Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

Floral visitor diversity of ruderal plants in San Gerardo de Dota,

Costa Rica: a highland agricultural-natural landscape

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

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

Alejandro Vargas-Rodríguez1, 2; https://orcid.org/0009-0007-6056-2717

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; geoo.roojas@gmail.com (*Correspondence),

nicolegamcr@gmail.com, alejandro.vargas_r@ucr.ac.cr, eric.fuchs@ucr.ac.cr, b.karina.montero@gmail.com, ruth.mad-

rigalbrenes@ucr.ac.cr, gilbert.barrantes@gmail.com; phanson91@gmail.com

2. Centro de Investigación en Biodiversidad y Ecología Tropical, 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 31-VIII-2024. Corrected 13-III-2025. Accepted 25-III-2025.

ABSTRACT

Introduction: Wild plants rely mainly on insects for pollination, and many of these plants are essential to main-

taining a diverse and abundant community of crop insect-pollinators. In Costa Rican highland ecosystems, the

diversity and abundance of insect floral visitors have been poorly studied, despite their importance and proximity

to crops in this area.

Objective: to determine the richness and composition of floral visitor insect species of native and ruderal herba-

ceous plants close to cultivated areas in San Gerardo de Dota, Costa Rica.

Methods: We systematically collected flower-visiting insects along transects in two different sites and identified

them to the lowest taxonomic level. We estimated alpha diversity for each season and 11 plant groups created

specifically for this study. We defined these plant groups based on flower morphology, life history traits, and their

taxonomic relatedness. We also compared the insect community composition across seasons and plant groups.

Results: We collected a total of 1306 insects, mainly flies (Diptera), from 62 families on 46 plant species during

12 sampling visits. Insect diversity (alpha diversity) increased during the rainy season, possibly because resources

(e.g., food and reproductive sites) for flies increase during this season. Insect species composition varied among

plant groups. The most abundant insect communities overlapped extensively among plant groups, but other com-

munities compose mainly by some tachinids, chloropids and wasps did not overlap between other plant groups.

Conclusion: Seasonal differences in flower-visiting insects could be attributed to a greater availability of

resources during the rainy season. Differences in the composition of visitor insects across plant groups were

likely influenced by temporal variation in blooming of the different plant groups, blooming intensity, and flower

https://doi.org/10.15517/rev.biol.trop..v73iS2.64684

SUPPLEMENT

SECTION: MUSEUM

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

INTRODUCTION

Plant-pollinator interactions in natural

ecosystems play an essential role in the repro-

duction of flowering angiosperm plants (Fon-

taine et al., 2006), and around 94 % of the

tropical plant species rely on insects for pollina-

tion (Ollerton et al., 2011). Additionally, over

60 % of global food production depends, to

varying degrees, on insect pollination (Hoehn

et al., 2008; Klein et al., 2007). Native pollinat-

ing insects improve the quality and quantity of

pollination-dependent crop yields (Carvalheiro

et al. 2011; Garibaldi et al., 2013; Hoehn et al.,

2008; Klein et al., 2007; MacInnis & Forest,

2019; Pérez-Méndez et al., 2020). However,

despite the role played by insect pollinators,

knowledge of the diversity and composition of

flower-visiting insects in tropical ecosystems

remains limited (Aizen et al., 2008). Under-

standing insect interactions in natural ecosys-

tems surrounding cultivated areas is critical

for ensuring the long-term viability of these

ecosystem services.

In highland ecosystems, the diversity and

abundance of some insect pollinating groups

such as Hymenoptera, Lepidoptera and Cole-

optera are lower compared to flies, which play

a greater role as pollinators in these ecosys-

tems (Brenes, 2017; Cristóbal-Pérez et al., 2024;

Inouye et al., 2015; Lefebvre et al., 2018; Maglia-

nesi et al., 2020). When comparing ecosystems

of different altitudes in the montane forest and

paramo of Costa Rica, results show that both

traits. To preserve the rich diversity of floral visitors and the pollination services they provide, a diverse array of

ruderal plants must be maintained.

Keywords: Diptera; Hymenoptera; insect communities; pollinators; flower-visiting insects.

RESUMEN

Diversidad de visitadores florales de plantas ruderales en San Gerardo de Dota, Costa Rica:

un paisaje agrícola y natural de zonas altas

Introducción: Las plantas silvestres dependen principalmente de insectos para su polinización, y a su vez, muchas

de estas plantas son esenciales para mantener una comunidad de insectos polinizadores estable, que beneficia a

las especies cultivadas. En los ecosistemas de zonas altas de Costa Rica, la diversidad y abundancia de insectos

visitadores florales ha sido poco estudiada, a pesar de su importancia y de la proximidad de cultivos en el área.

Objetivo: Determinar la riqueza y composición de especies de insectos visitadores florales de plantas herbáceas

nativas y ruderales en un paisaje agrícola en la zona de San Gerardo de Dota, Costa Rica.

Métodos: Recolectamos insectos visitadores florales sistemáticamente por dos años, a lo largo de transectos

en dos sitios, y los identificamos al nivel taxonómico más bajo posible. Estimamos la diversidad alfa para las

estaciones seca y lluviosa y entre grupos de plantas. Estos grupos de plantas fueron definidos con base en sus

características florales, otros rasgos de vida, y su relación taxonómica. Además, comparamos la composición de

insectos visitadores florales entre estos grupos.

Resultados: Colectamos un total de 1306 insectos, principalmente moscas, de un total de 65 familias en 46 espe-

cies de plantas durante 12 visitas de muestreo. La diversidad alfa de insectos, particularmente de moscas (Diptera)

fue mayor durante la época lluviosa, debido, posiblemente, a la mayor disponibilidad de recursos (e.g., alimento

y sitios para reproducción) para este grupo de insectos. La composición de especies varió entre plantas agrupadas

por su morfología floral. Algunas de las comunidades de insectos se traslaparon extensivamente en algunos gru-

pos de plantas, mientras que para otras comunidades el traslape fue mucho menor.

Conclusión: Las diferencias estacionales en los insectos visitadores florales se pueden atribuir a la mayor dispo-

nibilidad de recursos durante la época lluviosa. Las diferencias en la composición de insectos visitadores florales

entre los distintos grupos de plantas fueron probablemente influenciadas por variaciones temporales en las

floraciones, la intensidad de estas floraciones y las características de las flores en cada grupo de plantas. Para con-

servar la diversidad de insectos visitadores florales y los servicios de polinización que estos proveen, es necesario

mantener una diversidad alta de plantas ruderales.

Palabras clave: Dípteros; Himenópteros; comunidades de insectos; polinizadores; insectos visitantes de flores.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

pollinator interaction networks and species

richness are lower in the Páramo (Cristóbal-

Pérez et al., 2023; Cristóbal-Pérez et al., 2024).

At high elevations, insects tend to be more

generalist, which allows them to forage in wild

plants like herbs and shrubs that are in bloom

at the moment (Cristóbal-Pérez et al., 2024).

Flower-visiting insects also have a greater sen-

sitivity to seasonal environmental fluctuations

at higher elevations. For example, the decrease

in precipitation and temperature experienced

during the dry season negatively impacts the

richness and abundance of pollinating insects

in these montane habitats because availability

of resources for insects decreases with the prog-

ress of the dry season, and low temperatures

limit the flying capability of insects (Cristóbal-

Pérez et al., 2023; Kaiser-Bunbury et al., 2010;

Memmott et al., 2007; Minachilis et al., 2021).

Therefore, it is important to evaluate and

understand the role of insect communities in

the wild vegetation surrounding crops that rely

on entomophilous pollination and are located

close to protected natural areas. It has been

shown that protected areas around crops pro-

vide important ecosystem services by maintain-

ing pollinator populations (Klein et al., 2003).

Because there has been an increase in the culti-

vation of crops (e.g., avocados, apples) in some

Costa Rican highland communities, studying

floral visitation in the surrounding vegetation

allows us to assess the ecosystem services that

protected areas provide to crops and the com-

munity as a whole.

The objective of this study was to charac-

terize the communities of insect floral visitors

of herbaceous and shrubby vegetation in the

natural areas surrounding crops in a highland

agricultural landscape. Specifically, we focused

on determining the richness and abundance

of floral visiting insects of herbaceous and

shrubby vegetation in the San Gerardo de

Dota area throughout the year to evaluate the

potential role of these plants in maintaining

the community of pollinating insects, which

could contribute to the pollination of crops in

this area. Knowing the communities of floral

visitors and pollinating insects is crucial to the

preservation of these ecosystems and promot-

ing the continuous development of sustainable

human activities.

MATERIALS AND METHODS

Study Site: The study site was located in

the mountainous region of San Gerardo, Dota,

San José province, Costa Rica (9°40’ N; 83°58’

W), between 2 180 and 2 400 m a.s.l. The vege-

tation on the site is typical of the lower montane

forest, consisting of heterogeneous evergreen

forests, with a 20-25 m canopy with abundant

moss and small epiphytes (Hartshorn, 1991).

Some plants, common at higher elevations also

grow at this altitude, like Quercus spp. which

can reach 50 m in height (Hartshorn, 1991).

This region possesses a unique combination of

natural protected areas, low-intensity commer-

cial agriculture (mostly avocado, blackberry,

plum, and apple crops), and low-impact nature

tourism. The mean annual temperature at this

site is 16.9° C, with minimum temperatures of

12.5° C in January and February, and maxi-

mum temperature of 19.5-20.5 °C. Minimum

and maximum temperatures are reached dur-

ing the dry season (amply daily variation), but

temperatures are also high at the beginning of

the rainy season (May-July). The mean annual

precipitation is of 2 600 mm (Climate-data.

org, 2021). Precipitation has a strong seasonal-

ity with a dry season from December through

April, and the rainy season begins in May and

extends throughout November (Climate-data.

org, 2021).

Sampling Sites: Four transects, two in

each of the two sampling sites, were established

to assess the diversity of floral visiting insects

of wild plant species (Fig. 1). Transects (150 m

x 2 m) were selected based on two criteria: 1.

Sites included a perceivable high richness and

abundance of native and naturalized herba-

ceous and shrubby plants with flowers; 2. sites

were near or within cultivated areas. The first

site selected was “Tajo”, a secondary growth

area on the edge of the main road along a

quarry (9°34’17’’ N; 83°48’49’’ W). The second

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

transect, named “Suria”, was located along a

secondary road (9°32’51’’ N 83°48’45’’ W).

Sites were highly diverse and shared only a few

species between them. Both sites were located

between 200 m and 500 m from a farm. In each

transect we collected insects from vines, her-

baceous plants, and small and medium-sized

shrubs (< 2 m high); rare species or those with

low insect visitation were not considered for

analyses. All plants were identified to the spe-

cies level (Table 1).

Data collection: We collected insects that

were in contact (any part of their body) with

flowers from 7:00 to 13:00 hours; sampling

was interrupted if rain began early. At each

site, two transects of 150 x 2 m were used to

search for flowering plants (Fig. 1), and sam-

plings encompassed between 0.5 and 5 hours

per transect, depending on weather conditions

and species flowering phenology. We walked at

a slow, steady pace and stopped and collected

insects for about 5 min in individual flower-

ing plants but collected for up to 15 min in

large flower patches. Entomological nets or

transparent plastic bags were used to collect

flower-visiting insects. Sampling sessions were

conducted between July 2021 and August 2022.

Identification: Each collected insect was

identified to the lowest possible taxon using

the keys of the Central American Manual of

Diptera (Brown et al., 2009; Brown et al., 2010),

the Manual of North American Bees (Michener

et al., 1994), and comparison with specimens

of the Entomology Collection of the Museum

of Zoology at the University of Costa Rica and

the National Museum of Costa Rica. The insect

specimens from this study are deposited in

the Entomology Collection of the Museum of

Fig. 1. Map of the two selected sampling sites in San Gerardo de Dota, Costa Rica. Transects used within the sites to collect

and record flower-visiting insects are indicated by blue and orange lines, for the Tajo and Suria sites, respectively.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

Table 1

List of herbaceous and shrubby plant species on which insects were collected in two natural areas adjacent to crops in San

Gerardo de Dota, Costa Rica. Plant groups are comprised of species that combine similar flower morphology and habit. Monthly

flowering is indicated by the gray cells, and the percentage of insects captured per plant species in each group is included.

Group Genus/Species % Jan Feb Mar Apr May Jun Jul Aug Set Oct Nov Dec

Asteraceae-1 Hypochaeris radicata 46.88

Crepis capillaris 42.86

Sonchus oleraceus 10.27

Asteraceae-2 Dahlia imperialis 9.09

Vigueira cordata 3.98

Bidens reptans 44.89

Bidens pilosa 40.91

Leucanthemum vulgare 1.14

Asteraceae-3 Ageratina bustamenta 38.00

Ageratum conyzoides 24.00

Pseudognaphalium attenuatum 4.67

Conyza sumatrensis 8.00

Jaegeria hirta 4.00

Clibadium leiocarpum 21.33

Open-flowers Monochaetum floribundum 2.15

Rubus adenotrichus 4.30

Rubus costaricanus 4.30

Impatiens sodenii 5.38

Wigandia urens 55.91

Senna guatemalensis 7.53

Passiflora ligularis 20.43

Cucurbitaceae-vines Sechium pittieri 99.15

Cyclanthera langaei 0.85

Small-flower-vines Muehlenbeckia tamnifolia 98.20

Cissus obliqua 1.80

Tubular-flowers Fuchsia paniculata 2.47

Thunbergia alata 2.47

Brugmansia arborea 25.93

Hemichaena fruticosa 3.09

Phaseolus dumosus 6.79

Ipomoea purpurea 59.26

Herbs-1 Veronica serpyllifolia 8.33

Geranium seemannii 66.67

Lepidium virginicum 18.75

Arenaria lanuginosa 2.08

Hypericum thesiifolium 4.17

Herbs-2 Verbena littoralis 64.47

Spermacoce remota 35.53

Herbs-3 Persicaria capitata 80.00

Rumex obtusifolius 4.21

Trifolium repens 11.58

Solanum americanum 4.21

Lopezia miniata Lopezia miniata 100.00

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

Zoology at the University of Costa Rica. Plant

identification was carried out through the col-

lection of herbarium specimens and the col-

laboration of the plant taxonomist Dr. Alfredo

Cascante. These identifications yielded lists of

insect and plant genera and species.

Statistical analysis data curation and

handling: We classified the sampled plants into

eleven plant groups based on floral morphology

(shape and size), plant size, and the taxonomic

relationship of the plant species in that order

of priority. The names of the plant groups

are shown in Table 1, and each plant group’s

morphological and general traits are grouped

in Table 2. Floral morphology and flower size

are related to the types/groups of pollinators

that visit the flowers, so this classification

allows species with few visits to be included in

the analyses (Dellinger, 2020). The number of

insects collected for each plant group was plot-

ted using ggplot2 (Wickham et al., 2016).

For alpha diversity analyses, we created an

abundance matrix, with groups of plants and

seasons as rows and insect species as columns.

Data consisting of insects recorded on only 1

or 2 plants, 1 or 2 insects captured of the same

species or morphospecies, or captured in sam-

pling sessions lasting less than 2 hours, were

considered insufficient and were excluded from

the analyses. Data handling was performed

using the dplyr (Wickham et al., 2023) and

tidyverse (Wickham et al., 2019) packages in

the R statistical language (R Core Team, 2024).

Because there were many cells with zeros,

analyzing beta diversity required two additional

modifications to the data matrix. The first

modification consisted of combining the abun-

dance by morphospecies within each insect

family; the taxa that were identified as species

were maintained as such. The second modifi-

cation consisted of combining the data from

every two sampling sessions. These modifica-

tions allowed the evaluation of beta diversity

across plant groups and seasons.

Analysis of alpha diversity patterns: We

used Hill numbers (D0, D1, and D2) to com-

pare alpha diversity of flower-visiting insects

between sites (i.e., Suria and Tajo) and seasons

(dry and rainy). All three statistics compare dif-

ferent aspects of diversity among plant groups

and seasons: D0 estimates species richness, D1

(Hill-Shannon) estimates diversity with equal

Table 2

General characteristics and flower morphology of the species included in each plant group.

Plant group Flower morphological and plant description

Asteraceae-1 Dandelion type flowers with homogamous lingulate capitula.

Asteraceae-2 Daisy type flowers with heterogamous radiate capitula.

Asteraceae-3 Discal type flowers with both heterogamous discoid and homogamous discoid capitula.

Open flowers Open to bowl-shaped flowers of varied shapes, colors, and sizes.

Cucurbitaceae-vines Actinomorphic unisexual flowers, with big anthers that are fussed in the middle, greenish white

color.

Small-fower-vines Panicles or cymes of minute cup-shaped white flowers with visible anthers.

Tubular-flowers Tube, bell or funnel-shaped big to medium flowers of various pink, yellow and purple colors.

Vines or trees. Purple, white or yellow.

Herbs-1 Herbs with tiny to small 4 to 5 petal rotate flowers purple, white and yellow.

Herbs-2 Herbs with clusters of tiny salverform-shaped flowers, purple and white.

Herbs-3 Herbs with tiny bell-shaped flowers packed in panicles, and one species of Solanum with a small

star-shaped flower with joined big stamens at the center. Pink, white or yellow.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

weight for rare and common species, and D2

(Hill-Simpson) estimates diversity with great-

er weight for common species (Chao et al.,

2014b). We estimated diversity with respect to

the number of individuals and sample coverage

(sample completeness) (Roswell et al., 2021), as

well as rarefaction curves.

Considering that the results from all three

estimators show the same trend (Fig. 1 Supple-

mentary Material), we only present the results

of the Hill-Shannon estimator, which weights

equally both rare and abundant species (Alber-

di & Gilbert, 2019). This estimator is recom-

mended when the sampling may not accurately

reflect the real number, in this case, of insect

floral visitors (Alberdi & Gilbert, 2019). We

performed these analyses with the iNEXT

package, using the iNext and ggiNEXT func-

tions (Chao et al., 2014a; Chao et al., 2014b;

Hsieh et al., 2022). The total richness of visiting

insects of each plant group was estimated with

the ChaoRichness function of the iNEXT pack-

age (Chao, 1984).

Analysis of species composition (beta

diversity): To compare species composition of

insect communities (beta diversity) between

plant groups and seasons, we used a non-met-

ric multidimensional scaling (NMSD) analysis

based on a Bray-Curtis dissimilarity matrix

with 1 000 permutations (Oksanen et al., 2022).

We then conducted a distance-based PER-

MANOVA (Permutational Multivariate Analy-

sis of Variance) with the adonis function of

the vegan package (Oksanen et al., 2022). We

included season and plant group as predictor

variables in the model.

We evaluated the assumption of the homo-

geneity of variance of the data with the betadis-

per function (Oksanen et al., 2022); variances

were homogeneous between seasons (F = 0.29,

p = 0.98), and among groups of plants (F = 0.29,

p = 0.99). Lastly, we compared the dissimilar-

ity, species turnover, and nesting of insect spe-

cies communities between seasons and plant

groups, using the beta.pair.abund function of

the betapart package (Baselga, 2023). We also

used the bipartite package’s visweb function to

plot the network matrix to show the interac-

tions between the taxa and plant groups (Dor-

mann et al., 2008).

RESULTS

We collected 1 306 insects from 62 families

on 43 shrubs, lianas and small herbaceous plant

species over the course of 29 sampling sessions

(97 hours). We established 11 plant groups

to categorize plants, with insects assigned to

each plant group (Table 1). For most plant

groups, there were flowers available year-round

(e.g., Asteraceae-1, tubular-flowers), but not

all species within a group produced flowers

throughout the entire study period (e.g., Ipo-

mea purpurea, Persicaria capitata). Differ-

ences in number of flowering plant species

likely responded to species specific phenologies

and mortality caused by seasonal changes in

precipitation.

Most insects collected were of the orders

Diptera (27 families, 611 individuals), Hyme-

noptera (14 families, 530 individuals) and Cole-

optera (8 families, 90 individuals). The number

of flower visitors varied depending on the sea-

son and plant group, but flies, bees, and wasps

visited flowers in most plant groups (Fig. 2,

Table 1 Supplementary Material, Table 2 Sup-

plementary Material, Table 3 Supplementary

Material). Only three visits of hummingbirds

(possibly Selasphorus flammula and Panterpe

insignis) were observed.

Alpha diversity: The diversity (alpha) of

insects, as estimated by Hill-Shannon, varied

among sites and seasons. In both sites, the high-

est diversity of insects was recorded during the

rainy season, but diversity was larger at the Tajo

site for both seasons, particularly in the rainy

season (Fig. 3). Differences in alpha diversity

between sites are likely influenced by the larger

number of species and individuals collected in

the Tajo transect (Fig. 3), which is adjacent to

a large tract of protected montane forest. The

richness curves and Chao estimates between

the plant groups show no apparent differences

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

Fig. 2. Composition and abundance of insect orders collected in each group of plants at the study sites.

Fig. 3. Diversity of insects collected in two sites (Suria and Tajo) in both the dry and rainy seasons is shown in lines of

different colors and the 95% upper and lower confident limits are represented with the shaded area that surrounds the curve.

The percentage coverage of the Hill-Shannon estimator is indicated for each site-season combination.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

between the richness of the plant groups, due

to their wide confidence intervals (Table 4

Supplementary Material, Fig. 2 Supplementary

Material).

Community analysis (beta diversity):

The composition of insects differed between

seasons (F = 2.44, P = 0.003, R2 = 0.03) and

between plant groups (F = 2.86, P = 0.001, R2

= 0.37), but most of the variance explained was

attributed to differences between plant groups.

Insect communities of some plant groups over-

lapped extensively. This occurred, for example,

with the two plant groups that comprise Astera-

ceae. In contrast, insect communities associated

with other plant groups (e.g., tubular flowers,

small herbs-2) showed little overlap with com-

munities of other plant groups (Fig. 4, Fig. 3

Supplementary Material, Fig. 4 Supplementary

Material, Fig. 5 Supplementary Material).

Species dissimilarity differed significantly

between seasons (t = -2.87, P = 0.005; Fig. 5A).

This difference was likely a consequence of a

more heterogeneous distribution of insect spe-

cies among plant groups during the dry season.

Species turnover did not show a significant dif-

ference between the dry and rainy seasons (t =

-0.27, P = 0.79, Fig. 5B), suggesting that there

was not a notable change in the composition

of species between seasons. However, species

nestedness changed drastically between dry

and rainy seasons (t = -4.65, P < 0.001, Fig. 5C),

suggesting that during the dry season flower-

visiting insects in different plant groups are

Fig. 5. Comparison of insect communities between dry and rainy seasons A. Total dissimilarity. B. Species turnover. C.

Species nestedness. The line is the average value of the betapar estimates, the boxes represent the beta-diversity standard

deviation of the statistical estimates calculated from the upper and lower intervals. The total dissimilarity and nesting were

significantly different between the dry and rainy seasons.

Fig. 4. Non-metric multidimensional scaling analysis

(NMDS) of the composition of flower-visitor insects

based on the Bray-Curtis index, using the abundance

of insects collected in each plant group. Plant groups

follow Table 1 and are shown in different colors: Orange:

Asteraceae-1, Yellow: Asteraceae-2, red: Asteraceae-3, Navy

blue: Cucurbit-vines, Blue: Lopezia miniata, Green: Open-

flowers, Orange-red: Small-flower-vines, Dark gray: Small-

herbs-3, Light gray: Herbs-1, Black: Herbs-2, Light blue:

Tubular-flowers. The verified model’s voltage was 0.2135.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

subsets of the communities of insects attracted

to flowers in the rainy season.

DISCUSSION

We found a predominance of flies (Dip-

tera) in flower-visiting insect communities,

which is consistent with previous research on

insect flower visitors in Costa Rica’s high-

lands and similar regions (Arroyo et al., 1984;

Cristóbal-Pérez et al., 2024; Elberling & Olesen,

1993). At high elevations, flies far exceed the

abundance of other floral visitors such as bees,

butterflies, and beetles (Cristóbal-Pérez et al.,

2024). Abundant flies like hoverflies, are associ-

ated with multiple plant groups and potentially

play an important role in plant pollination in

natural environments at high elevations (Jauker

& Wolters, 2008; Montero et al., 2025). Other

abundant groups of flies, such as Muscidae and

Tachinidae, can also play an important role

as pollinators (Orford et al., 2015) and were

diverse in some plant communities, particularly

during the rainy season (Cristóbal-Pérez et al.,

2024; Kearns, 1992).

Bees, native and managed, were the sec-

ond most diverse group of flower visitors. For

instance, the native Lasioglossum sp., Meliwil-

lea bivea, Partamona grandipennis, and Bom-

bus ephippiatus, as well as honeybees, were

very abundant visitors of most plant groups.

Social insects, such as the aforementioned bees

(except Lasioglossum), form large colonies with

high caloric demands, and as a result they tend

to be more generalists, relying on a diverse

array of plant species to meet their caloric

needs (Roubik, 1989; Potts et al., 2003). During

the dry season, there is a reduction in richness

and diversity in the insect communities com-

posed of a subset of communities associated

with different plant groups during the rainy

season. However, insects tend to use a wide

range of flowers as a possible consequence

of a reduction in resource availability during

the dry season, as predicted by the theory of

optimal foraging (Cristóbal-Pérez et al., 2024;

Fontaine et al., 2008; Robinson & Wilson,

1998). Similar patterns of visitation have been

observed in other habitats with limited resourc-

es (Dupont et al., 2003; Smith-Ramírez et al.,

2005; Souza et al., 2017).

The dissimilarity in the composition of

insect visitors among habitats increased in

the dry season, likely as a consequence of

the notable reduction in richness, mainly of

some Diptera, and a reduction of flowering

plants during this season, which results in

more heterogeneous communities of flower

visitors (Orford et al., 2015). On the contrary,

the onset of the rainy season favors both the

reproduction of insects and the richness of

blooming plant species, increasing the richness

of floral visiting insects in these environments

(Cristóbal-Pérez et al., 2024; Inouye et al.,

2015). The differences between the communi-

ties of insects associated with different groups

of plants indicate the coexistence of both spe-

cific and generalist floral visitors, which visit

various types of plants depending on the season

or flowering periods (Fig. 4, Cristóbal-Pérez et

al., 2024). Changes in richness are more notice-

able in Diptera, which do not typically fluctuate

on a seasonal basis but rather respond to non-

seasonal fluctuations in environmental factors

such as temperature, moisture, wind and light

intensity (Inouye et al., 2015; Kudo et al., 2023).

Except for some hoverflies that are also present

in the dry season.

Some groups of plants, such as herbaceous

plants types 1 and 2, attracted groups of flower-

visiting insects that differed substantially from

other insect communities that visit other plant

groups like tubular-flower plants, small-flower

vines and, to a lesser extent, Asteraceae-3 (Fig.

4). For example, some species in the Astera-

ceae type 3 plant group, such as Ageratina

bustamenta, had their flowering peak in the

dry season,which only a few other plants come

into flower in those months. Blooming at this

particular time attracts a distinct communi-

ty of flower-visiting insects, such as the bee

Exomalopsis sp. (Janovský & Štenc, 2023; Junk-

er et al., 2013; Olesen et al., 2008). Other spe-

cies, such as Muehlenbeckia tamnifolia, present

in the plant group Small-flower-vines, were also

visited by a large and diverse insect community

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64684, mayo 2025 (Publicado May. 15, 2025)

of both flies and wasps, that were not present

in other plant groups as it has been registered

for other species of the genus (Primack, 1978).

Tubular-flower plants such as Ipomoea sp. and

Brugmansia sp. were visited primarily by bees,

but also by a group of small insects that use

these flowers for their reproduction and feed-

ing, such as some Drosophilidae flies and Niti-

dulidae beetles (e. g., Conotelus sp.) (Ishikawa

et al., 2022; Da Paz et al., 2013; Santos et al.,

2020; Schmitz & Valente, 2019). Differences

between insect groups are likely associated with

temporal correlation between the phenology

of some plant groups and some insect groups,

abundance of flowers or by the preference of

some insects for specific flowering plants (Da

Paz et al., 2013; Janovský & Štenc, 2023).

Open-flowered plants together with cucur-

bit-vines, herbs-3 and, to a lesser extent, Astera-

ceae groups 1 and 2 shared a large proportion of

their floral visiting insect communities. Open-

flowered plants, like cup-shaped flowers and

Asteraceae flowers that have accessible pollen

and nectar, are more likely to have a wider array

of visitors (Herrera, 2019; Ollerton et al., 2007).

However, these open-flowered groups were

visited by fewer species, in contrast to Astera-

ceae-3 which was visited by a large community

of insects (Fig. 2 Supplementary Material). This

suggests that accessibility to floral rewards is

not the only factor influencing visitation, but

the type and quality of resources, as well as

color and odor, abundance and phenology may

also play an important role in selecting the

insect groups that visit different groups of plants

(Fenster et al., 2004; Herrera, 2019; Junker et al.,

2013; Pardo et al., 2020, Reverté et al., 2016).

Naturalized herbaceous plants (all Astera-

ceae-1 and some in herbaceous plants) were

visited by insects that also visited a wide array

of plants (Fig. 4). In this study, the rarest

or least frequent native floral visitor insects

mainly visited native species, such as cucurbits

or small-flowered vines (Fig. 5 Supplemen-

tary Material). This is an interesting result that

suggests that maintaining a diverse group of

native herbaceous plant species is important

for the conservation of flower-visiting insect

communities and the role they play in provid-

ing pollination services to local plants and

cultivars (Montero et al., 2025). Introduced or

naturalized plant species can provide additional

and novel resources for abundant groups of

insects (Memmott & Waser, 2002).

In conclusion, the interaction between

plants with different flower morphology and

phenology and visiting insect communities are

essential to maintain the high species richness

of insects and plants in this ecosystem. The

richness of flower-visiting insects varied among

plant groups on a seasonal basis. During the

rainy season the richness and diversity of flow-

er-visiting insects increased, as did the diversity

and abundance of flowering plants. Some plant

groups share the most abundant visitor insect

communities; however, other plant groups are

only visited by specific insect groups, and floral

rewards and morphology likely influence these

differences. Therefore, to maintain the diverse

community of floral visitors and the pollination

services they provide, it is necessary to main-

tain a large diversity of native plants, since they

provide food and shelter for adults and possibly

for their eggs and larvae.

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

a18v73s2-suppl1

ACKNOWLEDGMENTS

We appreciate E. Jacob Cristóbal-Pérez

for his guidance in some aspects of the data

analysis, and Alfredo Cascante Marin for his

help identifying the plants. We also extend

our gratitude to the people and farmers of

San Gerardo, particularly Gerardo Chacón and

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64684, mayo 2025 (Publicado May. 15, 2025)

Fernando Chacón, for all their hospitality and

help. 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.

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