Pesticides and earthworms. A review

Agronomy for Sustainable Development, Jan 2014

Earthworms provide key soil functions that favour many positive ecosystem services. These services are important for agroecosystem sustainability but can be degraded by intensive cultural practices such as use of pesticides. Many literature reports have investigated the effect of pesticides on earthworms. Here, we review those reports to assess the relevance of the indicators of earthworm response to pesticides, to assess their sensitivity to pesticides, and to highlight the remaining knowledge gaps. We focus on European earthworm species and products authorised in Europe, excluding natural compounds and metals. We consider different organisation levels: the infra-individual level (gene expression and physiology), the individual and population levels (life-history traits, population density and behaviour) and the community level: community biomass and density. Our analysis shows that earthworms are impacted by pesticides at all organisation levels. For example, pesticides disrupt enzymatic activities, increase individual mortality, decrease fecundity and growth, change individual behaviour such as feeding rate and decrease the overall community biomass and density. Insecticides and fungicides are the most toxic pesticides impacting survival and reproduction, respectively.

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Pesticides and earthworms. A review

Agron. Sustain. Dev. Pesticides and earthworms. A review Cline Pelosi 0 1 2 3 Sbastien Barot 0 1 2 3 Yvan Capowiez 0 1 2 3 Mickal Hedde 0 1 2 3 Franck Vandenbulcke 0 1 2 3 0 Y. Capowiez INRA, UMR406 UAPV , 84914 Avignon Cedex 9 , France 1 S. Barot IRD, UMR7618 Bioemco , 75230 Paris Cedex 05 , France 2 F. Vandenbulcke LGCgE-Lille 1EA4515 , Equipe Ecotoxicologie, 59650 Villeneuve d'Ascq , France 3 F. Vandenbulcke Universite Lille Nord de France-Lille 1 , 59000 Lille , France Earthworms provide key soil functions that favour many positive ecosystem services. These services are important for agroecosystem sustainability but can be degraded by intensive cultural practices such as use of pesticides. Many literature reports have investigated the effect of pesticides on earthworms. Here, we review those reports to assess the relevance of the indicators of earthworm response to pesticides, to assess their sensitivity to pesticides, and to highlight the remaining knowledge gaps. We focus on European earthworm species and products authorised in Europe, excluding natural compounds and metals. We consider different organisation levels: the infra-individual level (gene expression and physiology), the individual and population levels (life-history traits, population density and behaviour) and the community level: community biomass and density. Our analysis shows that earthworms are impacted by pesticides at all organisation levels. For example, pesticides disrupt enzymatic activities, increase individual mortality, decrease fecundity and growth, change individual behaviour such as feeding rate and decrease the overall community biomass and density. Lumbricidae; Organisation levels; Plant protection products; Biomarkers; Insecticides; Fungicides; Herbicides - Contents 1. Introduction 2.1.1. Literature review 2.2.1. Literature review 2.4. Synthesis 3. Sources of variability in earthworm response to pesticides 3.1. Biological models 3.2. Physico-chemical conditions and duration of exposure 4. Knowledge gaps 4.1. Representativeness 5. Conclusion 1 Introduction Fig. 1 Pesticide application in a field Fig. 2 Pictures showing some of the roles of earthworms in soil structure (a, b) and as a trophic resource for other organisms (c, d) Copyright Y. Capowiez Copyright C. Pelosi Copyright M. Solari Copyright J. Dormion, Taupgreen products authorised in Europe, i.e. excluding natural compounds and metals. 2.1 Response at infra-individual level 2.1.1 Literature review 2.1.2 Indicators at infra-individual level I I ) ) d d rsd itrs tec itsr tec a s . le s . le rch rre A lo rre A lo o te nd (c te nd (c n . a a . a a i L ) s L ) s tllecedo ,.itfead t(hguob iilcnoga ,.tifead t(ghuob iilcnoga ltreduu N co tiaho ,ity cd irou rrepo (1989 tssea t v n lug itca tah avh ,)4 2 om d ieg , e 0 8 C an lo ty se w n b 0 6 y o iitv rae rog itco cen (21 211 and ititv ssa tah acE frsan ssay rduo iad 82 O ay ac ym tsop h t a p vo N (IS ssa hE od ih 1 1 8 3 2.2.1 Literature review 2.2.2 Indicators and effects at individual and population levels Fig. 3 Cocoons of earthworms Copyright INRA, G. Bouloux fo ita 0 0 o th lau ixm r 1 0 nd tie v a reb ten , 1 In In F H w rs F F F lt n u n u u e d e d d v a v a u u A J J d n it(raconodun iecadno ir)auvoh ,litraogvhw d itrcuondop ,liiteagvhw in itrrcedoupdo ,tilrsavuhv itcuond adnw lravv v a n row and rrepo trho isu ep av eb ruv an re r u g a R S S G G o d . h , n ea ta a ,irednaA lllopboo itlrcaooh .itfaead itfead itfead .ilisconga ,.tifeadE iisveanE ittsrsrree ircubuLm trrceodpo ltrceaubu .iilsconga . A c E . . h t t h ) ,ilrravuvogw adn itrrceuopdon ,ilireavvugw adn ccnooo tircdopuno l(faeadn tiscunoopnm ,littrrayogow and tirrceopduon ltitraaoynd iteghw lttiraaoynd tirrceuopdon ltitraayndo tirrceuopdon S S M M M M A C D G A C ied ied iced ied ied iced ic ic ti ic ic it b g c b b c r e r r e e un sn e e s n H F I H H I s e u e te in e r id le ah cy id ho am zo sp lg am sp t a o o t o ace id ph on ace ph ro im on hp ro on o z a s o a l n g o l g h e r h h r C B O P C O lreo iazm tae tae+ lreo irfso h d o s h y co en teh ho co rp t b p t o e r e l c a im ly c h 2 D .l nd .l .l a a ) a a te in 07 te te o m 0 u u ia sa (2 oh oh V V X Y Z Z Z 2 A E A l ) 45 th s ti + n y c ) o o d d lav sek on tc , w a u i 30 rg 8 ro s i o u , ( 2 p ay rv e c d ,15 06 ro (r 8 ( 8w (co rpo e d su 7 2 d ay ro ee a no ayd adn rfo dn tio n n d w th ti a y c a c 2 sy 12 til 8 ow du 21 .4 sk h ud 1 a a d r e t , d d tr n g ro d te e w ro V V X Y Z n i r h t e tih lo p a n irnuoE iit(sscedw )sseonp lteohym czeaobn irezabndm tsaehpoy -acbdyhm tirreehpm ireazbndm a l a y a M M C G L C C Fig. 4 Effect of different concentrations of imidacloprid on the digging behaviour of two earthworm species (adapted from Capowiez et al. 2006) A. icterica (endogeic) A. nocturna (anecic) 0.5 mg kg-1 imidacloprid 1 mg kg-1 imidacloprid 2.3 Response at community level Fig. 5 Illustration of the earthworm sampling method combining a a chemical extraction and b hand-sorting 2.3.2 Effect of pesticides at community level 404020 cm 252520 cm 303030 cm 303030 cm 5050NA cm 0.1 m235 cm NANA25 cm 0.064 m2NA cm 0.25 m2NA cm Pelosi et al. (2009b) Blakemore (2000) Scullion et al. (2002) Scullion et al. (2007) Tarrant et al. (1997) Irmler (2010) Eltun et al. (2002) Year of sampling Sampling Sampling method* volume Siegrist et al. (1998) Switzerland Chromic luvisol Hutcheon et al. (2001) UK Sandy clay Organic vs. integrated vs. conventional Organic vs. biodynamic vs. conventional Integrated vs. conventional 1990 to 2000 Spring and fall F Effect size Effect size Earthworm density 2.non-cereal crop 3.unkown crop 4.grassland Earthworm biomass 2.non-cereal crop 3.unkown crop 2.4 Synthesis 3 Sources of variability in earthworm response to pesticides 3.1 Biological models Fig. 7 Different earthworm species from the three ecological groups (Bouch, 1972): a epigeic, b endogeic and c anecic Eisenia fetida Copyright C. Pelosi Copyright C. Pelosi Copyright C. Pelosi Aporrectodea caliginosa Allolobophora rosea Lumbricus terrestris Octalasion cyaneum Aporrectodea longa 4 Knowledge gaps 4.1 Representativeness 4.2 Difficulties in scaling up from infra-individual to community levels 5 Conclusions Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited. 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Céline Pelosi, Sébastien Barot, Yvan Capowiez. Pesticides and earthworms. A review, Agronomy for Sustainable Development, 2014, 199-228, DOI: 10.1007/s13593-013-0151-z