BioControl

pp 1–21

Biological control using invertebrates and microorganisms: plenty of new opportunities

  • Joop C. van Lenteren
  • Karel Bolckmans
  • Jürgen Köhl
  • Willem J. Ravensberg
  • Alberto Urbaneja
Open Access
Article

Abstract

In augmentative biological control (ABC), invertebrate and microbial organisms are seasonally released in large numbers to reduce pests. Today it is applied on more than 30 million ha worldwide. Europe is the largest commercial market for invertebrate biological control agents, while North America has the largest sales of microbials. A strong growth in use of ABC, particularly of microbial agents, is taking place in Latin America, followed by Asia. The current popularity of ABC is due to (1) its inherent positive characteristics (healthier for farm workers and persons living in farming communities, no harvesting interval or waiting period after release of agents, sustainable as there is no development of resistance against arthropod natural enemies, no phytotoxic damage to plants, better yields and a healthier product, reduced pesticide residues [well below the legal Maximum Residue Levels (MRLs)], (2) professionalism of the biological control industry (inexpensive large scale mass production, proper quality control, efficient packaging, distribution and release methods, and availability of many (>440 species) control agents for numerous pests), (3) a number of recent successes showing how biological control can save agricultural production when pesticides fail or are not available, (4) several non-governmental organizations (NGOs), consumers, and retailers demanding pesticide residues far below the legal MRLs, and (5) policy developments in several regions of the world aimed at reduction and replacement of synthetic pesticides by more sustainable methods of pest management. We are convinced, however, that ABC can be applied on a much larger area than it is today. We plead in the short term for a pragmatic form of agriculture that is adaptable, non-dogmatic and combines the sustainability gain from all types of agriculture and pest management methods. We then propose to move to “conscious agriculture”, which involves participation of all stakeholders in the production and consumer chain, and respects the environment and resource availability for future generations. Were “conscious agriculture” to be considered a serious alternative to conventional farming, ABC would face an even brighter future.

Keywords

Augmentative biological control Pest control policies Benefits of biological control Market developments in biological control Worldwide use of biological control Integrated pest management Conscious agriculture 

Introduction

Politicians, policy makers, retailers, consumers, growers and grower organizations are increasingly asking for and speaking about biological control. Hardly a day passes during which we, the authors of this paper, do not receive a question on how to control a certain pest, disease or weed, where to obtain biological control agents, and how to stimulate use of this environmentally safe pest management method. The European Union (EU) has been advocating the use of biological control since 2009 in its Sustainable Use of Pesticides Directive (EC 2009). The President of China recently launched a “National research program on reduction in chemical pesticides and fertilizers in China” involving more than 340 million US$, indicating a need for the development and application of non-chemical control methods. Together, the authors of this paper have been working in the field of augmentative biological control (ABC) for more than 150 years. We noted a hesitant start to ABC in the 1970s, then a burst of activity took place over the next 25 years. During the first decade of the twenty-first century fewer new biological control agents came to the market, but during the second decade we again experienced a new phase with strong growth in both the development of new agents and a market for biological control (van Lenteren 2012; Tables 1, 2 and 3 in this paper).
Table 1

Worldwide use of major augmentative biological control programs (after van Lenteren and Bueno 2003), with updates and supported with references when large differences in areas under control existed between 2003 and 2016

Natural enemy

Pest and crop

Area under control (in ha)

Trichogramma spp.

Lepidopteran pests in vegetables, cereals, cotton

10 million, former USSRa

Trichoderma spp.

Soil diseases various crops

5 million, Brazil, Europeb

Trichogramma spp.

Lepidopteran pests in various crops, forests

4 million, Chinac

Cotesia spp.

Sugarcane borers

3.6 million, South America, Chinad

Metarhizium anisoplae

Lepidopteran pests in sugar cane

2 million, Brazile

Trichogramma spp.

Lepidopteran pests in corn, cotton, sugarcane, tobacco

1.5 million, Mexico

Trichogramma spp.

Lepidopteran pests in cereals, cotton, sugarcane, pastures

1.2 million, South America

AgMNPV

Soybean caterpillar in soybean

1 million, Brazil

Beauvaria bassiana

Coffee berry borer in coffee, whitefly in several crops

1 million, Brazilf

Entomopathogenic fungi

Coffee berry borer in coffee

0.55 million, Colombiag

Trichogramma spp.

Lepidopteran pests in cereals and rice

0.3 million, SouthEast Asia

Trichogramma spp.

Lepidopteran pests in sugar cane and tomato

0.3 million, NorthEast Africa

Predatory mites

Spider mites in greenhouses, fruit orchards, tea and cotton

0.07 million Chinah

Trichogramma spp.

Ostrinia nubilalis in corn

0.05 million, Europe

Orgilus sp.

Pine shooth moth, pine plantations

0.05 million, Chile

>30 spp. of nat. enemies

Many pests in greenhouses and interior plant-scapes

0.05 million, worldwide

Egg parasitoids

Soybean stinkbugs in soybean

0.03 million, South America

Five spp. of nat. enemies

Lepidoptera, Hemiptera, spider mites in orchards

0.03 million, Europe

aRecent data about use of Trichogramma in Russia were not available

bBettiol W and Pedrazzoli D, personal communication 2016

cLiu et al. (2014)and Wang et al. (2014)

dParra JRP and Pedrazzoli D, personal communication 2016

eBettiol W and Pedrazzoli D, personal communication 2016

fBettiol W and Parra JRP, personal communication 2016

gAristizabal et al. (2016)

hYang et al. (2014)

Table 2

Additional natural enemy species to the table of van Lenteren (2012), “Commercial availability of invertebrate natural enemies used worldwide in augmentative biological control, with region of use, year of first use and market value.”

Natural enemy

Classification

Region where usedb

Target(s)

Year of first use

Market valuea

Adalia spp.

Coleoptera

Latin America

Aphids

1941

M

Ageniaspis citricola

Hymenoptera

Latin America

Lepidopterans

1998

M

Allotropa convexifrons

Hymenoptera

Europe

Pseudococcids

2005

S

Allotropa musae

Hymenoptera

Europe

Pseudococcids

2006

S

Amblydromalus limonicus

Acari

Europe

Thrips, whiteflies, tarsonomids

2013

L

Amblyseius aizawai

Acari

Asia

Mites

1992

M

Amblyseius longispinosus

Acari

Asia

Mites

1990

S

Amblyseius makuwa

Acari

Asia

Mites

1991

S

Amblyseius mckenziei

Acari

Europe

Mites

1985

S

Amblyseius nicholsi

Acari

Asia

Mites in citrus

1980

L

Amblyseius spp.

Acari

Australia

Mites in citrus

1990

L

Anagyrus kamali

Hymenoptera

Latin America

Pseudococcids

1990

S

Anagyrus sinope

Hymenoptera

Europe

Pseudococcids

2006

S

Anaphes nitens

Hymenoptera

Europe

Coleopterans

1995

S

Anastatus japonicus

Hymenoptera

Asia

Hemipterans

1970

L

Anastatus sp.

Hymenoptera

Asia, Australia

Hemipterans

2010

S

Anastatus tenuipes

Hymenoptera

North America

Cockroaches

1970

S

Androlaelaps casalis

Acari

Europe

Mites on vertebrates

2008

M

Anisopteromalus calandrae

Hymenoptera

Europe, North America

Coleopterans

1990

S

Aphidius sp.

Hymenoptera

Latin America

Aphids

1980

S

Billaea claripalpis

Diptera

Latin America

Lepidopterans

1976

S

Bracon brevicornis

Hymenoptera

Europe

Lepidopterans

2000

S

Cephalonomia tarsalis

Hymenoptera

Europe

Coleopterans

1995

S

Ceraeochrysa cincta

Neuroptera

Latin America

Aphids

1990

S

Ceraeochrysa smithi

Neuroptera

Latin America

Aphids

1995

S

Cheyletus eruditus

Acari

Europe

Vertebrate mites

2004

S

Chouioia cunea

Hymenoptera

Asia

Lepidopterans

2005

M

Chrysoperla asoralis

Neuroptera

Latin America

Aphids

1990

S

Chrysoperla cinta

Neuroptera

Latin America

Aphids

1990

S

Chrysoperla comanche

Neuroptera

North America

Aphids

1990

M

Chrysoperla lucasina

Neuroptera

Europe

Aphids

1995

M

Chrysoperla (=Chrysopa) sinica

Neuroptera

Asia

Aphids, lepidopterans

2000

M

Coccidophilus citricola

Coleoptera

Latin America, Europe

Diaspidids

1982

S

Coccidoxenoides peregrinus

Hymenoptera

North and Latin America

Diaspidids, pseudococcids

2006

S

Comperia merceti

Hymenoptera

North America

Cockroaches

1980

S

Copidosoma sp.

Hymenoptera

Latin America

Lepidopterans

1995

S

Cotesia marginiventris

Hymenoptera

North America

Lepidopterans

1990

S

Cotesia plutellae

Hymenoptera

North America

lepidopterans

1995

M

Cryptolaemus montrouzieri

Coleoptera

Europe, South America

Mealybugs

1927

M

Cycloneda limbifer

Colecoptera

Europe

Aphids

1990

S

Diachasmimorpha longicaudata

Hymenoptera

Latin America

Dipterans

1990

M

Dibrachys cavus

Hymenoptera

Europe

Dipterans

1990

S

Dirhinus giffardii

Hymenoptera

Latin America

Dipterans

1990

S

Elasmus albipennis

Hymenoptera

Europe

Lepidopterans

1995

S

Encarsia perniciosi

Hymenoptera

Europe

Scales

1932

L

Encarsia sp.

Hymenoptera

Latin America

Whiteflies

1995

S

Ephedrus cerasicola

Hymenoptera

Europe

Aphids

2008

L

Ephedrus plagiator

Hymenoptera

Europe

Aphids

2010

M

Eretmocerus hayati

Hymenoptera

Australia

Whiteflies

2006

M

Eriopsis connexa

Coleoptera

Latin America

Coccids, Aphids, hemipterans

2000

S

Eucanthecona furcellata

Hemiptera

Asia

Aphids, lepidopterans

1996

S

Euseius gallicus

Acari

Europe

Thrips, whitefly

2013

M

Euseius ovalis

Acari

Europe

Thrips, whitefly

2008

M

Euseius stipulatus

Acari

Europe, South America

Mites

2006

M

Forficula sp.

Dermaptera

Asia

Lepidopterans

2010

S

Galendromus (Metaseiulus) annectens

Acari

North America

Mites

1990

M

Galendromus (Metaseiulus) helveolus

Acari

North America

Mites

1999

S

Galendromus (Metaseiulus) pyri

Acari

North America

Mites

1995

L

Galeolaelaps gillespieii

Acari

North America

Dipterans, thrips

2010

L

Geocoris punctipes

Hemiptera

North and Latin America

Lepidopterans, whiteflies

2000

S

Gynaeseius liturivorus

Acari

Asia

Thrips, whitefly

2013

M

Habrobracon sp.

Hymenoptera

Latin America

Lepidopterans

1986

S

Haplothrips brevitubus

Thysanoptera

Asia

Thrips

2010

S

Heterorhabditis indica

Nematoda

North America

Coleopterans, dipterans

2000

S

Hydrotaea aenescens

Diptera

Europe, North America

Dipterans

2000

S

Lariophagus distinguendus

Hymenoptera

Europa

Coleopterans

1995

S

Leis (Harmonia) dimidiata

Coleoptera

Europe

Aphids

1995

S

Leminia biplagiata

Coleoptera

Asia

Aphids, whiteflies

1998

S

Leptomastix algirica

Hymenoptera

Europe

Pseudococcids

2011

S

Leptopilina heterotoma

Hymenoptera

Europe

Dipterans

2007

S

Lydella jalisco

Diptera

Latin America

Lepidopterans

1996

S

Macrocentrus prolificus

Hymenoptera

Latin America

Lepidopterans

2005

S

Mallada basalis

Neuroptera

Asia

Aphids, thrips, etc.

2000

M

Mantis religiosa

Mantodea

North America

Many pests

1970

S

Megastigmus brevivalvus

Hymenoptera

Australia

Hymenopterans

1995

S

Megastigmus trisulcus

Hymenoptera

Australia

Hymenopterans

1995

S

Menochilus sexmaculatus

Coleoptera

Asia

Aphids, whiteflies

2010

S

Metagonistylum minense

Diptera

Latin America

Lepidopterans

1980

S

Micromus variegatus

Neuroptera

North America

Aphids

2010

L

Necremnus artynes

Hymenoptera

Europe

Lepidopterans

2010

S

Neodryinus typhlocybae

Hymenoptera

Europe

Planthoppers

2007

S

Neoseiulus (Amblyseius) barkeri

Acari

Europe, Latin America

Thrips

1981

S

Neoseiulus longispinosus

Acari

Latin America

Mites

2005

S

Nephus quadrimaculatus

Coleoptera

Europe

Aphids, pseudococcids

2005

S

Olla abdominalis (=v-nigrans)

Coleoptera

North and Latin America

Aphids, hemipterans

1990

S

Orius sauteri

Hemiptera

Asia

Aphids, mites, thrips,

2005

M

Orius vicinus

Hemiptera

New Zealand

Thrips, aphids, mites

2010

M

Pentalitomastix plethoricus

Hymenoptera

North America

Lepidopterans

1980

S

Peristenus relictus

Hymenoptera

North America

Hemipterans

2001

L

Podisus sp.

Hemiptera

Latin America

Lepidopterans

1985

S

Praon sp.

Hymenoptera

Latin America

Aphids

1980

S

Propylaea japonica

Coleoptera

Asia

Aphids

2014

S

Propylaea quatuordecimpunctata

Coleoptera

Europe

Aphids

1995

S

Scymnus loewii

Coleoptera

New Zealand

Aphids

1995

S

Sphaerophoria rueppellii

Diptera

Europe

Aphids

2015

S

Stagmomantis carolina

Mantodea

North America

Many pest species

1990

S

Steinernema scapterisci

Nematoda

North America

Orthopterans

1990

S

Stethorus punctipes

Coleoptera

North America

Mites

1980

S

Stethorus sp.

Coleoptera

Latin America

Mites

1995

S

Sympherobius barberi

Neuroptera

North America

Pseudococcids, aphids, etc.

1980

L

Sympherobius maculipennis

Neuroptera

Latin America

Pseudococcids

1990

S

Sympherobius sp.

Neuroptera

Latin America

Whiteflies

1995

S

Synopeas sp.

Hymenoptera

Latin America

Dipterans

1990

S

Tamarixia radiata

Hymenoptera

Latin America

Psyllids

2010

L

Tamarixia triaozae

Hymenoptera

North and Latin America

Psyllids

2001

L

Telenomus podisi

Hymenoptera

Latin America

Hemipterans

2004

M

Telenomus sp.

Hymenoptera

Latin America

Lepidopterans

1990

S

Tenodera aridifolia sinensis

Mantodea

North America

Many pest species

1990

S

Tetrastichus hagenowi

Hymenoptera

Asia

Cockroaches

1980

S

Tetrastichus howardii

Hymenoptera

Latin America

Lepidopterans

1995

S

Thyphiodromus pyri

Acari

Latin America

Mites

2000

M

Transeius (=Amblyseius) montdorensis

Acari

Europe

Thrips, whiteflies, tarsonomids

2004

S

Trichogramma achaeae

Hymenoptera

Europe

Lepidopterans

2012

M

Trichogramma bactrae

Hymenoptera

Latin America, Asia

Lepidopterans

1980

M

Trichogramma confusum (=chilonus)

Hymenoptera

Asia, Australia

Lepidopterans

1970

L

Trichogramma embryophagum

Hymenoptera

Europe

Lepidopterans

1994

M

Trichogramma euproctidis

Hymenoptera

Europe

Lepidopterans

1960

M

Trichogramma fuentesi

Hymenoptera

Latin America

Lepidopterans

1990

S

Trichogramma japonicum

Hymenoptera

Asia

Lepidopterans

1990

S

Trissolcus basalis

Hymenoptera

Latin America

Hemipterans

1995

S

Typhlodromus occidentalis

Acari

Australia

Mites

1970

M

Wollastoniella rotunda

Hemiptera

Asia

Thrips

2005

S

Xenostigmus bifasciatus

Hymenoptera

Latin America

Aphids

2002

S

Xylocoris flavipes

Hemiptera

North America

Coleopterans

2000

S

A table listing all species used in biological control of invertebrates is provided as Supplementary electronic information

aMarket value: L large (hundred thousand to millions of individuals sold per week), M medium (ten thousand to a hundred thousand individuals sold per week), S small (hundreds to a few thousands individuals sold per week) In case of doubt, when numbers sold per week could not be estimated from published material, the market value was rated as S

bAfrica North = North of Sahara; Africa South = South of Sahara; North America = Canada + USA; Latin America = the Caribbean, Central and South America

Table 3

Registered microbial biological control agents for augmentative biological control in Australia (AUS), Brazil (BR), Canada (CA), European Union (EU), Japan (J), New Zealand (NZ) and United States of America (USA)

Microorganisma

Typeb of organism

Country/region where approved

Target(s)

Adoxophyes orana GV V-0001

V

EU, J

Summer fruit tortrix

Agrobacterium radiobacter

B

NZ (1975)

Crown gall

Agrobacterium radiobacter K1026

B

USA

Crown gall

Agrobacterium radiobacter K84

B

CA, J, USA

Crown gall

Alternaria destruens 059

F

USA

Cuscuta spp. (dodder)

Ampelomyces quisqualis AQ10

F

EU, USA

Powdery mildew

Anagrapha falcifera NPV

V

USA

Anagrapha falcifera

Anticarsia gemmatalis NPV

V

BR

Anticarsia gemmatalis

Aspergillus flavus NRRL 21882

F

BR, USA

Aspergillus flavus mycotoxine

Aspergillus flavus AF36

F

USA

Aspergillus flavus mycotoxine

Aureobasidium pullulans DSM 14940 and DSM 14941

Y

EU, CA

Bacterial and fungal flower and foliar diseases

Autographa californica NPV

V

CA

Autographa californica

Bacillus amyloliquefaciens (formerly B. subtilis) MBI 600

B

CA, J, EUc, NZ (2009, 2012), USA

Seed treatment, soil borne diseases

Bacillus amyloliquefaciens AH2

B

EUc

Fungal soil diseases

Bacillus amyloliquefaciens AT-332

B

J

Botrytis, powdery mildew

Bacillus amyloliquefaciens bs1b

B

NZ (2010)

Foliar diseases

Bacillus amyloliquefaciens PTA-4838

B

USA

Nematodes

Bacillus amyloliquefaciens ssp. plantarum (syn. Bacillus subtilis var. amyloliquefaciens) D747

B

CA, EU, J, NZ (2010)

Seedling fungal pathogens

Bacillus cereus BP01

B

USA

Foliar plant growth regulator

Bacillus firmus i-1582

B

CA, EU, NZ (2016)

Nematodes

Bacillus licheniformis SB3086

B

USA

Fungal foliar diseases

Bacillus mycoides J CX-10244

B

CA, USA

Cercospora leaf spot on sugar beet

Bacillus popilliae

B

USA

Japanese beetle

Bacillus pumilus GB34

B

USA

Root diseases of soy beans

Bacillus pumilus QST 2808

B

BR, EU, USA

Fungal foliar diseases

Bacillus subtilis ATCC 6051

B

NZ (2012)

Fungal foliar diseases

Bacillus subtilis GB03

B

CA, USA

Fungal diseases

Bacillus subtilis HAI-0404

B

J

Foliar diseases

Bacillus subtilis IAB/BS03

B

EUc

Foliar fungal and bacterial diseases

Bacillus subtilis KTSB

B

NZ (2008)

Foliar diseases

Bacillus subtilis QST 713

B

BR, CA, EU, J, NZ (2001), USA

Fungal foliar diseases

Bacillus subtilis var. amyloliquefaciens FZB24

B

CA, EUc, USA

Fungal foliar diseases

Bacillus subtilis Y 1336

B

J

Botrytis, powdery mildew

Bacillus thuringiensis EG-7826

B

BR

Lepidopteran caterpillars

Bacillus thuringiensis BMP 123

B

BR

Lepidopteran caterpillars

Bacillus thuringiensis CryC encapsulated in killed Pseudomonas fluorescens

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis CrylA(c) and CrylC in killed Pseudomonas fluorescens

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis EG 2348

B

BR, EU

Lepidopteran caterpillars

Bacillus thuringiensis SA-11

B

BR, CA, EU

Lepidopteran caterpillars

Bacillus thuringiensis SA-12

B

BR, CA, EU

Lepidopteran caterpillars

Bacillus thuringiensis Serotype H-14

B

CA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai

B

CA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai

B

AUS (2000)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai ABTS-1857

B

EU, NZ (1999)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai NB200

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai GC-91

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai GC-91

B

BR, EU

Lepidopteran caterpillars

Bacillus thuringiensis ssp. aizawai/kurstaki

B

NZ (1995)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. galleriae SDS-502

B

CA

Beetles

Bacillus thuringiensis ssp. israelensis

B

USA

Mosquitoes

Bacillus thuringiensis ssp. israelensis EG2215

B

USA

Mosquitoes

Bacillus thuringiensis ssp. israeliensis (serotype H-14) AM65-52

B

CA, EU

Mosquitoes

Bacillus thuringiensis ssp. kurstaki

B

AUS (1994), BR, EU, J, NZ, USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki ABTS 351

B

EU

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki PB 54

B

EU

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki (ALL STRAINS)

B

CA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki 3a,3b var SA-12

B

AUS (1996)

Cotton bollworm

Bacillus thuringiensis ssp. kurstaki BMP123

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki EG

B

BR

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki EG2348

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki EG2371

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki EG7826

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki EG7841

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis kurstaki evb-113-19

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki encapsulated in killed Pseudomonas fluorescens

B

USA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki h-3a,3b hd1

B

NZ (1996)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki h-3a,3b, hd 263

B

NZ (2000)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki h-3a,3b, SA-11

B

NZ (1995)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki HD-1

B

AUS (2000), BR, CA

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki SA-11

B

AUS (2008)

Lepidopteran caterpillars

Bacillus thuringiensis ssp. kurstaki SA-12

B

AUS (2005)

Cotton bollworm

Bacillus thuringiensis ssp. san diego encapsulated in killed Pseudomonas fluorescens

B

USA

Beetles

Bacillus thuringiensis ssp. tenebrionis NB 176

B

CA, EU

Beetles

Beauveria bassiana 147

F

EUc

Red palm weevil, soft bodied insects

Beauveria bassiana 447

F

USA

Ants

Beauveria bassiana ANT-03

F

CA

Soft bodied insects

Beauveria bassiana ATCC 74040

F

EU, NZ (2013), USA

Spidermites, whitefly, thrips, aphids

Beauveria bassiana CG 716

F

BR

Whitefly, spidermites, beetles

Beauveria bassiana GHA

F

CA, EU, J

Whitefly, thrips, aphids

Beauveria bassiana HF23

F

CA

Soft bodied insects

Beauveria bassiana IBCB 66

F

BR

Whitefly, spidermites, beetles

Beauveria bassiana IMI389521

F

EUc

Beetles in stored grain

Beauveria bassiana k4b1

F

NZ (2005)

Thrips

Beauveria bassiana k4b3

F

NZ (2009)

Sucking insects

Beauveria bassiana NPP111B005

F

EUc

Banana weevil, red palm weevil

Beauveria bassiana PL63

F

Br

Whitefly, spidermites, beetles

Beauveria bassiana PPRI 5339

F

CA, EUc

Soft bodies insects, caterpillars

Beauveria brongniartii NBL 851

F

J

Long horn beetle etc.

Burkholderia (Pseudomonas) cepacia M54

Y

USA

Damping off diseases, nematodes

Burkholderia (Pseudomonas) cepacia J82

Y

USA

Damping off diseases, nematodes

Candida oleophila isolate I-182

Y

USA

Post-harvest fungicide

Candida oleophila O

Y

EU

Post-harvest fungicide

Chondrostereum purpureum PFC 2139

F

CA, USA

Inhibits sprouting/regrowth of shrubs and trees

Chromobacterium subtsugae PRAA4-1T

B

EUc

Various insects and mites

Clavibacter michiganensis ssp. michiganensis bacteriophage

BP

CA

Clavibacter michiganensis ssp. michiganensis

Colletotrichum gloeosporioides f. sp. aeschynomene

F

USA

Northern jointvetch (Aeschynomene virginica)

Condylorrhiza vestigialis NPV

V

BR

Condylorrhiza vestigialis (Braz. poplar moth)

Coniothyrium minitans CON/M/91-08

F

CA, EU, USA

Sclerotinia spp.

Cydia pomonella GV (Mexican strain and various other strains)

V

AUS (2010), CA, EU, NZ (1999), USA

Codling moth

Cydia pomonella GV V22 (CPGV-V22)

V

AUS (2015)

Codling moth

Erwinia carotovora CGE234

B

J

Bacterial soft rot in potato and vegetables

Fusarium sp. L13

F

EUc

No information found about target

Gliocladium catenulatum J1446

F

CA, EU, USA

Foliar fungal diseases

Gliocladium virens G-21

F

USA

Damping off diseases

Helicoverpa armigera NPV

V

AUS (2002), Br, EU, USA

Helicoverpa ssp.

Helicoverpa zea NPV

V

AUS (1999), Br, USA

Helicoverpa ssp.

Homona magnanima GV

V

J

Tea leaf roller, tTea tortorix

Isaria fumosorosea Apopka 97 (formely Paecilomyces fumosoroseus)

F

EU, J, USA

Soft bodied insects

Isaria fumosorosea Fe 9901

F

CA, EU

soft bodied insects

Lactobacillus casei LPT-111

B

CA

Various weeds in lawns

Lactobacillus plantarum BY

B

J

Soft rot

Lactobacillus rhamnosus LPT-21

B

CA

Various weeds in lawns

Lactococcus lactis ssp. cremoris M11/CSL

B

CA

Various weeds in lawns

Lactococcus lactis ssp. lactis LL102/CSL

B

CA

Various weeds in lawns

Lagenidium giganteum

F

USA

Mosquitoes

Lecanicillium lecanii (formerly Verticillium lecanii) K4V1 + K4V2

F

NZ (2012)

Thrips, whitefly, aphids, mealy bug, psyllid and passion vine hopper

Lecanicillium lecanii (formerly Verticillium lecanii) K4V2

F

NZ (2012)

Whitefly, thrips, aphids, passion vine hopper

Lecanicillium muscarium (formerly Verticillium lecanii) Ve6

F

EU, J

Whitefly, thrips

Lymantri dispar NPV

V

CA, USA

Lymantra dispar

Metarhizium anisopliae

F

AUS

Redheaded pasture cockchafer

Metarhizium anisopliae

F

AUS

Greyback canegrub

Metarhizium anisopliae var. acridum

F

AUS

Locusts

Metarhizium anisopliae ESF1

F

USA

Termites

Metarhizium anisopliae IBCB 348

F

Br

Leafhoppers

Metarhizium anisopliae PL 43

F

Br

Leafhoppers

Metarhizium anisopliae SMZ-2000

F

J

Aphids, thrips, whitefly

Metarhizium anisopliae var. anisopliae BIPESCO 5/F52

F

CA, EU, USA

Black vine weevil, thrips

Metschnikowia fructicola NRRL Y-27328

Y

EUc

Post-harvest diseases

Muscodor albus QST 20799

F

USA

Bacteria, fungi, and nematodes

Myrothecium verrucaria dried fermentation solids and solubles

F

USA

Nematodes

Neodiprion abietis NPV

V

CA

Balsam fir sawfly

Neodiprion lecontei NPV

V

CA

Redheaded pine sawfly

Nosema locustae

M

CA, USA

Grasshoppers, locusts, crickets

Orgyia pseudotsugata NPV

V

CA, USA

Ddouglas-fir tussock moth

Paecilomyces lilacinus

F

BR

Root knot nematodes

Paecilomyces lilacinus 251

F

EU

Root knot nematodes

Paecilomyces tenuipes T1

F

J

Whitefly, aphids, powdery mildew

Pantoea agglomerans C9-1

B

CA, USA

Fire blight in apples and pears

Pantoea agglomerans E325

B

CA

Fire blight in apples and pears

Pantoea agglomerans p10c

B

NZ (2006)

Fire blight in apples and pears

Pasteuria nishizawae Pn1

B

CA, EUc, USA

Nematodes (Heterodera, Globodera)

Pepino mosaic virus CH2 isolate 1906

V

EU

Pepino mosaic virus

Pepino Mosaic Virus isolate VC 1

V

EUc

Pepino mosaic virus

Pepino Mosaic Virus isolate VX 1

V

EUc

pepino mosaic virus

Phlebiopsis gigantea (several strains)

F

EU

Root run (Heterobasidion annosum) in conifers

Phlebiopsis gigantea VRA 1992

F

CA

Root run (Heterobasidion annosum) in conifers

Phoma macrostoma

F

CA

Broadleaf weeds in turf grass

Phytophthora palmivora MWV

F

USA

Strangler vine (Morenia orderata)

Plodia interpunctella granulosis virus

V

USA

Plodia interpunctella

Pochonia chlamydosporia PC10

F

BR

Nematodes

Pseudomonas aureofaciens Tx-1

B

USA

Fungal diseases in turf grass

Pseudomonas chlororaphis 63-28

B

USA

Pythium spp., Rhizoctonia solani, Fusarium oxysporum

Pseudomonas chlororaphis MA342

B

EU

Seed-borne pathogens on barley and oats

Pseudomonas fluorescens G 7090

B

J

Bacterial and black rot in lettuce/cabbage

Pseudomonas fluorescens 1629RS

B

USA

Frost prevention in fruits, almond, potato, tomato

Pseudomonas fluorescens A506 (syn. 006418)

B

CA, USA

Frost prevention in fruits, almond, potato, tomato

Pseudomonas fluorescens CL145A

B

CA

Zebra mussel

Pseudomonas rhodesiae HAI-0804

B

J

Bacterial diseases in citrus, peach, plum

Pseudomonas sp. DSMZ 13134

B

EU

Rhizoctonia solani in potato

Pseudomonas syringae 742RS

B

USA

Frost prevention in fruits, almond, potato, tomato

Pseudomonas syringae ESC 10

B

CA, USA

Post-harvest diseases in various fruits

Pseudomonas syringae ESC-11

B

USA

Post-harvest diseases in various fruits

Pseudozyma flocculosa PF-A22 UL

F

EUc, USA

Powdery mildew on roses and cucumbers

Puccinia thlaspeos

F

USA

Isatis tinctoria, dyer’s woad

Purpureocilium lilacinum PL 11

F

EUc

Nematodes

Pythium oligandrum M1

F

EU

Fungal diseases in cereals and oil seed rape

Saccharomyces cerevisiae extract hydrolysate

Y

USA

Bacterial diseases

Saccharomyces cerevisiae LAS02

Y

EU

Fungal diseases in fruits

Sclerotinia minor IMI 3144141

F

CA

Dandelion in turf

Serratia entomophila 626

B

NZ (1994)

Grass grubs

Spodoptera exigua NPV

V

EU, USA

Spodoptera exigua (beet army worm)

Spodoptera frugiperda NPV 3AP2

V

USA

Spodoptera frugiperda

Spodoptera littoralis NPV

V

EU

Spodoptera littoralis (cotton leaf worm)

Streptomyces acidiscabies RL-110T

B

CA

Dandelion on turf grass

Streptomyces griseoviridis K61

B

CA, EU, USA

Fungal soil diseases in vegetables, ornamentals

Streptomyces lydicus ATCC 554456

B

NZ (2013)

Soil borne and foliar diseases

Streptomyces lydicus WYEC 108

B

CA, EU, NZ (2009), USA

Soil borne and foliar diseases

Talaromyces flavus SAY-Y-94-01

F

J

Fungal and bacterial diseases

Trichoderma asperellum (formerly T. harzianum) ICC012

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma asperellum (formerly T.viride) T25

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma asperellum (formerly T. harzianum) TV1

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma asperellum SF 04 (URM) 5911

F

BR

Damping off, Sclerotinia sclerotiorum

Trichoderma asperellum T211

F

BR

Damping off, Sclerotinia sclerotiorum

Trichoderma asperellum T34

F

CA, EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma atroviridae SKT-1

F

J

Bacterial seedling blight and grain rot, seedling fungal blight

Trichoderma atroviride (5 strains)

F

NZ (1991)

Wound pathogens

Trichoderma atroviride (formerly T. harzianum) IMI 206040

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma atroviride (formerly T. harzianum) T11

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma atroviride ag1, ag2, ag3, ag5, ag11, ag15

F

NZ (1987)

Wound pathogens

Trichoderma atroviride I-1237

F

EU

Wound pathogens and fungal soil diseases

Trichoderma atroviride lu132

F

NZ (2004)

Foliar diseases

Trichoderma atroviride SC1

F

EU

Wound pathogens

Trichoderma gamsii (formerly T. viride) ICC080

F

EU

Fungal soil diseases in vegetables, ornamentals

Trichoderma hamatum TH382

F

USA

Fungal soil diseases in vegetables, ornamentals

Trichoderma harzianum

F

AUS (2004)

Eutypa dieback in grapes

Trichoderma harzianum KRL-AG2 (syn. T22)

F

CA, EU, USA

Fungal soil diseases in vegetables, ornamentals

Trichoderma harzianum ESALQ-1306

F

BR

Damping off, Sclerotinia sclerotiorum

Trichoderma harzianum IBL F006

F

BR

Damping off, Sclerotinia sclerotiorum

Trichoderma harzianum ITEM 908

F

EU

Soil borne diseases

Trichoderma harzianum T-39

F

USA

Fungal soil diseases in vegetables, ornamentals

Trichoderma polysporum ATCC 20475

F

USA

Wound pathogens

Trichoderma polysporum IMI 206039

F

EU

Botrytis cinerea, Chondrostereum purpureum

Trichoderma stromaticum CEPLAC 3550

F

BR

Witch’s broom

Trichoderma virens G-41

F

CA

Fungal soil diseases in vegetables, ornamentals

Trichoderma viride ATCC 20476

F

USA

Wound pathogens

Typhula phacorrhiza 94671

F

CA

Snow molds in turf

Ulocladium oudemansii U3

F

NZ (2004)

Foliar diseases, Pseudomonas syringae

Verticillium albo-atrum (formerly V. dahliae) WCS850

F

CA, EU, USA

Dutch elm disease

Xanthomonas campestris pv. vesicatoria bacteriophage

BP

USA

Xanthomonas campestris pv. vesicatoria

Simply said, biological control is the use of a population of one organism to reduce the population of another organism. Biological control has been in use for at least 2000 years, but modern use started at the end of the nineteenth century (DeBach 1964; van Lenteren and Godfray 2005). Four different types of biological control are known: natural, conservation, classical, and augmentative biological control (Eilenberg et al. 2001; Cock et al. 2010). Natural biological control is an ecosystem service (Millennium Ecosystem Assessment 2005) whereby pest organisms are reduced by naturally occurring beneficial organisms. This occurs in all of the world’s ecosystems without any human intervention, and, in economic terms, is the greatest contribution of biological control to agriculture (Waage and Greathead 1988). Conservation biological control consists of human actions that protect and stimulate the performance of naturally occurring natural enemies. This form of biological control is currently receiving a lot of attention for pest control. Conservation biological control of plant diseases is focused on the role of the natural microbiome in suppressing plant diseases in soil and crop residues, and of the natural microbiome in and on plants in providing resilience to pest and pathogen infection (Mendes et al. 2011; Weller et al. 2002). In classical biological control, natural enemies are collected in an exploration area (usually the area of origin of the pest) and then released in areas where the pest is invasive, often resulting in permanent pest population reduction and enormous economic benefits (see Cock et al. 2010). As this was the first type of biological control deliberately and widely practiced, it is called “classical” biological control (DeBach 1964). In augmentative biological control (ABC), natural enemies (parasitoids, predators or micro-organisms) are mass-reared for release in large numbers either to obtain immediate control of pests in crops with a short production cycle (inundative biological control) or for control of pests during several generations in crops with a long production cycle (seasonal inoculative biological control) (Cock et al. 2010; Lorito et al. 2010; Parnell et al. 2016; van Lenteren 2012).

This paper is focussed on augmentative biological control (ABC). It has been applied with success for more than 100 years in several cropping systems (Gurr and Wratten 2000; Cock et al. 2010). In this paper, we illustrate (1) the important role ABC is playing today, (2) how many biological control agents are commercially available and against which pests they are applied, (3) in what way ABC can result in cleaner, greener, healthier and more sustainable agriculture through policy measures and regulations, and, finally, (4) the need for a type of agriculture that respects the environment and optimizes use of ecosystem services.

Note: in this paper we often use the word ‘pest’ as defined by FAO/IIPC (1997), which includes animal pests, weeds and diseases.

Where is augmentative biological control currently applied?

Large scale regular releases and mass production of natural enemies means that ABC is often a commercial activity (van Lenteren 2012). ABC is thought to have been used for the first time in China around 300 AD (van Lenteren and Godfray 2005). Modern ABC started in the 1880s with the use of the insect pathogen Metarhizium anisopliae by Metchnikoff in Russia for control of beetles in various crops (MacBain Cameron 1973). Today, ABC is applied in many areas of agriculture, such as fruit and vegetable crops, cereals, maize, cotton, sugarcane, soybean, grapes and many greenhouse crops (Table 1), and is often part of an Integrated Pest Management (IPM) program that provides an environmentally and economically sound alternative to chemical pest control (van Lenteren and Bueno 2003; Cock et al. 2010). Increasingly, seed treatments with microbial biological control agents are also used as a form of ABC (Abuamsha et al. 2011). We estimate that in 2015 ABC was applied on more than 30 million ha worldwide (Table 1).

Since the 1970s, ABC has moved from a cottage industry to professional research and production facilities, as a result of which many efficient agents have been identified, quality control protocols, mass production, shipment and release methods matured, and adequate guidance for farmers has been developed (van Lenteren 2003, 2012; Cock et al. 2010; Ravensberg 2011). In this paper we will not describe the process of collection, evaluation, development of mass production and registration of biological control agents in detail. Information concerning these factors for invertebrate biological control agents can be found in Cock et al. (2010) and for microbial biological control agents in Köhl et al. (2011), Ravensberg (2011) and Parnell et al. (2016). When searching for natural enemies, it is not unusual to find dozens or more species attacking a certain pest, but criteria such as population growth rate, host range, and adaptation to crop and climate can often be used to quickly eliminate clearly inefficient species. The most promising species are compared by using characteristics such as efficacy of pest control, potential environmental risks and economy of mass rearing. For the screening of microbial control agents, large collections of hundreds or thousands of isolates are typically established and high throughput screening assays are increasingly applied to assess important traits such as cold tolerance, metabolite production and efficacy against the target pest.

Important recent successes in the use of ABC include the virtually complete replacement of chemical pesticides by predators (mites and hemipterans) to control thrips and whiteflies on sweet peppers in greenhouses in Spain (Calvo et al. 2012), and hemipteran predators to control new invasive pests like the South American pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) (Urbaneja et al. 2012). These examples show how well biological control with invertebrate biological control agents can function in modern agriculture, and that they can actually save agriculture in large areas that otherwise would have had to terminate vegetable production. Another recent success deals with the importance of microbial control agents. The invasion of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), into Brazil in 2012 caused tremendous damage to corn, cotton, and soy, as pesticides were not effective due to resistance, or were simply not available. Emergency approvals of the entomopathogenic bacterium Bacillus thuringiensis and baculovirus products provided farmers with the only effective control method at the time (Pratissoli et al. 2015).

Europe is still the largest commercial market for ABC with invertebrate biological control agents, which is partly due to political support of biological control within IPM programs (EC 2009), but also due to consumer demand, pressure by NGOs (e.g., Greenpeace 2007) and a well-functioning, highly developed biological control industry. The next largest market is North America, followed by Asia, Latin America, Africa and the Middle East. A strong growth of ABC with arthropods is taking place in Latin America and the same is expected to occur in Asia (Dunham 2015; ResearchandMarkets 2016b). According to the latest marketing reports (e.g., ResearchandMarkets 2016a) North America is now the largest market for biopesticides, followed by Europe.

Commercially available biological control agents

Cock et al. (2010) mentioned 170 species of invertebrate biological control agents that have been used in ABC in Europe. Van Lenteren (2012) provided a list of about 230 species of invertebrate biological control agents that have been used in pest management worldwide, but recognised that this list was not yet complete. Collection of new data in 2016 showed the use of almost 350 natural enemy species (Table in Supplementary electronic information). There are about 500 commercial producers of invertebrate biological control agents worldwide, although most of these employ less than ten people each. Less than ten producers employ more than 50 staff, with the largest producer having about 1400 employees. In addition to commercial producers, there are hundreds of government-owned production units, particularly in China, India and Latin America. Also, and especially in Latin America, some large-scale farmers and growers are involved in producing their own natural enemies. In addition to the species listed in Table 2, invertebrates are commercially produced for biological control of weeds (40 species), for soil improvement (six species), as feed and food (40 species), and as pollinators (ten species). These species are not listed in Table 2.

After predators and parasitoids, microbial biological control agents are the next most commonly used organisms in ABC. As far as we are aware, Table 3 may be the first list published about microbial biological control agents registered worldwide. Although we realize the list is not yet complete, it provides information on about 209 microbial strains from 94 different species commercially available for control of pests. Information we could obtain on registered strains was not always consistent. In some cases agents seem registered without strain information or under different strain identifications for different regions, so that some organisms may be listed more than once in Table 3. Microbial biological control agents are produced by approximately 200 manufacturers, but this is an underestimate as no data are available for China or India (Dunham 2015). There is a great diversity of manufacturers and often they are specialised in one or two types of microorganisms and production methods. The majority of manufacturers are small to medium-sized companies. Recently, large multinational agro-chemical companies are getting involved in the production and marketing of so-called biopesticides, again through the acquisition of small to medium-sized companies. New companies are still founded on a regular basis, and acquisitions and mergers occur frequently. There is a similar trend to consolidation as that which occurred in the seed and chemical pesticides business in the past decades.

Viability of commercial biological control market

Producers of natural enemies are understandably reluctant to provide data about market developments, profit margins and sales volumes. In 2015, the global pesticide market had a value of US$ 58.46 billion (ResearchandMarkets 2016a). The global market of biological control agents (invertebrates and microorganisms) was approximately US$ 1.7 billion in 2015 (Dunham 2015; Dunham W, personal communication 2016), which is less than 2% of the pesticide market. Growth of the market for synthetic pesticides is expected to be between 5 and 6% over the next five years (Research and Markets 2016b), but interestingly, growth of the biological control market has been faster: it showed an annual increase of sales of 10% before 2005 and more than 15% per year since 2005 (Dunham 2015; Dunham W, personal communication 2016). The largest European biological control companies are still getting the main part of their income from sales of invertebrate biological control agents, but the contribution of microbial biological control agents is steadily increasing. Commercial ABC is used in protected crops (e.g., vegetables, ornamentals) and high-value outdoor crops (e.g., strawberries, vineyards), contributing to about 80% of the market value of invertebrate biological control agents. Biological control programs for each of these crops may involve up to 15–20 different species of natural enemies (van Lenteren 2000). The remaining 20% of the market value for natural enemies comes from application of relatively simple, cheap but effective biological control programs often using only one biological control agent (e.g., Trichogramma spp. against lepidopterans in cereals and sugarcane, and Cotesia spp. against lepidopterans in sugarcane). Almost 40% of the income of the European companies originates from invertebrate biological control agents sold for control of thrips, another 30% for control of whitefly, 12% for control of spider mites, 8% for control of aphids, and the remaining 10% for control of various other pests (Bolckmans K, personal communication 2016). Since 2005, predatory mites have contributed enormously to the growth of the market for invertebrate biological control agents as a result of: the (re)discovery of their use for control of whiteflies (Nomikou et al. 2001), finding more efficient species for thrips control (Messelink et al. 2006), the development of techniques to enhance dispersal and establishment of predatory mites in crops (Messelink et al. 2014), and the development of new highly economic production technologies (Bolckmans et al. 2005).

The recent increase in annual market growth for biological control agents is the result of many factors. Compared with synthetic chemical pesticides, ABC agents show important inherent positive characteristics: they are less detrimental to the health of farm workers and persons living in farming communities; they do not have a harvesting interval or re-entry period as do pesticides; they are more sustainable, as there has been no development of resistance against arthropod ABC agents; they do not cause phytotoxic damage to plants and, as a result, most farmers report better yields and healthier crops after switching to biocontrol-based IPM. Increasingly, produce in Europe and North America can only be sold when residue levels are well below the legal MRLs because of retailers demands. In some cases low residue levels give farmers a preferred partnership with retailers who prefer to buy products with less residues. Furthermore, biological control might contribute to considerable reduction in emission of greenhouse gasses in comparison with pesticide use (Heimpel et al. 2013).

In addition to these inherent advantages of biological control, consumers have and will increasingly express concerns about food safety and environmental impact issues in relation to synthetic pesticide use, though they often have no direct way to influence crop protection policies. However, food retailers and supermarkets cleverly exploit this and use these two concerns increasingly in advertising their produce. In many countries, retailers and supermarkets more strongly restrict use of pesticides than do government policies (Buurma et al. 2012), and, particularly in Europe, the effect of NGOs reporting on excess residue levels and illegal use of pesticides has had a positive effect on the use of biological control (e.g., Greenpeace 2007). Adoption of IPM programs in the EU, in which biological control is a cornerstone, has increased interest in and application of ABC (Lamichhane et al. 2017). Concurrently with the adoption of this IPM approach, it was announced that a large number of pesticides were to be legally discontinued and this has also led to requests for ABC solutions. Policy measures such as a strong reduction in use of synthetic pesticides in China have also opened avenues for ABC. A number of other national measures have been shown to stimulate use of ABCs. Examples are fast track and priority registration of low risk pest control agents such as ABC’s similar to the special registration procedure for biopesticides in the USA (EPA 2017), subsidizing biological control agents to growers (several countries in the EU) and application of pesticide levies (e.g., Denmark).

However, ABC, and biological control in general, also face a very serious problem. Pests have been accidentally exported for many years, but at an ever increasing rate (Bacon et al. 2012). Until recently, potential biological control agents could be collected in the country of origin of the pest, evaluated, mass produced and released when an effective agent was found. But today, under the Convention on Biological Diversity (CBD 1993) countries have sovereign rights over their genetic resources and agreements governing the access to these resources and the sharing of benefits arising from their use need to be established between involved parties [i.e., Access and Benefit Sharing (ABS) (Cock et al. 2010)]. This means that currently, permission to sample potential biological control agents can only be granted by the country that has sovereign rights over the genetic resources and collection of new natural enemies has become increasingly difficult or impossible in countries which have first accidentally exported the pest, a situation which seems very unreasonable.

What might boost future use of ABC?

First, we expect that the above-mentioned factors that are responsible for the recent growth of ABC will play an even more important role in the near future, as their influence will spread to other countries and regions worldwide due to support for “greener” agriculture by consumers, NGOs, governments and growers. Another influential issue accelerating use of ABC relates to changing regulations. Regulations should facilitate the use of innovative sustainable solutions resulting in a choice for the ecological best pest control option. This can be realized by fast track registration, priority registration, and use of a combination of comparative assessment of pest control methods together with the substitution principle, through which an environmentally safer pest control method can substitute for a synthetic pesticide (EC 2009). Also zonal authorization (e.g., authorization for all of the EU instead of registration per country), permanent registration (instead of reregistration after 10–15 years) and mutual recognition of registration by member states in the EU are all measures that are likely to result in increased application of microbial biological control, and are now considered for low risk substances including ABC’s in the EU. The changes in registration procedures will result in faster registration of more microbial biological control agents and, logically, in lower product costs. The Environmental Protection Agency (EPA) in the USA is already applying several of the above-mentioned factors related to registration of ABC’s, but the EU is slow in adopting specific criteria and procedures for biological control agents. Development of a specific protocol for registration of microbial biological control agents that will be used locally or worldwide, would be another big step forward in making use of biological control more attractive and accessible for farmers.

Removal of pesticides from the market due to observed health, non-target and environmental effects (e.g., the recent development concerning neonicotinoids; EASAC 2015), the development of resistance that makes pesticides less effective, and the appearance of new pests for which no pesticides are available (e.g., Tuta absoluta invasion in Europe in 2006, Urbaneja et al. 2012) all stimulate use of ABC. Non-governmental organizations (NGOs) have in several cases successfully used information about environmental effects and illegal use of pesticides to initiate a change from chemical to biological control [e.g., in 2005 in the Almeria region in Spain, chemical control of pests in sweet pepper was replaced by biological control in a period of two years (Calvo et al. 2012)]. A very fast change from chemical control to biological control as in sweet peppers in Spain also occurred for other crops in that region. In the 1980s there was a similar drastic change from chemical to biological control in vegetable production in Northwest Europe (van Lenteren 2000), though this was not caused by a pesticide scandal like the one concerning sweet pepper production in Spain (Greenpeace 2007), but by growers recognition of the inherent positive characteristics of biological control mentioned above, and by resistance of several insect pests to conventional chemical pesticides. The development of new and better biological control solutions, improved and more stable formulations for microbial biological control agents and their use as seed treatments, more convenient application methods for invertebrate biological control agents (equipment to release biological control agents in crops, use of drones, etc.) and increasingly stable formulations of microbial biological control agents, have also contributed to growth in uptake of biological control. Interestingly, growers quickly took up the extra knowledge and methods to make biological control a success, and in quite a number of cases came up with new insights and technologies to improve release and establishment of invertebrate biological control agents. They also stimulated researchers and the biological control industry to provide new invertebrate biological control agents for emerging pests. We hope farmer’s organizations will create a new renaissance in crop protection by seeing the many positive sides, including economics, of ABC. In their own interest they should become much more proactive and demand priority and fast track registration of innovative sustainable control methods.

Finally, application of the “true cost” principle for chemical pesticides would strongly increase the market for biological control. Pesticides are subsidized by governments because the industry is not held responsible for human illnesses and deaths as a result of chronic exposure to pesticides, and also does not have to provide the funding to repair damage done to the environment (e.g., reduction of biodiversity, limiting or even preventing the functioning of ecosystem services such as pest and disease control, pollination and cleaning of (drinking) water). Thus, pesticide costs related to harmful effects on human health and the environment are externalized and are actually paid by society, which is unethical and unscrupulous because the pesticide industry only reaps the economic benefits without being responsible for these costs. Benefit-cost ratios of chemical pesticides are usually said to be in the order of 4 when these “external hidden” costs are not taken into account (e.g., Pimentel and Burgess 2014). If true costs were applied to pesticides their benefit-cost ratio would still in most cases be higher than 1, in other cases close to 1, and in some cases even below 1, and, according to Bourguet and Guillemaud (2016) “the profitability of pesticides has, indeed, been overestimated in the past.” Realistic pricing involving true costs would result in much higher costs of chemical pesticides and fairer competition with non-chemical alternative controls. Although hidden costs of pesticides have been documented since the 1980s, they have seldom resulted in an increase of pesticide prices. A first step to true cost pricing would be to apply levies on synthetic pesticides resulting both in higher, thus more realistic pricing, as well as in fairer competition with prices of biological control agents used in IPM programs.

And what next?

Too often the following reasoning is used to justify the use of synthetic pesticides: agriculture has to feed some ten billion people by the year 2050, so we need to strongly increase food production, which can only be achieved with usage of synthetic pesticides. This reasoning is simplistic, erroneous and misleading. Simplistic because it ignores a multitude of other approaches to pest, disease and weed control that we summarize below under IPM, erroneous as sufficient healthy food can be produced without synthetic pesticides (e.g., IPES-Food 2016; Ponisio et al. 2014; UN 2017), and misleading in that it minimizes the importance of a well-functioning biosphere and high biodiversity for the long-term sustainable production of healthy food for a growing human population (De Vivo et al. 2016; Erisman et al. 2016; IPES-Food 2016; Tillman et al. 2012). This short-sighted mercenary attitude might actually result in very serious environmental problems in the near future (e.g., van Bavel 2016). A more sensible approach to food production is to ask ourselves: (1) how can we create a healthy and well-functioning biosphere in which biodiversity is treasured instead of strongly reduced, both because of its necessity for sustainable food production and maintaining a hospitable biosphere for humans (utilitarian approach), as well as because of our ethical responsibility (ethical approach), (2) how can healthy food best be produced in this well-functioning biosphere, and (3) what kind of pest, disease and weed management fits in such a production system.

From the time agriculture developed some 10,000 years ago until only 65 years ago, agriculture was, after periods with slash and burn activities, an holistic activity, based on a systems approach. Farming societies had to design plant production and crop protection programs based on prevention of pests. This true form of IPM included, among others, planning of crop combinations, crop rotation, tillage, use of resistant or tolerant crop cultivars, choice of the right planting and harvesting periods, biological, mechanical and physical control etc. (e.g., Ehler 2006). Due to an understanding of plant genetics, the development of synthetic fertilizers and pesticides, agricultural research changed from an holistic approach to an extremely reductionist science where pests are avoided by a prophylactic approach consisting of calendar sprays or by curative treatments. A total systems approach to agriculture no longer seemed necessary, but this is a short-sighted and dangerous viewpoint and the ever increasing use of synthetic pesticides has resulted in a serious loss of biodiversity (e.g., EASAC 2015), which in turn resulted in prevention or reduction in functioning of the ecosystem services of pest reduction, pollination and water purification (Millennium Ecosystem Assessment 2005). A prophylactic approach is also an exorbitant input of resources with financial consequences of billions of US$ (Costanza et al. 1997; Pimentel and Burgess 2014; Bourguet and Guillemaud 2016).

Lewis et al. (1997) made a plea to return to a system approach based on true IPM. True IPM is a durable, environmentally and economically justifiable system in which pest damage is prevented through the use of natural factors limiting pest population growth, and only—if needed—supplemented with other, preferably non-chemical measures (Gruys, P. in van Lenteren 1993). As stated above, there are many alternatives for synthetic pesticides, and cultural methods together with modern plant breeding and biological control within true IPM programs have been shown to provide excellent yields (e.g., Radcliffe et al. 2009). The fact that more creativity, knowledge and ecological insight are needed to be able to apply such pesticide-free crop management schemes should no longer be an excuse to use unsustainable, environmentally unsafe and toxic synthetic pesticide programs (UN 2017). We are not advocating a dogmatic, one-sided pest control approach, and we also do not support a static holistic approach in which (agro-)ecosystems are seen as non-changing functional units. Instead we propose to combine the sustainability gain from all types of agriculture and pest prevention/control methods, and consider agro-ecosystems as constantly changing systems. In such an approach, we are convinced that ABC can be applied much more than it is today, but we also know it will not solve all pest problems. A seriously neglected form of biological control, conservation biological control, should be the basis of most crop protection programs by providing sufficient invertebrate biological control agents and undisturbed buffering microbiomes in soils and plants when pests invade an agro-ecosystem (Gruys 1982; Blommers 1994; Berendsen et al. 2012). Delaying or preventing sprays will result in the reduction of secondary pests that arise after killing natural enemies of pest organisms. These often cause resurgence problems when synthetic pesticides are used. Host-plant resistance is one of the important cornerstones of IPM and should play a more important role in pest prevention. In IPM we are not dependent on full resistance, often partial host-plant resistance is enough because pest populations develop more slowly and natural enemies can more easily reduce such populations. Both classic and modern plant breeding, including CRISPR-Cas and RNAi, will help us design robust IPM programs. In order to obtain more governmental and public support, we—researchers and practitioners of biological control—will have to collaborate with all stakeholders in pest management to involve them and make them aware of the important economic, environmental, societal and environmental benefits of biological control. Recent experiences in New Zealand, where farmers pushed for and implemented biological control (Hardwick et al. 2016), protected crops in South-eastern Spain (growers and public embraced biological control: Jacas and Urbaneja 2009) and weed control in South Africa (public supported weed biological control in the working for water program: Moran et al. 2005) shows that widely disseminated information about successes of biological control projects result in strong public support and increased government funding.

In conclusion, we see the urgent need for a new type of agriculture that is somewhere between conventional and organic, is flexible and non-dogmatic. We might address it as Conscious Agriculture, a term which we borrowed from the conscious capitalism movement (Mackey and Sissodia 2014). Conscious agriculture involves participation of all stakeholders in the production and consumption chain, and respects the environment and resource availability for future generations. This is in contrast with conventional agriculture which concentrates on profit maximization and externalizing the cost of the harmful effects on human health, society and the environment (Robinson 2007; Erisman et al. 2016). Conscious agriculture fits seamlessly into a “common agricultural and food policy” as recently published in a position paper by Fresco and Poppe (2016). They review societal challenges and options for innovation, and conclude that such a policy should not concentrate on agriculture only, but needs to be developed with participation of all stakeholders, and will help “the entire food chain—from farm to fork, from animal breeding to human food production—to cope with the challenges of the coming decades”. Within conscious agriculture, the first line of crop protection consists of strictly enforced quarantine regulations, prevention of pest development by cultural methods, host-plant resistance, classical and conservation biological control, preventative releases of natural enemies (an aspect of ABC) and use of banker plants to establish natural enemy populations before pests establish (Messelink et al. 2014). When pests exceed acceptable population levels, i.e. when economic damage is expected to occur, augmentative biological control should be the first option for pest management, if needed in combination with other IPM tactics. Were “conscious agriculture” to be considered a serious alternative to conventional farming, augmentative biological control would face an even brighter future.

Acknowledgements

The following persons/organizations are thanked for corrections and additions to Tables 2 and 3: ABC Bio (Brazil), Wagner Bettiol (Embrapa, Brazil) Vanda H.P. Bueno (ESALQ/USP, Brazil), Patrick DeClercq (Ghent University, Belgium), William Dunham (DunhamTrimmer, USA), Philip Elmer (Plant & Food Research, Hamilton, New Zealand), Tom Groot (Koppert Biosystems, The Netherlands), Tobias Laengle (Agriculture and Agri-Food Canada), Lynn LeBeck (ANBP, USA), Li Liying (Guandong Entomological Institute, China), Antoon Loomans (NVWA,The Netherlands), Ricardo Machado and Danilo Pedrazzoli (Koppert Biosystems, Brazil), Dean Metcalf (Metcalf Bio Control, Australia), José R.P. Parra (ESALQ/USP), Amy Roberts (TSG, USA), Tetsuo Wada (Arysta, Japan). The participants of the IOBC Global Workshop on “Biological Control: Concepts and Opportunities” (October 2015, Engelberg, Switzerland) are thanked for the suggestions related to factors stimulating use of Augmentative Biological Control, as are Barbara Barratt, Russell Messing and two anonymous reviewers for improving the manuscript.

Supplementary material

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Supplementary material 1 (PDF 124 kb)

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© The Author(s) 2017

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Joop C. van Lenteren
    • 1
    • 2
  • Karel Bolckmans
    • 3
  • Jürgen Köhl
    • 4
  • Willem J. Ravensberg
    • 5
  • Alberto Urbaneja
    • 6
  1. 1.Laboratory of EntomologyWageningen UniversityWageningenThe Netherlands
  2. 2.Laboratory of Chemical Ecology and Insect Behavior, Department of Entomology and AcarologyESALQ/USPPiracicabaBrazil
  3. 3.Biobest NVWesterloBelgium
  4. 4.Wageningen University & ResearchWageningenThe Netherlands
  5. 5.Koppert Biological SystemsBerkel en RodenrijsThe Netherlands
  6. 6.Centro de Protección Vegetal y Biotecnología, Unidad de Entomología UJI-IVIAInstituto Valenciano de Investigaciones Agrarias (IVIA)MoncadaSpain

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