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Applied Soil Ecology
journal homepage: www.elsevier.com/locate/apsoil
Multitrophic interactions between maize mycorrhizas, the root feeding
insect Phyllophaga vetula and the entomopathogenic fungus Beauveria
bassiana
Guadalupe Zitlalpopoca-Hernandez
a
, Miguel Bernardo Najera-Rincon
b
, Ek del-Val
a,e
,
Alejandro Alarcon
c
, Trevor Jackson
d
, John Larsen
a,
⁎
a
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro 8701 Ex-hacienda
San José de la Huerta, 58190 Morelia, Michoacán, Mexico
b
Campo Experimental Uruapan, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP),Av. Latinoamericana 1101, Los Angeles, 60150
Uruapan, Michoacán, Mexico
c
Posgrado de Edafología, Colegio de Postgraduados, Carretera México-Texcoco km. 36.5 56230 Montecillo, Texcoco, Mexico
d
AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch 8140, New Zealand
e
Escuela Nacional de Estudios Superiores Unidad Morelia Universidad Nacional Autónoma de México (UNAM), Antigua Carretera a Pátzcuaro 8701 Ex-hacienda San
José de la Huerta, 58190 Morelia, Michoacán, Mexico
ARTICLE INFO
Keywords:
Biocontrol
Root health
Herbivory
Microbial interactions
Arbuscular mycorrhiza
ABSTRACT
Root feeding larvae of Phyllophaga vetula causes severe damage in maize agroecosystems and their conventional
management with chemical pesticides adversely affects the environment. Plant beneficial rhizosphere micro-
organisms such as mycorrhzial and entomopathogenic fungi (EPF) offer an alternative sustainable pest
management strategy, but their successful integration in agroecosystems requires profound knowledge about
their ecology. Here we explored interactions between a commercial isolate of the EPF Beauveria bassiana and
indigenous maize mycorrhizas and their single and combined effects against root herbivory from the insect
larvae P. vetula. Maize plants were grown in a greenhouse for seven weeks in pots with P limited soil with all
possible combinations of the three main factors including native arbuscular mycorrhizal fungi (AMF) (without
and with), EPF (without and with) and P. vetula (without and with).
Root herbivory by P. vetula reduced plant growth and nutrition, and in addition reduced AMF root
colonization. In contrast, AMF improved plant growth and P nutrition, but also reduced the population density
of B. bassiana. Inoculation with B. bassiana increased root dry weight and counteracted a decrease in shoot N
content from P. vetula root herbivory, despite that only 5% of P. vetula larvae were infected with B. bassiana. Dual
inoculation with AMF and B. bassiana increased plant growth and N shoot content allowing the plants to
compensate for the damage caused by P. vetula herbivory. In conclusion our results show that combination of
native AMF populations and the EPF B. bassiana induce tolerance in maize from root herbivory by P. vetula in
terms of plant growth performance and nutrition.
1. Introduction
Maize is one of the world basic crops for human consumption and
animal fodder (FAOSTAT, 2009). In Mexico, which is the origin of
domestication of maize with a diverse genetic population (Sánchez
et al., 2000), maize is covering around 36% of all arable land and is
being cultivated by small holders and at industrial scale (Paliwal,
2001).
Root feeding insects of the white grub complex Phyllophaga spp.
(Coleoptera: Melolonthidae) cause severe yield losses in maize agroe-
cosystems in Mexico due to their high abundance, diversity and wide
distribution (Jackson and Klein, 2006; Rodríguez del Bosque and
Morón, 2010).
Conventionally chemical insecticides are used to manage root
feeding insects, which however have strong environmental impacts
contaminating soil and water ecosystems and adversely affect human
health (Gómez-Arroyo et al., 2011). Development of insecticide resis-
tance is another concern (Oerke, 2006), which causes new pest
outbreaks increasing the amount of insecticides applied to agroecosys-
tems. Also possible non-target effects of pesticides on plant beneficial
http://dx.doi.org/10.1016/j.apsoil.2017.03.014
Received 5 November 2016; Received in revised form 11 March 2017; Accepted 13 March 2017
⁎
Corresponding author.
E-mail address: jlarsen@cieco.unam.mx (J. Larsen).
Applied Soil Ecology 115 (2017) 38–43
0929-1393/ © 2017 Elsevier B.V. All rights reserved.
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