Ant fauna associated with Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae) fern galls

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

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.

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, 2003)	2	16.67	29.5±14.8	59	14.79	Rainy
Crematogaster sericea Forel, 1912	Native (Longino, 2003)	1	8.33	4	4	4	Dry
Camponotus crassus Mayr, 1862	Native (Fernández & Sendoya, 2004)	3	25.0	14.6±6.7	34	8.52	Dry and rainy
Procryptocerus sampaioi Forel, 1912	Native (Baccaro et al., 2015)	3	25.0	8.6±6.7	8.6±6.7	6.52	Dry and rainy
Tapinoma atriceps Emery, 1888	Native (Shattuck, 1994)	2	16.67	67.5±88.4	135	33.83	Dry and rainy
Wasmannia auropunctata (Roger, 1863)	Native (Longino and Fernández, 2007)	1	8.33	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.

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.

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Publication Dates

• Publication in this collection
  13 June 2019
• Date of issue
  Apr-Jun 2019

History

• Received
  18 Sept 2018
• Accepted
  26 Feb 2019