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Prevalence of entomophthoralean fungi

(Entomophthoromycota) of aphids in relation
to developmental stages

Article in Pest Management Science · November 2015

DOI: 10.1002/ps.4188

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Research Article
Received: 12 June 2015 Revised: 29 October 2015 Accepted article published: 18 November 2015 Published online in Wiley Online Library:

(wileyonlinelibrary.com) DOI 10.1002/ps.4188

Prevalence of entomophthoralean fungi

(Entomophthoromycota) of aphids in relation
to developmental stages
Romina G Manfrino,a* Alejandra C Gutierrez,a Manuel E Rueda Páramo,a
César E Saltob and Claudia C López Lastraa

Abstract
BACKGROUND: Transmission of fungal pathogens of aphids may be affected by the host developmental stage. Brassica and
Lactuca sativa L. crops were sampled in Santa Fe, Argentina, to determine the prevalence of fungal-diseased aphids and
investigate the differences between developmental stages of aphids.

RESULTS: The fungal pathogens identified were Zoophthora radicans (Bref.) A. Batko, Pandora neoaphidis (Remaud. & Hennebert)
Humber and Entomophthora planchoniana Cornu. Their prevalence on each crop was calculated. The numbers of infected aphids
were significantly different between the different developmental stages on all crops except B. oleracea var. botrytis L.

CONCLUSIONS: The entomophthoralean fungi identified are important mortality factors of aphids on horticultural crops
in Santa Fe. The numbers of infected nymphs and adults were significantly different, nymphs being the most affected
developmental stage.
© 2015 Society of Chemical Industry

Keywords: aphids; entomophthoralean fungi; developmental stages; Argentina

1 INTRODUCTION recorded on cereal crops,11 as well as on Capsicum annuum L. and

Aphids are one of the most important factors limiting horticul- Solanum melongena L.12
tural crop production in Argentina.1 Brevicoryne brassicae (L.) and Generally, the development of epizootics depends on the host
Nasonovia ribisnigri (Mosley) are the main species of aphids on population dynamics13 and on the host developmental stages
Brassica crops and on Lactuca sativa L., respectively, in the world.2 susceptible to infection. Because aphids are hemimetabolous,
Aphids are controlled mainly by chemical insecticides, but this nymphs live and feed on colonies together with adults, resulting
practice creates human health and environmental problems and in the entire population being susceptible to attack by fungal
pathogens.
has adverse effects on non-target fauna.
The aim of this study was to determine the fungal infection
Entomophthoralean fungi have been found to be important
levels in aphid populations according to their developmental
antagonists of aphids under field conditions3 and have the poten-
stage (nymphs and adults, apterae and alatae).
tial to induce epizootics that drastically reduce aphid densities.4,5
Entomophthoralean fungi have been recorded infecting aphids
on horticultural crops worldwide. MacLeod6 found infections of
Pandora neoaphidis (Remaud. & Hennebert) Humber of 76.1% on
2 MATERIALS AND METHODS
2.1 Field surveys
Macrosiphum pisi Kaltenbach on horticultural crops in Canada.
Surveys were conducted in conventional crop fields in Monte Vera
MacLeod et al.7 recorded the fungus Entomophthora planchoni-
(31∘ 32′ 58.21′′ S, 60∘ 41′ 34.74′′ W), Santa Fe Province, Argentina.
ana Cornu destroying a population of Aphis rumicis Linnaeus in
Studies were conducted on Lactuca sativa L., Brassica oleracea var.
England. McLeod et al.8 also recorded epizootics of P. neoaphidis
on Myzus persicae (Sulzer) on Spinacia oleracea L. in Arkansas.
In Spain, Díaz et al.9 identified P. neoaphidis on Macrosiphum
∗ Correspondence to: Romina G Manfrino, Centro de Estudios Parasitológicos y
euphorbiae (Thomas), N. ribisnigri, Aphis fabae Scopoli and Aphis
de Vectores, UNLP-CONICET, Boulevard 120, entre 61 y 62, La Plata 1900, Buenos
gossypii Glover on horticultural crops, and Conidiobolus corona- Aires, Argentina. E-mail: romimanfrino@hotmail.com
tus (Constantin) on A. fabae on Beta vulgaris var cicla (chard)
during spring and on M. euphorbiae on lettuce crops during a Centro de Estudios Parasitológicos y de Vectores (CEPAVE), UNLP-CONICET, La
Plata, Buenos, Aires, Argentina
autumn. In Argentina, Scorsetti et al.10 cited epizootiological stud-
ies of P. neoaphidis on N. ribisnigri (Mosley) on lettuce crops. b Instituto Nacional de Tecnología Agropecuaria (INTA), Área Investigación
Prevalence of entomophthoralean fungi on aphids has also been Agronomía, Protección Vegetal, Rafaela, Santa Fe, Argentina

Pest Manag Sci (2016) www.soci.org © 2015 Society of Chemical Industry

 www.soci.org RG Manfrino et al.

italica Plenck, B. oleracea var. botrytis L. and B. oleracea var. capitata Brassica crops, while N. ribisnigri was the main species found on
L. The periods of observations on each crop were: L. sativa from L. sativa.
16 June to 7 September 2010; B. oleracea var. italica Plenck from The averages of healthy and infected aphids were calculated
28 December 2012 to 31 May 2013 (spring–summer in Argentina) per sample date and are shown in Table 2. To calculate the
(designated B. oleracea var. italica 1) and from 25 March to 24 July averages, all species of aphids were considered together (aphids
2013 (autumn–winter in Argentina) (designated B. oleracea var. not discriminated by species).
italica 2); B. oleracea var. botrytis from 1 June to 16 July 2010 and The fungal species recorded from aphids on Brassica crops
from 8 April to 20 July 2011; B. oleracea var. capitata from 18 May were Zoophthora radicans (Bref.) A. Batko, P. neoaphidis and E.
to 5 August 2010. planchoniana, whereas those recorded from aphids on L. sativa
The daily data of average temperatures and relative humidity were P. neoaphidis and E. planchoniana.
were obtained from the Faculty of Hydrological Sciences of the
Universidad Nacional del Litoral.
3.1 Population variations
On B. oleracea var. capitata, we observed high population densities
2.2 Aphid sampling
of both healthy and infected aphids during the first week of sam-
Aphid populations were sampled weekly. To this end, 20 plants of
pling (18 May 2010). The number of infected aphids significantly
each crop species were randomly selected and checked for the
decreased in the next and subsequent weeks, and then started to
presence of aphids. All aphids were quantified but in the count
increase again after the fourth week. The highest percentage of
were not discriminated by species. Quantification was done in
infection was 75.6% (n = 45). On L. sativa, the level of infection was
situ. For identification of aphid species, healthy living aphids were
variable throughout the period of observations. The highest per-
collected and transferred into plastic cups with lids (150 cm3 ), and
centage of infection was 60.9% (n = 87). On both crops, the highest
subsamples were then transferred to Eppendorf microcentrifuge
percentages of infection were observed on 16 July 2010 (Table 2).
tubes (1.5 cm3 ). These subsamples were preserved in 70% ethanol.
When we studied and compared the prevalence of entomoph-
Aphids were identified to species level using the keys of Blackman
thoralean fungi of aphids on B. oleracea var. botrytis during the
and Eastop.2
2 years of study, we found that during 2010 infected aphids
were recorded throughout the period of observations. The
2.3 Identification of fungal pathogens highest percentage of infection in 2010 (64.4%, n = 73) was
Dead aphids with evidence of external fungal growth (mycelia observed on 8 July. During 2011, the density of healthy aphids
growth or sporulation) were examined under a stereomicroscope remained low during the period of observations, and the pro-
and a compound microscope for the presence of rhizoids, cys- portion of infected aphids varied widely among sampling dates.
tidia and/or spores. Dead aphids without external signs of mycosis The highest percentage of infection in 2011 (96%, n = 75) was
were placed on petri dishes (60 mm diameter) with a filter paper recorded on 24 June. The number of infected aphids significantly
moistened with a few drops of distilled water (humid chambers) decreased in the following week and decreased to zero in the
and maintained at 20 ∘ C for 24–72 h to allow the development last week of sampling, coinciding with the end of the crop cycle
of overt mycoses. Living aphids with apparent symptoms of infec- (Table 2).
tion (infection is evidenced by colour change of the aphid and Regarding the comparison of the prevalence of entomophtho-
limited mobility) were also transferred to humid chambers and ralean fungi of aphids between seasons, on B. oleracea var. italica 1
maintained under the same conditions detailed above to facilitate we observed a gradual increase in the population of healthy aphids
the development of infection. Fungal structures were mounted from December to 14 February 2013. On this date, we observed a
in lactophenol/aceto-orcein (1:1) or stained with 1% aceto-orcein peak in the aphid population density (x = 259.6 aphids plant−1 )
plus glycerine for semi-permanent mounts. Fungal structures from and then a decrease in the number of healthy aphids. The first
dead infected aphids were measured to allow species identifica- colonies of infected aphids were recorded on 15 March 2013, and
tion. Fungal species were identified according to taxonomic keys the peak of infection level was observed on 8 April 2013 (25.4%;
and monographs of Bałazy,14 Humber15 and Keller.16 n = 503). After this date, the number of healthy and infected aphids
decreased (Table 2).
2.4 Statistical analyses On B. oleracea var. italica 2, the density of healthy and infected
The numbers of healthy and infected aphids in each develop- aphids varied widely. The peak in the density of healthy aphids
ment stage (nymphs, apterae and alate adults) were compared by was 21.1 aphids plant−1 and was recorded on 7 June 2013. The
parametric ANOVA and Tukey’s (HSD) post hoc test with P = 0.05 infection levels varied between 6.1% (n = 196) and 58.2% (n = 67)
after log transformation of data. The risk of infection at the differ- throughout the period of observations. The highest percent-
ent developmental stages was compared with logistic regression. age of infection was 58.2% (n = 67), recorded on 24 June 2013
The Mann–Whitney U-test was used to compare the density of (Table 2).
healthy and infected aphids between crops. Analyses were per- The density of healthy aphids was higher on B. oleracea var.
formed using InfoStat17 statistical software. italica 1 than in B. oleracea var. italica 2 (P < 0.05; Mann–Whitney
U = 5637.0), and the occurrence of infected aphids was more
common on B. oleracea var. italica 2, where infected aphids were
3 RESULTS recorded throughout the period of observations (Table 2). On
Brevicoryne brassicae L., M. persicae, Myzus ascalonicus Doncaster, B. oleracea var. italica 1, the occurrence of infected aphids was
Myzus sp., Lipaphis erysimi Kaltenbach, Lipaphis pseudobrassicae restricted to March and April, when the temperature decreased
(Davis), Pemphigus populitransversus Riley, A. gossypii and N. ribis- and the percentage humidity increased (more than 65%). The
nigri were the aphid species found infesting the crops studied percentage of infection was higher on B. oleracea var. italica 2
(Table 1). Brevicoryne brassicae was the predominant species on than on B. oleracea var. italica 1 (Table 2). The number of infected

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Prevalence of entomophthoralean fungi on aphids www.soci.org

Table 1. Entomophthoralean fungi identified on aphids on Brassica and L. sativa crops in Argentina

Crop Host Fungal species Date

Brassica oleracea var. capitata Myzus persicae Z. radicans 18-05-2010

E. planchoniana 01-06-2010
Myzus sp. Z. radicans 16-06-2010
B. brassicae Z. radicans 24-06-2010
08-07-2010
16-07-2010
Lipaphis erysimi
Lipaphis pseudobrassicae
Pemphigus populitransversus
Myzus ascalonicus
Lactuca sativa Aphis gossypii P. neoaphidis 16-06-2010
Myzus persicae P. neoaphidis 24-06-2010
E. planchoniana 08-07-2010
Myzus sp. P. neoaphidis 16-07-2010
05-08-2010
Nasonovia ribisnigri P. neoaphidis
E. planchoniana
Brassica oleracea var. botrytis Myzus persicae P. neoaphidis 01-06-2010
Lipaphis pseudobrassicae 16-06-2010
24-06-2010
Myzus sp. P. neoaphidis
08-07-2010
B. brassicae Z. radicans 16-07-2010
05-05-2011
13-05-2011
19-05-2011
24-06-2011
01-07-2011
08-07-2011
Brassica oleracea var. italica B. brassicae P. neoaphidis 15-03-2013
Z. radicans 25-03-2013
M. persicae P. neoaphidis 05-04-2013
08-04-2013
Z. radicans
19-04-2013
22-04-2013
23-04-2013
07-05-2013
17-05-2013
22-05-2013
31-05-2013
07-06-2013
14-06-2013
24-06-2013
16-07-2013
24-07-2013

aphids was significantly higher on B. oleracea var. italica 2 (P < 0.05; B. oleracea var. italica 2, the risk that alate adults would be infected
Mann–Whitney U = 641). was greater than the risk that nymphs would be infected (Table 3).
On B. oleracea var. botrytis (2010) and on both crops of B. oleracea
var. italica, the risk that apterous adults would be infected was
3.2 Association between infection levels and greater than the risk that nymphs would be infected (Table 3). On
developmental stages B. oleracea var. italica 1, the risk that nymphs would be infected was
On all crops except B. oleracea var. botrytis (2011), the proportions greater than the risk that alate adults would be infected (Table 3).
of infected aphids were significantly different between develop- On B. oleracea var. botrytis (2010), L. sativa, B. oleracea var. capitata
mental stages (P < 0.05). Between nymphs and apterous adults and B. oleracea var. italica 2, the risk that alate adults would be
there were significant differences (P < 0.05) on all crops except B. infected was greater than the risk that apterous adults would be
oleracea var. botrytis (2010). When comparing nymphs and alate infected (Table 3). B. oleracea var. italica 1 was the only crop where
adults, we found significant differences on all crops except B. oler- the risk that apterous adults would be infected was greater than
acea var. italica 1 and L. sativa (P > 0.05). There were significant the risk that alate adults would be infected.
differences between apterous adults and alate adults on all crops
except B. oleracea var. botrytis (2011) (P > 0.05) (Table 3).
Regarding the infection risk between developmental stages 4 DISCUSSION AND CONCLUSIONS
(Table 3), we found that on L. sativa and B. oleracea var. capitata The prevalence of entomophthoralean fungi in aphids has been
the risk that nymphs would become infected was greater than the previously studied. In Argentina, we have previously recorded P.
risk that apterous adults would become infected (Table 3). Also, on neoaphidis causing mortalities of up to 97% (n = 257) on aphids
L. sativa, B. oleracea var. capitata, B. oleracea var. botrytis (2010) and on cereal crops.11 On horticultural crops, Scorsetti et al.10 recorded

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 www.soci.org RG Manfrino et al.

Table 2. Mean number of healthy and infected aphids and percentage of infection by sampling datea

Crops Sample date Healthy aphids Infected aphids Percentage of infection

Brassica oleracea var. capitata 18-05-2010 11.80 (10.2) c 3.60 (5.7) b 23.4
01-06-2010 7.20 (8.2) b 1.05 (1.3) a 12.7
16-06-2010 0.80 (2.7) a 0.95 (1.7) a 54.3
24-06-2010 0.85 (2.5) a 0.55 (0.9) a 39.3
08-07-2010 1.58 (3.8) a 0.84 (0.9) a 34.8
16-07-2010 0.55 (1.3) a 1.70 (3.1) a 75.6
05-08-2010 0.00 (0.0) a 0.00 (0.0) a 0
Lactuca sativa 16-06-2010 1.50 (2.1) b 0.60 (0.8) ab 26.8
24-06-2010 3.20 (4.1) c 0.75 (1.2) ab 19
08-07-2010 1.55 (1.3) b 1.85 (1.9) bc 54.4
16-07-2010 1.70 (2.3) b 2.65 (4.0) c 60.9
05-08-2010 0.00 (0.0) a 0.30 (0.0) a 100
07-09-2010 0.00 (0.0) a 0.00 (0.0) a 0
Brassica oleracea var. botrytis (2010) 01-06-2010 10.40 (5.5) b 1.85 (1.8) ab 14
16-06-2010 4.10 (6.5) a 4.00 (4.0) b 49.4
24-06-2010 4.40 (7.9) a 2.85 (3.8) ab 39.3
08-07-2010 1.30 (2.6) a 2.35 (3.9) ab 64.4
16-07-2010 0.95 (2.6) a 0.95 (1.9) ab 50
Brassica oleracea var. botrytis (2011) 08-04-2011 0.85 (3.5) a 0.00 (0.0) a 0
05-05-2011 1.25 (2.3) a 0.05 (0.2) a 3.8
13-05-2011 4.10 (8.2) b 0.65 (2.4) a 13.7
19-05-2011 2.30 (4.9) ab 0.25 (0.7) a 9.8
27-05-2011 0.00 (0.0) a 0.00 (0.0) a 0
13-06-2011 0.00 (0.0) a 0.00 (0.0) a 0
24-06-2011 0.15 (0.6) a 3.60 (9.1) b 96
01-07-2011 0.75 (2.4) a 0.65 (1.6) a 46.4
08-07-2011 0.00 (0.0) a 0.20 (0.4) a 100
20-07-2011 0.25 (1.1) a 0.00 (0.0) a 0
Brassica oleracea var. italica 1 28-12-2012 0.00 (0.0) a 0.00 (0.0) a 0
04-01-2013 0.00 (0.0) a 0.00 (0.0) a 0
08-01-2013 3.05 (3.4) a 0.00 (0.0) a 0
15-01-2013 1.95 (8.0) a 0.00 (0.0) a 0
23-01-2013 13.40 (17.2) ab 0.00 (0.0) a 0
08-02-2013 73.15 (165.9) c 0.00 (0.0) a 0
14-02-2013 259.60 (191.9) e 0.00 (0.0) a 0
22-02-2013 121.10 (146.1) d 0.00 (0.0) a 0
15-03-2013 55.40 (59.1) b 1.00 (4.2) a 1.8
25-03-2013 15.80 (14.6) ab 0.50 (1.8) a 3.1
05-04-2013 16.65 (16.3) ab 1.00 (3.0) a 5.7
08-04-2013 18.75 (10.7) ab 6.40 (12.0) b 25.4
19-04-2013 3.05 (7.4) a 0.00 (0.0) a 0
23-04-2013 6.65 (5.6) ab 0.40 (0.8) a 5.7
07-05-2013 0.75 (0.4) a 0.00 (0.0) a 0
17-05-2013 0.10 (0.4) a 0.00 (0.0) a 0
22-05-2013 1.00 (3.8) a 0.00 (0.0) a 0
31-05-2013 0.50 (2.2) a 0.00 (0.0) a 0
Brassica oleracea var. italica 2 25-03-2013 1.45 (2.1) a 0.10 (0.4) a 6.5
05-04-2013 11.05 (6.4) c 2.10 (3.7) cd 16
08-04-2013 5.40 (4.3) ab 1.50 (1.1) abcd 21.4
19-04-2013 1.25 (3.0) a 0.45 (0.7) abc 26.5
22-04-2013 5.05 (12.0) ab 0.35 (1.1) ab 6.5
07-05-2013 3.55 (6.3) ab 0.40 (0.5) ab 10.1
17-05-2013 4.75 (7.1) ab 0.75 (1.3) abcd 13.6
22-05-2013 9.20 (13.7) bc 0.60 (2.2) abc 6.1
31-05-2013 4.30 (11.8) ab 0.55 (1.7) abc 11.3
07-06-2013 21.35 (20.5) d 2.30 (3.7) d 9.8
14-06-2013 3.60 (6.9) ab 1.50 (2.9) abcd 29.4
24-06-2013 1.40 (3.2) a 1.95 (4.7) bcd 58.2
16-07-2013 1.25 (3.9) a 0.25 (0.4) ab 16.7
24-07-2013 0.65 (2.0) a 0.30 (0.9) ab 31.6
a Entries show the mean number (± SE) of healthy and infected aphids. Means sharing the same lower-case letter are not statistically different (P > 0.05).

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Prevalence of entomophthoralean fungi on aphids www.soci.org

Table 3. Comparison of the number of infected aphids between developmental stages and between observation dates

Comparison between developmental stages Logistic regression Comparison between observation dates
Crop Chi square Stagesa Signif. Risk Signif. Chi square Signif.

L. sativa 0.000 N & aa 0.002 2.25 0.001 45.79 0.000

N & al 0.096 0.37 0.002
aa & al 0.001 0.16 0.106
B. oleracea var. capitata 0.000 N & aa 0.034 1.55 0.000 88.39 0.000
N & al 0.000 0.09 0.034
aa & al 0.000 0.05 0.000
B. oleracea var. botrytis (2010) 0.000 N & aa 0.063 0.84 0.001 97.14 0.000
N & al 0.000 0.05 0.393
aa & al 0.000 0.06 0.000
B. oleracea var. botrytis (2011) 0.423 N & aa 0.212 – – 185.65 0.000
N & al 0.863 – –
aa & al 0.405 – –
B. oleracea var. italica (summer–spring) 0.000 N & aa 0.000 0.54 0.000 2094.07 0.000
N & al 0.338 1.62 0.000
aa & al 0.026 2.99 0.342
B. oleracea var. italica (autumn–winter) 0.000 N & aa 0.002 0.60 0.000 159.37 0.000
N & al 0.000 0.16 0.002
aa & al 0.000 0.27 0.000
a N: nymphs; aa: apterous adults; al: alate adults.

P. neoaphidis from N. ribisnigri on L. sativa, with a prevalence of most of the host population consisted of nymphs. According
56.6% (n = 30), while we have previously recorded infection levels to Steinkraus,14 dense populations of aphid nymphs may allow
of P. neoaphidis and of E. planchoniana on aphids on S. melongena fungal pathogens to spread rapidly. Scorsetti et al.10 found that
and on C. annuum and observed the development of epizootics N. ribisnigri was equally susceptible to fungal disease throughout
of these fungal species on M. persicae.12 In the present study, we its life cycle. Kim and Roberts21 suggested that early instars of cot-
found P. neoaphidis, E. planchoniana and Z. radicans parasitising ton aphids can escape from fungal infection owing to the combi-
four aphid species. Zoophthora radicans was recorded causing nation of three factors: the low number of conidia attached to their
epizootics on B. brassicae, reaching levels of 96% (n = 75) on B. cuticles, the low levels of conidium germination and quick moult-
oleracea var. botrytis during 2011. ing. These factors would promote the removal of conidia before
The highest percentages of infection recorded in this study coin- the germ tube penetrates into the haemolymph of the host.
cided with periods of high relative humidity and comparatively This study represents the first record of prevalence on lettuce
low temperatures. Comparison of the prevalence recorded on and Brassica crops in Santa Fe Province, Argentina. It also repre-
B. oleracea var. italica between the two periods of observations sents an advance in the study of the epidemiology of entomoph-
(spring–summer and autumn–winter) allowed variables such as thoralean fungi on aphids in relation to developmental stages of
type of crop or species of aphid host to be separated from the aphids.
analysis, confirming that the conditions of temperature and rel-
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