Parasitoids attacking agricultural pests in Ecuador

ANARTIA

Publicación del Museo de Biología de la Universidad del Zulia

ISSN 1315-642X (impresa) / ISSN 2665-0347 (digital)

Anartia, 33 (diciembre 2021): 7-26

Diversity of native and exotic parasitoids attacking agricultural

pests in Ecuador: are Ecuadorian biocontrol programs

in decline?

Diversidad de parasitoides nativos y exóticos que atacan plagas agrícolas

en Ecuador: ¿están en declive los programas de biocontrol ecuatorianos?

Dorys T. Chirinos1, María Anchundia1, Rossana Castro1, Jessenia Castro Olaya1,

Juan E. Geraud2 & Takumasa Kondo3

1Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Portoviejo, Ecuador.

2Facultad de Agronomía, Universidad del Zulia, Maracaibo, Zulia. Venezuela.

3Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), Palmira, Colombia.

Correspondence: Dorys T. Chirinos: dorys.chirinos@utm.edu.ec

(Received: 05-09-2021 / Accepted: 14-11-2021 / Online: 31-12-2021)

ABSTRACT

In Ecuador, agriculture is an important economic activity. Crops are grown mainly in the regions of the continental area:

Amazon, Andes and Coast. We conducted this study to elaborate a compendium about the diversity of parasitoids of agri-

cultural insect pests and to estimate the trend of biocontrol by the use of these natural enemies. Approximately 200taxa of

parasitoids were found to be reported controlling various pests that aect cultivated crops in continental Ecuador. e ma-

jor parasitoids referred in biological control in Ecuador are Telenomus spp. (Hymenoptera: Platygastridae), Trichogramma

spp. (Hymenoptera: Trichogrammatidae) and Encarsia spp. (Hymenoptera: Aphelinidae). e results suggest a decreasing

trend in the use of parasitoids as biocontrol agents from 1980 to the present (R2: 0.80, P<0.0001). In this paper, we discuss

the probable explanations of this trend.

Keywords: Biological control, hymenopterans, natural enemies, insect pests, tachinid ies, wasps.

RESUMEN

En Ecuador, la agricultura es una actividad económica importante. Los cultivos se siembran principalmente en las regiones

del área continental: Amazonia, Andes y Costa. Realizamos este estudio para elaborar un compendio sobre la diversidad de

parasitoides de plagas insectiles agrícolas y estimar la tendencia del biocontrol mediante el uso de estos enemigos naturales.

Se encontró que aproximadamente 200 taxa de parasitoides controlan varias plagas que afectan los cultivos en el Ecuador

continental. Los principales parasitoides utilizados en el control biológico en Ecuador son Telenomus spp. (Hymenoptera:

Platygastridae), Trichogramma spp. (Hymenoptera: Trichogrammatidae) y Encarsia spp. (Hymenoptera: Aphelinidae).

Los resultados sugieren una tendencia decreciente en el uso de parasitoides como agentes de control biológico desde 1980

hasta el presente (R2: 0,80, P <0,0001). En este artículo, discutimos las posibles explicaciones de esa tendencia.

Palabras clave: avispas, control biológico, enemigos naturales, himenópteros, moscas taquínidas, plagas.

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

INTRODUCTION

Historically, agriculture constitutes one of the funda-

mental pillars of the economy in Ecuador, through export

or local trade of a variety of crops, including banana, ca-

cao, coee, sugarcane, owers, vegetables, corn and potato

(Castillo et al. 2020, Peñalver-Cruz et al. 2019). ese

crops are mainly cultivated in the continental region of

the country, which is geographically divided by the An-

dean Mountains into three zones: the Coast, the Andes

and the Amazon (Fig. 1). roughout the crop produc-

tion process, biological competitors may appear, among

which insect pests stand out, whose populations must be

controlled to avoid adverse eects on productivity (Savary

et al. 2012, Culliney 2014).

In integrated pest management programs the rst pest

control alternative that must be considered is biological

control (Metcalf & Luckmann 1975). Although Ecuador

has a high diversity of agricultural pest species, there is also

a signicant ecological richness, as well as a considerable

abundance of natural enemies, among which parasitoids

stand out. In fact, parasitoids have been used extensively

for pest control in the coastal region since the 1980s (Cas-

tillo 2020). Additionally, in Ecuador, the existing infor-

mation on biological control of insect pests is limited to

conference reports, abstracts and proceedings (Castillo

2019). However, in certain cases such information is not

readily available (Castillo 2019) and furthermore, the in-

formation on parasitoid inventories associated to natural

biological control is dicult to access.

is study had two objectives: 1) to elaborate a com-

pendium of information about the diversity of parasit-

oids involved in biocontrol in Ecuador, with emphasis

on natural biological control and 2) to estimate the trend

of biocontrol as a pest control strategy since 1937 in this

country.

MATERIAL AND METHODS

Data selection

Studies involving parasitoids were obtained from the

databases, Scielo, the repositories of the National Insti-

tute of Agricultural Research (INIAP) of Ecuador and

Google Scholar. A literature search was carried out for

papers published between 1937 and 2020 that included

the keywords: agricultural pests, augmentative-, natural-,

conservation-, classical biological control, crops, diversity,

Figure 1. (A) Map of America illustrating the location of Ecuador (B) Map of Ecuador showing the regions: Andes, Amazon and Coast.

Parasitoids attacking agricultural pests in Ecuador

Ecuador, inventory of natural enemies, parasitism rates,

parasitoids, and pest management. We included technical

reports, conference abstracts, theses, book chapters, books

and scientic papers.

Data recording

We recorded studies in classical biological control,

augmentative biological control and natural biological

control. In the cases of classical biological control, the fol-

lowing were included: crop name, insect host, parasitoid

species, year of introduction, country of origin, region of

Ecuador where the control was carried out and the positive

or negative eect of the control. For studies on augmenta-

tive biological control, cases reported since the programs

began, and the time of application were reviewed.

Analysis of data

Once the information was collected, we plotted the fol-

lowing: a) parasitoid species by insect host per crop, indi-

cating the interactions between the trophic levels of each

agroecosystem, b) number of parasitoid species for each of

the geographical regions of continental Ecuador for those

species with three or more reports. We also conducted a

principal component analysis to associate the parasitoids

reported by geographical region. To obtain the principal

components, a standardization of the data was executed

(mean 0 and standard deviation 1), to avoid that the vari-

ables with greater variance dominated the others. Finally,

a regression model was estimated between the years of the

studies (X) versus the number of parasitoids (Y), adjusting

to a polynomial function (P < 0.0001).

Although the use of parasitoids began in 1937, only ve

studies with parasitoids were conducted in approximately

ve decades (1937-1979). Given that the substantial in-

crease in biocontrol programs with parasitoids began

in 1980, analyses were carried out evaluating the period

1980-2020.

RESULTS

Approximately 200 taxa of parasitoids were found to

be controlling various pests that aect cultivated crops in

continental Ecuador during the period 1937-2020. Among

the referred parasitoids, 10% belonged to the Order Dip-

tera, while 90% were found from the Order Hymenoptera.

Within the latter, the most abundant group was the super-

family Chalcidoidea followed by Platygastroidea.

Classical biological control

e rst classical biological control program was im-

plemented in Ecuador by Luis Rodríguez Torres who

introduced and established during 1937-1947 the aph-

elinid, Aphelinus mali Haldeman, 1851 (Hymenoptera:

Aphelinidae) to control the woolly apple aphid, Eriosoma

lanigerum Hausmann, 1802 (Hemiptera: Aphididae)

(Merino 1984). Later, in 1955, the parasitoid, Amitus hes-

peridum Silvestri, 1927 (Hymenoptera: Platygastridae)

was imported from Mexico with the intention of reduc-

ing the damage caused by the citrus blacky, Aleurocan-

thus woglumi Ashby, 1915 (Hemiptera: Aleyrodidae) on

citrus trees (Browning 1992, Merino 1984). Another pest

of citrus trees, the purple scale, Lepidosaphes beckii (New-

man, 1869) (Hemiptera: Diaspididae) was also the subject

of classic biological control program, using the parasitic

wasp, Aphytis lepidosaphes Compere, 1955 (Hymenop-

tera: Aphelinidae) (Merino & Vazquez 1962). ose pro-

grams were conducted in the Andean region with satis-

factory results. Unfortunately, the obtained references do

not present quantitative levels of parasitism and degrees of

infestation before and aer the programs were conducted.

e sugarcane borer, Diatraea saccharalis (Fabricius,

1794) (Lepidoptera: Crambidae) constitutes a major

problem in the coastal region where most sugarcane is

planted (Mendoza 2018). Although the parasitoid, Bil-

laea claripalpis Wulp, 1896 (Diptera: Tachinidae) was

known to occur in Ecuador as a biocontrol agent for this

pest, its parasitism rates were very low (18%) (Gaviria

1981). For this reason, a biological control program was

put into practice with a race of B. claripalpis introduced

from Peru back in 1965. At the time, the Peruvian race

was crossed with the native one, obtaining progeny that

showed a parasitism rates as high as 87.9%, which signi-

cantly reduced the infestation levels of the sugarcane borer

(Gaviria 1981).

Approximately 15 years later, two additional parasit-

oids of D. saccharalis were imported from Venezuela, the

parasitic ies, Lydella minense (Townsend, 1927) and

Lixophaga diatraeae (Townsend, 1916) (Diptera: Tachini-

dae) (Mendoza et al. 2005). However, none of those spe-

cies adapted to the Ecuadorian coast’s environment. At the

same time, the parasitic wasp, Cotesia avipes (Cameron,

1891) (Hymenoptera: Braconidae), was introduced from

Colombia, which together with B. claripalpis has been

able to regulate the populations of D. saccharalis (CIN-

CAE 2013, Mendoza 2018).

Castillo et al. (2020) refer several imports of egg para-

sitoids made from Colombia in 1983 with dierent levels

of success. Telenomus sp. (Hymenoptera: Platygastridae)

resulted in an eective control of the South American

white borer, Rupela albina Becker & Solis, 1990 (Lepi-

doptera: Crambidae) in rice. However, it is unknown if

Trichogramma semifumatum (Perkins, 1910) and Tricho-

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

gramma pretiosum Riley, 1871 (Hymenoptera: Tricho-

grammatidae), which were imported to control the bor-

ers, D. saccharalis and Diatraea lineolata (Walker, 1856)

(Lepidoptera: Crambidae), have had any eect controlling

the pests.

Between the years 1970 and 1990, cotton was pro-

duced on the Ecuadorian coast (FAO: Food and Agri-

culture Organization of the United Nations 2017) and in

1988 the parasitoid Bracon kirkpatricki (Wilkinson, 1927)

(Hymenoptera: Braconidae) was imported from Colom-

bia to control the pink bollworm, Pectinophora gossypiella

(Saunders, 1844) (Lepidoptera: Gelechiidae), with unsat-

isfactory results (Castillo et al. 2020). at same year, the

species Diachasmimorpha longicaudata Ashmead (Whar-

ton, 1987) (Hymenoptera: Braconidae), Psyttalia concolor

(Szépligeti, 1910) and Aganaspis daci (Weld, 1951) (Hy-

menoptera: Figitidae), were imported from the U.S.A.

for the biocontrol of fruit ies, Anastrepha spp. (Diptera:

Tephritidae) in cherimoya (Castillo et al. 2020). However,

those introductions did not show conclusive results. In

the Guayas province in the Ecuadorian coast, a classical

biological control program using the parasitoid D. longi-

caudata, introduced from Peru to control Anastrepha spp.

on various fruit trees was carried out in various locations

(Arias et al. 2009).

e coee berry borer, Hypothenemus hampei (Ferrari,

1867) (Coleoptera: Curculionidae) was detected in the

Zamora Chinchipe province (Amazon region) in 1981,

spreading to all other coee-producing areas of Ecuador

(Mendoza et al. 1994). In an eort to the control this de-

structive pest, during 1987-1988, two parasitoids, Prorops

nasuta Waterston, 1923 and Cephalonomia stephanoderis

Betrem, 1861 (Hymenoptera: Bethylidae) were intro-

duced by INIAP from Kenya and Togo in coee-produc-

ing provinces belonging to the three regions of continen-

tal Ecuador (Mendoza et al. 1994). Aer the quarantine

process and laboratory rearing, the species were released

(Klein Koch et al. 1988, Mendoza et al. 1994). Out of

the two parasitoids, C. stephanoderis was the best adapted

(82.0% parasitism) than P. nasuta (22.5%) (Klein Koch et

al. 1988).

A decade later, the parasitoid, Phymastichus coea La

Salle, 1990 (Hymenoptera: Eulophidae) was introduced

from Colombia, mediated by the Integrated Management

of Coee Berry Borer Project, and conducted by the Na-

tional Association of Coee Exporters of Ecuador (AN-

ECAFE), together with the International Institute for

Biological Control (Delgado et al. 2002). e wasps were

released during 2000 and 2001 in six Ecuadorian provinc-

es, reporting averages of parasitism that varied from 20 to

30% (Delgado et al. 2002).

Augmentative biological control

Some introduced parasitoid species were mass reared

and released during 1980-1990. Trichogramma sp. was

extensively released in the coastal region for the control

of eggs of various lepidopterous pests on cotton, soybean,

corn, as well as for the control of Tuta absoluta (Meyrick,

1917) (Lepidoptera: Gelechiidae) in tomato (Arias et al.

1992). In addition, there are also reports of releases of the

species Trichogramma fasciatum (Perkins, 1912) and T.

pretiosum in tomatoes grown in the Andes to control T.

absoluta (Castillo et al. 2020). Telenomus sp. was also used

in 1980 in an augmentative biological control program of

Diatraea spp. in corn (Arias et al. 1996). Subsequently, the

parasitoid, Encarsia formosa Gahan, 1924 (Hymenoptera:

Aphelinidae) was used in biocontrol programs of white-

y species (Hemiptera: Aleyrodidae) on tomato in the

Chimborazo province of the Andean region (Castillo et

al. 2020).

Most of the augmentative biological control programs

carried out since the 1980s were not sustainable over time.

However, the species B. claripalpis and C. avipes continue

to be released in sugarcane elds in the coastal region be-

cause they are considered the most eective methods for

controlling the sugarcane borer, D. saccharalis (CINCAE

2013, Mendoza 2018).

Currently, parasitoids are used as one of the pest man-

agement strategies in ower crops due to international

requirements. An example of this is the release of the para-

sitic wasp Diglyphus isaea (Walker, 1838) (Hymenoptera:

Eulophidae) for the control of the leafminer, Liriomyza

huidobrensis (Blanchard, 1926) (Diptera: Agromyzidae)

that causes losses in Gypsophila sp. summer owers (Prado

et al. 2018). Reported results of releases of D. isaea indicate

its important role as a biological control agent because of

the high percentages of parasitism (90%) associated with

low infestations of L. huidobrensis (Prado et al. 2018).

Parasitoids by crop and geographical region

e parasitoids reported for Ecuador are shown in Ta-

bles 1-12 and Figures 2-8. Each gure illustrates the inter-

connections, crop-insect host-parasitoid. Associated with

four important maize pests, 34 taxa of parasitoids have

been reported, four identied up to family, 11 at generic

level and 19 to species level (Table 1, Fig. 2).

On bananas and plantains, 22 genera and eight species

of parasitoids have been recorded as biocontrol agents for

fourteen phytophagous insects and one of those genera is a

hyperparasitoid (Table 2, Fig. 3). Interestingly, 77% of the

referred parasitoids associated with bananas and plantains

attack defoliator caterpillars. Attacking ve pests on Citrus

spp., 20 parasitoids have been reported belonging to eight

Parasitoids attacking agricultural pests in Ecuador

Table 1. Parasitoids reported in association with pests on corn, Zea mays L.

Pest Parasitoid Region Reference

Diatraea spp.

Billaea claripalpis

Cotesia flavipes

Lixophaga spherophori

Palpozenilla diatraeae

Palpozenilla sp.

Pediobius furvus

Coast Arias 2021, Páliz &

Mendoza 1999

Dalbulus maidis Gonatopus bartletti Coast Valarezo et al. 2009

Heliothis spp.

Glyptapanteles militaris

Lespesia spp.

Campoletis argentiflora

Chelonus texanus

Cotesia marginiventris

Encarsia spp.

Gonia sp.

Hyposoter albipes

Hyposoter exiguae

Conura igneoides

Therion californicum

Whinthemia sp.

Coast Mendoza 1994a, 1994b

Mocis latipes

Diptera: Sarcophagidae

Diptera: Tachinidae

Hymenoptera: Braconidae

Hymenoptera: Chalcididae

Coast Arias et al. 1996, Páliz

& Mendoza 1999

Spodoptera frugiperda

Chelonus sp.

Eiphosoma sp.

Euplectrus sp.

Meteorus sp.

Rogas sp.

Telenomus alecto

Telenomus remus

Coast Arias 2021, Mendoza

1994a, 1994b

Various Lepidoptera

Telenomus spp.

Trichogramma fasciatum

Trichogramma pretiosum

Trichogramma spp.

Andes Coast Benzing et al. 1997, Crespo

& Ramakrishna 1989,

Páliz & Mendoza 1999

genera and 12 species (Table 3, Fig. 4). Two important

pests of cassava in Ecuador are controlled by 17 primary

parasitoids (seven genera and ten species), and one associ-

ated hyperparasitoid has been reported (Table4, Fig.5A).

Eleven parasitoids (six genera and ve species) parasitize

two relevant pests associated with coee (Table5, Fig. 5B).

On vegetables, 13 taxa of insect pests have been re-

corded, which are controlled by 20 parasitoids classied in

eight genera and 12 species (Table 6). On the other hand,

17 parasitoids (11 genera and six species) are reported

parasitizing several species of phytophagous insects on

various fruit trees (Table 7). In rice agroecosystem, there

are ve major pests, which are controlled by 22 parasitoids

(17 genera and ve species) (Table 8, Fig. 6A). Four phy-

tophagous species that feed on sugarcane are attacked by

ten taxa of parasitoids, six identied to the genus level and

four to species level (Table 9, Fig. 6B).

Reports of parasitoids associated with eight phytopha-

gous insects in cacao date from 1980. In this agroeco-

system, 13 primary parasitoids (one species and 12 gen-

era) and one hyperparasitoid, were detected (Table 10,

Fig.7A). Additionally, two taxa of parasitoids were report-

ed attacking Neuroptera and Araneae (taxa with predatory

habits). In legumes (Fabaceae), 14 taxa of parasitoids were

mentioned (one species and 13 genera) that parasitize ten

insect hosts (Table 11, Fig. 7B).

Of the 12 phytophagous insects reported on palms,

two species belong to the family Chrysomelidae (Cole-

optera) and the rest to dierent families of Lepidoptera,

from which parasitoids belonging to six genera and seven

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

Figure 2. Parasitoids associated with pests that attack corn, Zea mays L. e arrows show the interconnections in the agroecosystem.

Pests are indicated in red letters and parasitoids in blue.

Figure 3. Parasitoids associated with pests that attack bananas and plantains. e arrows show the interconnections in the agroecosys-

tem. Pests are indicated in red letters, parasitoids in blue and hyperparasitoids in purple.

Parasitoids attacking agricultural pests in Ecuador

Table 2. Parasitoids reported in association with pests on bananas and plantains.

Pest Parasitoid Reference

Aleurotrixus floccosus Encarsia sp.

Eretmocerus sp.

Signiphora sp. Arias 2021

Anthichoris viridis, Caligo eurilochus, Caligo

teucer, Megalopyge sp., Opsiphanes tamarindi,

Phobetron sp., Sibine apicalis, Oiketicus kirbyi

Carinodes sp.

Casinaria sp.

Brachymeria incerta

Chetogena sp.

Cotesia opsiphanes

Cotesia sp.

Elachertus sp.

Iphiaulax sp.

Lampocryptidea sp.

Lespesia sp.

Macrocentrus sp.

Megaselia sp.

Meteorus sp.

Microgaster sp.

Neotheronia sp.

Rogas sp.

Sarcodexia lambens

Sarcodexia sternodontis

Sarcophaga sp.

Stenomesius ceramidiae

Systropus sp.

Telenomus sp.

Whinthemia sp.

Xenufens forsythi

Arias 2021, Arias et al. 1992,

Armijos 2008, Boucek 1962,

Malo & Willis 1961, Ramon 2010

Chaetanaphothrips signipennis,

Frankliniella parvula Megaphragma sp. Arias 2021

Dysmicoccus sp., Pseudococcus sp. Hambletonia pseudococcina Arias 2021,

Contreras-Miranda et al. 2021

Planococcus citri Leptomastix dactylopii

species have been reported (Table 12, Fig. 8). Using the

data reported in these studies, we estimated that the low-

est percentage of parasitoid taxa were found in sugarcane

and coee (4.8%), whereas the highest proportion of para-

sitoids is found in corn crop (14.8%), followed by those

observed in Musaceae (13.5%).

e major parasitoids used in biological control in Ec-

uador are Telenomus spp., Trichogramma spp., and Encarsia

spp. (Tables 1-12). Of the total of studies that involve para-

sitoids, 69.1, 19.6 and 11.3% have been carried out on the

Coast, Andes and Amazon, respectively. Principal Com-

ponent Analysis shows that parasitoids are conspicuously

associated with geographical regions, in the Coast and

the Andes. Doryctobracon crawfordi (Viereck, 1911) (Hy-

menoptera: Braconidae) is associated to the Andes while

Telenomus spp. and Trichogramma spp. are closely associ-

ated with the Coast (Fig. 9). ese dierences are likely to

be associated to the dierent crops grown in these regions.

Although Telenomus spp. and Trichogramma spp. are

the most noted parasitoids in biocontrol, most of the pro-

grams using parasitoids of these genera were conducted in

the 1990s (Arias et al. 1996, INIAP, 1996, Benzing et al.

1997, Mendoza 1994a, 1944b, Páliz & Mendoza 1999).

In the case of species of the genus Encarsia, studies in-

dicate its greater importance as a natural biological con-

trol, from 1990 to the present (Mendoza 1994a, 1994b

Valarezo et al. 2011, Dueñas et al. 2018, Zambrano et al.

2021).

Parasitoids in biocontrol: a declining strategy?

Despite the diversity of parasitoid species recorded in

Ecuador, the data seem to indicate a decreasing trend in

their use as a pest control strategy. e regression model

calculated between the number of parasitoids used in bio-

control (Y) versus the years of study (X) shows an increase

beginning in the 1980s reaching its maximum inection in

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

Table 3. Parasitoids reported in association with pests on citrus, Citrus spp.

Pest Parasitoid Region Reference

Aleurocanthus woglumi Amitus hesperidum Andes Browning 1992, Merino 1984

Aleurothrixus floccosus

Amitus spinifera

Cales noacki

Encarsia sp.

Eretmocerus sp.

Andes, Coast Arias et al. 1992, Cañarte-Bermúdez

& Navarrete-Cedeño 2019, Valarezo

2011, Valarezo et al. 2011

Anastrepha fraterculus,

Anastrepha striata Aganaspis pelleranoi Coast Valarezo 2011

Ceratitis capitata Diachasmimorpha longicaudata Andes Valarezo et al. 2011

Diaphorina citri Diaphorencyrtus aligarhensis

Tamarixia radiata Andes, Coast Chávez et al. 2019, 2017, Cuadros et

al. 2020, Erráez et al. 2020, Portalanza

et al. 2017, Valarezo et al. 2011

Lepidosaphes beckii Aphytis lepidosaphes Andes Merino & Vázquez 1962

Phyllocnistis citrella

Ageniaspis citricola

Cirrospilus sp.

Elasmus tischeriae

Galeopsomyia sp.

Horismenus sp.

Andes, Coast Cañarte-Bermúdez et al. 2020,

Cañarte-Bermúdez & Navarrete-

Cedeño 2019, Valarezo et al. 2004

Toxoptera aurantii

Aphelinus flavipes

Aphidius matricariae

Aphidius sp.

Diaeretus sp.

Lysiphlebus sp.

Andes, Coast Cañarte-Bermúdez & Navarrete-Cedeño

2019, Cañarte-Bermúdez et al. 2020,

Valarezo et al. 2011

Figure 4. Parasitoids associated with pests that attack citrus, Citrus spp. e arrows show the interconnections in the agroecosystem.

Pests are indicated in red letters and parasitoids in blue.

Parasitoids attacking agricultural pests in Ecuador

Table 4. Parasitoids reported in association with pests on cassava, Manihot esculenta Crantz.

Pest Parasitoid Region Reference

Erinnyis ello

Cotesia americanus

Cotesia congregata

Cotesia sp.

Chetogena scutellaris

Euplectrus sp.

Oencyrtus submetalicus

Telenomus dilophonotae

Telenomus sphingis

Thysanamyia sp.

Trichogramma exiguum

Trichogramma fasciatum

Trichogramma minitum

Trichogramma sp.

Amazon,

Coast

Hinostroza et al.

2014, Rogg 2000

Hemiptera: Aleyrodidae

Amitus macgowni

Encarsia sp.

Eretmocerus sp.

Euderomphale sp.

Signiphora aleyroidis *

Andes, Coast Trujillo et al. 2004

* Hyperparasitoid.

Table 5. Parasitoids reported in association with pests on coee, Coea arabica L.

Pest Parasitoid Region Reference

Hypothenemus hampei

Prorops nasuta Amazon, Andes Klein Koch et al. 1988

Mendoza et al. 1994

Cephalonomia stephanoderis Andes, Coast Mendoza et al. 1994b,

Klein Koch et al. 1988

Phymastichus coffea Coast Delgado et al. 2002

Perileucoptera coffeella

Catolaccus sp.

Cirrospilus sp.

Horismenus cupreus

Mirax sp.

Prigalio sp.

Tetrastichus sp.

Viridipyge letifer

Zagrammosona sp.

Coast Anchundia 1994,

Mendoza et al. 1994,

Sotomayor & Duicela 1995

Figure 5. Parasitoids associated with pests that attack A: cassava, Manihot esculenta Crantz, B: coee, Coea arabica L. e arrows

show the interconnections in the agroecosystem. Pests are indicated in red letters, parasitoids in blue and hyperparasitoids in purple.

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

Table 6. Parasitoids reported in association with pests on vegetables and other transitory crops.

Crop Pest Parasitoid Region Reference

Crucifers Plutella xylostella

Diadegma insulare

Diadegma majale

Diadegma sp.

Oomyzus sp.

Andes Gavilanes 2018, Lalangui

& Caicedo 2018

Brevicoryne brassicae Diaeretiella rapae Andes, Coast Zamorano 2012

Summer flowers Liriomyza huidobrensis Diglyphus isaea Andes, Coast Prado et al. 2018

Melon, pepper,

tobacco

Hemiptera:

Aleyrodidae

Amitus fuscipennis

Amitus sp.

Encarsia nigricephala

Encarsia sp.

Eretmocerus sp.

Andes, Coast Arias et al. 2008, Dueñas

et al. 2018, Navarrete et al.

2017, Valarezo et al. 2008

Aphis gossypii

Myzus persicae Aphidius spp.

Lysiphlebus testaceipes Coast Arias 2021, Dueñas et al. 2018,

Paredes 2011, Toledo et al. 2018

Potato Phthorimaea operculella

Symmetrischema tangolias

Tecia solanivora Copidosoma koehleri Andes Báez & Gallegos 2011

Tomato

Prodiplosis longifila Synopeas sp. Coast Arias 2021, Valarezo et al. 2011

Spodoptera sunia Telenomus remus Coast Arias 2021

Tuta absoluta Encarsia porteri Andes Benzing et al. 1997

Unidentified plants, cotton Bemisia spp. Encarsia lanceolata

Encarsia pergandiella Schuster et al. 1998,

Zambrano et al. 2021

Unidentified vegetables Unidentified Lepidoptera Incamyia chilensis

Trichogramma sp. Andes Andrade 1990

Table 7. Parasitoids reported in association with pests on various fruit trees.

Crop Pest Parasitoid Region Reference

Avocado Caloptilia azaleella Telenomus sp. Andes Venegas et al. 2018

Cherimoya

Guava,

Fruit trees

Anastrepha spp.

Ceratitis capitata

Aceratoneuromya indica

Aganaspis pelleranoi

Coptera haywardi

Diachasmimorpha longicaudata

Doryctobracon crawfordi

Sycophila sp.

Utetes anastrephae

Andes, Coast

Arias 2021,

Arias & Carrasco 2004,

Feicán et al. 1999,

León & Larriva 2019,

Minga et al. 2020,

Tigrero 2007, Valarezo 2011

Little orange Neoleucinodes elegantalis

Bracon sp. Andes, Amazon Noboa et al. 2017

Chelonus sp. Andes, Amazon Noboa et al. 2017

Copidosoma sp. Andes, Amazon Sosa 2009, Noboa et al. 2017

Lixophaga sp. Amazon, Andes Noboa et al. 2017

Lymeon sp. Andes Sosa 2009

Meteorus sp. Andes Sosa 2009

Mango Dysmicoccus brevipes Aenasius sp.

Cheiloneurus sp.

Metaphycus sp. Coast Arias 2021

Fruit trees Aleurothrixus floccosus Encarsia sp. Coast Valarezo et al. 2011

Parasitoids attacking agricultural pests in Ecuador

Table 8. Parasitoids reported in association with pests on rice, Oryza sativa L.

Pest Parasitoid Region Reference

Diatraea spp. Telenomus alecto Coast INIAP 1996

Rupela albinella Telenomus rowanii

Strabotes sp. Coast INIAP 1996, Arias 2021

Spodoptera sp. Euplectrus sp. Coast INIAP 1996

Syngamia sp. Bracon sp.

Conura sp. Coast INIAP 1996

Oebalus spp.,

Tibraca limbativentris

Telenomus sp.

Trichopoda sp.

Trissolcus basalis Coast Arias 2021, Arias et al. 1996

Tagosodes orizicolus

Anagrus sp.

Elenchus sp.

Gonatopus sp.

Haplagonatopus hernandenze

Paranagrus perforator

Coast Arias 2021

Various Lepidoptera

Conura sp.

Euplectrus sp.

Goniozus sp.

Hormius sp.

Pseudochaeta sp.

Stantonia sp.

Telenomus sp.

Trichogramma sp.

Coast Arias 2021, Arias et al. 1996,

Castillo et al. 2020

Figure 6. Parasitoids associated with pests that attack A: rice, Oryza sativa L. B: sugarcane, Saccharum ocinarum L. e arrows show

the interconnections in the agroecosystem. Pests are indicated in red letters and parasitoids in blue.

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

Table 10. Parasitoids reported in association with pests on cacao, eobroma cacao L.

Pest Parasitoid Region Reference

Aphid or Lepidoptera Ceraphron sp.*

Coast Páliz et al. 1982

Cecidomyiids Laptacis sp.

Platygaster sp.

Synopeas sp.

Unidentified larvae and pupae Brachymeria cominator

Unidentified Aranae** Trimorus sp.

Unidentified Diptera Trichopria sp.

Unidentified Lepidoptera

and Coleoptera

Cotesia sp.

Asobara sp.

Chelonus sp.

Dissomphalus sp.

Meteorus sp.

Unidentified Lepidoptera, Hemiptera,

Coleoptera, Neuroptera** Bothriothorax sp.

Tachinaphagus sp.

* Hyperparasitoid, **Predator.

Table 9. Parasitoids reported in association with pests on sugarcane, Saccharum ocinarum L.

Pest Parasitoid Region Reference

Diatraea saccharalis

Billaea claripalpis Coast CINCAE 2013, Gaviria 1981,

Mendoza 2018, Risco 1960

Ipobracon sp. Coast Mendoza et al. 2005, Mendoza 2018

Cotesia flavipes Coast CINCAE 2013, Mendoza 2018

Telenomus sp. Coast Mendoza et al. 2005, Mendoza 2018

Trichogramma spp. Coast Mendoza et al. 2005, Mendoza 2018

Duplachionaspis divergens Encarsia sp. Coast Mendoza et al. 2013, Mendoza et al. 2005

Perkinsiella saccharicida

Anagrus optabilis

Aprostocetus sp.

Ootetrastichus sp. Coast Mendoza et al. 2005, Arias 2021

Pseudogonatopus sp. Coast Mendoza et al. 2005, 2018

Coast Mendoza et al. 2005

Praelongorthezia praelonga Gitona brasiliensis Coast Mendoza et al. 2005, Mendoza 2013

the following decade (1990), and subsequently decreased

from the 2000s to the present. e estimated model ex-

plains this trend with a high and signicant coecient of

determination (R2 = 0.8093, P <0.0001) (Fig. 10). e use

of parasitoids have probably been replaced by other pest

control strategies.

We emphasize that in Ecuador there is an extensive leg-

islation that regulates the importation and use of biocon-

trol agents whose responsibility is assigned to the Agency

for the Regulation of Control and Phytosanitary Control

(AGROCALIDAD). is agency also regulates chemical

pesticides, restricting the use of highly toxic molecules and

the indiscriminate applications of pesticides.

However, surveys carried out with farmers in recent

years have diagnosed an excessive use of insecticides to

control arthropod pests in dierent crops (Bravo-Zamora

et al. 2020, Chirinos et al. 2020, Reinoso 2015, Valarezo et

al. 2008). Additionally, the adverse eects of insecticides

on the health of farmers and consumers have also been

documented in Ecuador in the last decade (González-An-

drade et al. 2010, Guevara et al. 2016, Lindao et al. 2017).

With respect to the environment, insecticide residues

Parasitoids attacking agricultural pests in Ecuador

Table 11. Parasitoids reported in association with pests on legumes.

Pest Parasitoid Region Reference

Anticarsia gemmatalis Euplectrus sp.

Glyphapanteles sp. Coast Mendoza 1994a

Bemisia tabaci Encarsia desantisi

Encarsia nigricephala

Eretmocerus sp. Coast Arias 2005, 2021

Hedylepta indicata Cotesia sp.

Brachymeria sp.

Macrocentrus sp. Coast Mendoza 1994a

Liriomyza sativae

Chrysocharis sp.

Closterocerus sp.

Ganaspidium sp.

Neochrysocharis sp.

Coast Chirinos et al. 2017

Liriomyza huidobrensis Halticoptera sp. Andes Chirinos et al. 2020

Pseudoplusia includens Litomastix truncatella Coast Mendoza 1994a

Euchistus sp.

Nezara viridula Oencyrtus sp.

Telenomus sp. Coast Arias 2005

Anticarsia gemmatalis

Pseudoplusia includens

Spodoptera spp.

Epinotia aporema

Cydia favibora

Trichogramma sp. Coast Arias et al. 1992, Arias

2005, Mendoza 1994a

Figure 7. Parasitoids associated with pests that attack A: cacao, eobroma cacao L., B: legumes e arrows show the interconnections

in the agroecosystem. Pests are indicated in red letters, parasitoids in blue and hyperparasitoids in purple.

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

Figure 8. Parasitoids associated with pests that attack palms (Arecaceae). e arrows show the interconnections in the agroecosystem.

Pests are indicated in red letters and parasitoids in blue.

Table 12. Parasitoids reported in association with pests on palms (Arecaceae).

Pest Parasitoid Region Reference

Brassolis astyra

Peleopoda arcanella

Herminodes insulsa

Opsiphanes cassina

Opsiphanes sophorae

Oiketicus kirbyi

Brachymeria spp.

Conura sp.

Xanthozona melanopyga Amazon Rogg 2000

Euprosterna elaeasa Brachymeria sp. Amazon Mexzón & Chinchilla 1996

Hispoleptis subfaciata Conura hispinephaga Amazon Mexzón & Chinchilla 1996

Hispoleptis subfaciata Zaommomyia sp. Amazon Mexzón & Chinchilla 1996

Oiketicus kirbyi Conura elaeisis Amazon Mexzón & Chinchilla 1996

Saliana severus Brachymeria annulata Amazon Mexzón & Chinchilla 1996

Opsiphanes cassina Xenufens forsythi Coast Yoshimoto 1976

Saliana severus Trissolcus urichi Amazon Mexzón & Chinchilla 1996

Sibine nesea Cotesia sp. Amazon Mexzón & Chinchilla 1996

Spaethiella tristis Horismenus sp. Amazon Mexzón & Chinchilla 1996

Spodoptera spp. Telenomus remus Amazon Rogg 2000

Parasitoids attacking agricultural pests in Ecuador

Figure 9. Principal component analysis between the geographical areas of continental Ecuador and the most studied parasitoids. Pe-

riod 1980-2020.

Figure 10. Regression model between the number of parasitoids studied and the years of study. Period 1980-2020.

Chirinos, Anchundia, Castro, Castro Olaya, Geraud & Kondo

have been detected in the Guayas river basin in the coastal

region in areas close to banana and pineapple producing

farms (Deknock et al. 2019).

Regarding ecological imbalances, several studies report

the suppressive eect of insecticide applications on para-

sitoids. Chirinos et al. (2017) recorded parasitoids asso-

ciated with the leafminer y Liriomyza sativae Blanchard

on beans, Phaseolus vulgaris L. and observed population

outbreaks of this phytophagous species, caused by the in-

terference with parasitism due to weekly sprays of lambda

cyhalothrin + thiamethoxam. In a eldwork conducted on

melon, Cucumis melo L. in the coastal region, Navarrete et

al. (2017) found lower rates of parasitism (3 to 7%) when

formulations based on imidacloprid and neem (Azadi-

rachta indica Juss.) were applied. A eld assay determined

the adverse eects of applications of insecticides based on

neem on the parasitism rates of Ageniaspis citricola Log-

vinovskaya, 1983 (Hymenoptera: Encyrtidae) on Citrus

aurantifolia (Christm.) Swingle (Cañarte-Bermúdez et al.

2020).

e frequent spraying of insecticides could be the con-

sequence of several factors, among which stand out a dis-

connection between research and crop production, the

farmer’s perception of the damage caused by pests, the lack

of knowledge about biological control and the excessive

reliance on pesticides as a method of control. e report

made by Delgado et al. (2002) analyzed the results of the

introductions of parasitoids to control H. hampei in cof-

fee. is study pointed out that biological control could

be potentially eective and reduce the use of insecticides

and lower production costs. However, they refer to the im-

portance of a greater sociological interaction between the

links in the researcher - producer chain to achieve these

objectives (Delgado et al. 2002).

Citrus farmers from the Coast indicated that they

mainly use chemical control due to the lack of knowledge

of the importance of the use and action of parasitoids in

pest management (Sornoza-Robles et al. 2020). Mendoza

et al. (2005) reported that the establishment of integrated

pest management programs in sugarcane are limited by the

alarming perception that farmers have about the damage

caused by a pest, as well as the excessive condence they

place on pesticides to control pests, which leads to their

dependence and abuse of these products. us, insecticide

applications seem to prevail in the control of agricultural

pests in Ecuador. Cañarte-Bermúdez & Navarrete-Cedeño

(2019) mentioned that 62% of citrus growers use chemi-

cal insecticides. All the vegetable farmers surveyed in ve

provinces of the Andean and coastal regions reported

spraying insecticides to control the main pests with a range

of 1 to 3 weekly sprays (Chirinos et al. 2020).

Since the late 1990s, some studies have focused at re-

ducing the use of pesticides in Ecuador and conserving

the action of natural enemies, including parasitoids. Fe-

icán et al. (1999) reported that one of the strategies for

the integrated management of fruit ies is the action of

the parasitoid D. crawfordi, and that it is essential for its

preservation to avoid the indiscriminate use of pesticides.

e introduction of D. longicaudata in 2005 for the con-

trol of fruit ies was aimed at encouraging fruit growers

to contribute to a production with less pesticide residues

(Arias et al. 2009). In an inventory of parasitoids associat-

ed with the fruit borer, Neoleucinodes elegantalis Guenée,

1854 (Lepidoptera: Crambidae) in Solanum quitoense

Lamarck, Noboa et al. (2017) reported that the parasitoid

species detected in that study could be used in the bio-

logical control of this pest to reduce the use of pesticides

in this crop.

e use of parasitoids in biological control programs

has great potential in the Neotropical region due to their

natural occurrence, considering that natural enemies have

probably co-evolved within the plant-herbivore system,

forming part of the ecosystem (Colmenarez et al. 2018).

e structural and functional analysis of benecial ento-

mofauna could form the basis for conservation biological

control programs (DeBach 1974). e two main strategies

of conservation biological control consist of: 1) habitat

modication to improve survival, longevity and reproduc-

tion of natural enemies and, 2) reducing the exposure of

natural enemies to pesticides (Löhr et al. 2018). In the

neighboring country, Colombia, studies on conservation

biological control in crops such as sugarcane, chili, oil

palm, coee and ornamental plants have been conducted

(Kondo et al. 2020). On the other hand, in Ecuador, un-

fortunately, with the synthesis of pesticides from 1945 on-

wards, the use of biological control decreased (Dangles et

al. 2009) due to the simplistic perspective in which this

alternative was framed. e bias in the use of this strategy

has resulted in ecological imbalances, environmental crises

and adverse economic and social eects (Metcalf & Luck-

mann 1975).

CONCLUSIONS

is review represents a compendium of about 200

taxa of parasitoids reported attacking agricultural pests in

continental Ecuador with an emphasis on natural biologi-

cal control. e major parasitoids reported are: Telenomus

spp. (Hymenoptera: Platygastridae), Trichogramma spp.

(Hymenoptera: Trichogrammatidae) and Encarsia spp.

(Hymenoptera: Aphelinidae), being the rst two parasit-

oids mainly referred in biological control programs con-

Parasitoids attacking agricultural pests in Ecuador

ducted between the 1980s and 1990s. e results suggest

a decreasing trend in the use of parasitoids as biocontrol

agents from 1980 to the present.

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