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Mutualistic interaction of aphids and ants in pepper,

Capsicum annuum and Capsicum frutenscens (Solanaceae)

Diana Nataly Duque-Gamboa

*; https://orcid.org/0000-0003-1859-8381

Anderson Arenas Clavijo

; https://orcid.org/0000-0001-5639-5273

Andres Posso-Terranova

; https://orcid.org/0000-0002-2647-3397

Nelson Toro-Perea

; https://orcid.org/0000-0002-2835-7285

1. Centro de Investigación e Innovación en Bioinformática y Fotónica (CIBioFi), Universidad del Valle, Cali, Colombia;

diana.nataly.duque@correounivalle.edu.co (*Correspondence)

2. Departamento de Biología, Universidad del Valle, Cali, Colombia; anderson.arenas@correounivalle.edu.co

3. Seed and Developmental Biology, Global Institute for Food Security - GIFS, University of Saskatchewan, Saskatoon,

Canada; andres.posso@usask.ca

4. Centro de Investigación e Innovación en Bioinformática y Fotónica (CIBioFi), Universidad del Valle, Cali, Colombia;

nelson.toro@correounivalle.edu.co

Received 10-VIII-2020. Corrected 08-IV-2021. Accepted 06-V-2021.

ABSTRACT

Introduction: Adequate biological identification is fundamental for establishing integrated pest management

programs and identifying the trophic and mutualist relationships that can affect pest population dynamics.

Aphids are the main pest of pepper Capsicum spp. (Solanaceae) crops in Southwestern Colombia, due to their

role as vectors of viruses. However, the identification of aphid species is complex, limiting the investigations

performed to address their interactions with other organisms. Ants and aphids present a facultative mutualistic

relationship, that promotes the growth of hemipteran colonies, for this reason, the study of the ecological mutu-

alistic association between aphids and ants is important. Objective: The main objective was to discriminate the

aphid species present in commercial crops of Capsicum spp., and to identify the ant community that attends the

aphid colonies and its effects on the size of the aphid colonies. Methods: Aphid species, and their ant mutualist,

were collected from Capsicum annuum and Capsicum frutescens, in the Cauca valley, Southwestern Colombia.

We used the DNA barcoding approach to identify aphid species, and the ants were identified by morphology-

based taxonomy. To evaluate the effect of ant care on the size and structure of aphid colonies, generalized linear

models were calculated using as the response variables the total number of aphids for each colony and the pro-

portion of nymphs. Results: The aphid species that attack pepper crops, are: Aphis gossypii and Myzus persicae

(Hemiptera: Aphididae), with A. gossypii being the species that interacts with ants (19 ant species). A. gossypii

colonies attended by ants had larger sizes and more nymphs per colony, than those not attended. Conclusions:

Although the aphid-ant interaction is not species-specific, it is necessary to consider its role in the propagation of

viral diseases in peppers and to determine how this interaction may affect regional biological control strategies.

Key words: Aphis gossypii; Myzus persicae; COI; DNA barcoding; ants.

Duque-Gamboa, D.N., Arenas Clavijo, A., Posso-Terranova, A.,

Toro-Perea, N. (2021). Mutualistic interaction of aphids

and ants in pepper, Capsicum annuum and Capsicum

frutenscens (Solanaceae). Revista de Biología Tropical,

69(2), 626-639. https://doi.org/10.15517/rbt.v69i2.43429

https://doi.org/10.15517/rbt.v69i2.43429

Herbivorous insects become pests of culti-

vated systems (Mazzi & Dorn, 2012), because

of the increasing nutritional value of plants via

the addition of nitrogen and homogenization of

plant communities in the agricultural system

(Matson, Parton, Power, & Swift, 1996; Altieri,

1999; Rusch, Bommarco, & Ekbom, 2017).

Aphids (Hemiptera: Aphididae) are among the

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leading insect pests worldwide due to the phys-

iological stress their feeding generates in their

host plants and their ability to transmit phy-

topathogenic viruses (Goggin, 2007; Brault,

Uzest, Monsion, Jacquot, & Blanc, 2010).

The identification of aphid species is com-

plex due to their evolutionary tendency of

losing taxonomically useful morphological

characters and their environmental plasticity

(Foottit, 1997; Foottit, Maw, Von Dohlen, &

Hebert, 2008). Classical morphological and

taxonomical identification involves micromet-

ric measurements of certain characteristics

at specific developmental stages, which are

usually during the adult stage of the female

(Holman, 1974), thus requiring the rearing

of insects (Blackman & Eastop, 2007). The

presence of different morphological variants

in the same species increases the difficulty

of identifying these insects and subsequently

identifying and characterizing species-specific

relationships at different levels, such as her-

bivore-host, parasitoid-host and virus-vector

relationships (Foottit et al., 2008; Miller &

Foottit, 2009; Nie, Pelletier, Mason, Dilworth,

& Giguère, 2011; Pelletier et al., 2012).

A useful complement in the identification

of species of the family Aphididae has been

the use of the mitochondrial region called the

“DNA barcode”, which corresponds to a frag-

ment of approximately 700 base pairs at the

5 ‘end of the cytochrome c oxidase I (COI)

gene (Foottit et al., 2008; Miller & Foottit,

2009; Chen, Jiang, & Qiao, 2012). This tech-

nique proposed by Hebert, Cywinska and Ball

(2003), has allowed for the rapid identifica-

tion of aphid species by considering genetic

distance thresholds specific to this group and

comparing the sequences with those available

in public reference databases (Coeur d’acier

et al., 2014). DNA barcoding has also con-

tributed to the discrimination of cryptic aphid

species (Piffaretti et al., 2012), the association

of morphological variants with different devel-

opmental stages in the same species (Miller &

Foottit, 2009) and the establishment of differ-

ent morphotypes that a species can present in

different host plants (Lokeshwari, Kumar, &

Manjunatha, 2014).

Another advantage of molecular techniques

is the identification of species at any develop-

mental stage of the pest (Armstrong & Ball,

2005). This type of reliable and early detec-

tion is of great phytosanitary value because it

allows for a timely and adequate response to

a potential impact (Armstrong & Ball, 2005;

Mazzi & Dorn, 2012). At the same time, proper

identification of the species is also essential for

establishing integrated pest management (IPM)

and clarifying different ecological and trophic

interactions that may affect the biological con-

trol of pests (Foottit, Maw, Havill, Ahern, &

Montgomery, 2009; Pelletier et al., 2012).

Among the different ecological interac-

tions that aphids establish with other organ-

isms, the mutualistic relationship with ants

(Hymenoptera: Formicidae) is noteworthy.

Although this interaction is facultative and

not species-specific (Buckley, 1987; Collins &

Leather, 2002), it contributes to the population

growth of aphids, which provide sugar secre-

tions to ants while the ants offer protection

from generalist and specialist aphidophagous

predators (Styrsky & Eubanks, 2007; Powell

& Silverman, 2010a). Negative aspects of this

interaction may include reduced size and repro-

ductive fitness of aphids and its predation by

ants (Billick, Hammer, Reithel, & Abbot, 2007;

Yao, 2014; Hosseini, Hosseini, Katayama, &

Mehrparvar, 2017). This mutualist association

can interfere with integrated pest management

and this interference is why its description in

agricultural systems is relevant.

Aphids are the main pest of the pepper

Capsicum spp. in Colombia because they can

transmit phytopathogenic viruses of the genera

Potyvirus and Cucumovirus (Van Emden &

Harrington, 2003), which affect these crops

(Pardey & García, 2011), and depending on the

level of incidence of the disease, and the age

of the crop plants at the time of the infection,

losses in the crop may reach 100 % (Kenyon,

Kumar, Tsai, & Hughes, 2014). However, the

morphological identification of these aphids is

complex, aphid species identity and diversity

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are unknown, therefore, the ecological inter-

actions with other insects in this agricultural

system are not well identified. For this reason,

this study sought to identify both the aphid

species present in the pepper crops, cayenne

pepper Capsicum annuum L. and tabasco pep-

per Capsicum frutescens L. (Solanaceae), in

Southwestern Colombia, as well as mutualistic

ant species associated with the care of aphid

colonies and to evaluate the effect of ant care

on the size of the aphid colonies. Finally, the

present study aimed to explore and illustrate

the plant-aphid-ant interaction networks in

Capsicum spp. commercial farming systems.

MATERIALS AND METHODS

Obtaining insects: Commercial crops of

Capsicum spp. were visited in seven loca-

tions in Valle del Cauca, Southwestern Colom-

bia, Bolivar (04°17’60.0” N & 76°12’28.8”

W), Roldanillo (4°24’14.4” N & 76°08’42.0”

W; 04°28’30.0” N & 76°07’04.8” W), Toro

(04°36’21.6” N & 76°04’58.8° W; 04°36’21.6”

N & 76°05’24.0” W), Dagua (03°45’10.8° N

& 76°39’21.6” W), Guacari (03°45’00.0” N

& 76°19’30.0” W), Rozo (03°37’15.2” N &

76°25’14.5” W; 03°37’10.6” N & 76°23’22.9”

W), Vijes (03°42’18.0” N & 76°25’48.0” W);

and they included four cayenne pepper (C.

annuum) and six tabasco pepper (C. frutescens)

sampling sites (Fig. 1). Each location was vis-

ited at two phenological stages between Janu-

ary (before flowering) and August (flowering

and fruiting stage) of 2017. The area analysed

corresponds to the inter-Andean valley of the

Cauca river, located between the Western and

central mountain ranges. In this regional scale,

the surface covered is an inter-Andean tectonic

depression between 900 m to 1 000 m of eleva-

tion, it presents 23.3 ± 6 ° C and 79 ± 24 % RH

(Instituto Geográfico Agustín Codazzi, 1998;

Cueto, 2006; Montoya-Colonia, 2010).

Because aphids enter the fields of tabasco

pepper crops in Southwestern Colombia from

the edges and present an aggregate distribution

Fig. 1. Geographical location of the sampled sites. Yellow indicates the localities with tabasco pepper (C. frutescens) crops

and red indicates the localities with cayenne pepper (C. annuum) crops.

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pattern (Tálaga et al., 2017), a manual sampling

of aphids was performed, covering the perime-

ter of the cultivated area, in plants separated by

20 m to avoid the collection of aphids belong-

ing to the same colony and to obtain a good

representation of the diversity of these insects.

The individual colonies of aphids as well as the

associated ants that were observed attending

the aphid colonies were manually collected in

90 % ethanol, separated in the laboratory, and

stored at -20 °C until analysis.

Identification of aphids and mutual-

istic ants: To identify the aphids present in

the crops, the apterous adult insects collected

were grouped according to the macroscopic

morphological characteristics described by

Holman (1974). For the DNA extraction and

COI sequencing procedures, specimens of each

morphological variant were randomly selected

in each crop and sampled locality.

DNA extraction was performed using the

complete body of each aphid and the commer-

cial animal tissue kit from QIAGEN following

the manufacturer’s recommendations. Ampli-

fication of the COI fragment (658 base pairs)

was performed using primers LCO1490 (5’

ggtcaacaaatcataaagatattgg-3’) and HCO2198

(5’-taaacttcagggtgaccaaaaaatca-3’) (Folmer,

Black, Hoeh, Lutz, & Vrijenhoek, 1994) in 25

μL of amplification cocktail with 1X PCR buf-

fer solution, 2 mM MgCl2, 0.05 mM dNTPs,

0.25 μM of each primer, 1U of Taq DNA

polymerase, and 5-10 ng of DNA. The tem-

perature profile for the reaction included an

initial denaturation step for 5 min at 92 °C,

which was followed by 35 cycles of 30 s at 94

°C, 1 min at 52 °C, and 1 min at 72 °C; and a

final extension for 5 min at 72 °C. Sequenc-

ing was performed via the specialized supplier

Macrogen USA, and the sequences obtained

were edited and aligned using Mega 7 (Kumar,

Stecher, Tamura, & Dudley, 2016).

The COI identification sequence was

mainly based on three aspects: the neighbour

joining (NJ) analysis based on the Kimura two-

parameter (K2P) nucleotide substitution model

(Kumar et al., 2016), the estimation of genetic

distances between COI haplotypes estimated

with the K2P model using Mega 7 (Kumar et

al., 2016) and a comparison of the similarity

and sequence homology of the unique haplo-

types obtained for aphids with those available

in public databases, such as the NCBI GenBank

(Hebert et al., 2003; Ratnasingham & Hebert,

2007). Sequences representing each haplotype

per species on the different host plants were

deposited in GenBank under the unique acces-

sion codes MK766466-MK766469.

To estimate the genetic distancing thresh-

olds expected for the species found, the haplo-

types reported in the NCBI database and their

intraspecific and interspecific differentiation

values were compared with those obtained by

analysing the distance values in the collected

aphids via the Automatic Barcode Gap Discov-

ery ABGD programme (Puillandre, Lambert,

Brouillet, & Achaz, 2012).

The identification of ants was performed

at the Laboratory of Ant Biology and Ecology,

Universidad del Valle (Cali, Colombia) using

specialized taxonomic keys (Fernández, Guer-

rero, & Delsinne, 2019), the AntWeb v8.41

digital tool (California Academy of Sciences,

2020), and by direct comparison with speci-

mens deposited at the Entomological Museum

of Universidad del Valle (MUSENUV).

Mutual association between aphids and

ants: To visualize the structural patterns of

the host plant-aphid-ant trophic network, the

programme Food Web Designer 3.0 was used

(Sint & Traugott, 2016). To evaluate the effect

of ant care on the size and structure of aphid

colonies, generalized linear models were cal-

culated using the programme R V3.4.4 (R Core

Team, 2018). The response variables were the

total number of aphids for each colony and

the proportion of nymphs, with the latter used

as a measure of the reproductive success of

the colony.

RESULTS

Identification of pest aphids: The 1 504

apterous adult insects collected were grouped

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according to the macroscopic morphological

characteristics described by Holman (1974)

in two groups corresponding to the genera

Aphis (N= 1 460) and Myzus (N= 45). Aphis

presented 4 colour variants, while Myzus pre-

sented only one.

Among the 144 specimens selected for

the COI characterization, a total of 124 aphids

of the genus Aphis were obtained, and they

included four colour variants, yellow (21 speci-

mens from tabasco pepper and 18 from cay-

enne pepper), beige (13 sampled in tabasco

pepper and 15 from cayenne pepper), green

(22 specimens from tabasco pepper and 19

from cayenne pepper), brown (5 specimens

collected in tabasco pepper and 11 from cay-

enne pepper), while a total of 20 aphids of the

genus Myzus were obtained, and they included

a single colour pattern in both hosts. The NJ

analysis based on the K2P nucleotide substitu-

tion model (Fig. 2) indicated that the different

morphological groups corresponded to two

genetic groups, with each genetic group only

presenting one haplotype. The genetic distance

estimated with the K2P model among the COI

haplotypes was 9.3 %. A comparison of the

haplotypes obtained with those available in

the NCBI database indicated a similarity and

homology of sequences of 100 %, with the col-

lected specimens in group 1 corresponding to

the species Aphis gossypii (Glover, 1877) and

those in group 2 corresponding to the species

Myzus persicae (Zulser, 1776).

The haplotype sequences of A. gossypii

(69 haplotypes, 276 sequences) and M. persi-

cae (24 haplotypes, 101 sequences) available in

the NCBI were analysed with ABGD software,

and variation of less than 2 % was expected at

the intraspecific level and the differentiation

between these two species ranged between 9

and 11 %. These findings indicate that the dis-

tance value observed for this marker (9.3 %)

between the two genetic groups of aphids col-

lected in the cultivation of Capsicum spp. (Fig.

2) corresponded to interspecific differentiation.

Mutualistic association between aphids

and ants: We found 23 colonies of M. persi-

cae, with 19 in cayenne pepper crops and 4 in

tabasco pepper; however, none of the colonies

showed an association with ants (Fig. 1). We

also found a total of 408 colonies of A. gos-

sypii, with 192 in C. frutescens and 216 in C.

annuum; and of these colonies, 46 C. frutes-

cens colonies and 48 C. annuum colonies were

attended by ants, for an incidence of ant care of

23.9 and 22.2 %, respectively (Fig. 1, Table 1).

A total of 19 ant species were recorded from

colonies of A. gossypii, and they represented

four subfamilies and eight tribes, which are

Fig. 2. Neighbour joining (NJ) analysis based on the K2P model with 1 000 bootstrap samples using 144 COI sequences of

aphids collected in cayenne (C. annuum) and tabasco (C. frutescens) pepper crops in Southwestern Colombia.

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TABLE 1

Record of ant species that attend colonies of A. gossypii in crops of Capsicum spp. in Southwestern Colombia

Ant species

Cayenne pepper C. annuum Tabasco pepper C. frutescens

Bolívar Roldanillo Toro Dagua Guacarí Rozo Vijes

Azteca instabilis (Smith, 1862)

0 0 1 0 0 0 0

Brachymyrmex heeri (Forel, 1874)

2 7 5 0 0 0 6

Brachymyrmex longicornis (Forel, 1907)

0 2 2 0 0 0 0

Brachymyrmex obscurior (Forel, 1893)

0 0 1 0 0 0 0

Camponotus brevis (Forel, 1899)

0 0 3 0 0 0 0

Camponotus lindigi (Mayr, 1870)

0 0 0 4 4 0 0

Cardiocondyla obscurior (Wheeler, 1929)

0 0 0 0 0 0 1

Crematogaster abstinens (Forel, 1899)

0 0 0 0 1 0 0

Dorymyrmex brunneus (Forel, 1908)

0 0 1 1 2 1 1

Linepithema neotropicum (Wild, 2007)

0 0 0 0 1 0 0

Monomorium floricola (Jerdon, 1851)

2 1 1 0 0 3 1

Nylanderia steinheili (Forel, 1893)

0 0 1 0 0 0 0

Paratrechina longicornis (Latreille, 1802)

1 2 1 0 6 0 0

Pheidole sp.1

0 0 0 2 9 0 0

Pseudomyrmex simplex (Smith, 1877) 0 0 0 0 1 0 0

Solenopsis geminata (Fabricius, 1807)

0 0 0 1 0 0 0

Tapinoma melanocephalum (Fabricius, 1793)

1 2 3 0 0 0 0

Tetramorium bicarinatum (Nylander, 1846)

9 0 0 0 0 0 0

Tetramorium simillimum (Smith, 1851)

0 0 0 1 0 0 0

Number of mutualistic events recorded 15 14 19 9 24 4 9

Number of species involved in mutualistic interaction 5 5 10 5 7 2 4

Fig. 3. Network illustrating the mutualistic relationship between ants and aphids that attack cayenne pepper C. annuum and

tabasco pepper C. frutescens crops in Southwestern Colombia.

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listed in Table 1. Of the 19 species, 11 and 12

attended colonies of A. gossypii in cayenne

and tabasco pepper crops, respectively (Fig.

3). Of these ant species, Brachymyrmex heeri

(Forel, 1874), Dorymyrmex brunneus (Forel,

1908), Monomorium floricola (Jerdon, 1851)

and Paratrechina longicornis (Latreille, 1802)

were found in common between the two crops.

B. heeri represented 21 % of the interactions

with aphids, as summarised in Table 1. The

locality with the largest number of ant species

attending to aphids was Toro, with a total of 10

species recorded. Finally, the species with the

greatest distribution was M. floricola, which

was recorded in five locations.

The colonies collected from M. persicae

had an average colony size of 3 aphids, while

A. gossypii had an average colony size of 10.5

aphids. Because only A. gossypii showed an

interaction with ants, generalized linear models

were estimated using the data of this species.

This analysis indicates that A. gossypii colonies

had a greater number of individuals when they

were attended by ants for both crops (P < 0.05),

while the proportion of nymphs per colony was

higher in colonies attended by ants for tabasco

pepper (P < 0.001) (Fig. 4, Table 2).

DISCUSSION

The biological identification of insect pests

whose taxonomy is complex, such as aphids, is

fundamental for establishing trophic interac-

tions that may affect integrated pest manage-

ment. Our results support the implementation

of DNA barcoding as a cost-efficient aphid

identification tool for non-specialists (Mazzi

& Dorn, 2012) because aphid species could

be differentiated with certainty on a regional

spatial scale using 9.5 % of the adult specimens

collected based on this tool and the availabil-

ity of reference sequences in the NCBI. Other

researchers have concluded that this tool is par-

ticularly helpful in identifying aphids, such as

A. gossypii, which has different colour patterns

in different hosts, e.g., Malvaceae, Cucurbita-

ceae and Solanaceae (Lokeshwari et al., 2014).

Although aphids in warm areas are anholo-

cyclic and reproduce only by parthenogenesis

(Blackman, 1974; Dixon, Kindlmann, Leps, &

TABLE 2

Generalized linear models for colony size (number of individuals) and proportion of nymphs in colonies of A. gossypii

established in cayenne pepper C. annuum and tabasco pepper C. frutescens

Crop Response var. Distr. error P (Chi) DF resid. Dev. Resid

Effect of ants on

aphid colonies?

C. annuum

Colony size Negative binomial 0.0321 214 4.59 Yes

Nymphs/colony Binomial 0.0619 214 3.49 No

C. frutescens

Colony size Negative binomial < 0.001 190 29.99 Yes

Nymphs/colony Binomial < 0.001 190 12.28 Yes

Fig. 4. Effect of ant care on the size of colonies and

proportion of nymphs in colonies of A. gossypii established

in cayenne and tabasco crops. The error bars indicate 95 %

confidence intervals.

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Holman, 1987), different phenotypes are pre-

sented depending on the stage of development

of the insect, the host plant and environmental

stress (Lokeshwari et al., 2014). Tálaga et al.,

(2017) reported that in C. annuum, M. persicae

has a conserved phenotype during its differ-

ent stages of development; however, on this

same host, A. gossypii is polymorphic for body

colour, and has a total of eleven phenotypes

throughout its development. Our results are

consistent with those reported by Tálaga et al.,

(2017) because we showed that in C. annuum

and C. frutescens, the aphid M. persicae is

monomorphic while A. gossypii shows poly-

chromy. This pattern was consistent in the dif-

ferent locations of the inter-Andean valley of

Southwestern Colombia. The molecular marker

used here efficiently complemented the identi-

fication based on macroscopic morphological

characteristics.

Although the DNA barcode has reported

as a tool for conducting studies of genetic

diversity and population genetics (Hebert &

Gregory, 2005), in the case of Aphididae, intra-

specific variation at the mitochondrial level is

low (Xu, Chen, Cheng, Liu, & Francis, 2011).

Moreover, the genetic diversity of these insects

is much lower in areas where their introduction

is more recent (Figueroa et al., 2005), which

may explain the absence of intraspecific haplo-

type variation of A. gossypii and M. persicae at

the sampled spatial scale because although the

geographic origin of A. gossypii and M. persi-

cae is not clear, Aphidinae is presumably native

to temperate regions, especially of the Northern

Hemisphere (Kim, Lee, & Jang, 2011). The

polyphagous species A. gossypii, for example,

presents an intraspecific differentiation of 0.62

% according to Foottit et al., (2008), whose

study included specimens from locations that

span the geographic range of the species.

Many species of the family Aphididae

are important pests in agriculture worldwide

because in addition to direct damage to plants

caused by their feeding, they transmit phyto-

pathogenic viruses (Blanc, Uzest, & Drucker,

2011; Fereres & Raccah, 2015). Capsicum spp.

crops worldwide are affected by viral diseases

belonging to the families Bromoviridae and

Potyviridae, and both A. gossypii and M. per-

sicae are vectors of these phytopathogens

(Kenyon et al., 2014). A. gossypii is a compe-

tent vector of cucumber mosaic virus (CMV)

(Bromoviridae) and of chilli veinal mottle virus

(CVMV) (Potyviridae) (Hooks & Fereres,

2006; Kenyon et al., 2014), while M. persicae

has been reported as a vector of CMV, pepper

veinal mottle virus (PVMV) (Potyviridae) and

potato virus Y (PVY) (Potyviridae) (Palukaitis,

Roossinck, Dietzgen, & Francki, 1992; Mar-

tín, Collar, Tjallingii, & Fereres, 1997). In

Southwestern Colombia, the pepper deforming

mosaic virus (PepDMV) (Potyviridae: Poty-

virus) has been reported as the predominant

viral disease agent in Capsicum spp. (Pardey,

Posso-Terranova, & García, 2005); however,

the persistence, distribution, and insect vec-

tors of these diseases in these crop systems are

unknown. A. gossypii and M. persicae have

not been reported as PepDMV vectors; how-

ever, it is necessary to evaluate their role in the

transmission of this disease because insects of

Aphididae are strongly associated with viruses

of the family Potyviridae.

The colonies of M. persicae were found in

lower proportions and densities in comparison

to the colonies of A. gossypii on cayenne and

tabasco peppers, although both aphid species

present similar values in terms of life cycle

duration, longevity and fertility when grown

on cayenne pepper under laboratory conditions

(Tálaga et al., 2017). The low density in the

colonies of M. persicae compared to those of

A. gossypii on the same hosts can be explained

by the regional context of the agricultural

system of peppers in Southwestern Colombia.

In Colombia, peppers are intensively planted

in large-scale mechanized agricultural sys-

tems (Corporación Colombia Internacional,

2006), although on a small scale, they are also

planted in home gardens. These crops grow as

a sun-exposed monocrop in the inter-Andean

valley of the Cauca River, with an average

temperature of 23.3 ± 6 °C and relative humid-

ity of 79 ± 2.4 %. These conditions limit the

development of M. persicae, which has lower

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reproductive performance and slower devel-

opment time compared to A. gossypii when

the daily temperature is above 20 °C (Satar,

Kersting, & Uygun, 2008). A. gossypii shows

optimal reproductive development above 17 °C

on plants of Capsicum spp. (Satar et al., 2008),

explaining why the regional conditions of the

inter-Andean valley of the Cauca River possi-

bly constitute an advantage for the colonization

of pepper plants by this aphid.

The ants present in the pepper crops did

not attend to colonies of M. persicae, and the

number and density of their colonies were

lower than those of A. gossypii. Previous stud-

ies have reported that A. gossypii frequently

establishes interactions with ants (Kaplan &

Eubanks, 2002; Kaplan & Eubanks, 2005;

Powell & Silverman, 2010a) while M. per-

sicae, which is considered a non-mutualistic

species of aphid, does not (Powell & Silver-

man, 2010b). Although M. persicae has the

same ability to produce sugar exudates with

carbohydrate quality similar to that generated

by other aphid species (Hogervorst, Wäck-

ers, & Romeis, 2007), the ants do not interact

with the colonies of this insect, and when both

species are present, M. persicae is preferably

consumed by the ants as prey (Powell & Sil-

verman, 2010b). The response behaviour of

M. persicae to potential predators explains

why it does not establish a relationship with

ants because this species of aphid rapidly

disperses from the colony when disturbed by

natural enemies and ants (Nault, Montgomery,

& Bowers, 1976; Belliure, Amorós-Jiménez,

Fereres, & Marcos-García, 2011). Attendance

by ants is more likely when the aphid spe-

cies presents swarming behaviour because the

area attended by ants is smaller (Stadler &

Dixon, 2005). In myrmecophiles (e.g., differ-

ent species of the genus Aphis), the aphids of

the colony are less easily dispersed or do not

disperse in their interaction with ants because

the alarm response is suppressed, which pro-

motes the swarming behaviour of the colony

(Nault et al., 1976).

Not all ant species attend to aphid colonies,

and those that are involved in this interaction

are opportunistic species that frequent extraflo-

ral nectaries as a source of energetic resources

(Delabie, 2001). In this study, species of For-

micinae, Dolichoderinae and Myrmicinae were

reported, and the genera reported in these

subfamilies have been previously involved in

this type of interaction with different species of

Aphididae (Katayama & Suzuki, 2003; Stadler

& Dixon, 2005; Buffa, Jaureguiberry, & Del-

fino, 2009; Silva & Perfecto, 2013; Campos &

Camacho, 2014). The species of these subfami-

lies are considered omnivorous, opportunistic

ants that are typical of agroecosystems and

intervened habitats (Fontenla & Alfonso-Sim-

onetti, 2018). Some species of Pseudomyrmex

have been reported in this interaction with scale

insects (Delabie, 2001; Ramírez, de Ulloa,

Armbrecht, & Calle, 2001; Buffa et al., 2009)

and aphids (Delfino, 2005; Silva & Perfecto,

2013). Species of this genus are considered to

be general foragers and opportunistic predators

(Fontenla & Alfonso-Simonetti, 2018).

A. gossypii colonies attended by ants had a

greater number of individuals, which may pro-

mote infestations of Capsicum spp. in South-

western Colombia. Ant care is influenced by

the quality (composition) and quantity of the

honeydew (Völkl, Woodring, Fischer, Lorenz,

& Hoffmann, 1999; Katayama & Suzuki,

2002), which indicates that a larger colony may

be more tractive to be attended by ants. Howev-

er, studies carried out by Hosseini et al., (2017),

indicate that regardless of the initial size of the

colony, this interaction generates an increase in

the density of the colony and the growth rate

is higher compared to the unattended colonies.

On the other hand, aphids in small colonies

invest more energy supplying the supply of

honeydew for ants; in large colonies, this effort

is less because more individuals contribute to

supply the demand for this substance (Kata-

yama & Suzuki, 2002).

Studies carried out by Hosseini et al.,

(2017) and de Siqueira, Fagundes, Sperber

and Fernandes (2011), indicate that this ant

aphid interaction generates positive effects

on the yield and biomass production of crop

plants, among others, because the spread of

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microorganisms is prevented by avoiding the

accumulation of aphid secretions, and the

abundance of other herbivores is reduced.

The interaction between A. gossypii and ants

is of interest in biological control because

ants interfere in the predation of this aphid

by aphidophagous generalists, such as Hip-

podamia convergens Guérin-Méneville, 1842

(Coleoptera: Coccinellidae) and Chrysoperla

carnea (Stephens) (Neuroptera: Chrysopidae)

(Kaplan & Eubanks, 2002; Powell & Sil-

verman, 2010a). Similarly, ant care reduces

parasitism rates in A. gossypii colonies (Powell

& Silverman, 2010a). Despite the fact that

direct ant interference by potential predators

or parasitoids was not observed in the field,

our results indicate a positive effect of ant care

on the reproductive effectiveness of the colony

(increased production of nymphs). In the con-

text of aphids as virus vectors, the mutualistic

interaction between aphids and ants of the

Solenopsis invicta Buren species in tomato

(Solanum lycopersicum L.) promotes aphid

abundance and results in an increase in the

number of plants affected by CMV (Cooper,

2005). Though, it is necessary to consider the

aphid-ant interaction role in the propagation of

viral diseases in commercial crops of Capsicum

spp. and to determine how this interaction may

affect regional biological control strategies.

The aphid species that infest commercial

crops of cayenne pepper C. annuum and tabas-

co pepper C. frutescens are A. gossypii and M.

persicae, which are potential vectors of the

virus that affect Capsicum spp. in Southwest-

ern Colombia. A total of 19 ant species were

found attending the A. gossypii aphids, whose

attended colonies were significantly larger than

those not attended by ants in commercial

crops. The mutualistic aphid-ant relationship

thus promotes an increase in the size of the

colonies of this aphid species. It is advisable

to explore the effect that ants can have on the

effectiveness of aphidophagous generalists and

specialists in the context of integrated pest

management for aphids in pepper crops in

Southwestern Colombia.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

The authors thank the farmers who allowed

us to sample their crops and the technical team

of Hugo Restrepo & Co. for their field assis-

tance. This research was co-financed by the

General System of Royalties of Colombia

(CIBIOFI BPIN-2013000100007), COLCIEN-

CIAS, Government of Valle del Cauca, Uni-

versidad del Valle (Internal Call for Mobility

Support - CIAM). We are grateful to the Post-

graduate School in Biological Sciences at the

University of Valle and Wilmar Torres for their

advice on the statistical analyses.

RESUMEN

Interacción mutualista de pulgones y hormigas

en pimiento, Capsicum annuum y

Capsicum frutenscens (Solanaceae)

Introducción: La adecuada identificación biológica

es fundamental para establecer programas de manejo

integrado de plagas e identificar las relaciones tróficas y

mutualistas que pueden afectar la dinámica poblacional de

insectos plaga. Los áfidos son las principales plagas del ají

Capsicum spp. (Solanaceae) en el suroccidente colombia-

no, debido a su rol como vectores de virus. Sin embargo,

su identificación es compleja, y limita las investigaciones

que intentan revelar sus interacciones con otros organis-

mos. Las hormigas y los áfidos presentan una relación

mutualista facultativa, que promueve el crecimiento de las

colonias de los hemípteros, por esta razón, el estudio de la

asociación ecológica y mutualista entre áfidos y hormigas

es importante. Objetivo: El principal objetivo de esta

investigación fue discriminar las especies de áfidos presen-

tes en cultivos comerciales de Capsicum spp., e identificar

la comunidad de hormigas que atiende las colonias de

áfidos y su efecto en el tamaño de las colonias de áfidos.

Métodos: los áfidos, y las hormigas mutualistas de estos

áfidos, se recolectaron de Capsicum annuum y Capsicum

frutescens, en el valle del rio Cauca, en el suroccidente

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colombiano. Se empleó el Código de barras del ADN para

identificar las especies de áfidos, y las hormigas se identi-

ficaron empleando taxonomía basada en morfología. Para

evaluar el efecto que tiene el cuidado de las hormigas sobre

el tamaño de las colonias de áfidos, se empleó un modelo

lineal generalizado, utilizando como variables de respuesta

el número total de áfidos por cada colonia y la proporción

de ninfas por colonia. Resultados: Las especies de áfidos

que atacan los cultivos de ají, son: Aphis gossypii y Myzus

persicae (Hemiptera: Aphididae), siendo A. gossypii la

especie que interactúa con hormigas (19 especies). Las

colonias de A. gossypii atendidas por hormigas presentan

mayor tamaño y número de ninfas, que aquellas desaten-

didas. Conclusiones: Aunque la interacción áfido-hormiga

no es especie específica, es necesario considerar su rol en la

propagación de enfermedades virales en plantas cultivadas

y determinar cómo esta interacción puede afectar la imple-

mentación de estrategias de control biológico.

Palabras clave: Aphis gossypii; Myzus persicae; COI;

código de barras del ADN; hormigas.

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