Journal Information
Vol. 63. Issue 2.
Pages 101-103 (April - June 2019)
Share
Share
Download PDF
More article options
Visits
...
Vol. 63. Issue 2.
Pages 101-103 (April - June 2019)
Short Communication
DOI: 10.1016/j.rbe.2019.02.004
Open Access
Ant fauna associated with Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae) fern galls
Visits
...
Marcelo Guerra Santosa,
Corresponding author
marceloguerrasantos@gmail.com

Corresponding author.
, Gabriela Fraga Portoa, Isabella Rodrigues Lancellottia, Rodrigo M. Feitosab
a Universidade do Estado do Rio de Janeiro, Departamento de Ciências Faculdade de Formação de Professores, Núcleo de Pesquisa e Ensino de Ciências, São Gonçalo, Rio de Janeiro, RJ, Brazil
b Universidade Federal do Paraná, Departamento de Zoologia, Laboratório de Sistemática e Biologia de Formigas, Curitiba, PR, Brazil
Article information
Abstract
Full Text
Bibliography
Download PDF
Statistics
Figures (1)
Tables (1)
Table 1. Ants recorded in senescent stem galls of Microgramma squamulosa (Kaulf.) de la Sota. Number of galls with ants (n=12). Number of ants (n=399).
Abstract

Galls are neoformed plant structures created by cell hyperplasia and hypertrophy induced by a number of organisms, especially insects. After adult insects hatch, senescent galls may remain on the host plant and be occupied by a succession of fauna, the most important and dominant being ants. This study aimed at characterizing the ant fauna successor of stem galls induced by microlepidoptera in Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae). Four collections were carried out in the municipality of Nova Friburgo, Rio de Janeiro state, Brazil. The galls were packed in plastic bags and taken to the laboratory. Ants were euthanized and conserved in 70° GL alcohol and later identified. A total of 49 stem galls were collected and analyzed, 15 containing microlepidoptera galler larvae, one a parasitoid wasp and 33 without the microlepidoptera or parasitoid (67%). Twelve of these galls (39%) contained ants. Six ant species were recorded (Camponotus crassus, Crematogaster curvispinosa, Crematogaster sericea, Procryptocerus sampaioi, Tapinoma atriceps, and Wasmannia auropunctata), all native to Brazil. Ant occupation in M. squamulosa seems to be associated with senescent galls due to hatching of the galler insect, which leaves a hole that allows ants to colonize it, in other words, an opportunistic domatia. Senescent galls resulting from the death of galler insects do not seem to facilitate ant occupation.

Keywords:
Ecosystem engineers
Fern–insect interactions
Myrmecophily
Pteridophytes
Full Text

Galls are neoformed plant structures created by cell hyperplasia and hypertrophy. They can be induced by organisms such as fungi, bacteria, nematodes, mites and insects; however, the last two stand out for the gall diversity they induce in plants (Mani, 1964; Raman, 2007; Shorthouse et al., 2005). Inducers establish a parasitic relationship with the host plant, manipulating its metabolism (Mani, 1964; Raman, 2007).

Galler insects are among the most specialized and sophisticated herbivores, considered ecosystem engineers, due to their ability to structurally alter leaves, stems, roots, flowers or fruits and form new habitats (Jones et al., 1994; Wright and Jones, 2006; Cornelissen et al., 2016). Insect galls are induced by oviposition and/or development of their larvae in plant tissues (Shorthouse et al., 2005). After adult insects hatch, senescent galls may remain on the host plant and be occupied by a succession of fauna, the most important and dominant being ants (Mani, 1964; Almeida et al., 2014). Senescent galls provide shelter and a nesting site for many ant species, mainly arboreal ants (Santos et al., 2017; Almeida et al., 2014). However, in the galler-fern-ant system, the importance of ants to the gall/plant remains unclear.

In addition to shelter, some galls are a food source for many ant species. Moreover, certain galls induced by Eriophyidae, Homoptera, Hymenoptera and Diptera may produce honeydew, which attracts flying insects and ants (Mani, 1964; Washburn, 1984).

Because ferns do not have flowers, most researchers have long ignored the potential of fern-animal interactions (Watkins Jr. et al., 2008). However, these interactions may occur via herbivory (Mehltreter, 2010), with the presence of domatia (Gómez, 1974), leaf nectaries (Koptur et al., 1982), crypticity (Santos and Wolff, 2015) and galls (Santos et al., 2019).

Although they are more frequent in spermatophytes, galls can also be found in ferns and lycophytes (Santos et al., 2019). In Brazil, galls have been recorded on 16 fern species induced by mites (Eriophyidae) and insects of the orders Lepidoptera, Thysanoptera, Hemiptera and Diptera, the last being the most frequent galler represented by the Cecidomyiidae family (Santos and Maia, 2018).

Galls have been recorded in three Microgramma C. Presl (Polypodiaceae) species, M. squamulosa (Kaulf.) de la Sota and M. vacciniifolia (Langsd. & Fisch.) Copel. in Brazil (Santos and Maia, 2018), and M. percussa (Cav.) de la Sota in Costa Rica (Santos et al., 2019). Moreover, several species of this genus of fern contain domatia (Mehltreter, 2010).

Two gall morphotypes were recorded in Microgramma squamulosa, a neotropical epiphyte fern (Rocha et al., 2014). One is a stem gall (Fig. 1A) induced by Tortrimosaica polypodivora Brown & Baixeras, 2004 (Tortricidae: Lepidoptera) (Kraus et al., 1993; Brown et al., 2004), and the other a conical leaf gall induced by a yet-to-be-identified Cecidomyiidae (Diptera) (Santos and Maia, 2018). Both morphotypes occur in the states of Rio de Janeiro and São Paulo, Brazil (Santos and Maia, 2018). Earlier fieldwork found ants occupying senescent galls of M. squamulosa (Fig. 1D). As such, this short communication aims at characterizing the ant fauna successor of stem galls induced by Tortrimosaica polypodivora in M. squamulosa. The galls were collected in a forest area of the Nova Friburgo Country Club (22°17′31.6″S 42°32′25.1″W) and Praça do Suspiro (Suspiro Square) (22°16′45.8″S 42°32′08.9″W), both located in the municipality of Nova Friburgo, Rio de Janeiro state, Brazil. Collections were carried out in the dry (April 2016 and June 2017) and rainy seasons (October 2017 and February 2018), according to Barbieri's classification (2005) for the Brazilian Southeast region.

Fig. 1.

(A) Stem gall on Microgramma squamulosa (arrow); (B) Ecdyse of the microlepidoptera galler that emerged from the gall (arrow); (C) hole left by the exiting galler (arrow); (D) sectioned gall exhibiting ants living inside.

(0.63MB).

We performed an active search of trees at the two collection sites and all galls found were packed in plastic bags and sorted in the laboratory. All biological voucher material was deposited in the herbarium of the Faculdade de Formação de Professores da Universidade do Estado do Rio de Janeiro (RFFP) and the Padre Jesus Santiago Moure Entomological Collection, Universidade Federal do Paraná, Department of Zoology (DZUP).

The galls were sectioned in the laboratory and all ants euthanized and fixed in 70° GL alcohol. They were identified by Dr. Rodrigo M. Feitosa, in the Laboratory of Systematics and Ant Biology at Universidade Federal do Paraná.

A total of 49 stem galls from M. squamulosa were collected and analyzed, 15 containing microlepidoptera galler larvae, one a parasitoid wasp and 33 without the microlepidoptera or parasitoid (67%). Twelve of these galls (36%) contained ants and twenty-one were empty.

Six ant species, belonging to five genera were recorded (Crematogaster, Camponotus, Procryptocerus, Tapinoma and Wasmannia), all native to Brazil (Table 1). Except for Crematogaster sericea, all the ant species established nests inside galls, with both immature and sexual individuals present, indicating they are being used by colonies for shelter. Furthermore, all ants that occupied galls are arboreal, which was expected because the galls were found in an epiphytic fern (M. squamulosa). In relation to food habits, all the ant species observed here can be considered generalists (Baccaro et al., 2015).

Table 1.

Ants recorded in senescent stem galls of Microgramma squamulosa (Kaulf.) de la Sota. Number of galls with ants (n=12). Number of ants (n=399).

Species  Origin  Occurrence (No. of galls)  Absolute frequency (%)  Number of ants per gall  Absolute density  Relative density (%)  Season 
Crematogaster curvispinosa Mayr, 1862  Native (Longino, 200316.67  29.5±14.8  59  14.79  Rainy 
Crematogaster sericea Forel, 1912  Native (Longino, 20038.33  Dry 
Camponotus crassus Mayr, 1862  Native (Fernández & Sendoya, 200425.0  14.6±6.7  34  8.52  Dry and rainy 
Procryptocerus sampaioi Forel, 1912  Native (Baccaro et al., 201525.0  8.6±6.7  8.6±6.7  6.52  Dry and rainy 
Tapinoma atriceps Emery, 1888  Native (Shattuck, 199416.67  67.5±88.4  135  33.83  Dry and rainy 
Wasmannia auropunctata (Roger, 1863)  Native (Longino and Fernández, 20078.33  141  141  35.34  Dry 

The genera Camponotus and Crematogaster are among the most frequent gall successors in angiosperm galls (Mani, 1964) and inhabitants of Microgramma spp. (Gómez, 1974) and Lecanopteris spp. domatia (Gay, 1993), both genera belonging to the family Polypodiaceae.

The species with the highest frequency in galls were Camponotus crassus and Procryptocerus sampaioi, occurring in three galls each, and those with the greatest density were Tapinoma atriceps and Wasmannia auropunctata (Table 1). Crematogaster curvispinosa was only recorded in the rainy season, C. sericea and W. auropunctata only in the dry season, and C. crassus, P. sampaioi and T. atriceps were found in both seasons (Table 1).

According to Mehltreter, 2010, interactions between ferns and ants can be neutral or mutualistic. The presence of domatia in epiphytic ferns of the genus Microgramma, subgenus Solanopteris (Gómez, 1974; Lellinger, 1977), as well as in Lecanopteris (Gay, 1993), may establish a mutualistic relation with a number of ant species. However, in some situations, ants can be opportunists and inhabit organ cavities (primarily stems and petioles) of ferns produced by the action of herbivores, which Mehltreter et al. (2003) referred to as opportunistic domatia.

The possible nutritional benefits for plants promoted by these ants, especially nitrogen, remains to be assessed. For exemple, in the tissues of an epiphyte fern [Antrophyum lanceolatum (L.) Kaulf. – Pteridaceae], Watkins Jr. et al. (2008) found high levels of nitrogen from waste produced by the nests of ants associated with this plant. These authors suggest that animals may provide substantial nutritional benefits to plants with little or no investment, not requiring specialized structures such as domatia or leaf nectaries. Thus, the hypothesis that the nests of gall-dwelling ants supply nutritional support to the epiphyte fern M. squamulosa has yet to be tested.

In M. squamulosa, ant occupation seems to be associated with senescent galls caused by galler insect hatching (Fig. 1B), which leaves a hole (Fig. 1C) that allows ants to enter and colonize it, in other words, an opportunistic domatia (sensu Mehltreter et al., 2003). Senescent galls due to death of galler insects seem not to facilitate this occupation by ants.

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgements

The authors would like to thank The National Council for Scientific and Technological Development (CNPq), Carlos Chagas Filho Research Support Foundation of Rio de Janeiro state (FAPERJ), and Incentive Program for Scientific, Technical and Artistic Production of Rio de Janeiro State University (PROCIENCIA-UERJ) for funding. We are also grateful to Anderson dos Santos Portugal, Arthur Flores Ribeiro and Mariana Fernandes da Rocha from the UERJ Biodiversity Teaching and Research Laboratory for help in data collection.

References
[Almeida et al., 2014]
M.F.B. Almeida, L.R. Santos, M.A.A. Carneiro.
Senescent stem-galls in trees of Eremanthus erythropappus as a resource for arboreal ants.
Rev. Bras. entomol., 58 (2014), pp. 265-272
[Baccaro et al., 2015]
F.B. Baccaro, R.M. Feitosa, F. Fernandez, I.O. Fernandes, T.J. Izzo, J.L.P. Souza, R. Solar.
Guia para os gêneros de formigas do Brasil.
Editora INPA Manaus, (2015),
[Barbieri, 2005]
P.R.B. Barbieri.
Um estudo sobre as estações seca e chuvosa nas regiões Sul e Sudeste do Brasil e sua associação com a circulação atmosférica na América do Sul.
Instituto Nacional de Pesquisas Espaciais, São José dos Campos, Brazil, (2005),
[Brown et al., 2004]
J.W. Brown, J. Baixeras, J.A. Solorzano-Filho, J.E. Kraus.
Description and life history of an unusual fern-feeding tortricid moth (Lepidoptera: Tortricidae) from Brazil.
Ann. Entomol. Soc. Am., 97 (2004), pp. 865-871
[Cornelissen et al., 2016]
T. Cornelissen, F. Cintra, J.C. Santos.
Shelter-building insects and their role as ecosystem engineers.
Neotrop. Entomol., 45 (2016), pp. 1-12
[Fernández and Sendoya, 2004]
F. Fernández, S. Sendoya.
Synonymic list of Neotropical ants (Hymenoptera: Formicidae).
Biota Colombiana, 5 (2004), pp. 3-105
[Gay, 1993]
H. Gay.
Rhizome structure and evolution in the ant-associated epiphytic fern Lecanopteris Reinw (Polypodiaceae).
Bot. J. Linn. Soc., 113 (1993), pp. 135-160
[Gómez, 1974]
L.D. Gómez.
Biology of the potato-fern Solanopteris brunei.
Brenesia, 4 (1974), pp. 37-61
[Jones et al., 1994]
C.G. Jones, J.H. Lawton, M. Shachak.
Organisms as ecosystem engineers.
Oikos, 69 (1994), pp. 373-386
[Koptur et al., 1982]
S. Koptur, A.R. Smith, I. Baker.
Nectaries in some Neotropical species of Polypodium (Polypodiaceae): preliminary observations and analyses.
Biotropica, 14 (1982), pp. 108-113
[Kraus et al., 1993]
J.E. Kraus, G. Montenegro, A.J. Kim.
Morphological studies on entomogenous stem galls of Microgramma squamulosa (Kauf.) Sota (Polypodiaceae).
Am. Fern. J., 83 (1993), pp. 120-128
[Lellinger, 1977]
D.B. Lellinger.
Nomenclatural notes on some ferns of Costa Rica Panama, and Colombia.
Am. Fern. J., 67 (1977), pp. 58-60
[Longino, 2003]
J.T. Longino.
The Crematogaster (Hymenoptera, Formicidae Myrmicinae) of Costa Rica.
Zootaxa, 151 (2003), pp. 1-150
[Longino and Fernández, 2007]
J.T. Longino, F. Fernández.
Taxonomic review of the genus Wasmannia.
pp. 271-289
[Mani, 1964]
M.S. Mani.
Ecology of Plant Galls.
Springer-Science, (1964),
[Mehltreter, 2010]
K. Mehltreter.
Interactions of ferns with fungi and animals.
Fern Ecology, pp. 220-254
[Mehltreter et al., 2003]
K. Mehltreter, P. Rojas, M. Palacios-Rios.
Moth larvae-damaged giant leather-fern Acrostichum danaeifolium as host for secondary colonization by ants.
Am. Fern. J., 93 (2003), pp. 49-55
[Raman, 2007]
A. Raman.
Insect-induced plant galls of India: unresolved questions.
Curr. Sci., 92 (2007), pp. 748-757
[Rocha et al., 2014]
L.D. Rocha, G.M. Costa, G. Gehlen, A. Droste, J.L. Schmitt.
Morphometric differences of Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae) leaves in environments with distinct atmospheric air quality.
An. Acad. Bras. Ciênc., 86 (2014), pp. 1137-1146
[Santos et al., 2017]
L.R. Santos, R.M. Feitosa, M.A.A. Carneiro.
The role of senescent stem-galls over arboreal ant communities structure in Eremanthus erythropappus (DC) MacLeish (Asteraceae) trees.
Sociobiology, 64 (2017), pp. 7-13
[Santos and Maia, 2018]
M.G. Santos, V.C. Maia.
A synopsis of fern galls in Brazil.
Biota Neotrop., 18 (2018), pp. e20180513
[Santos et al., 2019]
M.G. Santos, P. Hanson, V.C. Maia, K. Mehltreter.
A review of galls on ferns and lycophytes.
Environ. Entomol., 48 (2019), pp. 53-60
[Santos and Wolff, 2015]
M.G. Santos, V.R.S. Wolff.
Two species of armored scale insects (Hemiptera: Diaspididae) associated with sori of ferns.
EntomoBrasilis, 8 (2015), pp. 232-234
[Shattuck, 1994]
S.O. Shattuck.
Taxonomic Catalog of the Ant Subfamilies Aneuretinae and Dolichoderinae (Hymenoptera: Formicidae).
University of California Press, (1994),
[Shorthouse et al., 2005]
J.D. Shorthouse, D. Wool, A. Raman.
Gall-inducing insects – Nature's most sophisticated herbivores.
Basic Appl Ecol., 6 (2005), pp. 407-411
[Washburn, 1984]
J.O. Washburn.
Mutualism between a cynipid gall wasp and ants.
Ecology, 65 (1984), pp. 654-656
[Watkins et al., 2008]
J.E. Watkins Jr., C.L. Cardelús, M.C. Mack.
Ants mediate nitrogen relations of an epiphytic fern.
New Phytolog., 180 (2008), pp. 5-8
[Wright and Jones, 2006]
J.P. Wright, C.G. Jones.
The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges.
BioScience, 56 (2006), pp. 203-209
Idiomas
Revista Brasileira de Entomologia

Subscribe to our newsletter

Article options
Tools
en pt
Cookies policy Política de cookies
To improve our services and products, we use "cookies" (own or third parties authorized) to show advertising related to client preferences through the analyses of navigation customer behavior. Continuing navigation will be considered as acceptance of this use. You can change the settings or obtain more information by clicking here. Utilizamos cookies próprios e de terceiros para melhorar nossos serviços e mostrar publicidade relacionada às suas preferências, analisando seus hábitos de navegação. Se continuar a navegar, consideramos que aceita o seu uso. Você pode alterar a configuração ou obter mais informações aqui.