Natural enemies used in biological control
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1 Natural enemies used in biological control Dr. Mor Salomon The Israel Cohen Institute for Biological control The Plants production and marketing board
2 What are Natural Enemies? Organisms that kill or reduce the population of another organism Biological control Predators Parasitoids Nematodes Pathogens Development achieved by feeding on other organisms: Predators Parasitoids Feed on another organism many individuals Free living a singe individual Bound to their host
3 Predators Gambusia affinis Mosquitofish Mayna Acridotheres tristis Ducks Mosquito larvae Grasshopper Green-rice leafhopper
4 Predators Important natural enemies for applied biological control are Insects & Mites
5 Feeding strategy Most predators are entomophagous insects Entomophagy Monophagous feed on one type of prey (i.e. a specialist) Insects Phagein = Feeding Rodolia cardinalis feeds on Icerya purchasi
6 Monophagous predator Phytoseiulus persimilis Two-spotted spider mite Tetranychus urticae
7 Feeds on a limited range of prey Oligophagous predator Coccinella septempunctata Chilocorus kuwanae Feeds on closely related species of prey Pea aphid Euonymus scale
8 Polyphagous predator Feeds on a broad range of prey Aphids Green lacewing Thrips Leafminers Chrysoperla carnea Whiteflies Spider mite
9 Mouthparts Predators can have either: Biting mouthparts 1. Biting chewing mouthparts 2. Piercing Sucking mouthparts Examples: Tiger beetle Mandibles cut & chew; Maxillae manipulate the prey Cicendela sp. (Carabidae)
10 Green lacewing (Antlion; Neuroptera)
11 Mouthparts Piercing & sucking mouthparts Elongated labium Mandibles & maxillae = stylet for piercing Examples: Anchor stink bug Cicendela sp. (Pentatomidae) Minute pirate bug Orius sp. (Anthocoridae)
12 Assassin fly Velvet spider Zosteria sp. (Asilidae) Stegodyphus lineatus (Eresidae)
13 Beetles - Coleoptera Coleoptera - Beetles Bugs - Hemiptera Kingdom: Animalia Phylum: Arthropoda Class: Insecta Order: Coleoptera Cockchafer Melolontha sp. Family: Scarabaeidae Order: Coleoptera Stink bug Nezara marginata Family: Pentatomidae Order: Hemiptera Suborder: Heteroptera
14 Beetles - Coleoptera Coleoptera - Beetles Bugs - Hemiptera Kingdom: Animalia Phylum: Arthropoda Class: Insecta Order: Coleoptera Ground beetle Pasimachs elongatus Family: Carabidae Order: Coleoptera Stink bug Nezara marginata Family: Pentatomidae Order: Hemiptera Suborder: Heteroptera
15 Class: Insecta Life cycle Beetles life cycle 2-4 instars Order: Coleoptera Exarate pupa (Free appendages) Pterostichus melanarius Family: Carabidae
16 Ground beetles Natural enemies in agroecosystems Live and prey mostly on the ground Class: Insecta Order: Coleoptera Family: Carabidae Gypsy moth larva Clivinia fossor Pterostichus melanariu Colorado potato beetle larva carrot weevil Bird cherry-oat aphid
17 Ground beetles Class: Insecta Order: Coleoptera Family: Carabidae Fall armyworm Bimidion quadrimaculatum Black onion fly Onion root maggot Black bean aphid European corn borer
18 Ladybird beetles ~5,000 species in the family Most species eat primarily insects and mites Class: Insecta Order: Coleoptera Family: Coccinellidae Aphid colony Rodolia cardinalis prey on The cottony cushion scale, Icerya purchasi California; 1,888
19 Feeding behaviour Adults & larva feed on the same prey Highly specific diet Class: Insecta Order: Coleoptera Family: Coccinellidae Many species feed on pollen, nectar and honeydew Some ladybirds are species-specific, others eat several species Ladybirds are not effective at low population levels
20 Life cycle Eggs laid in clusters 4 instars Class: Insecta Order: Coleoptera Family: Coccinellidae Warning colours sucker Chilocorini: Partly exposed Coccinellinae: Exposed pupa Scymnini: Completely covered pupa
21 Biological control Cryptolaemus montrouzieri Hippodamia convergens Coccinella septempunctata Stethorus punctilum Harmonia axyridis Scymnus sp. Adalia bipunctata
22 Lacewings / Antlions Larva: predator Green lacewing Adult: honeydew, nectar, pollen Brown lacewing All predators Order: Neuroptera Families: Chrysopidae Prey: Aphids, whiteflies, thrips, spider mites, moth eggs, spider mites, mealybugs Aphids Hemerobiidae
23 Digger wasps 25% of species in the order are predators Ants control ground-dwelling insects Wasps paralyze insects Biological control of leaf-eating insects Class: Insecta Order: Hymenoptera Family: Sphecidae Vespidae Great golden digger wasp Sphex sp. Polistes humilis
24 Digger wasps 25% of species in the order are predators Ants control ground-dwelling insects Wasps paralyze insects Biological control of leaf-eating insects Class: Insecta Order: Hymenoptera Family: Sphecidae Vespidae reduced caterpillar numbers in cabbages Great golden digger wasp White cabbage butterfly Impractical in agriculture Polistes humilis
25 Hoverflies Resemble bees, but only one pair of wings Feed on aphids 500 eggs Class: Insecta Order: Diptera Family: Syrphidae Released in pepper Esiyrphus balteatus Marmalade hoverfly crops
26 Big-eyed bugs Most bugs are vegetarian Some important predators Prey: Lepidopteran eggs Plant bugs Whiteflies Mites aphids Class: Insecta Order: Hemiptera (bugs) Family: Lygaeidae Crops (e.g.): Cotton Ornamentals Strawberries Vegetable crops Geocoris sp. feeding on whitefly nymph
27 Assassin bugs Ambush predators Thin neck ; Strong piercing rostrum Highly polyphagous, including honeybees & spiders Crop (e.g.): sunflower, cotton Class: Insecta Order: Hemiptera (bugs) Suborder: Heteroptera (True bugs) Family: Reduviidae Good control in cotton Helicoverpa sp. (Lepidoptera Pristhesancus plagipennis Creoniades sp. Miridae (Grundy 2007)
28 Flower bugs Polyphagous predators Actively search for prey Important in many agricultural crops Order: Hemiptera Suborder: Heteroptera Family: Anthocoridae The common flower bug Anthocoris nemorum Pear Psylla Minute pirate bug Orius sp.
29 Flower bugs Polyphagous predators Actively search for prey Important in many agricultural crops Order: Hemiptera Suborder: Heteroptera Family: Anthocoridae Prey: greenfly red spider mite Crop: Hedgerows Agri. crops Wild plants The common flower bug Pear orchards Anthocoris nemorum Pear Psylla
30 Minute pirate bug 3 main species used as BCA: Orius laevigatus O. Majusculus O. insidiosus Order: Hemiptera Suborder: Heteroptera Family: Anthocoridae
31 Minute pirate bug Orius laevigatus O. majusculus Order: Hemiptera Suborder: Heteroptera Family: Anthocoridae Prey: Thrips Aphids Whiteflies Mites Moth eggs Omnivorous Introduced the most Mediterranean Flowers Europe Whole plant
32 Orius life cycle Hemimetabolus Egg: embedded in the leaf Adult Egg Order: Hemiptera Suborder: Heteroptera Family: Anthocoridae Nymph: yellowish wing buds at 5 th instar found on leaves Adult: brown / black occupy flower head 5 nymphal stages All instars feed on soft-bodied insects O. insidiosus nymph
33 Zoophytophagus plant bugs Most mirids are pests Order: Hemiptera Suborder: Heteroptera Family: Miridae Lygus sp. Pest in cotton, strawberry etc.
34 Zoophytophagus plant bugs Most mirids are pests Order: Hemiptera Suborder: Heteroptera Family: Miridae Efficient natural enemy of Tuta absoluta Nesidiocoris Tenuis Tomato leafminer; Tuta absoluta
35 Order: Hemiptera Omnivore Wide range of prey Suborder: Heteroptera Family: Miridae Effective in controlling whiteflies Used commercially Tomato (tunnel & glasshouse) Macrolophus caliginosus
36 Stink/Shield bugs Eject foul smell when disturbed Most species are pests Spined soldier bug Order: Hemiptera Suborder: Heteroptera Family: Pentatomidae Anchor bug Polyphagous predator e.g. mexican bean beetle Stiretrus anchorago Low abundance Low contribution to biological control Podisus maculiventris Polyphagous predator e.g. gypsy moth, corn borer, armyworm sp. etc. Classical biological control (e.g. Russia)
37 Predatory mites The most introduced NE Used commercially worldwide 1 st used on cucumber by Koppert 1960 s Kingdom: Animalia Phylum: Arthropoda Class: Arachnida Subclass: Acari Order: Mesostigmata Family: Phytoseiidae Phytoseiulus persimilis
38 Spider mites Pests in many crops around the world Two-spotted spider mite is the most important All stages feed on plant tissue and sap Subclass: Acari Order: Trombidiformes Family: Tetranychidae Adults & nymphs produce webs Difficult for predators to penetrate Tetranychus urticae Tetranychus urticae
39 Phytoseiulus persimilis Highly specific to spider mites Egg Subclass: Acari Order: Mesostigmata Family: Phytoseiidae Adult Larva doesn t eat Highly population growth than T. urticae 2 nymph stages eat all stages, but adults Disadvantage: No alternative prey Cannibalism Population decline
40 Above 30⁰C, P. persimilis growth declines Neoseiulus californicus Subclass: Acari Order: Mesostigmata Family: Phytoseiidae Prefer the larval & nymphal stages of T. urticae Consume less prey than P. persimilis, but more effective at low densities Generalist predator Used commercially in fruit & ornamental crops Tomato rust mite Aculops lycopersici Panonychus ulmi Fruit spider mite Neoseiulus californicus
41 Iphiseius degenerans Native to the mediterranean Subclass: Acari Order: Mesostigmata Family: Phytoseiidae Feeds on spider mites, thrips & pollen Not effective against T. urticae because of the web Used particularly in pepper crops Can survive and reproduce only on pollen
42 Amblyseius swirskii Native to the mediterranean Subclass: Acari Order: Mesostigmata Family: Phytoseiidae Suited for warm (25-28⁰C) and humid (60-70%) conditions Generalist predator: 1-2 instar thrips Eggs, 1 st larvae whitefly spider mites Can survive & reproduce on pollen Used commercially to control whiteflies Establish well in the crop
43 Spiders Most dominant predator in agro-ecosystems Consume many prey in short time Most BCA are specialists Spiders are generalist predators Survive at low pest population Phylum: Arthropoda Class: Arachnida Order: Aranea Family: Linyphiidae Gnaphosiidae Theriididae Spider BC = conservation of spiders (e.g. selective spraying) 3 main families in desert agro-ecosystems of wheat (Gavish et al. 2008) Gnaphosidae Linyphiidae Theridiidae
44 Parasitoids An organism that live in or on another animal (host), exploiting and killing it Aphytis melinus, a parasitoid of the California red scale Encarsia formosa, parasitoid of whitefly nymphs Occupy a host during development Adult is free-living
45 Parasites An organism that live in or on a host, exploiting but not killing it Blacklegged tick Occupy a host at all life stages
46 Ectoparasitoid A parasitoid that lives on the external surface of its host, feeding on it and killing it in the process. D. isaea pupae Diglyphus isaea Parasitoid of the vegetable leafminer
47 Endoparasitoid A parasitoid that lives inside the body of its host, feeding on it and killing it in the process. Don t cause immediate death of the host Feed on the essential tissues only at the end of development Protected inside the host Ageniaspis citricola parasitoid of the citrus leafminer
48 Types of parasitoids Idiobiont : prevent further development of the host after initial parasitization attack an immobile life stage (e.g. an egg or pupa) mostly ectoparasitoids Koinobiont : the host continues to develop after prasitization and is only killed when the parasitoid reaches maturity attack any life stage Both ecto- and endoparasitoids
49 Life-stages attacked Egg parasitoids Complete their development in the egg stage of the host Halyomorpha halys Brown stink bug Trissolcus halymorphae
50 Life-stages attacked Egg-larval parasitoids Attack the egg, but complete development at the larval stage Adult parasitoid emerge from the larva e.g. Chelonus annulipes attack the EU corn borer Chelonus sp. Egg-pupa parasitoids EU corn borer Attack the egg, but delay development and kill the host before pupation Adult parasitoid emerge from the pupa e.g. Fopius arisanus attack fruit fly eggs (e.g. ceratitis capitate)
51 Life-stages attacked Larva parasitoids Complete their development in the larval stage of the host Cotesia rubecula Parasitize 1 st instar (Baraconidae) Pieris rapae Small cabbage white butterfly
52 Life-stages attacked Larval-pupal parasitoids Deposit it s egg in or on the host larva Parasitoid larva completes development in host pupa Adult parasitoid emerge from the larva Picture by Yoav Gazit e.g. Diachasmimorpha kraussi attack the fruit fly Larval-adult parasitoids Deposit it s egg in or on the host larva Bactrocera latifrons Parasitoid larva completes development and kills host adult *rare in nature
53 Life-stages attacked Pupal parasitoids Complete their development in the host pupa Plutella xylostella Diadromus collaris (Ichneumonidae) Diamondback moth
54 Parasitoids as natural enemies Hymenoptera Diptera Leopidoptera Chalcidoidae Ichneumonidae Aphelinidae Braconidae Tachinidae Epipyroptera Trichogrammatidae Encytidae Mymaridae Eulophidae
55 Parasitoids as natural enemies Hymenoptera Chalcidoidae Ichneumonidae Trichogrammatidae Braconidae Aphelinidae Encytidae Phylum: Arthropoda Class: Insecta Order: Hymenoptera Super-Family: Chalcidoidea More than 30 species Important for biological control aphids Mymaridae Eulophidae Egg parasitoids whiteflies
56 Parasitoids as natural enemies Hymenoptera Chalcidoidae Ichneumonidae Trichogrammatidae Braconidae mealybugs Phylum: Arthropoda Class: Insecta Order: Hymenoptera Super-Family: Chalcidoidea Aphelinidae Encytidae aphids Mymaridae Eulophidae Egg parasitoids whiteflies Armoured scale insect
57 Encarsia formosa Used in BC of whitefly since 1972 Order: Hymenoptera Super-family: Chalcidoidea Family: Aphelinidae Skilled in finding whitefly patches Faster development than that of whiteflies (27 vs. 32 days) Encarsia formosa Preferred species Trialeurodes vaporariorum Greenhouse whitefly Bemisia tabaci Tobacco whitefly
58 Encarsia formosa o Females prefer to oviposit in 3 rd 4 th instar nymphs Super-family: Chalcidoidea Family: Aphelinidae o Larva develops in the 4 th instar of the host o Dark parasitized pupa o Adult emerge from the pupa Larval-pupa parasitoid o Adult feed on honeydew & larvae, i.e. host feeding
59 Eretmocerus eremicus Used in BC of whitefly since 1994 Ectoparasitoid Order: Hymenoptera Super-family: Chalcidoidea Family: Aphelinidae Female may lay eggs under already parasitized larvae (super-parasitism) E. eremicus More efficient than E. formosa Eretmocerus Mundus Native to the mediterranean Bemisia tabaci Tobacco whitefly Exclusively parasitize B. tabaci Used in BC of whitefly since 2002 E. mundus Trialeurodes vaporariorum Greenhouse whitefly
60 Aphelinus abdominalis Endoparasitoid of various sp. Order: Hymenoptera Super-family: Chalcidoidea Family: Aphelinidae The egg is injected to the underside of the aphid Wasp larvae develops inside the aphid and kills it when it pupates Host feeding on small nymphs Macrosiphus sp. Potato aphid Used in BC since 1993 Aphid mummies
61 Leptomastix dactylopii Specialist parasitoid Order: Hymenoptera Super-family: Chalcidoidea Family: Encyrtidae Endoparasitoid Female oviposit in 3 rd instar Larva consume the mealybug Pupate inside the dead mealybug Efficient searching behaviour Control pest at low densities Citrus mealybug Planococcus citri
62 Trichogramma brassicae Egg parasitoid of moths Order: Hymenoptera Super-family: Chalcidoidea Family: Trichogrammatidae 2-3 eggs are laid in each moth egg Wasp larva pupate inside the moth egg Used against the corn borer
63 Anagrus atomus Family of egg parasitoids Order: Hymenoptera Super-family: Chalcidoidea Family: Mymaridae Parasitize leafhopper eggs Enters the glasshouse naturally Not sufficient for effective control Empoasca vitis
64 Diglyphus isaea Ectoparasitoid Order: Hymenoptera Super-family: Chalcidoidea Family: Eulophidae Parasitize many sp. of leafminers Egg laid near paralayzed leafminer larva Larva pupates in the dead mine Host feeding Released to control leafminers in glasshouses, used since 1984 Tomato leafminer Liriomyza bryoniae
65 Aphid parasitoids 3 important Aphidius species Order: Hymenoptera Super-family: Ichneumonoidea Family: Braconidae A. colemani A. ervi A. matricariae Aphelinus abdominalis Aphis spp. Aulacorthum solani Aulacorthum spp. Myzus spp. Macrosiphum euphobiae Myzus persicae Macrosiphum spp. Commercially used for biological control Efficient at low densities Occur naturally Myzus spp. Commercially used for biological control Host feeding Glasshouse A. solani potato aphid M. euphobiae Potato aphid Aphis gossypii Cotton aphid
66 Aphedius colemani o Rapid population growth o Female lay >300 eggs o Parasitize nymphs & adult Order: Hymenoptera Super-family: Ichneumonoidea Family: Braconidae Egg o Cocoon inside the aphid cuticle Wasp emerge Wasp presence Secretion of warning substance larva Drop to the ground Some aphids die Adds to Biological control mummy with pupa Aphid mummy
67 Hyper-parasitoids o Parasitoids on aphid parasitoids o Serious threat to aphid control Order: Hymenoptera Super-family: Ceraphronoidea Family: Megaspilidae Dendrocerus carpenteri Ectoparasitoid of 4 th instar larva or pupa D. Carpentri larva eats Aphidius larvae from the outside & pupates D. carpenteri lay the egg next to Aphidius larva Aphidius larva Hyper-parasitoid emerge from the mummy Alloxysta spp. lay the egg inside the Aphidius larva
68 Opius pallipes & Dacnusa sibirica Endoparasitoids of leaf-miners Order: Hymenoptera Super-family: Ichneumonoidea Family: Braconidae Fast population growth than leaf-miners Egg-pupa parasitoids (prefer 1 st, 2 nd instar) Larva reach full development after leaf-miner pupation Super-parasitism occur, only 1 wasp will emerge D. sibirica used commercially D. sibirica O. pallipes
69 Opiinae o Endoparasitoids of fruit-flies (Tephritidae) Family: Braconidae Subfamily: Opiinae o Fruit fly egg is laid inside the fruit, the larva develop within, pupate on the ground o Wasps lay egg inside the egg or larva Fopius arisanus Bactrocera tryoni Ceratitis capitata o Wasp larva develop in the larva & pupa o Adult wasp emerge from the fly s pupa Introduced & established in IL Not sold commercially Diachasmimorpha kraussii
70 Parasitoid flies Large family of parasitoid flies Order: Diptera Family: Tachinidae Attack larvae of Lepidoptera & Coleoptera Egg deposited next to the host Maggot ingested with the leaf by caterpillar Maggot develops inside Voria ruralis maggot Pupate inside the host, killing the caterpillar Adult fly emerge
71 Entomopathogenic nematodes Nematodes are simple round-worms Colourless, un-segmented, lacking appendages Free-living, predaceous or parasitic Phylum: Nematoda Class: Chromadorea Order: Rhabditidae Microbial pathogens Entomopathogenic nematodes Predators Parasitoids Lethal to many insect pests, but safely applied Kill pest within hours Photo: Y. Wang
72 Nematode life cycle 2 genera used in BC: Steinernema Heterorhabditis Juvenile search for host Penetrate through body cavity Release symbiotic bacteria Feed on bacteria & liquefied host Develop & reproduce in the host Infective juveniles emerge Nematode-Bacterium complex
73 Symbiotic relationship with bacteria Bacterial Chamber Infective Juveniles Heterorhabditis Bacteriophora Donald Danforth Plant Science Center Curtesy of Roy Kaspi
74 Biological control Marketed world wide, against a broad range of pests Steinernema carpocapsae Effective against lepidopteran & coleoptera larva Sit-&-wait forager, called Ambusher Effective against highly mobile surface insects Heterorhabditis bacteriophora Active forager, called Cruiser Effective against sedentary insects White grub (larva of June beetle) Photo: Ganpati Jagdale
75 Conclusion Many groups are involved in biological control Efficient BCA are both generalists and specialists Effective biological control is cheap, safe and may hold for many years Success depends on understanding the pest-natural enemy interactions
76 Acknowledgments Photo: Y. Gazit Dr. Roy Kaspi Prof. Moshe Coll Yaniv, Assaf & Ayala for babysitting Most material taken from: Malais, M.H. & Ravensberg, W.J. Knowing and recognizing, the biology of glasshouse pests and their natural enemies. Koppert Biological Systems
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