Predator mortality depends on whether its prey feeds on organic or conventionally fertilised plants
Graphical abstract
Highlights
► Coccinellid mortality on plants in organic and synthetic fertilisers was tested. ► Mortality increased by 10% when eating aphids on plants in synthetic fertiliser. ► Two aphid prey species (Brevicoryne brassicae, Myzus persicae) gave same result. ► Sequestration of plant defences did not explain differential mortality. ► Predator efficacy for biocontrol may differ between conventional and organic farms.
Introduction
Interest in sustainable farming systems has led to comparisons of herbivore, predator and parasitoid invertebrate communities under organic and conventional agriculture in the context of both increased biodiversity and enhanced pest control (Letourneau and Bothwell, 2008, Macfadyen et al., 2009). Although species richness and abundance of predators and parasitoids can be increased under organic farming systems, this has not been shown to translate into a consistent reduction in populations of herbivores (Garratt et al., 2011, Letourneau and Bothwell, 2008), or an increase in rates of predation and parasitism (Garratt et al., 2010a, Macfadyen et al., 2009). The use of biological control programmes or measures to enhance natural enemy diversity assume that herbivore populations are regulated from the ‘top-down’ by their natural enemies (Hairston et al., 1960). A growing body of evidence shows that bottom-up factors such as plant quality can interact to affect the efficacy of natural enemies (Chaplin-Kramer et al., 2011, Price et al., 1980), but this has not been investigated in the context of organic and conventional farming systems.
Insect herbivore species differ in their response to the types of fertiliser used in organic and conventional agriculture, with some showing increased abundance on plants grown in synthetic fertilisers (Alyokhin et al., 2005, Garratt et al., 2010b, Ponti et al., 2007), while others are more abundant on plants in organic fertilisers (Culliney and Pimentel, 1986) or show no effect (Bengtsson et al., 2005, Costello and Altieri, 1995, Letourneau et al., 1996). This may be due to differences in herbivore species responses to plant structure or nutritional quality. For example, a specialist aphid feeding on Brassicas had increased abundance on plants grown in organic animal manure which had three times the concentrations of secondary metabolites (glucosinolates) found in synthetically fertilised plants, while populations of a generalist aphid were reduced (Staley et al., 2010). These changes to plant defensive chemistry in response to fertiliser type have been shown to alter competition between two herbivore species (Staley et al., 2011) and also have the potential to alter interactions between natural enemies and their prey.
Predators and parasitoids use volatile organic compounds (VOCs) emitted by the plant to locate their prey. These VOCs are breakdown products of secondary metabolites emitted by plants in response to herbivore feeding damage (Hopkins et al., 2009, Vet and Dicke, 1992). Some herbivore species have the ability to sequester these defensive chemicals, to use in their own defence against predators (Ratzka et al., 2002, Winde and Wittstock, 2011). The specialist Brassica aphid, Brevicoryne brassicae, has a defence system which mimics that of its host plants. Brevicoryne brassicae produces an enzyme (myrosinase), which catalyses the hydrolysis of glucosinolates to potentially toxic isothiocyanates (Kazana et al., 2007). The aphid accumulates sinigrin and other glucosinolate compounds, which are present in higher concentrations in the aphid than its host plant. If B. brassicae is attacked by a predator the myrosinase comes into contact with glucosinolates and volatile isothiocyanates are released (Francis et al., 2001b) resulting in high mortality of the first instar of the coccinellid Adalia bipunctata (Kazana et al., 2007, Pratt et al., 2008). By contrast, a more generalist aphid species (Myzus persicae) does not accumulate high concentrations of glucosinolates, and mortality of A. bipunctata larvae was lower when fed M. persicae compared with B. brassicae (Francis et al., 2001b). Some predators of B. brassicae also have reduced performance if feeding on hosts that have developed on plant species or cultivars with high concentrations of glucosinolates (Chaplin-Kramer et al., 2011, Kos et al., 2011), suggesting a direct link between plant glucosinolate concentration and herbivore defence against their natural enemies.
The concentration and type of fertiliser supplied to a plant can alter the concentration of foliar glucosinolates. For example, four of five glucosinolate compounds had higher concentrations in Brassica oleracea grown in organic fertilisers compared to synthetic fertilisers, in a field experiment (Staley et al., 2010). This may be because organic fertilisers provide a wide range of nutrients for plants, while the conventional mineral fertiliser only supplied nitrogen. For example, sulphur is an important prerequisite for the production of glucosinolates in Brassicas (Hopkins et al., 2009). Fertiliser type and herbivore feeding damage may also interact to affect foliar glucosinolate concentrations (Staley et al., 2011). We tested whether fertiliser type and concentration can affect the mortality of coccinellid larvae feeding on two aphid species from Brassica plants growing in fertilisers typical of organic and conventional farming systems. Glucosinolate concentrations were analysed in B. oleracea foliage and B. brassicae from the various fertiliser treatments. We hypothesised that sinigrin and other aliphatic glucosinolates would be present in higher concentrations in plants grown in organic fertilisers, and this would result in higher coccinellid larval mortality for those feeding on the specialist aphid B. brassicae. No effect of fertiliser was expected on coccinellid mortality when feeding on the more generalist M. persicae.
Section snippets
Fertiliser treatments
Soil was collected in May 2009 from a field experiment conducted at the University of Reading, UK (51°24′N, 0°57′W). Four fertiliser treatments had been added to 6 × 6 m plots in a fully factorial design for 2 years: (1) a conventional high concentration treatment consisting of ammonium nitrate (Nitram, 34.5% N) at 200 kg nitrogen per ha; (2) a conventional low concentration fertiliser treatment (ammonium nitrate (Nitram, 34.5% N) at 100 kg nitrogen per ha); (3) an organic high concentration
Predator performance
Mortality of A. bipunctata was reduced when feeding on M. persicae compared with B. brassicae (Z1,75 = 9.26, P < 0.001; Fig. 1). Adalia bipunctata feeding on aphids from synthetically fertilised plants had higher mortality compared with those eating aphids from organically fertilised plants (Z1,75 = −2.51, P = 0.012). Fertiliser concentration had no effect on the mortality of A. bipunctata (Z1,75 = −0.92, P = 0.36), nor was there an interaction between fertiliser type and concentration (Z1,75 = 0.76, P =
Discussion
Adalia bipunctata had a higher relative growth rate and lower mortality when feeding on M. persicae compared with B. brassicae, as found previously (Francis et al., 2001b, Kazana et al., 2007, Pratt et al., 2008). This differential mortality has been attributed to B. brassicae’s ability to sequester glucosinolates from its host plant, which are released as toxic isothiocyanates when under attack by predators (Kazana et al., 2007). Francis et al. (2001b) also showed that A. bipunctata mortality
Acknowledgments
Thanks to Tom Oliver for advice on culturing coccinellids, Numrah Nisar for assistance with glucosinolate analyses and to Mark Ramsden for comments on an earlier draft. Thanks also to Gilles San Martin for the coccinellid larval photograph in the graphical abstract. Funding was provided by BBSRC (Grant BB/D01154x/1).
References (37)
- et al.
Colorado potato beetle response to soil amendments: a case in support of the mineral balance hypothesis?
Agriculture Ecosystems & Environment
(2005) - et al.
Abundance, growth rate and parasitism of Brevicoryne brassicae and Myzus persicae (Homoptera, Aphididae) on broccoli grown in living mulches
Agriculture Ecosystems & Environment
(1995) - et al.
Ecological effects of organic agricultural practices on insect populations
Agriculture Ecosystems & Environment
(1986) - et al.
The chemical diversity and distribution of glucosinolates and isothiocyanates among plants
Phytochemistry
(2001) - et al.
The effects of farming system and fertilisers on pests and natural enemies: a synthesis of current research
Agriculture Ecosystems & Environment
(2011) - et al.
Effects of soil management on crop nitrogen and insect damage in organic vs. conventional tomato fields
Agriculture Ecosystems & Environment
(1996) - et al.
Insect herbivore counteradaptations to the plant glucosinolate–myrosinase system
Phytochemistry
(2011) - et al.
Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids
Annals of Applied Biology
(2012) - et al.
The effects of organic agriculture on biodiversity and abundance: a meta-analysis
Journal of Applied Ecology
(2005) - et al.
Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators
Journal of Applied Ecology
(2011)
The R Book
Effect of aphid host plant on development and reproduction of the third trophic level, the predator Adalia bipunctata (Coleoptera: Coccinellidae)
Environmental Entomology
Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata
Journal of Chemical Ecology
Tritrophic effects of organic and conventional fertilisers on a cereal-aphid-parasitoid system
Entomologia Experimentalis et Applicata
The effects of organic and conventional fertilizers on cereal aphids and their natural enemies
Agricultural and Forest Entomology
Community structure, population control and competition
The American Naturalist
Role of glucosinolates in insect-plant relationships and multitrophic interactions
Annual Review of Entomology
Fertilization mitigates chemical induction and herbivore responses within damaged oak trees
Ecology
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