pesticides [<xref rid="B70-insects-11-00764" ref-type="bibr">70</xref>]. Given the prohibitive costs of synthetic pesticides for African farmers, evolution of pesticide resistance will further compound losses on already resource-constrained farmers.</p></sec></sec><sec id="sec5-insects-11-00764"><title>5. Potential Use of Natural Substances</title><sec id="sec5dot1-insects-11-00764"><title>5.1. Botanicals</title><p>Botanical insecticides are naturally occurring chemicals extracted from plants with insecticidal properties [<xref rid="B61-insects-11-00764" ref-type="bibr">61</xref>,<xref rid="B143-insects-11-00764" ref-type="bibr">143</xref>]. They can be classified based on their chemical constituents into categories, namely, essential oils, flavonoids, alkaloids, glycosides, esters and fatty acids [<xref rid="B144-insects-11-00764" ref-type="bibr">144</xref>,<xref rid="B145-insects-11-00764" ref-type="bibr">145</xref>,<xref rid="B146-insects-11-00764" ref-type="bibr">146</xref>,<xref rid="B147-insects-11-00764" ref-type="bibr">147</xref>,<xref rid="B148-insects-11-00764" ref-type="bibr">148</xref>]. Plant derivatives and bioactive compounds have been used to manage different crop pests with notable success [<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>]. Their physiological effects on insects vary depending on the target site and mode of action [<xref rid="B61-insects-11-00764" ref-type="bibr">61</xref>], with most acting as repellents, feeding deterrents/antifeedants, toxicants, growth retardants, chemosterilants and attractants [<xref rid="B61-insects-11-00764" ref-type="bibr">61</xref>,<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>,<xref rid="B149-insects-11-00764" ref-type="bibr">149</xref>]. Plant parts used are dependent on the targeted bioactive compounds as well as their localised concentrations. However, use of barks, leaves, roots, flowers, seeds and stems is widely reported [<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>]. Common botanicals with reported insecticidal properties include neem (<italic>A. indica</italic>), garlic (<italic>Allium sativum</italic>), ginger (<italic>Zingiber officinale</italic>) and pyrethrum (<italic>Tanacetum cinerariifolium</italic>) [<xref rid="B63-insects-11-00764" ref-type="bibr">63</xref>,<xref rid="B143-insects-11-00764" ref-type="bibr">143</xref>].</p><p>Given the wide availability of botanicals, ease of application and low operational costs, botanicals are a viable option for sustainable <italic>T. absoluta</italic> management. <italic>Azadirachta indica</italic> and <italic>Jatropha curcas</italic> extracts have been reported as efficacious on <italic>T. absoluta</italic> eggs and larvae [<xref rid="B150-insects-11-00764" ref-type="bibr">150</xref>]. In an empirical study, four-day exposure to <italic>J. caurcas</italic> and <italic>A. indica</italic> seed extracts resulted in 18% and 25% egg mortalities, respectively, whilst 24-h treatment elicited larval mortalities ranging from 23.5 to 48.5% and 33 to 46.7%, respectively. In another study, Abdel-baky and Al-Soqueer [<xref rid="B151-insects-11-00764" ref-type="bibr">151</xref>] showed that simmondsin extracts, obtained from seeds of Jojoba, <italic>Simmondsia chinensis</italic> L., were effective in controlling 2nd instar larvae of <italic>T. absoluta</italic>. Field studies showed 71.82 and 74.26% larval mortalities following treatment using the biopesticides <italic>A. sativum</italic> and <italic>A. indica</italic>, respectively [<xref rid="B152-insects-11-00764" ref-type="bibr">152</xref>]. Furthermore, ethanolic leaf extracts of <italic>Piper amalago</italic> var. <italic>medium</italic>, <italic>P. glabratum</italic> and <italic>P. mikanianum</italic> significantly elicited <italic>T. absoluta</italic> larval mortalities [<xref rid="B153-insects-11-00764" ref-type="bibr">153</xref>]. <italic>Piper</italic> species have amides (e.g., piperamides) that are known to have neurotoxic and lipid metabolism effects [<xref rid="B154-insects-11-00764" ref-type="bibr">154</xref>], manifesting as knockdown and paralysis followed by death [<xref rid="B155-insects-11-00764" ref-type="bibr">155</xref>]. Several other plant extracts have been found to be effective against <italic>T. absoluta</italic> (<xref rid="insects-11-00764-t002" ref-type="table">Table 2</xref>). Given the efficacy of some of the reported botanicals, e.g., [<xref rid="B151-insects-11-00764" ref-type="bibr">151</xref>] (<xref rid="insects-11-00764-t002" ref-type="table">Table 2</xref>), using them in combination with soft pesticides and in an integrated approach could provide more optimised control. However, despite empirical support for the botanicals’ efficacy, their use in agriculture is currently limited in commercial use on vegetable and fruit crops with few prospects for commercial development of new products [<xref rid="B143-insects-11-00764" ref-type="bibr">143</xref>]. Several factors affect the wide success of botanicals as conventional pesticides; for example, availability of plant material, solvent types, rapid environmental degradation, registration bureaucracy, market opportunities and availability of competing products are some of the barriers to successful use of botanical insecticides [<xref rid="B143-insects-11-00764" ref-type="bibr">143</xref>].</p></sec><sec id="sec5dot2-insects-11-00764"><title>5.2. Entomopathogens</title><p>Entomopathogens, such as <italic>Metarhizium anisopliae</italic> var. <italic>anisopliae</italic> (Metsch.) Soroki, <italic>Beauveria bassiana</italic> (Balsamo) Vuillemin and <italic>Bacillus thuringiensis</italic> (Berliner) have shown efficacy against <italic>T. absoluta</italic> (<xref rid="insects-11-00764-t003" ref-type="table">Table 3</xref>) [<xref rid="B159-insects-11-00764" ref-type="bibr">159</xref>,<xref rid="B160-insects-11-00764" ref-type="bibr">160</xref>]. The soil dwelling bacterium <italic>B. thuringiensis</italic> is one of the most important microorganisms with entomopathogenic properties [<xref rid="B161-insects-11-00764" ref-type="bibr">161</xref>]. It is environmentally friendly and can be extensively used as part of an integrated approach to pest management [<xref rid="B81-insects-11-00764" ref-type="bibr">81</xref>]. Apart from Lepidoptera, <italic>B. thuringiensis</italic> was reported to exhibit insecticidal effects on many other insect orders [<xref rid="B161-insects-11-00764" ref-type="bibr">161</xref>], making it ideal for sustainable integrated management. Indeed, both <italic>B. bassiana</italic> and <italic>B. thuringiensis</italic> have been used to control an array of pest insects, including whiteflies, thrips and termites [<xref rid="B162-insects-11-00764" ref-type="bibr">162</xref>,<xref rid="B163-insects-11-00764" ref-type="bibr">163</xref>]. <italic>Bacillus thuringiensis</italic> has already been widely used in <italic>T. absoluta</italic> control [<xref rid="B160-insects-11-00764" ref-type="bibr">160</xref>,<xref rid="B161-insects-11-00764" ref-type="bibr">161</xref>]. Efficacy studies of <italic>B. bassiana</italic> and <italic>B. thuringiensis</italic> on <italic>T. absoluta</italic> showed that third instar larvae were most susceptible [<xref rid="B60-insects-11-00764" ref-type="bibr">60</xref>]. Furthermore, their interaction effects were synergistic in <italic>T. absoluta</italic> control. By contrast, Gonzalez-Cabrera et al. [<xref rid="B160-insects-11-00764" ref-type="bibr">160</xref>] found evidence that first instar larvae were the most susceptible to <italic>B. thuringiensis</italic> and that it could keep <italic>T. absoluta</italic> below economic thresholds [<xref rid="B164-insects-11-00764" ref-type="bibr">164</xref>]. Similarly, Biondi et al. [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>], reported that <italic>Wolbachia</italic> bacterial infection may potentially be efficacious for <italic>T. absoluta</italic> through its effects on reproduction. Spinosad, a fermentation product of <italic>S. spinosa</italic>, has also been used in <italic>T. absoluta</italic> control [<xref rid="B165-insects-11-00764" ref-type="bibr">165</xref>,<xref rid="B166-insects-11-00764" ref-type="bibr">166</xref>,<xref rid="B167-insects-11-00764" ref-type="bibr">167</xref>]. However, its continued use has been threatened by resistance [<xref rid="B168-insects-11-00764" ref-type="bibr">168</xref>]. Thus, there is need for complementary control options to fight <italic>T. absoluta</italic>, if pest populations are to be maintained below economic threshold levels [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. Regardless of sporadic resistance reports for these substances, they still remain reliable and efficacious sustainable options to pest control in integrated systems.</p></sec><sec id="sec5dot3-insects-11-00764"><title>5.3. Entomopathogenic Nematodes (EPNs)</title><p>Entomopathogenic nematodes (EPNs) (<xref rid="insects-11-00764-t003" ref-type="table">Table 3</xref>) are biological control agents that can kill insect pests using their coevolved mutualistic intestinal bacterium [<xref rid="B174-insects-11-00764" ref-type="bibr">174</xref>,<xref rid="B175-insects-11-00764" ref-type="bibr">175</xref>,<xref rid="B176-insects-11-00764" ref-type="bibr">176</xref>]. Their use in pest management is already widespread and have shown efficacy in diverse taxa [<xref rid="B177-insects-11-00764" ref-type="bibr">177</xref>]. Entomopathogenic nematodes have been used against similar Lepidopterans, e.g., false codling moth (<italic>Thaumatotibia leucotreta</italic>), codling moth (<italic>Cydia pomonella</italic>) and the sugarcane borer (<italic>Eldana saccharina</italic>) [<xref rid="B176-insects-11-00764" ref-type="bibr">176</xref>,<xref rid="B178-insects-11-00764" ref-type="bibr">178</xref>,<xref rid="B179-insects-11-00764" ref-type="bibr">179</xref>]. Recent studies have shown the EPNs <italic>Steinernema feltiae</italic>, <italic>S. carpocapsae</italic> and <italic>Heterorhabditis bacteriophora</italic> are effective against all larval instars of <italic>T. absoluta</italic> (<xref rid="insects-11-00764-t003" ref-type="table">Table 3</xref>) [<xref rid="B177-insects-11-00764" ref-type="bibr">177</xref>]. Similarly, Kamali et al. [<xref rid="B62-insects-11-00764" ref-type="bibr">62</xref>] reported high efficacy for <italic>S</italic>. <italic>carpocapsae</italic> and <italic>H. bacteriophora</italic> against fourth instar larvae. These results suggest scope for EPNs in <italic>T. absoluta</italic> management and can be an intergap component of an integrated management approach.</p></sec><sec id="sec5dot4-insects-11-00764"><title>5.4. Semiochemicals</title><p>Semiochemicals are chemicals mediating interactions across organisms by eliciting behavioural responses in recipient organisms within and across species. Sex pheromones have been, by far, the most widely used semiochemicals in pest management [<xref rid="B59-insects-11-00764" ref-type="bibr">59</xref>]. Semiochemical-based management of insects usually include pheromone lure and kill, mass trapping and disruption of mating activities [<xref rid="B47-insects-11-00764" ref-type="bibr">47</xref>,<xref rid="B180-insects-11-00764" ref-type="bibr">180</xref>]. Pheromones can also be effectively utilised in population monitoring to determine action thresholds, early pest detection and other manipulations of insect pest behaviour [<xref rid="B181-insects-11-00764" ref-type="bibr">181</xref>]. This form of control has been successfully implemented in South America, Europe, Asia and Africa in managing <italic>T. absoluta</italic> in greenhouses and open fields [<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>,<xref rid="B81-insects-11-00764" ref-type="bibr">81</xref>]. Using sex pheromones, Filho et al. [<xref rid="B182-insects-11-00764" ref-type="bibr">182</xref>] recorded 233 males/trap/day under greenhouse conditions. These trap catches can be used as part of a mass trapping <italic>T. absoluta</italic> control strategy. Pheromone-mediated control of <italic>T. absoluta</italic> is more recommended as a supplementary measure in combination with other management options. For example, a study in Egypt showed that a combined use of sex pheromone and other insecticides is effective against <italic>T. absoluta</italic> larvae [<xref rid="B183-insects-11-00764" ref-type="bibr">183</xref>]. Similarly, Cherif et al. [<xref rid="B184-insects-11-00764" ref-type="bibr">184</xref>] showed that mass trapping in combination with <italic>B. thuringiensis</italic> and cyromazin significantly reduced <italic>T. absoluta</italic> numbers. Other behaviour-modifying strategies, e.g., the push–pull strategies, have worked successfully for the management of other Lepidopteran pest insects [<xref rid="B185-insects-11-00764" ref-type="bibr">185</xref>]. However, to our knowledge, empirical studies showing the efficacy of a push–pull strategy in <italic>T. absoluta</italic> control in Africa is missing. Moreover, the use of a pheromone-mediated management system in Africa is also low due to high costs and limited availability. Nevertheless, semiochemicals represent an efficacious and sustainable approach to pest management.</p></sec><sec id="sec5dot5-insects-11-00764"><title>5.5. Sterile Insect Technique (SIT)</title><p>Sterile insect technique is an environmentally friendly control option aiming to suppress pest populations through F<sub>1</sub> generation sterility enabled by release of sterile males that mate with wild females [<xref rid="B186-insects-11-00764" ref-type="bibr">186</xref>], thereby producing non-viable offspring [<xref rid="B186-insects-11-00764" ref-type="bibr">186</xref>,<xref rid="B187-insects-11-00764" ref-type="bibr">187</xref>,<xref rid="B188-insects-11-00764" ref-type="bibr">188</xref>]. However, male sterilisation can reduce fitness thereby compromising field competitiveness [<xref rid="B189-insects-11-00764" ref-type="bibr">189</xref>]. As such, various mechanisms have been put in place to compensate for this reduced fitness and maintain optimal SIT efficacy in the field, including the use of low dosage gamma radiation and thermal preconditioning/acclimation [<xref rid="B186-insects-11-00764" ref-type="bibr">186</xref>,<xref rid="B190-insects-11-00764" ref-type="bibr">190</xref>].</p><p>Sterile insect technique has been used successfully for control of Lepidopterans, e.g., pink bollworm, <italic>Pectinophora gossypiella</italic> (Saunders) (Lepidoptera: Gelechiidae) [<xref rid="B191-insects-11-00764" ref-type="bibr">191</xref>]; false codling moth, <italic>T. leucotreta</italic> (Lepidoptera: Tortricidae) [<xref rid="B192-insects-11-00764" ref-type="bibr">192</xref>]; and codling moth, <italic>C. pomonella</italic> (Lepidoptera: Tortricidae) [<xref rid="B193-insects-11-00764" ref-type="bibr">193</xref>]. The technique can be used in an area-wide management approach, incorporating other options such as natural enemies, cultural control and the application of bio-rational pesticides [<xref rid="B194-insects-11-00764" ref-type="bibr">194</xref>,<xref rid="B195-insects-11-00764" ref-type="bibr">195</xref>]. Cagnotti et al. [<xref rid="B191-insects-11-00764" ref-type="bibr">191</xref>] reported that the inherited sterility control of <italic>T. absoluta</italic> can be combined with the use of the predator <italic>Tupiocoris cucurbitaceus</italic> in pest management. Given the efficacy of SIT in pest management, its environmental soundness coupled with a high compatibility with other control measures, SIT warrants exploration for use in <italic>T. absoluta</italic> management in Africa.</p></sec><sec id="sec5dot6-insects-11-00764"><title>5.6. Host Plant Resistance</title><p>Development of tomato cultivars resistant to pests is an important strategy in pest control using NSs and is one of the fundamental pillars of an integrated management approach [<xref rid="B196-insects-11-00764" ref-type="bibr">196</xref>]. While few moderately resistant tomato cultivars have been reported [<xref rid="B197-insects-11-00764" ref-type="bibr">197</xref>,<xref rid="B198-insects-11-00764" ref-type="bibr">198</xref>], the majority are highly susceptible to <italic>T. absoluta</italic> infestation. Three mechanisms may account for plant resistance to insect attack, namely antixenosis, antibiosis and tolerance [<xref rid="B199-insects-11-00764" ref-type="bibr">199</xref>]. Thus, tomato cultivars significantly differ in their susceptibility to <italic>T. absoluta</italic> [<xref rid="B200-insects-11-00764" ref-type="bibr">200</xref>,<xref rid="B201-insects-11-00764" ref-type="bibr">201</xref>,<xref rid="B202-insects-11-00764" ref-type="bibr">202</xref>,<xref rid="B203-insects-11-00764" ref-type="bibr">203</xref>], and that resistance is positively associated with trichomes density and the diversity and concentrations of host secondary metabolites [<xref rid="B201-insects-11-00764" ref-type="bibr">201</xref>,<xref rid="B202-insects-11-00764" ref-type="bibr">202</xref>,<xref rid="B204-insects-11-00764" ref-type="bibr">204</xref>]. Indeed, tomato plants possess glandular trichomes that produce volatile and non-volatile secondary metabolites, e.g., acyl sugars, terpenoids, phenylpropanoids, flavonoids and phenolic compounds [<xref rid="B200-insects-11-00764" ref-type="bibr">200</xref>,<xref rid="B205-insects-11-00764" ref-type="bibr">205</xref>]. Therefore, breeding programmes have targeted lines with high acyl sugars and other secondary metabolites, e.g., zingiberene for host resistance against pests in tomato production [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B136-insects-11-00764" ref-type="bibr">136</xref>]. Use of resistant varieties may also offer a cost effective and sustainable approach to the fight against the <italic>T. absoluta</italic> scourge in Africa.</p></sec><sec id="sec5dot7-insects-11-00764"><title>5.7. Use of Predators and Parasitoids</title><p>Several predators and parasitoid biological control agents have been demonstrated to suppress populations of the tomato pinworm below economic threshold levels (<xref rid="insects-11-00764-t004" ref-type="table">Table 4</xref>). Conservation and augmentative biological control programmes using predators and parasitoids have been developed for <italic>T. absoluta</italic> following its invasion in Europe [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>] and Africa [<xref rid="B31-insects-11-00764" ref-type="bibr">31</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>,<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>,<xref rid="B207-insects-11-00764" ref-type="bibr">207</xref>]. Hemipteran predators, notably anthocorids, geocorids, mirids, nabids and pentatomids, have been identified as <italic>T. absoluta</italic> biocontrol agents in both native and invaded areas [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. The generalist predators <italic>M. pygmaeus</italic>, <italic>N. tenuis</italic> and <italic>Dicyphus</italic> spp. [<xref rid="B208-insects-11-00764" ref-type="bibr">208</xref>] are the most common antagonists in European greenhouses [<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]. Their use has been complemented with <italic>B. thuringiensis</italic> sprays against the early larval infestations [<xref rid="B209-insects-11-00764" ref-type="bibr">209</xref>]. Adults and nymphs of <italic>M. pygmaeus</italic> and <italic>N. tenuis</italic> prey on <italic>T. absoluta</italic> eggs and larvae (preferably first instar) [<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>,<xref rid="B210-insects-11-00764" ref-type="bibr">210</xref>]. <italic>Dicyphus tamaninii</italic> has been reported as a predator of <italic>T. absoluta</italic> eggs and larvae in North Africa [<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>]. Other predators reported in Africa include <italic>N. tenuis</italic>, <italic>M. pygmaeus</italic>, <italic>M. caliginosus</italic>, <italic>D. tamaninii</italic>, <italic>R. segmentarius</italic> and <italic>D. errans</italic> [<xref rid="B13-insects-11-00764" ref-type="bibr">13</xref>]. In Spain, predatory lacewings (<italic>Chrysoperla carnea</italic>) and mites (<italic>Amblyseius swirskii</italic> Athias-Henriot and <italic>A. cucumeris</italic> Oudemans) have been reported as egg and larval biocontrol agents. Furthermore, predatory ants, e.g., <italic>Tapinoma nigerrimum</italic> (Nylander) has been identified as a biocontrol agent in North Africa (<xref rid="insects-11-00764-t004" ref-type="table">Table 4</xref>). Where available, conservation of these predators as NSs or mass rearing for use as augmentation or inoculative releases may offer a sustainable approach to the management of <italic>T. absoluta</italic>.</p><p>Hymenopteran egg parasitoids belonging to the genus <italic>Trichogramma</italic> have been reported as efficacious biological control agents in protected tomato crops [<xref rid="B211-insects-11-00764" ref-type="bibr">211</xref>,<xref rid="B212-insects-11-00764" ref-type="bibr">212</xref>]. For example, <italic>Trichogramma pretiosum</italic> (Riley) and <italic>Trichogramma achaeae</italic> (Nagaraja and Nagarkatti) have been used in <italic>T. absoluta</italic> management in both native and invaded European regions [<xref rid="B213-insects-11-00764" ref-type="bibr">213</xref>,<xref rid="B214-insects-11-00764" ref-type="bibr">214</xref>]. In Africa, egg parasitoids comprising especially <italic>Trichogramma</italic> spp. have shown potential for mass releases, e.g., in Tunisia [<xref rid="B215-insects-11-00764" ref-type="bibr">215</xref>]. Indeed, reports suggest that the parasitoid complex for larval <italic>T. absoluta</italic> comprise approximately 20 hymenopteran species (<xref rid="insects-11-00764-t004" ref-type="table">Table 4</xref>) [<xref rid="B207-insects-11-00764" ref-type="bibr">207</xref>,<xref rid="B216-insects-11-00764" ref-type="bibr">216</xref>,<xref rid="B217-insects-11-00764" ref-type="bibr">217</xref>]. Similarly, several <italic>T. absoluta</italic> larval parasitoids, including Eulophids, Braconids and Ichneumonids, have also been reported in the Mediterranean basin [<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>]. For example, the idiobiont <italic>Necremnus artynes</italic> parasitising third instars is widely documented [<xref rid="B218-insects-11-00764" ref-type="bibr">218</xref>]. Similarly, in Egypt, the larval parasitoid <italic>Stenomesius japonicus</italic> has been reported a desirable NS for <italic>T. absoluta</italic> biocontrol [<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>], while <italic>N. formosa</italic> (Westwood) has been reported in the Palearctic area, Asia, Africa and North America [<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]. As part of classical biocontrol, the larval parasitoid <italic>Dolichogenidea gelechiidivoris</italic> Marsh. (Syn.: <italic>Apanteles gelechiidivoris</italic> Marsh) was introduced from Peru into Africa [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>]. Progressive work has shown that <italic>D. gelechiidivoris</italic> prefers first and second instar larvae and is a highly efficacious parasitoid [<xref rid="B72-insects-11-00764" ref-type="bibr">72</xref>]. Conversely, few <italic>T. absoluta</italic> pupal parasitoids have been reported [<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]. Current research suggests Braconids, Chalcidids, Eulophids and Ichneumonids as potential pupal parasitoids [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>,<xref rid="B219-insects-11-00764" ref-type="bibr">219</xref>] (see <xref rid="insects-11-00764-t004" ref-type="table">Table 4</xref>). Given the diversity of African landscapes, and the diversity of both indigenous and exotic natural enemies as potent as NSs in pest control, using these in combination with other compatible NSs may be key to integrated management of <italic>T. absoluta</italic> in Africa.</p></sec></sec><sec id="sec6-insects-11-00764"><title>6. Use of Synthetic Pesticides and Integrated Pest Management</title><p>Regardless of their limitations, chemical pesticides continue to be an important component of integrated pest management (IPM) and can be a crucial pillar in <italic>T. absoluta</italic> management. Common active ingredients registered for <italic>T. absoluta</italic> control include pyrethroids [<xref rid="B51-insects-11-00764" ref-type="bibr">51</xref>], organophosphates [<xref rid="B3-insects-11-00764" ref-type="bibr">3</xref>] and diamides [<xref rid="B54-insects-11-00764" ref-type="bibr">54</xref>]. Laboratory bioassays using insecticides with some of these active ingredients showed very high efficacy for <italic>T. absoluta</italic> control [<xref rid="B29-insects-11-00764" ref-type="bibr">29</xref>,<xref rid="B70-insects-11-00764" ref-type="bibr">70</xref>,<xref rid="B234-insects-11-00764" ref-type="bibr">234</xref>,<xref rid="B235-insects-11-00764" ref-type="bibr">235</xref>,<xref rid="B236-insects-11-00764" ref-type="bibr">236</xref>]. Despite high laboratory efficacy, field <italic>T. absoluta</italic> optimal control remains a challenge owing to their cryptic leaf mining behaviour that renders contact insecticides ineffective. In addition, continuous use of these pesticides has also led to resistance development. Insecticides may also have adverse effects on the environment, beneficial arthropods and public health [<xref rid="B237-insects-11-00764" ref-type="bibr">237</xref>]. Thus, minimal insecticidal use is recommended in an IPM approach, which should rather be complemented with more environmentally benign NSs.</p><p>IPM encourages the use of eco-friendly strategies, such as NSs in biological control, used in compatible combinations with other efficacious methods, including the use of selective insecticides for pest control [<xref rid="B238-insects-11-00764" ref-type="bibr">238</xref>]. Thus, IPM comprises a cocktail of control practices, which may include cultural, chemical and biological control for the management of an economic pest species (<xref ref-type="fig" rid="insects-11-00764-f002">Figure 2</xref>) [<xref rid="B239-insects-11-00764" ref-type="bibr">239</xref>]. For <italic>T. absoluta</italic> management in Africa, and cognisant of all available control options discussed above, we propose the combination of compatible methods in an IPM approach and incorporating the use of sustainable NSs (see <xref ref-type="fig" rid="insects-11-00764-f002">Figure 2</xref>). This proposition is environmentally friendly, conserves biological diversity, including natural enemy populations, and presents little potentially negative public health implications. With the demerits associated with synthetic insecticides (see, e.g., [<xref rid="B53-insects-11-00764" ref-type="bibr">53</xref>,<xref rid="B164-insects-11-00764" ref-type="bibr">164</xref>]), IPM approaches may provide more lasting sustainable solutions to increased <italic>T. absoluta</italic> pest challenges [<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B60-insects-11-00764" ref-type="bibr">60</xref>] and indeed other pest species.</p></sec><sec id="sec7-insects-11-00764"><title>7. Potential for Natural Substances in Pest Control: Assets and Liabilities</title><sec id="sec7dot1-insects-11-00764"><title>7.1. Legislative and Regulatory Frameworks</title><p>Despite being major pillars to an integrated approach to <italic>T. absoluta</italic> sustainable management, there are major liabilities and bottlenecks associated with NS development and successful deployment in Africa. Some major liabilities for NSs include the increased number of complex guidelines, regulations and inadequate lobbying by biocontrol champions [<xref rid="B240-insects-11-00764" ref-type="bibr">240</xref>,<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B243-insects-11-00764" ref-type="bibr">243</xref>]. Furthermore, negative and often conflicting effects on chemical industry profitability and general farmer overreliance on pesticides [<xref rid="B137-insects-11-00764" ref-type="bibr">137</xref>,<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>] are some of the barriers to NSs, biological and low-risk pest management options. Policy guidelines in the production, exportation or importation, shipment, environmental risk assessment and field application of NSs are bureaucratic [<xref rid="B240-insects-11-00764" ref-type="bibr">240</xref>,<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B243-insects-11-00764" ref-type="bibr">243</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>]. Except for Kenya [<xref rid="B245-insects-11-00764" ref-type="bibr">245</xref>], policy and legislation governing NSs in Africa are mostly based on templates for synthetic chemical pesticides with a single active ingredient, and thus does not permit registration of NSs with complex multiple active compounds [<xref rid="B245-insects-11-00764" ref-type="bibr">245</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. This impedes the ability of resource-poor small and medium enterprises (SMEs) active in the NSs crop protection industry in African countries to register their products [<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. Governments need to create enabling legal and policy frameworks as pre-requisite for the promotion of the NS industry, particularly promoting existing SMEs [<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>] relative to multi-national companies. Available evidence suggests that the multi-national companies in the agrochemical industry are “unwilling” participants in creating an enabling legislative and registration environment for the NSs motion [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. Benjamin and Wesseler [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>] suggest that slow adoption of NSs may be caused by prolonged and prohibitive regulations. Therefore, changes in regulatory policies governing NSs in SSA should aim to reduce this bottleneck and make the toxicological evaluation regulations light touch [<xref rid="B240-insects-11-00764" ref-type="bibr">240</xref>,<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B245-insects-11-00764" ref-type="bibr">245</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. In light of this, African governments remain the main change agents [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>] through policy and regulatory adjustments that promote production, registration and marketing of NSs [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>].</p><p>In some cases, policies on NSs and IPM regulatory guidelines are elaborate on paper but lack implementation [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>]. This, in part, is supported by the lack of regulation on importation, trade and use as well as residue monitoring of unregistered/highly toxic pesticides [<xref rid="B45-insects-11-00764" ref-type="bibr">45</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. This may be largely due to a lack of funding [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>]. Therefore, monetary policies should enact direct funding of implementation of the proven NSs packages. Increased national funding will enhance research and development on NSs and their derivatives [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. However, research and developments funds are still limited in SSA due to restrictions attached to donor funds [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>].</p><p>Bureaucracy, inefficiency and prolonged government legislative processes are additional impediments to swift changes in NSs policies and legislative regulations [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>]. In addition, difficulty in harmonising regional polices due to fundamental mismatches or disagreements inhibits efficient movement of NSs across borders for purposes of research, propagation, pilot tests or field applications [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. Sub-Saharan Africa member states may need to adopt a common approach in interpretation of the Acts governing NSs, e.g., harmonised data requirements in toxicological studies or adoption of standard application forms and dossier formats for importation of NSs [<xref rid="B240-insects-11-00764" ref-type="bibr">240</xref>,<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B243-insects-11-00764" ref-type="bibr">243</xref>]. In addition, establishment of a central panel of pan-SSA experts may need to be developed to overlook NSs submissions [<xref rid="B243-insects-11-00764" ref-type="bibr">243</xref>]. If data requirements are harmonised, NSs approved in one country may be accepted in another without the drudgery and costs of repeated efficacy evaluations [<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B243-insects-11-00764" ref-type="bibr">243</xref>].</p><p>Encouragingly, related policy structural guidelines are in place for some countries [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>]. For example, the organic production of fruits and vegetables, e.g., in Kenya [<xref rid="B245-insects-11-00764" ref-type="bibr">245</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>], has very strict existing legislative measures that may be utilised as pedestals (asset) for building new guidelines for policy adjustments for NSs research and development [<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>]. Existing policies on conservation of biodiversity and protection of endangered species may be fundamental springboards for policy adjustments for the promotion of NSs. In addition, the Food and Agriculture Organisation (FAO) and Word Health Organisation (WHO) guidelines are freely available for adoption and modification where necessary [<xref rid="B251-insects-11-00764" ref-type="bibr">251</xref>]. The public outcry against pesticide-contaminated food and environment degradation reviewed in [<xref rid="B252-insects-11-00764" ref-type="bibr">252</xref>,<xref rid="B253-insects-11-00764" ref-type="bibr">253</xref>] may also be used as bottom-up pressure to justify policy modifications, promoting the use of NSs. For example, SSA governments can use the substitution principle, by replacing the most toxic pesticides (e.g., WHO hazard classes I and II) with the promising NSs [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B254-insects-11-00764" ref-type="bibr">254</xref>]. Alternatively, governments can increase tax on the most toxic pesticides and use that revenue to provide subsidies and financial incentives to early adopters or pesticide companies involved in the development of NSs [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B254-insects-11-00764" ref-type="bibr">254</xref>,<xref rid="B255-insects-11-00764" ref-type="bibr">255</xref>]. As the development and uptake of efficacious NSs increase, this may also positively affect farmer behaviour towards shifting from conventional pesticides to adoption of NSs.</p><p>Limited adoption in use of authorised pesticides of NSs is partly attributable to a lack of education and information [<xref rid="B45-insects-11-00764" ref-type="bibr">45</xref>,<xref rid="B256-insects-11-00764" ref-type="bibr">256</xref>,<xref rid="B257-insects-11-00764" ref-type="bibr">257</xref>,<xref rid="B258-insects-11-00764" ref-type="bibr">258</xref>]. However, evidence exists that some farmers in SSA are traditionally using NSs without anecdotal efficacy and safety validations [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>,<xref rid="B251-insects-11-00764" ref-type="bibr">251</xref>,<xref rid="B252-insects-11-00764" ref-type="bibr">252</xref>,<xref rid="B253-insects-11-00764" ref-type="bibr">253</xref>,<xref rid="B254-insects-11-00764" ref-type="bibr">254</xref>,<xref rid="B255-insects-11-00764" ref-type="bibr">255</xref>,<xref rid="B256-insects-11-00764" ref-type="bibr">256</xref>,<xref rid="B257-insects-11-00764" ref-type="bibr">257</xref>,<xref rid="B258-insects-11-00764" ref-type="bibr">258</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>]. Based on this, SSA governments and other stakeholders alike need to develop and consolidate NS-oriented educational programs to increase ecological literacy and reduce adoption barriers [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B256-insects-11-00764" ref-type="bibr">256</xref>,<xref rid="B258-insects-11-00764" ref-type="bibr">258</xref>]. It is therefore in the interest of SSA countries to modify policies enabling the development of simplified testing and validation protocols to legitimise existing NSs for improved use and expansion for the greater good.</p></sec><sec id="sec7dot2-insects-11-00764"><title>7.2. Economic Dynamics</title><p>The economic feasibility of NSs is ingrained in a functional biopesticide industry that, in turn, is rooted in SMEs and small-scale farmers or farmer groups [<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>,<xref rid="B260-insects-11-00764" ref-type="bibr">260</xref>]. This is because large companies are sceptical about the return on investment in NSs due to uncertainties regarding the market size (adoption issues), consistent supply of raw materials, uncertain patent issues and less than absolute efficacy [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>]. SMEs in SSA are not well developed due to financial constraints against the backdrop of prohibitive costs of investment on research and development for NSs [<xref rid="B240-insects-11-00764" ref-type="bibr">240</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>]. Consequently, instead of local production, most SSA agro-companies survive on distributing internationally sourced products [<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>], missing huge local investments opportunities. For example, <italic>B. thuringiensis</italic> (FlorBac WG<sup>®</sup>) and Spinosad (<italic>S spinosa</italic>, Spintordust<sup>®</sup>) distributed by SSA subsidiary agrochemical companies are produced outside the continent [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>]. This partly contributes to their premium prices, likely aiding their economic non-viability for the majority of resource-constrained farmers in SSA.</p><p>Estimation of the full economic value of NSs as a pest management tool is complex and depends on several factors, including the product being protected, the enterprise (e.g., farm), community structure to societal costs and benefits, as reviewed in [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>]. However, empirical evidence exists in support of financial sustainability for NSs versus conventional insecticides. For example, Amoabeng et al. [<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>] showed that pesticidal plants were more cost effective than synthetic insecticide in the control of the pests <italic>Brevicoryne brassicae</italic> (L.) (Hemiptera: Aphididae) and <italic>Plutella xylostella</italic> (L.) (Lepidoptera: Plutellidae) in cabbage. Similarly, McConnachie et al. [<xref rid="B261-insects-11-00764" ref-type="bibr">261</xref>] showed that the net present value of using a biocontrol agent <italic>Stenopelmus rufinasus</italic> (Gyllenhal; Coleoptera: Curculionidae) against the red waterfern <italic>Azolla filiculoides</italic> was US$1093 per hectare and US$206 million for the entire South Africa (with a benefit–cost ratio ranging from 2.5:1 to 15:1). While this study documented noble cost savings, Naranjo et al. [<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>] argues that the economic benefits of NSs are even higher. For example, by factoring avoided costs, e.g., public health protection, environmental damage costs, other maximum incremental social tolerable irreversible costs (MISTICs) and maintenance of essential ecological services [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B262-insects-11-00764" ref-type="bibr">262</xref>]. Factoring in all these variables thus reflects NSs may be way cheaper both in the short [<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>] and long term [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B263-insects-11-00764" ref-type="bibr">263</xref>] than conventional pesticides. These arguments reinforce the overall economic viability of NSs as a critical pillar for IPM [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B261-insects-11-00764" ref-type="bibr">261</xref>].</p><p>The market for NSs in SSA is underdeveloped, small and highly fragmented due to lack of investment, low ecological consciousness and farmers’ skewed behavioural perceptions towards pesticides preference, e.g., [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>,<xref rid="B255-insects-11-00764" ref-type="bibr">255</xref>], relative to NSs [<xref rid="B264-insects-11-00764" ref-type="bibr">264</xref>,<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>]. For example, in Ghana, only 14–25% of the farmer population are using NSs [<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>]. While studies show that this value may increase with increased education on NSs [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>], limited funding and stringent regulatory processes still remain significant bottlenecks [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>]. We thus suggest the use of a combination of enabling policy adjustments and direct funding and incentives for biocontrol practitioners to improve NS adoption. Through incentivising SMEs and mobilising farmer or community groups, SSA governments can encourage NS enterprises [<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>]. This system will build a strong localised production and trading system that can work as an encouraging baseline for private sector investment for scaling up [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>]. Previous studies suggest scaling up is the main pitfall for research and development initiatives on NSs in SSA [<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>]. Thus, this can be circumvented by managing the production and trading of NSs using economic product development pathways and commercial imperatives wrapped around government-supported SMEs.</p></sec><sec id="sec7dot3-insects-11-00764"><title>7.3. Ecological Perspectives</title><p>The main ecological assets of NSs in SSA include existing freely available rich biodiversity, known trophic systems and established harvesting and rearing/propagation protocols [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>]. Most NSs are highly specific, e.g., EPNs [<xref rid="B264-insects-11-00764" ref-type="bibr">264</xref>], microbial pesticides and parasitoids [<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>,<xref rid="B266-insects-11-00764" ref-type="bibr">266</xref>]. Thus, they have low impact on beneficial and non-target species [<xref rid="B252-insects-11-00764" ref-type="bibr">252</xref>,<xref rid="B266-insects-11-00764" ref-type="bibr">266</xref>,<xref rid="B267-insects-11-00764" ref-type="bibr">267</xref>,<xref rid="B268-insects-11-00764" ref-type="bibr">268</xref>] and hence contribute to maintenance of environmental integrity and conservation of biological diversity [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B257-insects-11-00764" ref-type="bibr">257</xref>]. In addition, production of NSs is ecologically benign and has a low carbon footprint [<xref rid="B267-insects-11-00764" ref-type="bibr">267</xref>]. Plant-based NSs, e.g., natural enemies, have the ability to sustainably self-propagate and disperse in space through inoculative releases [<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>]. This makes NSs a cost-effective management tool. Exhaustive benefits and assets of various NSs for the developing countries have fully been documented [<xref rid="B241-insects-11-00764" ref-type="bibr">241</xref>,<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>,<xref rid="B252-insects-11-00764" ref-type="bibr">252</xref>,<xref rid="B266-insects-11-00764" ref-type="bibr">266</xref>,<xref rid="B269-insects-11-00764" ref-type="bibr">269</xref>].</p><p>The liabilities of some NSs, e.g., predators and parasitoids (<xref rid="insects-11-00764-t002" ref-type="table">Table 2</xref>, <xref rid="insects-11-00764-t003" ref-type="table">Table 3</xref> and <xref rid="insects-11-00764-t004" ref-type="table">Table 4</xref>), include dependency on the host pest insect for survival [<xref rid="B264-insects-11-00764" ref-type="bibr">264</xref>,<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>,<xref rid="B270-insects-11-00764" ref-type="bibr">270</xref>]. This therefore means NSs need the presence of the pest, mediated by density-dependent factors and thus allowing some level of tolerable pest damage. Thus, use of preventive measures for pest management are not possible when using NSs. The action of NSs may also be slow when compared to synthetic insecticides, allowing some degree of pest damage on products. This may be undesirable for pest outbreaks that require rapid efficacy to bring populations below economic thresholds. Furthermore, this may also offset the quality of cosmetic products, e.g., the fruit and vegetable industry, whose Economic Injury Levels (EILs) are low [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>]. In addition, some NSs like parasitoids, EPNs and baculoviruses are highly sensitive to the biophysical environment [<xref rid="B264-insects-11-00764" ref-type="bibr">264</xref>,<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>,<xref rid="B266-insects-11-00764" ref-type="bibr">266</xref>,<xref rid="B271-insects-11-00764" ref-type="bibr">271</xref>], and thus their efficacy may vary in space. This makes the deployment of NSs challenging in largely rainfed, dry cropping systems in SSA [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>] or under rapidly shifting climate environments. Similar environmental limitations for NSs have been made for the biocontrol agents <italic>Romanomermis culicivorax</italic> [<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>], <italic>Steinernema carpocapsae</italic> [<xref rid="B272-insects-11-00764" ref-type="bibr">272</xref>] and other biocontrol approaches [<xref rid="B271-insects-11-00764" ref-type="bibr">271</xref>,<xref rid="B273-insects-11-00764" ref-type="bibr">273</xref>,<xref rid="B274-insects-11-00764" ref-type="bibr">274</xref>,<xref rid="B275-insects-11-00764" ref-type="bibr">275</xref>].</p><p>Other ecological limitations of NSs include a lack of sound and sustainable mass rearing and/propagation technologies that facilitate reliable product supply and reduce the costs of importation while safeguarding ecosystems [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>]. Use of botanicals as natural pesticides has been criticised owing to unsustainable harvesting of bioactive plant species [<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>,<xref rid="B250-insects-11-00764" ref-type="bibr">250</xref>]. In some cases, effective pesticidal plants that are not native to production areas, e.g., in a push–pull system [<xref rid="B185-insects-11-00764" ref-type="bibr">185</xref>], may become introduced weeds, thus increasing the cost of production. Lack of expertise and experience in the phytochemistry of plant-based NSs for extraction of active ingredients has also been a barrier to success. This expertise is needed for robust evidence-based safety screening to improve research and development processes.</p></sec><sec id="sec7dot4-insects-11-00764"><title>7.4. Farmer Perceptions and Social Dynamics</title><p>Natural substances are readily available for most small-scale, resource-poor farmers, and thus argued to be the most appropriate technology compatible with SSA [<xref rid="B247-insects-11-00764" ref-type="bibr">247</xref>]. The biggest asset for NSs is its relatively low public health risk. Small-scale farmers are largely poorly advised on the appropriate use and disposal of toxic synthetic pesticides [<xref rid="B45-insects-11-00764" ref-type="bibr">45</xref>,<xref rid="B137-insects-11-00764" ref-type="bibr">137</xref>,<xref rid="B276-insects-11-00764" ref-type="bibr">276</xref>]. Compounded by the aggressive promotion of synthetic pesticides that overshadows NSs [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B246-insects-11-00764" ref-type="bibr">246</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>,<xref rid="B277-insects-11-00764" ref-type="bibr">277</xref>], this makes the use of pesticides a significant public health threat for livelihoods in SSA. There is also limited infrastructure bridging researchers and farmers to facilitate knowledge transfer. As such, most research outputs on NSs remain as pilot projects or scholarly papers that are inaccessible to the small-scale farmers [<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B257-insects-11-00764" ref-type="bibr">257</xref>,<xref rid="B259-insects-11-00764" ref-type="bibr">259</xref>]. Nevertheless, behavioural studies show that while SSA farmers are solely used to pesticides, they are willing to adopt NSs if proven efficacious [<xref rid="B45-insects-11-00764" ref-type="bibr">45</xref>,<xref rid="B137-insects-11-00764" ref-type="bibr">137</xref>,<xref rid="B276-insects-11-00764" ref-type="bibr">276</xref>,<xref rid="B278-insects-11-00764" ref-type="bibr">278</xref>]. Players in research and development thus need to lobby for uptake of newly developed NSs technologies through engagement with relevant stakeholders.</p><p>Fluctuations in supply in NSs, e.g., botanicals, often reduce reliability of this tool for pest management [<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>]. Furthermore, vulnerability to the biophysical environment often compromises efficacy [<xref rid="B248-insects-11-00764" ref-type="bibr">248</xref>,<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>], leading to poor product quality and low market values [<xref rid="B249-insects-11-00764" ref-type="bibr">249</xref>]. The application of some NSs also requires significant adjustments in current farming methods, labour and skills [<xref rid="B277-insects-11-00764" ref-type="bibr">277</xref>]. For example, the use of parasitoids requires shift from monoculture to habitat management that encourages biodiversity conservation [<xref rid="B265-insects-11-00764" ref-type="bibr">265</xref>,<xref rid="B279-insects-11-00764" ref-type="bibr">279</xref>]. Without change in perception/behaviour, ecological literacy and financial incentives, farmers may not be socially ready for the changes facilitating the use of NSs. Farmers’ beliefs, attitude and behaviour are major factors influencing adoption of NSs. Creative persuasion of the non-conformers to NSs is needed to change their choice of pest management approaches [<xref rid="B242-insects-11-00764" ref-type="bibr">242</xref>,<xref rid="B244-insects-11-00764" ref-type="bibr">244</xref>,<xref rid="B277-insects-11-00764" ref-type="bibr">277</xref>]. Indeed, Goldberger et al. [<xref rid="B277-insects-11-00764" ref-type="bibr">277</xref>] showed that out of the three farmer categories, the “environmental stewards” and “networking farmers” are likely to partake in NSs compared to those farmers solely looking to maximise production. Similarly, mobilising farmers into networking groups may increase NS adoption [<xref rid="B256-insects-11-00764" ref-type="bibr">256</xref>,<xref rid="B277-insects-11-00764" ref-type="bibr">277</xref>], e.g., establishing social/networking groups that can implement specific NSs may be a fruitful endeavour for SSA [<xref rid="B255-insects-11-00764" ref-type="bibr">255</xref>,<xref rid="B256-insects-11-00764" ref-type="bibr">256</xref>]. These groups also facilitate ease of training and awareness campaigns on ecological literacy, economic feasibility and other assets of NSs.</p></sec></sec><sec sec-type="conclusions" id="sec8-insects-11-00764"><title>8. Conclusions</title><p>The continental invasion of <italic>T. absoluta</italic> represents a significant biosecurity threat that affects the majority of livelihoods dependant on agricultural sustenance. A number of biological and physiological factors discussed here may, in part, contribute to its current spread in African natural and agro-ecosystems. Insecticide use against <italic>T. absoluta</italic> has been the common default response to pest pressure. However, pesticide misuse affects the environment, public health, ecosystem services and often leads to pest resistance development. Thus, use of low-risk NSs and biocontrol methods in an integrated approach may be the sustainable solution to the <italic>T. absoluta</italic> problem in SSA. However, NSs also have their own liabilities as a pest management tool in African systems, argued from a legislative, economic, ecological and social standpoint. Elucidating these factors is critical in facilitating research and development of NSs in Africa and their consequent adoption as a sustainable tool for pest management.</p></sec></body><back><ack><title>Acknowledgments</title><p>The authors would like to acknowledge the Botswana International University of Science and Technology (BIUST) for all financial support availed to V.L.T., H.M. and C.N. and the University of the Free State (UFS) to R.M. and FN. Great appreciation goes to Gerald Chikowore for his input in the construction of Maps used in this paper. We also want to thank several anonymous referees for the valuable inputs in a previous version of this manuscript.</p></ack><notes><title>Author Contributions</title><p>Conceptualisation, C.N., H.M. and V.L.T.; methodology, C.N., V.L.T., H.M., R.M. and F.C.; validation, C.N., V.L.T., H.M., R.M. and F.C.; resources, C.N. and F.C.; original draft preparation, V.L.T., H.M., R.M. and C.N.; review and editing, C.N., V.L.T., H.M., R.M. and F.C.; supervision, C.N. and F.C.; project administration, C.N. and F.C.; funding acquisition, C.N. All authors have read and agreed to the published version of the manuscript.</p></notes><notes><title>Funding</title><p>This research received no external funding.</p></notes><notes notes-type="COI-statement"><title>Conflicts of Interest</title><p>The authors declare no conflict of interest.</p></notes><ref-list><title>References</title><ref id="B1-insects-11-00764"><label>1.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Olson</surname><given-names>L.J.</given-names></name></person-group><article-title>The economics of terrestrial invasive species: A review of the literature</article-title><source>Agric. Resour. Econ. 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Biol.</source><year>2019</year><pub-id pub-id-type="doi">10.1038/s42003-018-0257-6</pub-id></element-citation></ref></ref-list></back><floats-group><fig id="insects-11-00764-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Temperature and precipitation comparison between the <italic>T. absoluta</italic> native (South America) and invaded (Africa) regions. The maps generally show that the <italic>T. absoluta</italic> niche is largely similar between the native and invaded region and thus successful establishment is possible. Maps were drawn in ArcGIS 10.3 from ESRI with data obtained from WorldClim Ver 2.0.</p></caption><graphic xlink:href="insects-11-00764-g001"></graphic></fig><fig id="insects-11-00764-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Schematic representation of proposed integrated pest management programme for <italic>Tuta absoluta</italic>. The emphasis is on the use of NSs, low-risk substances and biological control agents (green). Classic examples of “agents” or model organisms used within each category are given. A holistic use, in a judicious combination with target specific pesticides (black), environmentally friendly and low risk techniques (blue) and good crop management, (grey) may help in the IPM of this pest insect. These methods should be used in the presence of sound legislative measures that promote integrated approaches to pest management. Note, these examples are not purely exhaustive, but provide baseline information for IPM.</p></caption><graphic xlink:href="insects-11-00764-g002"></graphic></fig><table-wrap id="insects-11-00764-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">insects-11-00764-t001_Table 1</object-id><label>Table 1</label><caption><p>Alternative host plants of <italic>Tuta absoluta</italic> reported in the literature. The list may not be purely exhaustive but was compiled using the literature available at the time of writing.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Family</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Host Plant</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Solanaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum tuberosum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum nigrum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B125-insects-11-00764" ref-type="bibr">125</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum melongena</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B128-insects-11-00764" ref-type="bibr">128</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum aethiopicum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B96-insects-11-00764" ref-type="bibr">96</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum anguivi</italic> Lam.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum macrocarpon</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum scabrum</italic> Mill.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum villosum</italic> Mill.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum aculeatissimum</italic> (Jacq.)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum coccineum</italic> (Jacq.)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum supinum</italic> Dunal</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B42-insects-11-00764" ref-type="bibr">42</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum americanum</italic> Mill.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B128-insects-11-00764" ref-type="bibr">128</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum bonariense</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B129-insects-11-00764" ref-type="bibr">129</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum elaeagnifolium</italic> Cav.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B129-insects-11-00764" ref-type="bibr">129</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum gracilius</italic> Herter</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B129-insects-11-00764" ref-type="bibr">129</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum hirtum</italic> Vahl</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B130-insects-11-00764" ref-type="bibr">130</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum pseudo-capsicum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B129-insects-11-00764" ref-type="bibr">129</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum sisymbrifolium</italic> Lamb</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B129-insects-11-00764" ref-type="bibr">129</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum dulcamara</italic> Linnaeus</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum lyratum</italic> Thunb.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B131-insects-11-00764" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solanum puberulum</italic> Nuttal ex Seemann</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B131-insects-11-00764" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nicotiana longiflora</italic> Cav.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nicotiana tabacum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nicotiana rustica</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nicotiana glauca</italic> (Graham)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Datura stramonium</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Datura quercifolia</italic> Kunth</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B128-insects-11-00764" ref-type="bibr">128</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Datura ferox</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B132-insects-11-00764" ref-type="bibr">132</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Xanthium brasilicum</italic> Vell.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Capsicum annum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-insects-11-00764" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Capsicum frutescens</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B96-insects-11-00764" ref-type="bibr">96</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nicandra physalodes</italic> (L.) Gaertner</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Lycium halimifolium</italic> Mill.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Lycium chilense</italic> (Coralillo)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B131-insects-11-00764" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Lycium hirsutum</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B82-insects-11-00764" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Physalis peruviana</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B133-insects-11-00764" ref-type="bibr">133</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Physalis angulata</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B130-insects-11-00764" ref-type="bibr">130</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Amaranthaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Amaranthus spinosus</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Amaranthus viridis</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Spinacia oleracea</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B126-insects-11-00764" ref-type="bibr">126</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Beta vulgaris vulgaris</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B126-insects-11-00764" ref-type="bibr">126</xref>,<xref rid="B134-insects-11-00764" ref-type="bibr">134</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chenopodium bonus-henricus</italic> (L.) Rchb.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B126-insects-11-00764" ref-type="bibr">126</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chenopodium rubrum</italic> (L.) S. Fuentes, Uotila & Borsch</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B126-insects-11-00764" ref-type="bibr">126</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chenopodium album</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B134-insects-11-00764" ref-type="bibr">134</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Fabaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaseolus vulgaris</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B135-insects-11-00764" ref-type="bibr">135</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Medicago sativa</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Vicia faba</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cucurbitaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Citrullus lanatus</italic> (Thunb.) Matsum. & Nakai</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B124-insects-11-00764" ref-type="bibr">124</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Convolvulaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Convolvulus arvensis</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B134-insects-11-00764" ref-type="bibr">134</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Calystegia sepium</italic> (L.) Brown</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B134-insects-11-00764" ref-type="bibr">134</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Malvaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Malva sylvestris</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-insects-11-00764" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Asteraceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Sonchus oleraceus</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Xanthium strumarium</italic> L.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B136-insects-11-00764" ref-type="bibr">136</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Poaceae</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Sorghum halepense</italic> (L.) Pers.</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B78-insects-11-00764" ref-type="bibr">78</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Brassicaceae</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Sinapis arvensis</italic> L.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B136-insects-11-00764" ref-type="bibr">136</xref>]</td></tr></tbody></table></table-wrap><table-wrap id="insects-11-00764-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">insects-11-00764-t002_Table 2</object-id><label>Table 2</label><caption><p>Insecticidal plants used to make botanicals used against <italic>Tuta absoluta</italic> (Eggs—E; Larvae—L; Pupa—P; Adults—A). The records were obtained from the literature at the time of writing and may not be purely exhaustive.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Natural Substance</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Species</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Host Developmental Stage</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Botanicals</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Azadirachtin</italic> spp.</td><td align="center" valign="middle" rowspan="1" colspan="1">E, L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B150-insects-11-00764" ref-type="bibr">150</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">Petroleum ether extract</td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B150-insects-11-00764" ref-type="bibr">150</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Jatropha curcus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B150-insects-11-00764" ref-type="bibr">150</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Allium sativum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Ocimum basilicum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Thymus vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Ricinus communis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Eucalyptus</italic> spp.</td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Melia azedarach</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Geranium</italic> spp.</td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Allium cepa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-insects-11-00764" ref-type="bibr">156</xref>,<xref rid="B157-insects-11-00764" ref-type="bibr">157</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Citrus aurantium</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B158-insects-11-00764" ref-type="bibr">158</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Piper amalago</italic> var. <italic>medium</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B153-insects-11-00764" ref-type="bibr">153</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Piper glabratum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B153-insects-11-00764" ref-type="bibr">153</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Piper mikanianum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B153-insects-11-00764" ref-type="bibr">153</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Simmondsia chinensis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B151-insects-11-00764" ref-type="bibr">151</xref>]</td></tr></tbody></table></table-wrap><table-wrap id="insects-11-00764-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">insects-11-00764-t003_Table 3</object-id><label>Table 3</label><caption><p>Microbials and other natural substances used as biopesticides against <italic>Tuta absoluta.</italic> (Eggs—E; Larvae—L; Pupa—P; Adults—A). The records were obtained from the literature at the time of writing and may not be purely exhaustive.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Type of Microbial</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Species</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Host</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bacillus thuringiensis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B160-insects-11-00764" ref-type="bibr">160</xref>,<xref rid="B169-insects-11-00764" ref-type="bibr">169</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Entomopathogens</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bacillus thuringiensis kurstaki</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B169-insects-11-00764" ref-type="bibr">169</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Beauveria bassiana</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B169-insects-11-00764" ref-type="bibr">169</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Metarhizium beauveria</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B170-insects-11-00764" ref-type="bibr">170</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Metarhizium anisopliae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B170-insects-11-00764" ref-type="bibr">170</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Baculoviruses</italic> (NPVs)</td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B171-insects-11-00764" ref-type="bibr">171</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Saccharopolyspora spinosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B172-insects-11-00764" ref-type="bibr">172</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Entomopathogenic nematodes</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Steinernema affine</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B172-insects-11-00764" ref-type="bibr">172</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Steinernema carpocapsae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B172-insects-11-00764" ref-type="bibr">172</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Steinernema feltiae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B62-insects-11-00764" ref-type="bibr">62</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Heterorhabditis bacteriophora</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B62-insects-11-00764" ref-type="bibr">62</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Other NSs</td><td align="center" valign="middle" rowspan="1" colspan="1">Pheromones</td><td align="center" valign="middle" rowspan="1" colspan="1">A</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B36-insects-11-00764" ref-type="bibr">36</xref>,<xref rid="B59-insects-11-00764" ref-type="bibr">59</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Antimicrobial peptides (AMPs)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">E, L, P</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B173-insects-11-00764" ref-type="bibr">173</xref>]</td></tr></tbody></table></table-wrap><table-wrap id="insects-11-00764-t004" orientation="portrait" position="float"><object-id pub-id-type="pii">insects-11-00764-t004_Table 4</object-id><label>Table 4</label><caption><p>Natural enemies (parasitoids and predators) reported in literature for <italic>Tuta absoluta.</italic> The list may not be purely exhaustive but was compiled using the available literature at the time of writing. (Eggs—E; Larvae—L; Pupa—P).</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Natural Enemy</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Species</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Host</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Parasitoids</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Agathis fuscipennis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B131-insects-11-00764" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Apanteles dignus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Apanteles gelechiidivoris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Baryscapus bruchophagi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Brachymeria secundaria</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bracon lucileae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bracon lulensis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bracon</italic> spp.</td><td align="center" valign="middle" rowspan="1" colspan="1">P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Bracon tutus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Campoplex haywardi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Capidosoma desantis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Capidosoma koehleri</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Cheolras semele</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Closterocerus clarus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Clostrocerus formosus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Copidosoma desantisi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Copidosoma koehleri</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Diadegma</italic> spp., <italic>D. ledicola</italic> and <italic>D. pulchripes</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Diglyphus crassinervis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Diglyphus isaea</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dineulophus phthormiaeae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dolichogenidea litae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Elachertus inunctus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B222-insects-11-00764" ref-type="bibr">222</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Elasmus phthorimaeae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Encarsia porteri</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B223-insects-11-00764" ref-type="bibr">223</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Goniozus nigrifemur</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Habrobracon didemie</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Habrobracon hebetor</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Habrobracon nigricans</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B224-insects-11-00764" ref-type="bibr">224</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Habrobracon osculator</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Halticoptera aenea</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B222-insects-11-00764" ref-type="bibr">222</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Hemiptarsenus zilahisebessi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B225-insects-11-00764" ref-type="bibr">225</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Hockeria unicolor</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>,<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Horismenus sp</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Hyposoter didymator</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B226-insects-11-00764" ref-type="bibr">226</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Necremnus artynes</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B218-insects-11-00764" ref-type="bibr">218</xref>,<xref rid="B225-insects-11-00764" ref-type="bibr">225</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Necremnus metalarus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Necremnus tidius</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B227-insects-11-00764" ref-type="bibr">227</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Neochrysocharis formosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B119-insects-11-00764" ref-type="bibr">119</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Neochrysocharis formosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B222-insects-11-00764" ref-type="bibr">222</xref>,<xref rid="B224-insects-11-00764" ref-type="bibr">224</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Neochrysocharis formosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pnigalio cristatus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pnigalio incompletus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pnigalio soemius</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pnigalio</italic> sp. <italic>soemius complex</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B222-insects-11-00764" ref-type="bibr">222</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudapanteles dignus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pteromalus intermedius</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B220-insects-11-00764" ref-type="bibr">220</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pteromalus semotus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Retisympiesis phthorimaea</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Retisympiesis phthorimaea</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Temelucha anatolica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma achaeae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B214-insects-11-00764" ref-type="bibr">214</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma achaeae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B224-insects-11-00764" ref-type="bibr">224</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma bactrae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma bourarachae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B228-insects-11-00764" ref-type="bibr">228</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma dendrolimi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma exiguum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma fasciatum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma lopezandinensis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma nerudai</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma pintoi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma pretiosum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>,<xref rid="B213-insects-11-00764" ref-type="bibr">213</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma rojasi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Trichogramma telengai</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>,<xref rid="B16-insects-11-00764" ref-type="bibr">16</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Zoophthorus macrops</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B221-insects-11-00764" ref-type="bibr">221</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Predators</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Amblyseius cucumeris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B229-insects-11-00764" ref-type="bibr">229</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Amblyseius swirskii</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B229-insects-11-00764" ref-type="bibr">229</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Brachygastra lecheguana</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Calosoma granulatum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Coleomegilla maculata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Cycloneda sanguinea</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dicyphus errans</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B230-insects-11-00764" ref-type="bibr">230</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dicyphus maroccanus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B230-insects-11-00764" ref-type="bibr">230</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dicyphus. tamaninii</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B206-insects-11-00764" ref-type="bibr">206</xref>,<xref rid="B229-insects-11-00764" ref-type="bibr">229</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Doru lineare</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Engytatus varians</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B229-insects-11-00764" ref-type="bibr">229</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Eriopsis conexa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Franklinothrips vespiformis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Labidura riparia</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Lebia concina</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Macrolophus pygmaeus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B231-insects-11-00764" ref-type="bibr">231</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nabis ibericus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B229-insects-11-00764" ref-type="bibr">229</xref>,<xref rid="B232-insects-11-00764" ref-type="bibr">232</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nesidiocoris tenuis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B231-insects-11-00764" ref-type="bibr">231</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Orius albidipennis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">-</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B230-insects-11-00764" ref-type="bibr">230</xref>,<xref rid="B233-insects-11-00764" ref-type="bibr">233</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Orius insidiosus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">E, L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Podisus nigrispinus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Polistes carnifex</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Polistes melanosoma</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Polistes versicolor</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Polybia ignobilis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Polybia scutellaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Protonectarina sylveirae</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Protopolybia exigua</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scolothrips sexmaculatus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solenopsis geminata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Solenopsis saevissima</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">L, P</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Synoeca cyanea</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B15-insects-11-00764" ref-type="bibr">15</xref>]</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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