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Ratatouille of flowers! Rats as potential pollinators of a petal-rewarding plant

in the urban area

Article in Ecology · June 2022

DOI: 10.1002/ecy.3778

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DOI: 10.1002/ecy.3778

THE SCIENTIFIC NATURALIST

Ratatouille of flowers! Rats as potential pollinators of a

petal-rewarding plant in the urban area

Carlos A. Matallana-Puerto1,2 |
dio Fernandes Cardoso3

João Custo
1
Grupo de Investigaci
on Biología para la Conservaci

on, Escuela de Biología, Facultad de Ciencias, Universidad Pedag

ogica y Tecnol

ogica de
Colombia, Tunja, Colombia
2
Programa de P

os-Graduação em Biologia Vegetal, Instituto de Biologia Vegetal, Universidade Estadual de Campinas, Campinas, Brazil
3
Instituto de Ciências da Natureza, Universidade Federal de Alfenas, Alfenas, Brazil

Correspondence
Carlos A. Matallana-Puerto
Email: ca.matallanap@gmail.com

Handling Editor: John J. Pastor

K E Y W O R D S : Acca sellowiana, Myrtaceae, pollination, urban ecology

It is estimated that 87.5% of angiosperms are pollinated
by animals (Ollerton et al., 2011) and 75% of the main
food crops depend on animals for fruit set and seed pro-
duction (Klein et al., 2007). Although abundant and eco-
logically important in many environments, mammals are
among the least studied pollinators, probably because
most of them have nocturnal habits, which makes field-
work difficult (Kleizen et al., 2008). It is estimated that
343 species of mammals are pollinators (Regan
et al., 2015). Most of them are bats (ca. 69%), followed by
nonflying mammals (ca. 31%) (Regan et al., 2015). This
latter group, which includes elephant shrews, marsupials,
primates, small carnivores, and rodents, can carry large
amounts of pollen and thereby mediate the reproduction
of the plants they visit (Goldingay et al., 1991).
Rodents can be important pollinators in some regions
of the Old World, such as South Africa and Australia;
studies in other geographical regions are still in their
incipient stage (Ratto et al., 2018). For instance, it is esti-
mated that the production of fruits and seeds by the
plants they visit can decrease 49% when their access is
restricted in controlled experiments (Ratto et al., 2018).
However, although they are important pollinators in
some systems, they are still treated mostly as exceptional
cases (Ollerton, 2017).
In this context, where research on rodent pollination
is lacking, any information is valuable. When talking to
older people, we have heard rumors that rats have been
seen in a tree species in Duitama city (Boyac
a, Colombia)
in broad daylight over several decades (M. C. Ballesteros
and H. M. Puerto, personal communication, 2019). This
tree is Acca sellowiana (Myrtaceae), commonly known in
the region as feijoa, a nonnative cultivated fruit plant
from northern Argentina and Uruguay and southern Bra-
zil (Keller & Tressens, 2007) that has been introduced in
different countries due to its important economic value
(Ramírez & Kallarackal, 2017). In Colombia, A.
sellowiana is cultivated in several regions located in
higher altitudes with colder climates, such as in the
Boyac
a department. This is the largest producer of the
fruit in the country and where both the fruit and derived
food and drinks are sold, representing an important eco-
nomic contribution to the region (Rodríguez &
Bermúdez, 1996). A. sellowiana flowers have fleshy white
petals with a purple interior, with many red stamens and
an upright red central pistil located above (Figure 1a).
The pollination process is unusual since the energy-rich
petals are the resource being consumed by birds that are
the main pollinators (Ramírez & Kallarackal, 2017). In
several Colombian cities, A. sellowiana is cultivated in
urban areas.
Thus, based on the information offered by some
inhabitants of the city, we wanted to determine whether
the rats were potential pollinators of the plant in urban

Ecology. 2022;e3778. https://onlinelibrary.wiley.com/r/ecy © 2022 The Ecological Society of America. 1 of 5

https://doi.org/10.1002/ecy.3778
2 of 5 MATALLANA-PUERTO AND CARDOSO

F I G U R E 1 (a) Detail of an Acca sellowiana flower showing its rewarding petals and the separation between anthers and stigma. Floral
visitors include (b) Elaenia frantzii, (c) Mimus gilvus, and (d) Rattus norvegicus. (e) Illustration of respective R. norvegicus evidencing the
consumption of the petals while its head contacts the reproductive structures. Bird photos and illustration were provided by Johana F.
Leguizam
on Arias and Pedro Lorenzo, respectively.

areas. For this, we carried out observations on 22 A.
sellowiana individuals to investigate the frequency of
visits by birds and rats, also recording their behavior to
determine whether they touch reproductive structures
and thus potentially pollinate the plants (Appendix S1:
Methodology). To verify whether any other mammal had
been reported visiting A. sellowiana flowers, we also con-
ducted a literature survey recording the identity of its
known visitors around the world and their respective
habitats (i.e., in the wild, croplands, and urban areas)
(Appendix S1: Methodology).
During the observation time (60 h), we recorded three
species of visitors. Two of them were birds with one indi-
vidual of Elaenia frantzii (Figure 1b) and five of Mimus
gilvus (Figure 1c). We also observed that the nonnative
brown rat, Rattus norvegicus (Figure 1d,e), was the most
frequent visitor to the flowers, with 43 individual visits,
which accounted for 88% of the total number of visits by
any animal (Figure 2a). Both rats and birds consumed
the petals of the flowers without causing any kind of
damage to reproductive structures. By touching both
anthers and stigmas, they can potentially transport and
transfer pollen. While the visits of the birds were fast and
restricted to one or two plant individuals, rats moved
within and between more than three individuals feeding
on petals for several hours, indicating that they have the
potential to promote xenogamy and highlighting their
role as potential pollinators.
In our literature survey, we found 10 publications
reporting A. sellowiana floral visitors from 12 different areas
and eight different countries (Figure 2b). Ten areas were
characterized as croplands, and one was in a wild popula-
tion of A. sellowiana in Argentina and another was in an
urban area of southern Brazil. Considering the data of this
present study, we found a total of 64 visitor records
(Appendix S2: Table S1). The most common group was
birds, with 34 records (25 species), accounting for 53% of all
occurrences. In seven studies, birds were considered the
ECOLOGY 3 of 5

F I G U R E 2 (a) Visitation frequency of three floral visitor species of Acca sellowiana (chi-square goodness-of-fit test: χ2 = 65.80;
p < 0.001). Different letters show significant differences at 0.05 level (pairwise chi-square tests). (b) Network between floral visitors (color
circles) and reference source (squares) obtained from our literature review. Due to the different taxonomic refinements, visitors are shown as
species of birds and insects in general. The current record of the mammal Rattus norvegicus is also shown. The reference lists the authors,
year, country of publication, and the type of habitat in which the floral visitors were recorded (wild, croplands, or urban). Bird photos were
provided by Johana F. Leguizam
on Arias.

most likely pollinators, visiting flowers even outside the
continent of origin of the plant, in Australia, New Zealand,
Japan, and the United States. Next, we also found four
orders of insects, which comprised 45% of records. These
included Hymenoptera (ants and bees), Coleoptera, Diptera,
and Thysanoptera. Only three studies recognized that bees
may be potential pollinators. One of them (Hickel &
Ducroquet, 2000) estimated that self-incompatible plants
exposed to bee visitation had only 3% of the fruit set.
According to the authors, this occurred because bees had
contact with the stigma only occasionally when collecting
pollen and the frequency of their visits was low. Based on
our literature review, we found that no other study reported
mammals as visitors.
The consumption of petals by rodents can influence
whether bird pollinators are attracted to flowers
(Rodríguez-Rodríguez & Valido, 2011). However, we
believe that in our system, this has little effect on the
reproduction of the plant since the activity of bird polli-
nators in the study area is low. This probably is related to
the urban environment, where the number of birds is
usually reduced (Aronson et al. 2014). Nevertheless,
according to our observations, the potential pollination
by rats can function not only as supplementary but as the
main source of fruit set in urban populations of this
important cultivated plant. This highlights how pollina-
tion systems can change in the urban environment.
A few Myrtaceae species are reported to be polli-
nated by birds, bats, and marsupials (Beardsell
et al., 1993; Gressler et al., 2006), mostly in the Austra-
lian region (Beardsell et al., 1993; Gressler et al., 2006).
However, the vertebrate-pollinated Myrtaceae from
Australia offer nectar as a resource. In the Neotropics,
the vertebrate-pollinated Myrtaceae species A.
sellowiana and Myrrhinum atropurpureum provide
their petals as a resource (Gressler et al., 2006). Hereto-
fore, the reported pollinators were exclusively birds,
and our study represents the first case of potential pol-
lination by rats that use floral whorls as a resource in
this family.
Our case is different from the general aspects of sys-
tems involving rodent pollination, which mainly involve
flowers at the ground level, with rigid whorls, dull colors,
nocturnal anthesis, a strong scent, and with nectar as a
reward (Johnson et al., 2001). In contrast, A. sellowiana
flowers are found in tree canopies, with diurnal anthesis,
without nectar and odor, and with petals as a resource.
In addition to our study, petal-rewarding plants visited by
rodents had only been reported in Cymbidium serratum
(Orchidaceae) (Wang et al., 2008). In some other cases,
rodent visits are associated with the consumption or
damage of reproductive structures (Biccard &
Midgley, 2009; Rodríguez-Rodríguez & Valido, 2011). In
these systems, the authors suggest that these negative
4 of 5
effects may be related to access to nectar. In our case, we
observed no damage to reproductive structures, probably
because petals are the resource and they are distant from
stamens and pistils.
Rats are mainly nocturnal and occupy cryptic micro-
habitats in cities (Feng & Himsworth, 2014). Here we
show that R. norvegicus adjust their behavior to exploit
the unusual resource provided by A. sellowiana, foraging
in tree canopies and during the day when the flowers are
open and fertile. Thus, our observations of species that do
not share a coevolutionary history highlight the diversity
of potential new interactions that can be established in
modified habitats via ecological fitting (sensu
Janzen, 1985), particularly for two introduced species.
Although urban environments are complex habitats
that can harbor several pollinator groups, cases involving
nonflying mammals are uncommon (Maruyama
et al., 2021). Rats are common in cities, but they are usually
considered a problem for human health (Tamayo-Uria
et al., 2014). Although rats do indeed pose a hazard for
human health, our results suggest a potential ecological
benefit of these animals. Further studies are needed to
quantify the effects of rat visitation on the fruit production
of this economically important species. Our study highlights
how different nonnative species (A. sellowiana and R.
norvegicus) establish new and fascinating interactions in
transformed environments and can promote ecosystem
services.
A C K N O WL E D G M E N T S
We are grateful to Angela Vianch
a S
anchez for identify-
ing the rat, to Lina Peña Ramírez and Jeniffer Go
mez
Camargo for identifying the birds, to Johana F. Leg-
uizam
on Arias for providing pictures of the birds, and
Pedro Lorenzo for the illustration of the rat. We thank
Gibby Zobel, Pietro K. Maruyama, and Vinícius L. G.
Brito for their comments in the manuscript.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
DATA AVAILABILITY STATEMENT
Data (Cardoso, 2022) are available in Figshare at https://
doi.org/10.6084/m9.figshare.19617927.v1.
ORCID
Carlos A. Matallana-Puerto https://orcid.org/0000-
0001-8910-2684
João Cust
odio Fernandes Cardoso https://orcid.org/
0000-0002-0411-8159
R EF E RE N C E S
Aronson, M. F. J., F. A. La Sorte, C. H. Nilon, M. Katti, M. A.
Goddard, C. A. Lepczyk, P. S. Warren, et al. 2014. “A Global
MATALLANA-PUERTO AND CARDOSO
Analysis of the Impacts of Urbanization on Bird and Plant
Diversity Reveals Key Anthropogenic Drivers.” Proceedings of
the Royal Society B: Biological Sciences 281: 20133330.
Beardsell, D., S. Obrien, E. Williams, R. Knox, and D. Calder. 1993.
“Reproductive Biology of Australian Myrtaceae.” Australian
Journal of Botany 41: 511–26.
Biccard, A., and J. J. Midgley. 2009. “Rodent Pollination in Protea
Nana.” South African Journal of Botany 75: 720–5.
Cardoso, J. C. 2022. “Data of “Ratatouille of Flowers! Rats as Poten-
tial Pollinators of a Petal-Rewarding Plant in an Urban Area”.”
Figshare. Journal contribution. https://doi.org/10.6084/m9.
figshare.19617927.v1.
Conole, L. E. 2004. “Satin Bowerbird Ptilonorhynchus Violaceus
and Grey Currawong Strepera Versicolor Eating Feijoa Acca
Sellowiana Petals.” Australian Field Ornithology 21:121–4.
Ducroquet, J. P. H. J., and E. R. Hickel. 1997. “Birds as Pollinators
of Feijoa (Acca sellowiana Bera).” Acta Horticulturae 452:
37–40.
Feng, A. Y. T., and C. G. Himsworth. 2014. “The Secret Life of the
City Rat: A Review of the Ecology of Urban Norway and Black
Rats (Rattus norvegicus and Rattus rattus).” Urban Ecosystem
17: 149–62.
Fischer, G. 2003. Ecofisiología, crecimiento y desarrollo de la feijoa.
In: Cultivo Poscosecha y Exportaci
on de la Feijoa (Acca
sellowiana Berg), edited by G. Fischer, D. Miranda, G. Cay
on,
and M. Mazorra, 9–26. Bogot
a, Colombia: Produmedios.
Freitas, T. C., G. T. Beskow, A. B. D. Henzel, G. C. Gomes, L. P.
Sousa, and A. L. M. Goulart. 2020. “Aves Visitantes Florais de
Acca sellowiana (Berg) Burret (goiabeira-serrana) em um
sistema agroflorestal no sul do Rio Grande do Sul, Brasil.”
Cadernos de Agroecologia 15.
Goldingay, R. L., S. M. Carthew, and R. J. Whelan. 1991. “The
Importance of Non-Flying Mammals in Pollination.” Oikos 61:
79–87.
Gressler, E., M. A. Pizo, and L. P. C. Morellato. 2006. “Polinização e
dispersão de sementes em Myrtaceae do Brasil.” Revista
Brasileira de Botânica 29: 509–30.
Hickel, E. R., and J. P. J. Ducroquet. 2000. “Insect Pollination of
Feijoa, Feijoa sellowiana (Berg), in Santa Catarina.” Revista
Brasileira de Fruticultura 22: 96–101.
Janzen, D. H. 1985. “On ecological fitting.” Oikos 45: 308–10.
Johnson, S. D., A. Pauw, and J. Midgley. 2001. “Rodent Pollination
in the African Lily Massonia depressa (Hyacinthaceae).” Amer-
ican Journal of Botany 88: 1768–73.
Keller, H. A., and S. G. Tressens. 2007. “Presencia en Argentina de
dos especies de uso múltiple: Acca sellowiana (Myrtaceae) y
Casearia lasiophylla (Flacourtiaceae).” Darwin 45: 204–12.
Klein, A. M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter, S. A.
Cunningham, C. Kremen, and T. Tscharntke. 2007. “Impor-
tance of Pollinators in Changing Landscapes for World Crops.”
Proceedings of the Royal Society B: Biological Sciences 274:
303–13.
Kleizen, C., J. Midgley, and S. D. Johnson. 2008. “Pollination Sys-
tems of Colchicum (Colchicaceae) in Southern Africa: Evi-
dence for Rodent Pollination.” Annals of Botany 102:
747–55.
Maruyama, P. K., J. L. S. Silva, I. N. Gomes, C. Bosenbecker, O.
Cruz-Neto, W. Oliveira, J. C. F. Cardoso, A. B. Stewart, and
A. V. Lopes. 2021. “A Global Review of Urban Pollinators and
Implications for Maintaining Pollination Services in Tropical
Cities.” EcoEvoRxiv. https://doi.org/10.32942/osf.io/bpyvd.
ECOLOGY
Ollerton, J., R. Winfree, and S. Tarrant. 2011. “How Many
Flowering Plants Are Pollinated by Animals?” Oikos 120:
321–6.
Ollerton, J. 2017. “Pollinator Diversity: Distribution, Ecological
Function, and Conservation.” Annual Review of Ecology, Evolu-
tion, and Systematics 48: 353–76.
Quintero, O. 2003. Selecci
on de cultivares, manejo del cultivo y reg-
ulaci
on de cosechas de feijoa. In: Cultivo Poscosecha y
Exportaci
on de la Feijoa (Acca sellowiana Berg), edited by G.
Fischer, D. Miranda, G. Cay
on, and M. Mazorra, 49–71.
Bogot
a, Colombia: Produmedios.
Ramírez, F., and J. Kallarackal. 2017. “Feijoa [Acca sellowiana (O.
Berg) Burret] Pollination: A Review.” Scientia Horticulturae
226: 333–41.
Ratto, F., B. I. Simmons, R. Spake, V. Zamora-Gutierrez, M. A.
MacDonald, J. C. Merriman, C. J. Tremlett, G. M. Poppy, K. S.-
H. Peh, and L. V. Dicks. 2018. “Global Importance of Verte-
brate Pollinators for Plant Reproductive Success: A Meta-Anal-
ysis.” Frontiers in Ecology and the Environment 16: 82–90.
Regan, E. C., L. Santini, L. Ingwall-King, M. Hoffmann, C.
Rondinini, A. Symes, J. Taylor, and S. H. M. Butchart. 2015.
“Global Trends in the Status of Bird and Mammal Pollinators.”
Conservation Letters 8: 397–403.
Rodríguez, L. F., and L. T. Bermúdez. 1996. “Perfil y caracterizaci
on
de la comercializaci
on y consumo de Feijoa en Boyac
a.”
Agronomía Colombiana 13: 56–62.
Rodríguez-Rodríguez, M. C., and A. Valido. 2011. “Consequences of
Plant-Pollinator and Floral-Herbivore Interactions on the
Reproductive Success of the Canary Islands Endemic Can-
arina canariensis (Campanulaceae).” American Journal of Bot-
any 98: 1465–74.
View publication stats
5 of 5
Santos, E., M. Vera, Y. Mendoza, S. D. Ceti, D. Cabrera, and B.
Vignale. 2010. Polinizadores de Acca sellowiana (Berg) Burret –
Guayabo del País. In: 5º Encuentro Nacional sobre Frutas Nativas.
Salto. Ed. INIA, Serie de Actividad de Difusi

on Nº 602.
Sazima, I., and M. Sazima. 2007. Petiscos florais: pétalas de Acca
sellowiana (Myrtaceae) como fonte alimentar para aves em

area urbana no Sul do Brasil. Biota Neotropica 7:307–311.
Stewart, A. M., and J. L. Craig. 1989. “Factors Affecting Pollinator
Effectiveness in Feijoa sellowiana.” New Zealand Journal of
Crop and Horticultural Science 17:145–54.
Tamayo-Uria, I., J. Mateu, F. Escobar, and L. Mughini-Gras. 2014.
“Risk Factors and Spatial Distribution of Urban Rat Infesta-
tions.” Journal of Pest Science 87: 107–15.
Wang, Y., Y. Zhang, X. K. Ma, and L. Dong. 2008. “The Unique
Mouse Pollination in an Orchid Species.” Nature Precedings.
https://doi.org/10.1038/npre.2008.1824.1.
SU PP O R TI N G I N F O RMA TI O N
Additional supporting information can be found online
in the Supporting Information section at the end of this
article.
How to cite this article: Matallana-Puerto,
Carlos A., and João Cust
odio Fernandes Cardoso.
2022. “Ratatouille of Flowers! Rats as Potential
Pollinators of a Petal-Rewarding Plant in the
Urban Area.” Ecology e3778. https://doi.org/10.
1002/ecy.3778