Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

Diversity and abundance of insect visitors in four crops within

a Costa Rican highland region

Nicole Gamboa-Barrantes1, 2*; https://orcid.org/0009-0005-1077-1495

Geovanna Rojas-Malavasi1, 2; https://orcid.org/0000-0002-4377-7288

Eric J. Fuchs1, 2; https://orcid.org/0000-0002-6645-9602

Paul Hanson1, 2; https://orcid.org/0000-0002-7667-7718

B. Karina Montero1, 2, 3; https://orcid.org/0000-0003-4246-6004

Manuel A. Zumbado4

Ruth Madrigal-Brenes1, 2; https://orcid.org/0000-0002-6636-4259

Gilbert Barrantes1, 2; https://orcid.org/0000-0001-8402-1930

1. Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica; nicolegamcr@gmail.com (*Correspondence),

geovanna.rojas@ucr.ac.cr, eric.fuchs@ucr.ac.cr, b.karina.montero@gmail.com, ruth.madrigalbrenes@ucr.ac.cr, gilbert.

barrantes@gmail.com; phanson91@gmail.com

2. Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET), Universidad de Costa Rica, San José,

Costa Rica.

3. Biodiversity Research Institute (CSIC-Oviedo, University-Principality of Asturias), University of Oviedo, Mieres,

Asturias, Spain.

4. Investigador Colaborador, Museo de Zoología, San José, Costa Rica; zzuman@gmail.com

Received 27-VIII-2024. Corrected 17-III-2025. Accepted 25-III-2025.

ABSTRACT

Introduction: The interaction between plants and pollinators is vital for the reproduction of approximately 90 %

of angiosperms and directly affects ecosystems and agriculture. In tropical regions, 94% of plants require animal

pollinators, and in Latin America, 58% of crops depend on pollination by insects. The stability and complexity of

plant-pollinator interactions are influenced by several factors, such as floral morphology, which influences nectar

accessibility and pollinator specialization.

Objective: To compare the diversity and abundance of insect floral visitors in avocado, apple, plum, and black-

berry crops in San Gerardo de Dota, Costa Rica.

Methods: We systematically collected flower-visiting insects in these crops and identified them taxonomically to

the lowest possible level. We then estimated alpha diversity for each crop and compared the community composi-

tion (beta diversity) of visiting insects among crops.

Results: In 12 sampling visits, we collected a total of 2806 insects from 75 families across all four crops. Alpha

diversity was greater in the avocado crop for all three indices (0D, 1D, and 2D). Apis mellifera was the most abun-

dant species in all four crops, but Diptera was the most common group of visiting insects in avocado, particularly

flies from the Syrphidae, Muscidae, Calliphoridae, Sarcophagidae, Sciaridae, and Tachinidae families. The insect

community of the avocado crop was different from that of the apple, plum, and blackberry crops; however, the

insect composition of the other crops was similar.

Conclusions: The avocado crop is generalist in terms of floral visitors; this may be attributed to the size of the

flower corolla, as flies with short mouthparts usually choose to feed on flowers with small corollas. Flowers of

https://doi.org/10.15517/rev.biol.trop..v73iS2.64701

SUPPLEMENT

SECTION: ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

INTRODUCTION

The interaction between plants and pol-

linators has been widely studied from an eco-

logical and evolutionary perspective and as part

of the environmental services that pollinators

provide (Percy et al., 2004; Pincebourde et

al., 2017; Sargent & Ackerly, 2008; Strauss &

Zangerl, 2009; Zebelo & Maffei, 2015). Animal-

mediated pollination is estimated to contribute

to the sexual reproduction of 90 % of the 250

000 angiosperm species (Kearns et al., 1998).

Plant-pollinator interactions directly influence

the development and sustainability of terres-

trial ecosystems, as well as human life (Aizen

et al., 2009), since many of the plants that

animals pollinate are an important food source

for people.

It is estimated that at least 35 % of global

crop production depends on animal pollination

(Nicholls & Altieri, 2012), and the importance

of pollinators in agricultural production has

been recognized worldwide (Intergovernmen-

tal Science-Policy Platform on Biodiversity

and Ecosystem Services [IPBES], 2016). For

instance, Nicholls and Altieri (2012) report

that the number of crops pollinated by animals

has rapidly increased in both developing and

developed nations, with 58 % of crops in Latin

America relying on insect pollination (Basual-

do et al., 2022). This highlights the importance

that service pollinators provides in natural and

agricultural ecosystems.

Plant-pollinator interactions are threat-

ened by different natural phenomena: climatic,

hydrological, meteorological, and geophysical

(Nicholson & Egan, 2019). However, anthropo-

genic factors, such as climate change and land

use change, pose a more serious threat to the

maintenance of pollination services (Hegland

the other crops have similar morphology and are mainly visited by bees. The native entomofauna are abundant

on the crop flowers, likely playing an important role as pollinators.

Keywords: avocado; plum; apple; blackberry; pollination; bees; flies.

RESUMEN

Diversidad y abundancia de insectos visitantes de cultivos en una región montañosa de Costa Rica

Introducción: La interacción entre plantas y polinizadores es vital para la reproducción del 90 % de las angiosper-

mas y afecta tanto a los ecosistemas como a la agricultura. En regiones tropicales, el 94 % de las plantas requieren

polinizadores, y en América Latina, el 58 % de los cultivos dependen de la polinización por insectos. La estabili-

dad y complejidad de estas interacciones están influenciadas por factores como la morfología floral, que afecta la

accesibilidad al néctar y la especialización de los polinizadores.

Objetivo: Comparar la diversidad y abundancia de insectos visitantes florales en cultivos de aguacate, manzana,

ciruela y mora en San Gerardo de Dota, Costa Rica.

Métodos: Se muestrearon sistemáticamente insectos visitantes en estos cultivos, identificándolos taxonómica-

mente al nivel más bajo posible. Se estimó la diversidad alfa para cada cultivo y se comparamos la composición

de la comunidad (diversidad beta) de insectos visitantes entre cultivos.

Resultados: Se recolectaron 2 806 insectos de 75 familias en los cuatro cultivos en 12 giras. La diversidad alfa

fue mayor en aguacate para los índices 0D, 1D y 2D. Apis mellifera fue la especie más abundante, pero Diptera fue

el grupo predominante en aguacate, especialmente moscas de las familias Syrphidae, Muscidae, Calliphoridae,

Sarcophagidae, Sciaridae y Tachinidae. La comunidad de insectos en aguacate fue diferente a la de los otros cul-

tivos, mientras que en los otros tres la composición fue similar.

Conclusiones: El aguacate es generalista en términos de visitantes florales, posiblemente debido al tamaño de su

corola, que atrae a moscas con piezas bucales cortas. Las flores de los otros cultivos tienen morfologías similares

y son visitadas principalmente por abejas. La entomofauna nativa es abundante en estos cultivos, probablemente

desempeñando un rol clave como polinizadores.

Palabras clave: aguacate; ciruela; manzana; mora; polinización; abejas; moscas.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

et al., 2009; Klein et al., 2006; Settele et al., 2016;

Stoddard, 2017). The negative effects of these

factors can directly affect entire communities

of plants and pollinators. The ongoing decline

of insect populations has influenced plants, as

well as other organisms (Visser & Both, 2005;

Abernethy et al., 2018; Cristóbal-Perez et al.,

2024). The predicted changes in climate and

land use will not only affect natural ecosystems

but will also have a strong negative impact on

the production of crops that rely on pollinators

for their reproduction (Winfree, 2010). Howev-

er, despite the urgency to maintain the viability

of pollinators and plant-pollinator interactions

(Galetto et al., 2022), information on the role

that natural insect communities play on crop

pollination is still scarce. There is a notable lack

of information on pollination services in neo-

tropical highlands, particularly in Costa Rica

(Garibaldi et al., 2011; Celis-Diez et al., 2023;

Montero et al., 2025).

In this study, we investigated the diver-

sity and abundance of insect floral visitors in

avocado, apple, plum, and blackberry crops in

a Costa Rican highland region. Two of these

crops—avocado and blackberry—are native

and naturally occur in the study area, whereas

apple and plum are exotic. To accomplish this

goal, we estimated insect alpha diversity on

each crop and compared the insect commu-

nity composition among crops. Because floral

morphology may influence the diversity and

abundance of insects that visit them, we clas-

sified the flowers by crop family: Rosaceae

(blackberry, apple, and plum) and Lauraceae

(avocado). We predicted that insect community

and abundance would differ between the two

plant families based on their floral morphol-

ogy. But the diversity and abundance of insects

are expected to be similar in apples, plums,

and blackberries.

MATERIAL AND METHODS

Study site: We conducted this research in

San Gerardo de Dota, Dota, San José, Costa

Rica (9°33’00” N, 83°48’39” W, 2 300 m eleva-

tion) between August 2021 and November

2022. This site is located at the upper basin

of the Savegre River and includes large tracts

of montane forest dominated by Quercus spp.

(Juárez et al., 2000). The region averages a

temperature of 14 °C and an annual precipita-

tion of 2 190 mm (Solano & Villalobos, 2001),

with two seasons: the dry season from Decem-

ber to March and the rainy season from April

through November.

Data collection: We sampled insects on

two avocado (Persea americana Mill.) farms,

two apple (Malus domestica Borkh.) farms,

one plum farm (Prunus domestica L.), and two

blackberry (Rubus spp.) farms. Avocado and

blackberry are native to the region, although

particularly avocado has been subject to arti-

ficial selection, while the other two crops are

introduced. The farms are approximately four

kilometers apart. The crops studied are the

most abundant crops in the region and have a

significant economic impact on local farmers.

We systematically selected avocado, apple,

and plum trees to collect insects. In each crop,

the first tree sampled corresponded to the first

tree we observed with abundant insect visitors;

we then moved northwesterly, collecting on

every third tree. When the limit of the crop

field was reached, we applied the same selec-

tion criteria, but in the opposite direction. For

blackberry, we selected those plants with abun-

dant open flowers due to the low flowering rate

of this crop.

We concentrated our sampling efforts dur-

ing the flowering peak of each crop between 6

and 13 sampling hours, depending on weather

conditions. Each tree (or bush) was sampled

for 15 min; if insects were not visiting the flow-

ers, we waited for another 10 min, and then

moved to another tree. Each crop was sampled

between two and seven times (for one to four

days each time), depending on their abundance

and flowering patterns. Thus, the number of

samplings was approximately proportional to

the number of plants in each crop.

We collected each insect using one of fol-

lowing three methods: clear plastic bags, insect

aspirators, or entomological nets. Each method

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

was used based on the insect size and the height

from the ground where it was foraging: an

entomological net for large insects or foraging

insects at > 1.60 m; a plastic bag for medium

insects 1-2 cm; and an aspirator for smaller

insects < 1 cm. We only collected insects whose

mouthparts or legs were in direct contact with

the flowers’ reproductive organs.

For very abundant insects (e.g., honey-

bees and some syrphid flies), we collected a

maximum of five insects of the same species

or morphospecies (in the case of syrphids) per

tree. This allowed us to have an appropriate

representation of the insects without impact-

ing their populations. Each insect was stored in

labeled vials with 70 % alcohol.

Taxonomic identification of insects: All

insects were identified to the lowest taxonomic

level possible, using specialized taxonomic keys

and/or comparing them with specimens from

the Diptera collection of the Department of

Natural History of the National Museum and

the criteria of expert taxonomists when needed.

For flies, we used the keys published by Brown

et al. (2009) & Brown (2009), and for bees the

key published by Michener et al. (1994). To

preserve individuals in better conditions for

identification, we used an air-drying procedure

with 100 % alcohol and hexamethyldisilazane

(HDMS) for small, soft-cuticle insects such

as flies (Nation, 1983). Vouchers of all col-

lected insects were deposited in the Museo de

Zoología, CIBET, Universidad de Costa Rica

(MZUCR).

Data preparation: Each sampling unit

consisted of at least two hours of sampling on

a particular crop, where at least two insects

were collected. We used a Pearson correla-

tion to determine the effect of sampling effort

(number of sampling units) on the number of

collected insects.

Alpha diversity: To describe diversity pat-

terns of crop insect floral visitors, we calculated

alpha diversity for each crop using the iNEXT

() function, and estimated the cover-based

Hill diversity using the estimateD () func-

tion of the iNEXT package (Chao et al., 2014;

Hsieh et al. 2016). We calculated three diversity

metrics (0D, 1D, and 2D): 0D estimates the spe-

cies richness and is more sensitive to sample

size and influenced by rare species; 1D gives

equal weight to rare species and abundant

species; and (2D) gives greater weight to the

dominant species (Chao et al., 2014; Roswell

et al., 2021). We used confidence intervals to

evaluate the differences across crops for each

diversity indicator (Chao et al., 2014). We also

generated rarefaction curves (ggiNEXT func-

tion, iNEXT package) for each crop, with a 95

% confidence interval (Chao et al., 2014). The

curves were estimated based on the abundance

method for both coverage and sampling to

determine the completeness of insect collec-

tions on each crop. Coverage is a statistical

procedure that determines the completeness of

the samples collected.

Beta Diversity: To compare the composi-

tion of the visiting insect community among

crops, we performed a non-metric multidi-

mensional scaling (NMSD) analysis based on

a Bray-Curtis dissimilarity matrix with 999

permutations with the metaMDS function from

the vegan package (Oksanen, 2022). We then

performed a non-parametric analysis of vari-

ance (PERMANOVA) using the adonis func-

tion from the same package, in which the

independent variable consisted of the type

of crop and the response was the distance

matrix. The betadisper function (vegan pack-

age) was used to test the assumption of homo-

geneity of variances among insect communities

(Oksanen, 2022). We used the R statistical lan-

guage, version 2023.12.1 (R Core Team, 2023),

for all statistical analyses.

RESULTS

General information: We conducted 30

sampling sessions (137 hours) and identified 2

806 insects from 75 families (Appendix Table

S1). After excluding the sampling units that did

not meet our minimum criteria (see methods)

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

and deteriorated insects that could not be iden-

tified, we ended up with a total of 2 774 insects.

We identified 2 061 insects to the genus level

representing 25 families, which were then clas-

sified as species or morphospecies (Appendix

Table S1). From the remaining insects, 676

were classified only to family level and 37 to

order level. The most abundant visitors were

flies (e.g., Syrphidae) followed by bees (e.g.,

Apis mellifera and Bombus spp.). The number

of species per sampling unit correlated with

the number of sampling hours (r = 0.62, p =

0.0002). Persea americana was the crop with the

highest number of trees sampled and insects

collected, as well as the largest number of sam-

pling sessions, while plum was the crop with

the smallest sample size (Table 1).

The most diverse group of floral visitors in

avocado plants were flies (91 % of the total flies

were collected in avocados), many of which

were absent or in very low numbers in other

crops. For example, 93 % of all syrphid flies

collected were captured on avocado flowers;

similarly, for Tachinidae (96.5 %), Calliphori-

dae (100 %), Sarcophagidae (99 %), Sciaridae

(94 %), and Muscidae (95 %). These families

account for 73 % of all flies collected on avo-

cado flowers. We found 39 families of insects

exclusively in avocado plants, but only two

unique taxa (Scoliidae and the order Psocop-

tera) were found in plum. There were also some

uncommon taxa collected exclusively in avo-

cado, apple, or blackberry (Appendix Table S1).

Alpha diversity: Flowering periods dif-

fered in number and synchrony across crops.

Avocado trees had more flowering events per

year, followed by blackberry, apple and plum

crops (Montero et al., 2025). Flowering was

artificially induced twice a year (in July-August

and January) in apples and plums, with flower-

ing bouts lasting about one month each. As a

result, sample completeness (coverage) varied

across the four crops, with avocado having the

highest (95 %), followed by blackberry (92 %),

apple (91 %), and plum (89 %). Thus, we stan-

dardized our samples by coverage to reduce the

effect of uneven sampling effort between crops,

allowing diversity measures to be more com-

parable among crops. The richness and diver-

sity of flower visitors (based on Hill-numbers,

Appendix Table S2) in avocado flowers was

much greater and differed notably from the

diversity estimated for the other crops (Fig. 1,

Fig. 2), as this crop attracts a larger diversity of

visitor insects. However, the other three crops

overlap in terms of richness and Hill-Shannon

diversity. The Hill-Simpson diversity index, pri-

marily affected by abundant species, was great-

er for blackberries in comparison to apple and

plum crops (Fig. 2). Therefore, insect visitors

on avocados, followed by insects on blackberry

crops, had a higher proportion of abundant

species. However, avocado flowers attracted the

largest richness of visitor insects, which varied

in abundance, as indicated by the higher values

of all three Hill-diversity indices (Fig. 1, Fig. 2).

Beta Diversity: The composition of insects

visiting avocado flowers did not overlap with

that of other crops (F = 2.62, P < 0.001,

R² = 0.34). Whereas the insect communities

that visit apple, plum, and blackberry flowers

exhibited a nearly complete overlap, indicating

that the insect communities of these crops are

Table 1

Summary of the data collected for each crop (Persea americana, Malus domestica, Rubus spp., and Prunus domestica). The

number of visits, the number of trees sampled, and the number of insects collected are included.

Crop Field Visits Sampled trees Collected insects Species/ morphospecies

Persea americana 7 120 2083 224

Malus domestica 5 39 263 38

Rubus spp. 5 37 275 38

Prunus domestica 2 28 163 33

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

most diverse and abundant groups. The diver-

sity and number of insects varied by crop. Avo-

cados had the greatest diversity and abundance

of floral insect visitors, as well as a different

composition of the insect visitor community.

Most flies (91 % of the flies) were captured on

avocado flowers. This group was represented

by six diverse families found almost exclu-

sively in avocado: Syrphidae, Calliphoridae,

Tachinidae, Sarcophagidae, Sciaridae and Mus-

cidae. On the contrary, apple, plum and black-

berry flowers were visited primarily by bees

(Appendix Table S1).

Honeybees (Apis mellifera), bumblebees

(Bombus spp.), and sweat bees (Halictidae –

Lasioglossum spp.) visit the flowers of all four

crops, while stingless bees (Meliponini – Meli-

willea bivea and Partamona grandipennis) were

absent in plum. Managed honeybees were the

most common visitor (as a species) of all four

crops. Their abundance is influenced by their

social behavior, recruitment foraging, construc-

tion of large colonies (Lowell et al., 2019), and

the leasing of hives by local farmers to improve

pollination of their crops. Our findings are

congruent with those reported in other stud-

ies (Carabalí-Banguero et al., 2021; Celis-Diez

et al., 2023; Ish-Am et al., 1999; Okello et al.,

2021), in which flies and bees are the dominant

flower visitors in these crops.

Alpha diversity: Avocados produce a large

number of small flowers with a relatively simple

floral morphology (Chanderbali et al., 2013),

which attracts a large number of insect species,

compared with apples, plums, and blackberry

flowers. This species also has a synchronous

dichogamy in which the female phase occurs

in the morning while the male phase occurs in

the afternoon (Davenport, 1986). This strategy

increases the probability of insect visitation

because pollen (male phase) and nectar (female

phase) can attract different groups of insects.

The diversity analyses plainly demonstrate the

disparities in species richness. The number

of species documented for the other crops

is significantly lower than that of avocado.

This abundant crop flowers during periods

Fig. 1. Diversity estimates are divided into three panels:

A. Richness (q = 0), B. Hill-Shannon (q = 1), and C.

Hill-Simpson (q = 2). They are based on coverage-based

rarefaction (solid line) for insect visitors sampled in apple

(Malus domestica), avocado (Persea americana), plum

(Prunus domestica, and blackberry (Rubus spp.).

highly similar (Fig. 3). The variance is homoge-

neous across crops (F = 0.64, P = 0.579).

DISCUSSION

We identified a rich community of insect

visitors in the flowers of all four crops, with flies

(181 species) and bees (19 species) being the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

when other native and ruderal species produce

fewer flowers, providing a valuable resource for

insects (Montero et al., 2025). Many insects,

especially flies, forage on a wide range of plants

in the montane forest and are attracted to

the relatively simple avocado flowers. Because

avocado is a native species, insects may have

evolved behaviors and adaptations to exploit

these flowers, contributing to the higher alpha-

diversity observed in avocado farms.

Differences in the other diversity estima-

tors (q = 1 and q = 2) for insects collected in

avocado flowers indicate that this crop attracts

a significantly high number of species that

vary in abundance. The flowers of this crop

attract a greater diversity of common species,

as shown by the Hill-Simpson estimator (q = 2),

and a greater quantity of both uncommon and

abundant species, as determined by the Hill-

Shannon estimator (q = 1). These estimators

are both influenced by the large number of fly

species from families such as Syrphidae, Calli-

phoridae, Tachinidae, Sarcophagidae, Sciaridae,

and Muscidae, and bees (Apis and Bombus) that

visit avocado flowers. Flies represent 73 % of all

insect visitors in avocado with some common

species but also with many uncommon species.

Several studies have shown that honeybees

are effective pollinators of avocado flowers

and that introducing honeybees increases yield

(Dymond et al., 2021; Vithanage, 1990). This is

likely important in San Gerardo, as farmers fre-

quently rent Apis mellifera colonies to increase

yield.However, a recent meta-analysis studied

the impact of insect pollinators on avocado

yield and found that native pollinators are just

as important as introduced bees (Dymond et

al., 2021). Therefore, cutting down on their

numbers through pesticide use or loss of natu-

ral habitat may lower pollinator abundance and

crop yields (Dymond et al., 2021 and references

therein). Like our findings, their review shows

that in some countries, local insects, such as

flies, are more prevalent and important pollina-

tors (Celis-Diez et al., 2023). This emphasizes

Fig. 2. Comparison of the three Hill-diversity estimates of insect visitors between fruit crops. Error bars depict 95 % CI.

Fig. 3. Non-metric multidimensional scaling (NMDS)

based on Bray-Curti’s index estimated from the abundance

of insect visitors, illustrating the clustering of sampling units

for each fruit crop (stress = 0.1922). Samples from fruits

correspond to: Persea americana (green), Malus domestica

(yellow), Rubus spp. (violet), and Prunus domestica (blue);

centroids are represented by squares. Ellipses denote the

standard 95 % confidence.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

the need to preserve natural habitat, which can

support populations of native insects that pro-

vide an ecosystem service by pollinating crops

like avocado (Dainese et al., 2019; Garibaldi et

al., 2011, Garibaldi et al., 2013).

Beta diversity: The community of floral

insect visitors in avocado also differs from the

community of insects that visit the other three

crops (Fig. 3). The insect community visiting

avocado flowers is mainly composed of flies

(Diptera). The majority of Diptera with short

lapping mouth parts typically consume nectar

from small flowers that have accessible nectar-

ies (Gilbert, 1981; Gilbert, 1985), and avocado

flowers fit these characteristics. Other studies

have also shown that flies are common visi-

tors of avocado flowers (Campbell et al., 2012;

Muñoz et al., 2021).

Role of insects on crop pollination: In

apple, plum, and blackberry crops, the number

of flies visiting the flowers was lower than the

number of bees and wasps, particularly in apple

and blackberry. Bumblebees visit flowers of all

four crops but primarily those of apple, plum,

and blackberry. With appropriate management,

they could serve as a good alternative to man-

aged honeybees, particularly because they are

efficient pollinators adapted to local conditions

(Freitas et al., 2009; Montero et al., 2025; Pérez-

Méndez et al., 2020). This difference in insect

community composition may be influenced by

differences in the morphology of avocado flow-

ers (Lauraceae) compared to apple, plum, and

blackberry (Rosaceae) flowers, but also by dif-

ferences in sample size between the abundant

avocado and the other less abundant crops.

Both factors need to be further explored.

We cannot be sure that the insect visitors

identified in this study act as crop pollinators;

however, flies, bees and other insects are likely

to do so, as species of the same families have

been reported as important pollinators of mul-

tiple crops. Syrphid flies and bees, for example,

rely solely on nectar and pollen for energy to

fly and lay eggs (Brown et al., 2009), playing

an important role as pollinators (Willmer et

al., 1994; Bataw, 1995; Mengual et al., 2009;

Pardo & Borges, 2020). In this study, syrphids

(Allograpta and Ocyptamus), bumble and hon-

eybees were common flower visitors of all

crops. Celis-Diez et al. (2023) also reported

Allograpta as the most frequent genus of hov-

erflies in avocado crops. This study also found

other flies (e.g., Calliphoridae) that have been

reported as avocado pollinators (Cook et al.,

2023). A recent study conducted in the same

area reported that many of the insects, particu-

larly flies and bees, collected on crop flowers

carried pollen not only from the crop in which

the insect was captured but also from other

crops and many native and ruderal plants in

the region (Montero et al., 2025). These find-

ings provide clear evidence that native insects

provide pollination services to crops.

It has been argued that a high abundance

of managed honeybees (Apis mellifera) is suf-

ficient to accomplish crop pollination (Breeze

et al., 2014). However, a large body of evidence

indicates that only a diverse community of pol-

linators can promote a long-term maintenance

of crops and natural communities (Katumo

et al., 2022), reducing pollen limitation and

increasing genetic diversity and quality of fruit

crops (Gómez et al., 2010; Katumo et al., 2022).

We found a diverse community of native insect

visitors in all crops that likely play an equal,

if not more important role, than the managed

bees because evidence indicates that maintain-

ing a diverse community of pollinators will

greatly increase crop production (see Table 1 in

Katumo et al., 2022). To preserve this rich com-

munity of crop native pollinators, it is essen-

tial that natural and seminatural areas near

crop fields are protected. These areas provide

resources (e.g., pollen and nectar) for native

pollinators during the non-flowering periods of

crops (Carvalheiro et al., 2011; Garibaldi et al.,

2013). As pointed out by Dymond et al. (2021),

there is a significant information gap about

wild pollinators in the tropics, particularly in

Central America. Given the abundance of wild

Lauraceae plants, including Persea america,

in this region, natural pollinators may be bet-

ter adapted to pollinate cultivated avocados,

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

thus contributing significantly to yield increase.

Therefore, our research contributes information

on the relative importance of these wild pol-

linators for avocado cultivation in this region.

Among the four crops, avocado stands

out due to the richness and abundance of

insect assemblages that visit its flowers. Several

factors likely contribute to this phenomenon.

The dichogamous flowering pattern, the asyn-

chrony in basipetal anthesis within and among

inflorescences, the small size of the stigma, the

release of a limited number of heavy pollen

grains, and the production of nectar in both

flower phases (female and male) all serve to

attract a large number of insects (Davenport,

1986). Additionally, the neighborhood effect

(Underwood et al., 2020) may further explain

the diverse entomofauna visiting avocado flow-

ers. The synchronized flowering at the crop-

field level provides an abundant resource that

attracts a larger number of insects compared to

the other, less abundant crops. However, despite

differences in the assemblages of insect visitors

among crops, local insects provide an impor-

tant ecosystem service to farmers, by acting as

pollinating agents for all crops.

Conclusions: The Costa Rican highlands

are highly diverse regions with extensive natu-

ral habitats, primarily consisting of tropical

montane forests. San Gerardo de Dota com-

bines low-level agriculture and ecotourism, and

it is surrounded by natural protected montane

forests. This is why San Gerardo supports a rich

community of native insects that visit and likely

pollinate the flowers of avocado, apple, plum,

and blackberry crops. These crops include both

exotic and native species. Despite this, native

insects –particularly flies– abundantly visit all

crops. This is an important finding, as studies

have shown that a diverse pollinator commu-

nity leads to larger yields and fruits of higher-

quality (Garibaldi et al., 2013). It also opens

the possibility of introducing other native and

exotic insect-pollinated crops in the highlands

of Costa Rica. However, avocado hosts a unique

group of insects. Its flowers are visited by the

largest community of insects, primarily flies,

which clearly diverged from the visitors of

apple, plum, and blackberry that are dominated

by native and managed bees. Natural habitats

serve as reservoirs for a wide range of potential

pollinators, which play a crucial role in enhanc-

ing pollination, thus providing an important

service to nearby farms by improving crop yield

(Carvalheiro et al., 2011; Garibaldi et al., 2013).

Ethical statement: The authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict 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 acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

See supplementary material

A10v73s2-suppl1

ACKNOWLEDGMENTS

We highly appreciate Alejandro Vargas,

John Angulo and Beatriz Picado for their col-

laboration in collecting and identifying insects.

We thank E. Jacob Cristóbal-Pérez for their

guidance in data analysis. We appreciate the

suggestions made by Sergio Jansen-Gonzáles

and an anonymous referee on the manuscript.

Financial support for this project was pro-

vided by Vicerrectoría de Investigación-UCR

(C1460, C0-517, C0-068, B6-A32) and MICIT-

CONICYT (FI-040B-19). This manuscript was

completed during EJF’s sabbatical leave.

REFERENCES

Abernethy, K., Bush, E. R., Forget, P. M., Mendoza, I., &

Morellato, L. P. C. (2018). Current issues in tropical

phenology: A synthesis. Biotropica, 50(3), 477–482.

https://doi.org/10.1111/btp.12558

Aizen, M. A., Garibaldi, L. A., Cunningham, S. A., & Klein,

A. M. (2009). How much does agriculture depend on

pollinators? Lessons from long-term trends in crop

production. Annals of Botany, 103(9), 1579–1588.

https://doi.org/10.1093/aob/mcp076

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

Basualdo, M., Cavigliasso, P., De Ávila, R. S., Aldea-

Sánchez, P., Correa-Benítez, A., Harms, J. M.,

Ramos, A. K., Rojas-Bravo, V., & Salvarrey, S. (2022).

Current status and economic value of insect-polli-

nated dependent crops in Latin America. Ecological

Economics, 196, 107395. https://doi.org/10.1016/j.

ecolecon.2022.107395

Bataw, A. A. M. (1995). Pollination ecology of cultivated and

wild raspberry (Rubus idaeus) and the behavior of visi-

ting insects. [PhD thesis, University of St. Andrews].

http://hdl.handle.net/10023/14205

Breeze, T. D., Vaissière, B. E., Bommarco, R., Petanidou, T.,

Seraphides, N., Kozák, L., Scheper, J., Biesmeijer, J. C.,

Kleijn, D., Gyldenkærne, S., Moretti, M., Holzschuh,

A., Steffan-Dewenter, I., Stout, J. C., Pärtel, M., Zobel,

M., & Potts, S. G. (2014). Agricultural policies exa-

cerbate honeybee pollination service Supply-Demand

mismatches across Europe. PLoS ONE, 9(1), e82996.

https://doi.org/10.1371/journal.pone.0082996

Brown, B. V., Borkent, A., Cumming, J. M., Wood, D. M.,

Woodley, N. E., & Zumbado, M. A. (Eds.). (2009).

Manual of Central American Diptera: Volume 1. NRC

Research Press.

Brown, B. V., Borkent, A., Cumming, J. M., Wood, D. M.,

Woodley, N. E., & Zumbado, M. A. (Eds.). (2010).

Manual of Central American Diptera: Volume 2. NRC

Research Press.

Campbell, A. J., Biesmeijer, J. C., Varma, V., & Wäckers, F.

L. (2012). Realizing multiple ecosystem services based

on the responses of three beneficial insect groups

to floral traits and trait diversity. Basic and Applied

Ecology, 13(4), 363–370. https://doi.org/10.1016/j.

baae.2012.04.003

Carabalí-Banguero, D., Montoya-Lerma, J., & Caraba-

lí, A. (2021). Native bees as putative pollinators

of the avocado Persea americana Mill. cv. Hass in

Colombia. International Journal of Tropical Insect

Science, 41 (4), 2915–2925. https://doi.org/10.1007/

s42690-021-00475-x

Carvalheiro, L. G., Veldtman, R., Shenkute, A. G.,

Tesfay, G. B., Pirk, C. W. W., Donaldson, J. S.,

& Nicolson, S. W. (2011). Natural and within-

farmland biodiversity enhances crop produc-

tivity. Ecology Letters, 14(3), 251–259. https://doi.

org/10.1111/j.1461-0248.2010.01579.x

Celis-Diez, J. L., García, C. B., Armestó, J. J., Abades, S.,

Garratt, M. P. D., & Fontúrbel, F. E. (2023). Wild

floral visitors are more important than honeybees as

pollinators of avocado crops. Agronomy, 13(7), 1722.

https://doi.org/10.3390/agronomy13071722

Chanderbali, A. S., Soltis, D. E., Soltis, P. S., & Wolsten-

holme, B. N. (2013). Taxonomy and botany. In B.

A. Schaffer, B. N. Wolstenholme & A. W. Whiley

(Eds.), The Avocado: Botany, Production, and Uses (pp.

31–50). CABI.

Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H.,

Colwell, R. K., & Ellison, A. M. (2014). Rarefaction

and extrapolation with Hill numbers: A framework

for sampling and estimation in species diversity stu-

dies. Ecological Monographs, 84, 45–67. https://doi.

org/10.1890/13-0133.1

Cook, D. F., Tufail, M. S., Voss, S. C., Deyl, R. A., Howse, E.

T., Foley, J., Norrish, B., Delroy, N., & Shivananjappa,

S. L. (2023). Blow flies (Diptera: Calliphoridae) have

the ability to pollinate Hass avocado trees within

paired tree enclosures. Journal of Applied Entomology,

147(8), 577–591. https://doi.org/10.1111/jen.13159

Cristóbal-Perez, J. E., Barrantes, G, Cascante-Marín, A.,

Hanson, P., Picado, B., Gamboa-Barrantes, N., Rojas-

Malavasi, G., Zumbado, M. A., Madrigal-Brenes, R.,

Martén-Rodríguez, S., Quesada, M., & Fuchs, E. J.

2024. Elevational and seasonal patterns of plant polli-

nator networks in two highland tropical ecosystems

in Costa Rica. PLoSONE, 19(1), e0295258.  https://

doi.org/10.1371/journal.pone.0295258

Dainese, M., Martin, E. A., Aizen, M. A., Albrecht, M.,

Bartomeus, I., Bommarco, R., Carvalheiro, L. G., Cha-

plin-Kramer, R., Gagic, V., Garibaldi, L. A., Ghazoul,

J., Grab, H., Jonsson, M., Karp, D. S., Kennedy, C. M.,

Kleijn, D., Kremen, C., Landis, D. A., Letourneau, D.

K., ... Steffan-Dewenter, I. (2019). A global synthesis

reveals biodiversity-mediated benefits for crop pro-

duction. Science Advances, 5(10) eaax0121. https://

doi.org/10.1126/sciadv.aax0121

Davenport, T. L. (1986). Avocado Flowering. In J. Janick

(Ed.), Horticultural reviews (Vol. 8, pp. 257–284).

John Wiley & Sons.

Dymond, K., Celis-Diez, J. L., Potts, S. G., Howlett, B.

G., Willcox, B. K., & Garratt, M. P. D. (2021). The

role of insect pollinators in avocado production: A

global review. Journal of Applied Entomology, 145(5),

369–383. https://doi.org/10.1111/jen.12869

Freitas, B. M., Imperatriz-Fonseca, V. L., Medina, L. M.,

Kleinert, A. de M. P., Galetto, L., Nates-Parra, G., &

Quezada-Eúan, J. J. (2009). Diversity, threats and con-

servation of native bees in the Neotropics. Apidologie

40, 332–346. https://doi.org/10.1051/apido/2009012

Galetto, L., Aizen, M. A., Del Coro Arizmendi, M., Freitas,

B. M., Garibaldi, L. A., Giannini, T. C., Lopes, A. V.,

Santo, M. M. D. E., Maués, M. M., Nates-Parra, G.,

Rodríguez, J. I., Quezada-Euán, J. J. G., Vandame,

R., Viana, B. F., & Imperatriz-Fonseca, V. L. (2022).

Risks and opportunities associated with pollinators’

conservation and management of pollination services

in Latin America. Ecología Austral, 32(1), 055–076.

https://doi.org/10.25260/ea.22.32.1.0.1790

Garibaldi, L. A., Steffan-Dewenter, I., Kremen, C., Morales,

J. M., Bommarco, R., Cunningham, S. A., Carvalheiro,

L. G., Chacoff, N. P., Dudenhöffer, J. H., Greenleaf,

S. S., Holzschuh, A., Isaacs, R., Krewenka, K., Man-

delik, Y., Mayfield, M. M., Morandin, L. A., Potts,

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64701, mayo 2025 (Publicado May. 15, 2025)

S. G., Ricketts, T. H., Szentgyörgyi, H., ... Klein, A.

M. (2011). Stability of pollination services decreases

with isolation from natural areas despite honey bee

visits. Ecology Letters, 14(10), 1062–1072. https://doi.

org/10.1111/j.1461-0248.2011.01669.x

Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen,

M. A., Bommarco, R., Cunningham, S. A., Kremen,

C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bar-

tomeus, I., Benjamin, F., Boreux, V., Cariveau, D.,

Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M.,

Ghazoul, J., Greenleaf, S., ... Klein, A. M. (2013). Wild

pollinators enhance fruit set of crops regardless of

honey bee abundance. Science, 339(6127), 1608–1611.

https://doi.org/10.1126/science.1230200

Gilbert, F. S. (1981). Foraging ecology of hoverflies: mor-

phology of the mouthparts in relation to feeding

on nectar and pollen. Ecological Entomology, 6(3),

245–262. https://doi.org/10.1111/j.1365-2311.1981.

tb00612.x

Gilbert, F. S. (1985). Ecomorphological relationships in

hoverflies (Diptera, Syrphidae). Proceedings of the

Royal Society of London B, 224(1234), 91–105. https://

doi.org/10.1098/rspb.1985.0023

Gómez, J. M., Abdelaziz, M., Lorite, J., Muñoz-Pajares,

A. J., & Perfectti, F. (2010). Changes in pollinator

fauna cause spatial variation in pollen limitation.

Journal of Ecology, 98(5), 1243–1252. https://doi.

org/10.1111/j.1365-2745.2010.01691.x

Hegland, S. J., Nielsen, A., Lázaro, A., Bjerk-

nes, A., & Totland, Ø. (2009). How does clima-

te warming affect plant-pollinator interactions?

Ecology Letters, 12(2), 184–195. https://doi.

org/10.1111/j.1461-0248.2008.01269.x

Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT: An

R package for interpolation and extrapolation of

species diversity (Hill numbers). Methods in Eco-

logy and Evolution, 7(12), 1451–1456. https://doi.

org/10.1111/2041-210X.12613

Intergovernmental Science-Policy Platform on Biodiversity

and Ecosystem Services. (2016). The assessment report

of the Intergovernmental Science-Policy Platform on

Biodiversity and Ecosystem Services on pollinators,

pollination and food production (S. G. Potts, V. L.

Imperatriz-Fonseca, & H. T. Ngo, Eds.). IPBES Secre-

tariat. https://doi.org/10.5281/zenodo.3402856

Ish-Am, G., Barrientos-Priego, F., Castañeda-Vildozola,

A., & Gazit, S. (1999). Avocado (Persea americana

Mill.) pollinators in their region of origin. Revista

Chapingo Serie Horticultura, 5, 137–143. https://doi.

org/10.5154/r.rchsh.1999.05.137

Juárez, M. E., Kappelle, M., & van Omme, L. (2000). Lista

de la flora vascular de la cuenca superior del Río

Savegre, San Gerardo de Dota, Costa Rica. Acta Botá-

nica Mexicana, 51, 1–12. https://doi.org/10.21829/

abm51.2000.848

Katumo, D. M., Liang, H., Ochola, A. C., Lv, M., Wang, Q.,

& Yang, C. (2022). Pollinator diversity benefits natural

and agricultural ecosystems, environmental health,

and human welfare. Plant Diversity, 44(5), 429–435.

https://doi.org/10.1016/j.pld.2022.01.005

Kearns, C. A., Inouye, D. W., & Waser, N. M. (1998).

Endangered mutualisms: The conservation of plant-

pollinator interactions. Annual Review of Ecology and

Systematics, 29(1), 83–112. https://doi.org/10.1146/

annurev.ecolsys.29.1.83

Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter,

I., Cunningham, S. A., Kremen, C., & Tscharntke, T.

(2006). Importance of pollinators in changing lands-

capes for world crops. Proceedings of the Royal Society

B: Biological Sciences, 274(1608), 303–313. https://doi.

org/10.1098/rspb.2006.3721

Lowell, E. S. H., Morris, J., Vidal, M. C., Durso, C., & Mur-

phy, J. M. (2019). The effect of specific cues on honey

bee foraging behavior. Apidologie, 50(4), 454–462.

https://doi.org/10.1007/s13592-019-00657-0

Mengual, X., Ruiz, C., Rojo, S., Ståhls, G., & Thompson,

F. C. (2009). A conspectus of the flower fly genus

Allograpta (Diptera: Syrphidae) with a description of

a new subgenus and species. Zootaxa, 2214(1), 1–28.

https://doi.org/10.11646/zootaxa.2214.1.1

Michener, C. D., McGinley, R. J., & Danforth, B. N. (1994).

The bee genera of North and Central America (Hyme-

noptera: Apoidea). Smithsonian Institution.

Montero, B. K., Gamboa-Barrantes, N., Rojas-Malavasi, G.,

Cristóbal-Perez, E. J., Barrantes, G., Cascante-Marín,

A., Hanson, P., Zumbado, M. A., Madrigal-Brenes,

R., Martén-Rodríguez, S., Quesada, M., & Fuchs,

E. J. (2025). Pollen metabarcoding reveals a broad

diversity of plant sources available to farmland flower

visitors near tropical montane forest. Frontiers in

Plant Science, 15, 1472066. https://doi.org/10.3389/

fpls.2024.1472066

Muñoz, A. E., Amouroux, P., & Zaviezo, T. (2021). Native

flowering shrubs promote beneficial insects in avo-

cado orchards. Agricultural and Forest Entomology,

23(4), 463–472. https://doi.org/10.1111/afe.12447

Nation, J. L. (1983). A new method using hexamethyldisila-

zane for the preparation of soft insect tissues for scan-

ning electron microscopy. Stain Technology, 58(6),

347–351. https://doi.org/10.3109/10520298309066811

Nicholls, C. I., & Altieri, M. A. (2012). Plant biodi-

versity enhances bees and other insect pollinators

in agroecosystems: A review. Agronomy for Sus-

tainable Development, 33(2), 257–274. https://doi.

org/10.1007/s13593-012-0092-y

Nicholson, C. C., & Egan, P. A. (2019). Natural hazards pose

threats to pollinators and pollination. Global Chan-

ge Biology, 26(2), 380–391. https://doi.org/10.1111/

gcb.14840

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64701, mayo 2025 (Publicado May. 15, 2025)

Okello, E. N., Amugune, N. O., Mukiama, T. K., & Lattorff,

H. M. G. (2021). Abundance and community com-

position of flower visiting insects of avocado (Persea

americana Mill.) in the East African region. Interna-

tional Journal of Tropical Insect Science, 41(4), 2821–

2827. https://doi.org/10.1007/s42690-021-00463-1

Oksanen, J. (2022). Vegan: Ecological diversity (vignette).

https://cran.r-project.org/web/packages/vegan/vig-

nettes/diversity-vegan.pdf

Pardo, A., & Borges, P. A. V. (2020). Worldwide importance

of insect pollination in apple orchards: A review.

Agriculture, Ecosystems & Environment, 293, 106839.

https://doi.org/10.1016/j.agee.2020.106839

Percy, D. M., Page, R. D. M., & Cronk, Q. C. B. (2004).

Plant–insect interactions: Double-dating associated

insect and plant lineages reveals asynchronous radia-

tions. Systematic Biology, 53(1), 120–127. https://doi.

org/10.1080/10635150490264996

Pérez-Méndez, N., Andersson, G. K. S., Requier, F., Hipóli-

to, J., Aizen, M. A., Morales, C. L., García, N., Genna-

ri, G. P., & Garibaldi, L. A. (2020). The economic cost

of losing native pollinator species for orchard pro-

duction. Journal of Applied Ecology, 57(3), 599–608.

https://doi.org/10.1111/1365-2664.13561

Pincebourde, S., van Baaren, J., Rasmann, S., Rasmont, P.,

Rodet, G., Martinet, B., & Calatayud, P. A. (2017).

Plant–insect interactions in a changing world. In

N. Sauvion, D. Thiéry, & P.-A. Calatayud (Eds.),

Advances in botanical research: Insect–plant interac-

tions in a crop protection perspective (Vol. 81, pp.

289–332). Academic Press. https://doi.org/10.1016/

bs.abr.2016.09.009

R Core Team. (2023). A language and environment for

statistical computing. R Foundation for Statistical

Computing. https://www.R-project.org/

Roswell, M., Dushoff, J., & Winfree, R. (2021). A conceptual

guide to measuring species diversity. Oikos, 130(3),

321–338. https://doi.org/10.1111/oik.07202

Sargent, R. D., & Ackerly, D. D. (2008). Plant–pollinator

interactions and the assembly of plant communi-

ties. Trends in Ecology & Evolution, 23(3), 123–130.

https://doi.org/10.1016/j.tree.2007.11.003

Settele, J., Bishop, J., & Potts, S. G. (2016). Climate change

impacts on pollination. Nature Plants, 2(7), 16092.

https://doi.org/10.1038/nplants.2016.92

Solano, J., & Villalobos, R. (2001). Aspectos fisiográ-

ficos aplicados a un bosquejo de regionalización

geográfico-climático de Costa Rica. Tópicos Meteo-

rológicos y Oceanográficos, 8(1), 26–39. https://www.

researchgate.net/publication/228799654_Aspectos_

Fisiograficos_aplicados_a_un_Bosquejo_de_Regio-

nalizacion_Geografico_Climatico_de_Costa_Rica

Stoddard, F. L. (2017). Climate change can affect crop polli-

nation in unexpected ways. Journal of Experimental

Botany, 68(8), 1819–1821. https://doi.org/10.1093/

jxb/erx075

Strauss, S. Y., & Zangerl, A. R. (2009). Plant–insect inte-

ractions in terrestrial ecosystems. In C. M. Herrera &

O. Pellmyr (Eds.), Plant–animal interactions: An evo-

lutionary approach (pp. 77–108). Blackwell Science.

Underwood, N., Hambäck, P. A., & Inouye, B. D. (2020).

Pollinators, herbivores, and plant neighborhood

effects. The Quarterly Review of Biology, 95(1), 37–57.

https://doi.org/10.1086/707863

Visser, M. E., & Both, C. (2005). Shifts in phenology due

to global climate change: The need for a yardstick.

Proceedings of the Royal Society B: Biological Scien-

ces, 272(1581), 2561–2569. https://doi.org/10.1098/

rspb.2005.3356

Vithanage, V. (1990). The role of the European honeybee

(Apis mellifera L.) in avocado pollination. Journal of

Horticultural Science, 65(1), 81–86. https://doi.org/10

.1080/00221589.1990.11516033

Willmer, P. G., Bataw, A. A. M., & Hughes, J. P. (1994).

The superiority of bumblebees to honeybees as

pollinators: Insect visits to raspberry flowers. Eco-

logical Entomology, 19(3), 271–284. https://doi.

org/10.1111/j.1365-2311.1994.tb00419.x

Winfree, R. (2010). Conservation and restora-

tion of wild bees. Annals of the New York Aca-

demy of Sciences, 1195(1), 169–197. https://doi.

org/10.1111/j.1749-6632.2010.05449.x

Zebelo, S. A., & Maffei, M. E. (2015). Role of early sig-

naling events in plant–insect interactions. Journal

of Experimental Botany, 66(2), 435–448. https://doi.

org/10.1093/jxb/eru480