biodiversity for food and agriculture
4.3 Associated biodiversity
4.3.5 Associated biodiversity for pest and disease regulation
Introduction
Pest, disease and weed regulation is a crucial eco-system service for food and agriculture. The direct
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providers of this service are a vast category of associated biodiversity known as biological control agents (BCA). Non-BCA biodiversity contributes indirectly to the creation of a pest-suppressive environment by, inter alia, providing alternative food sources and shelter for BCAs (e.g. Settle et al., 1996). BCAs can be deliberately introduced (aug-mentative and classical biological pest control) or managed indirectly by manipulating the local envi-ronment and wider landscape to promote their presence (conservation biological control). See Section 5.6.6 for further information on the roles of BCAs in integrated pest management.
BCAs are taxonomically diverse and include many species of bacteria, fungi, invertebrates and vertebrates. The most significant functional groups of BCAs are parasitoid insects, predators, herbivores, entomopathogenic organisms (bacte-ria, fungi, nematodes and viruses) and antifungal fungi (Box 4.4). The roles of birds in the supply of ecosystem services, including pest and disease regulation, are discussed in Box 4.5.
Relationships between the status of BCA pop-ulations and the supply of pest-control services are complex. The presence of more than one BCA species that preys on a given pest may not always add to the effectiveness of regulation services (Martin et al., 2013; Rafikov, Balthazar and von Bremen, 2008; Straub, Finke and Snyder, 2008). Generally speaking, however, so-called functional redundancy is considered likely to increase the resilience of pest-control services by reducing the risk that all BCAs for a particular pest will be lost (e.g. because of climate change) (Beed et al., 2011; Cock et al., 2011). An increase in the abundance and species richness of BCAs can sometimes lead to antagonistic relation-ships such as superpredation (predation of pred-ators) and hyperparasitoidism (parasitoidism of parasitoids) (Griffin, Byrnes and Cardinale, 2013; Holland et al., 2012; Landis, Wratten and Gurr, 2000; Martin et al., 2013). These kinds of trophic relationships among BCAs, and hence potentially the supply of pest-control services, are affected in turn by the characteristics of the local landscape. For example, Martin et al. (2013)
found that negative interactions among natural enemies constrained pest control as landscapes became more complex. However, other studies have found increasing landscape complexity to be correlated with increased diversity and effec-tiveness (timing) of BCA activity (e.g. Dominik et al., 2017; Settle et al., 1996).
The country reports list many associated bio-diversity species as being actively managed to provide pest- and disease-regulating services, whether directly or indirectly (e.g. via habitat pro-visioning for BCAs) (see Section 4.3.1). The major-ity are predatory and parasitoid invertebrates associated with crop production.
State of knowledge
The country reports indicate varying levels of knowledge on the status and trends of species that provide pest and disease control services.
A number of countries report extensive monitoring of relevant components of associated biodiversity.
Examples include Switzerland (agro-environment monitoring programmes implemented by the Federal Office for Agriculture), the United Kingdom (Bees, Wasps and Ants Recording Society;
Farmland Bird Indicator), the United States of America (National Invertebrate Genetic Resources Program) and Germany. Some countries report that monitoring activities are implemented on a less systematic basis. For example, Croatia men-tions that some monitoring of natural enemies (spiders and mites) is done under its Reporting and Early Warning System in Agriculture. Guyana notes that although it does not have monitor-ing programmes for associated biodiversity in its rice production systems, natural-enemy populations are recorded as part of pest- monitoring activities. Some countries note that some information on the status and trends of BCAs is obtained via individual research projects.
Moreover, even among countries that make no specific reference to the monitoring of BCAs or other components of biodiversity that contrib-ute to pest and disease control services, some of these species are probably covered by moni-toring programmes reported to be undertaken
Box 4.4
The main functional groups of biological control agents
Parasitoids. Species belonging to this group spend part of their life cycles (usually the larval stage) inside or on the surface of a host, killing it in the process. Approximately 10 percent of known insect species are parasitoids (Godfray, 1994). Parasitoid biological control agents are used in agricultural systems on a large scale in augmentative, classical and conservation biological control (Heimpel and Cock, 2018; Jonsson et al., 2008; Van Lenteren et al., 2018).
Examples include wasps of the suborder Apocryta and several families of flies, for example the Tachinidae family.
Predators. This group includes many arthropod species – including members of the Acari (mites), Araneae (spiders), Opiliones (harvestmen), Odonata (dragonflies), Hemiptera (e.g. assassin bugs), Thysanoptera (thrips), Neuroptera (lacewings), Coleoptera (beetles), Diptera (flies) and Hymenoptera (ants, bees and wasps) (Cock et al., 2011) – as well as a number of vertebrates (amphibians, birds, fish, mammals and reptiles). Predators help to control a wide range of pest species, although some may feed on useful species as well. Subcategories of this functional group include aerial, aquatic (subsurface- and surface-dwelling), vegetation-dwelling and ground-dwelling predators (Holland et al., 2012). The first group have good dispersion ability and can predate on pests in the air. Examples include many species of flying insects (e.g. families within the orders Odonata, Hymenoptera and Diptera) and insectivorous birds and bats. Aquatic predators include many species of insects, in both larval and adult forms. Aquatic predators used specifically as control agents include fish species in rice-field systems (e.g. common carp [Cyprinus carpio] and Nile tilapia [Oreochromis niloticus]), Labridae (wrasses) employed as removers of sea lice in salmon cages, and a number of carnivorous species (e.g. bronze featherback [Notopterus notopterus]) used to control tilapia breeding by predating on their young. Ground predators are associated with the soil surface and the upper layer of the soil.
Predatory mites of the family Phytoseiidae, for instance, play an important role in augmentative, classical and conservation biocontrol of pest mites and insects in open-field and greenhouse crops (Calvo et al., 2015; Maoz et al., 2014; Yaninek and Hanna, 2003). Other examples include ground and rove beetles. Predatory amphibians include
toads and frogs, although the importance of their role (as well as that of reptiles) in biological control remains poorly understood (Hocking and Babbit, 2014).
Entomopathogenic fungi. This group comprises members of the Fungi Kingdom that invade arthropod tissues and reproduce in them, killing the host. Several species (e.g. Beauveria bassiana and Metarhizium anisopliae) are important in the control of grasshoppers and locusts (Jaronski and Goettel, 1997).
Antifungal fungi. This group comprises members of the Fungi Kingdom that limit the development of fungal disease in plants by killing or competing with the disease-causing fungi or by promoting plant resistance. Examples include Trichoderma spp. (John et al., 2010; Zeilinger et al., 2016).
Entomopathogenic nematodes. These nematodes invade the tissues of many types of insects (including Lepidoptera, Coleoptera and Diptera). Important examples include Steinernema spp. and Heterorhabditis spp. (Cock et al., 2011).
Entomopathogenic bacteria. An important species in this category is the bacterium Bacillus thuringiensis, which synthesizes a compound (Bt) that is toxic to insects.
Entomopathogenic viruses. Although a number of virus families are known to infect arthropods, baculoviruses stand out within this group because of their ability to kill insects with high specificity. These viruses are commonly used as biopesticides against lepidopteran pests (e.g. the Anticarsia gemmatalis nuclear polyhedrosis virus used to control the velvetbean caterpillar on soybean and the Helicoverpa armigera nuclear polyhedrosis virus used to control the cotton boll worm [Reid, Chan and van Oers, 2014]).
Weed- and algae-damaging herbivores. Herbivores such as Curculionidae (weevils) and Chrysomelidae (leaf beetles) help control weeds in croplands (Cock et al., 2011).
Fish such as the grass carp (Ctenopharyngodon idella) are used in irrigation systems to control aquatic weeds (Halwart and Gupta, 2004). Rabbitfish (Siganus spp.) and scats (Scatophagus spp.) help control fouling epiphytic algae in marine fish cages.
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Box 4.5
The roles of birds in the supply of supporting and regulating ecosystem services
Pest control: Pest predation by birds enhances crop yields in many regions. More than 50 percent of bird species are primarily insectivores (Wenny et al., 2011).
The European pied flycatcher (Ficedula hypoleuca) has been shown to be a major suppressor of insects harmful to forest vegetation, especially destructive moths and caterpillars. Because of these benefits, plantation owners actively encourage the presence of pied flycatchers by providing them with nest-boxes (BirdLife International, 2015). The success of such schemes means the use of nest-boxes for flycatchers and tits has become a standard management tool throughout European forests (ibid.).
A study in a cacao agroforesty system in Central Sulawesi, Indonesia, found that exclusion of insectivorous birds and bats increased insect-herbivore abundance, despite the presence of other insectivorous predators, an effect that decreased the final crop yield by 31 percent, equating to a loss of USD 730 per ha per year (Maas, Clough and Tscharntke, 2013). A study in Costa Rica on the effect of bird predation on the coffee berry borer (Hypothenemus hampei), a pest that often devastates coffee crops, demonstrated that infestations nearly doubled when birds were excluded from foraging on coffee shrubs (Karp et al., 2013). Similarly, the findings of a study on a coffee farm in Jamaica led researchers to conclude that the value of coffee berry borer removal by birds equated to 12 percent of the total crop value (Johnson, Kellermann and Stercho, 2010).
Pollination: Birds are thought to be particularly important as pollinators in circumstances where the density and activity of pollinating insects is limited, for example in cold, high-rainfall or dry conditions or on isolated islands with poor insect colonization (Cronk and Ojeda, 2008).
Anderson et al. (2011b) demonstrated that seed output of the bird-pollinated shrub New Zealand gloxinia (Rhabdothamnus solandri) was 84 percent lower and shrub regeneration 55 percent lower at sites in New Zealand that had lost two out of three major avian pollinator species than at sites where all three species were present. Studies have demonstrated strong relationships between birds and the plants they pollinate: often the role of the bird species cannot be substituted by other pollinators such as insects (Nabhan and Buchmann, 1997).
Seed dispersal: Vertebrates, including birds, are the main seed dispersers for flowering and woody plants (Sekercioglu, 2006).Nearly 33 percent of bird species disperse seeds, primarily through fruit consumption, but also through scatter-hoarding of nuts and conifer seeds.
Seed dispersal benefits plants by increasing the likelihood that seeds will colonize areas with favourable germination conditions.
Removing carrion: Vultures fulfil an extremely important ecological role as scavengers, helping to keep the environment free of carcasses and waste that spread disease among people and livestock. Vultures in South Asia have declined drastically over recent decades. For example, the abundance of the Indian vulture (Gyps indicus) and the slender-billed vulture (Gyps tenuirostris) declined by 96.8 percent between 1992 and 2007 (Prakash et al., 2007).
This is largely because of widespread use of the anti-inflammatory drug “diclofenac” in livestock (Ogada, Kessing and Virani, 2012). The drug is highly toxic to vultures, which ingest it when feeding on livestock carcasses. Declines in vulture populations meant that carcasses became more prevalent, which in turn led to increases in feral dog populations, and hence increased the risk to humans of contracting rabies via dog bites (Markandya et al., 2008). Based on the costs of commercial carcass-disposal plants, the value of a single vulture has been estimated at about 600 000 Indian rupees (approximately USD 9 200) (IUCN, 2016a). India, Nepal and Pakistan banned the use of diclofenac as a veterinary drug in 2006, and surveys suggest that vulture populations have stabilized, although numbers still remain too low across the region (e.g. Prakash et al., 2012).
Source: Provided by the Royal Society for the Protection of Birds (RSPB) and Birdlife International.
for other purposes or for which the purpose is not specified. It is also likely that the status of managed BCAs is at least to some degree moni-tored, although this is often not stated explicitly in the country reports. Monitoring programmes for pests and diseases themselves exist through-out the world. Notwithstanding these various
strands of reporting, however, many country reports note major weaknesses in monitoring programmes for BCAs.
Status and trends
While, as described above, the state of knowledge remains very far from complete, the country reports TABLE 4.5
Examples of associated-biodiversity species or species groups that contribute to pest and disease regulation reported to be under threat
Country Species/group Degree of threat Main threat(s)
Argentina Insectivorous birds Moderate Loss of habitat in production zones, agrochemicals
Belgium
Alauda arvensis (Eurasian skylark) VU Intensive agriculture Perdix perdix (grey partridge) VU
Emberiza citrinella (yellowhammer) Threatened Miliaria calandra (corn bunting) Threatened
Burkina Faso Bats High Poaching, habitat destruction, pesticide susceptibility
Cook Islands
Collocalia sawtelli (Atiu swiftlet) EN Acrocephalus kerearako (Cook Islands
reed warbler) EN
Pomarea dimidiata (Rarotonga
monarch) EN
Aplonis cinerascens (Rarotonga
starling) EN
Estonia
Coracias garrulus (European roller) CR Changes in use of arable land (e.g. drainage, changes in mechanization, changes in crops), disappearance of dead, hollow and dry trees, pollution, acidification
Cucujus cinnaberinus (flat bark beetle) CR
Forestry, disappearance of dead, hollow and dry trees, changes in tree species in forests, changes in the age structure of forests, disappearance of old forests and/or big trees, clear-cutting
Calosoma inquisitor (lesser searcher
beetle) CR Forestry
Guyana Synallaxis kollari (hoary-throated
spinetail) EN
Ireland Odonata (damselfly and dragonfly species)
EN: 2 species VU: 2 species NE: 9 species Lebanon Carduelis carduelis (European
goldfinch) EN Loss of habitat (mainly caused by fires), climate change,
illegal hunting, pollution
Norway
Spider species in livestock
grassland-based systems EN: 3 species
VU: 25 species Habitat loss due to land-use change, pollution Spider species in rainfed crop systems VU: 8 species
Centipede species in semi-natural
forests VU: 5 species Habitat loss due to land-use change
Spider species in semi-natural forests EN: 3 species VU: 23 species
(Cont.)
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Country Species/group Degree of threat Main threat(s)
Panama
Tinamus major (great tinamou) EN Crypturellus soui (little tinamou) EN Crax rubra (great curassow) EN Nothocercus bonapartei (highland
tinamou) EN
Pharomachrus mocinno (resplendent
quetzal) EN
Odontophorus gujanensis (marbled
wood-quail) EN
Geotrygon chiriquensis (Chiriquí
quail-dove) EN
Slovenia
Alauda arvensis (Eurasian skylark) VU Habitat loss
Crex crex (corncrake) EN
Otus scops (Eurasian scops owl) EN Jynx torquilla (Eurasian wryneck) VU Lanius minor (lesser grey shrike) VU Lanius collurio (red-backed shrike) VU Lullula arborea (woodlark) EN
Sri Lanka Spider species Threatened: 100 species
EN: 40 species
CR: 21 species Habitat loss, excessive use of pesticides
Switzerland
Bat species
NT: 7 species (23%) On Swiss Red List: 15 species (50%)
Renovation and reassignment of historic buildings, intensive agriculture and forestry practices, land-use changes, use of pesticides. Habitat fragmentation due to the presence of infrastructure (e.g. communication routes, lights)
Odonata (damselfly and dragonfly species)
EX: 2 species (3%) CR: 12 species (16%) EN: 7 species (10%) VU: 5 species (7%)
Habitat loss (e.g. fragmentation, drainage)
Carabidae (ground beetle and tiger
beetle species) On Swiss Red List: 148
species (29%) Habitat loss (e.g. draining of moors), intensive agriculture
Chrysopidae (lacewing species) On Swiss Red List: 21
species (18%) Loss of habitat for larvae
Notes: Countries followed the IUCN Red List Categories and Criteria (IUCN, 2012) (CR [Critically Endangered]; EN [Endangered]; EX [Extinct]; NT [Near Threatened); VU [Vulnerable]) except where stated otherwise. The numbers in the “Degree of threat” column indicate the numbers of species in the respective risk category and the percentages indicate the proportion of the evaluated species in the respective taxonomic group falling within the respective risk category. See Cordillot and Klaus (2011) for more information on the Swiss Red List classification system. Analysis based on 91 country reports.
Source: Country reports prepared for The State of the World’s Biodiversity for Food and Agriculture.
TABLE 4.5 (Cont.)
Examples of associated-biodiversity species or species groups that contribute to pest and disease regulation reported to be under threat
provide a number of indications of the status of individual BCA species, groups of BCAs or species categories that include substantial numbers of BCAs. For example, Bangladesh reports a decline
in spiders and predatory insects in crop fields.
Nepal mentions a general decline in the diver-sity of the natural enemies of pests. The United Kingdom reports that its indicator for farmland
birds (many of which are insectivorous)43 declined by 55 percent between 1970 and 2013. Similarly, the United States of America reports a decline of almost 40 percent in its grassland bird index between 1968 and 2014. India notes the decline of parasitoid wasps (Ichneumonidae, Braconidae families) and parasitoid flies (Tachinidae). Table 4.5 presents examples from the country reports of the reported risk status of components of associated biodiversity that contribute to pest and disease control, along with (where available) the main reported threats to these species.
Countries’ responses on trends in the supply of pest- and disease-regulation services in particular production-system categories are summarized in Table 4.4. Reports of decreasing trends predom-inate in all three crop production-system catego-ries, while increasing trends predominate in mixed systems. In all other production-system categories, trends are mixed (i.e. neither positive nor negative nor stable trends predominate). Many countries report factors that are threatening BCAs in and around production systems, including the use of agrochemicals (particularly pesticides), habitat loss and fragmentation, overexploitation and climate change. For further discussion of drivers of change, see Chapter 3.