Rediscovery after three decades of the freshwater sponge Metania kiliani on a terrestrial fern

Redescoberta após três décadas da esponja de água doce Metania kiliani sobre uma samambaia terrestre

ABSTRACT

This study presents the second record of Metania kiliani (Porifera: Metaniidae) three decades after its description in 1992. The sponge was found on a herbarium specimen of the terrestrial fern Actinostachys pennula (Schizaeaceae), which is typically known to be absent from flooded environments. As sponges need at least some weeks to establish themselves on a support, this first record of a freshwater sponge on this fern suggests that A. pennula can withstand prolonged submergence. This is the first record of M. kiliani for the state of Roraima, Brazil.

KEYWORDS:
Actinostachys; Amazonia; Metaniidae; Porifera; Schizaeaceae; white-sand vegetation

RESUMO

Este estudo apresenta o segundo registro de Metania kiliani (Porifera: Metaniidae) três décadas após sua descrição em 1992. A esponja foi encontrada sobre um espécime de herbário da samambaia terrestre Actinostachys pennula (Schizaeaceae), tipicamente conhecida por estar ausente em ambientes alagados. Como as esponjas precisam de pelo menos algumas semanas para se estabelecerem sobre um suporte, este primeiro registro de uma esponja de água doce nesta samambaia sugere que A. pennula pode suportar submersão prolongada. Este é o primeiro registro de M. kiliani para o estado de Roraima, Brasil.

PALAVRAS-CHAVE:
Actinostachys; Amazônia; Metaniidae; Porifera; Schizaeaceae; vegetação de areia branca

Freshwater sponges are sessile filtering organisms that need support to grow, such as rocks, trunks, branches, leaves, or roots of submerged vegetation, and can grow on different types of substrates (Manconi and Pronzato 2002). They can be found in permanent or seasonal freshwater environments. As sessile filtering organisms, freshwater sponges tend to settle on substrates far from the bottom sediments of the water body, as a high amount of suspended particles can clog their pores. Usually, they prefer pristine aquatic environments, which makes them good bioindicators (Volkmer-Ribeiro and Parolin 2010). Worldwide, there are 9,602 known species of benthic sponges (de Voogd et al. 2023). The monophyletic order Spongillida Manconi & Pronzato, 2002 is composed exclusively of about 250 freshwater species (Morrow and Cárdenas 2015) distributed in continental aquatic ecosystems (Pinheiro and Calheira 2020). The catalog of Brazilian Porifera lists 61 species of freshwater sponges (Pinheiro et al. 2025).

In areas subject to periodic flooding, freshwater sponges can use trees as support (Manconi and Pronzato 2016). In Amazonia, there are abundant floodplain forests that may be flooded by blackwater or whitewater rivers (known as igapó and várzea, respectively) (Prance 1979) as well as lower white-sand vegetation (known as campinas or campinaranas) (Adeney et al. 2016). These environments are subject to strong seasonal cycles, variable water table levels, and different levels of hydromorphism, resulting in different plant communities and phytophysiognomies (Prance 1979; Adeney et al. 2016). In such variable environments, some species of freshwater sponges are subject to seasonal stages of growth and budding through gemmules. Gemmules are cryptobiotic asexually formed resistant structures containing totipotent cells covered by collagen and silica that can resist desiccation and anoxia. They can regenerate the entire animal during the next flood season (Manconi and Pronzato 2016). Because of gemmules, freshwater sponges present a random distribution and a wide geographic scale (Pronzato and Marconi 1994).

Ferns are a monophyletic group, sister to seed plants (Pryer et al. 2001). Their photosynthetic organs, the fronds, are also responsible for vegetative reproduction, spore dispersal, and other functions (Corvez et al. 2012). They exhibit an extensive spectrum of antagonistic and mutualistic relationships with fungi and animals (Mehltreter et al. 2010). Most interactions between ferns and other organisms are neutral (e.g., Moran et al. 2003) or mutualistic (e.g., Gómez 1974; Almeida 2018). There is no known interaction between poriferans and ferns.

Schizaeaceae is a fern family with two genera, Actinostachys Wall. with 15 species, and Schizaea Sm. with about 20 species (Kessler and Smith 2017). Actinostachys is widely distributed in tropical regions (Kessler and Smith 2017). In the Amazon region, A. pennula (Sw.) Hook. is commonly found in savannas, terra firme forests, coastal vegetation, riparian forests, and campinaranas (Santiago and Almeida 2023). While most ferns thrive in wet environments, as they need water for reproduction (Page 2002), only a few can withstand submersion (Walker and Sharpe 2010). Notably, there is no record in the literature of this tolerance in A. pennula.

Here we report the first record of the freshwater sponge, Metania kilianiVolkmer-Ribeiro & Costa, 1992 (Metaniidae) growing on a fern, Actinostachys pennula (Schizaeaceae), based on a herbarium record. The presence of an M. kiliani specimen was noted on an A. pennula specimen deposited in the herbarium at Universidade Federal de Pernambuco - UFPE (UFP89884) (acronym according to Thiers 2023) (Figure 1). The A. pennula material was composed of seven fronds of about 28 cm in length (Figure 1a). Metania kiliani was observed growing on one of the fronds, approximately 6 cm in size, at 9 cm above ground level (Figure 1a). The sponge specimen was detached and deposited in the Porifera collection at UFPE (UFPEPOR2999).

Figure 1
A - Specimen of the sponge Metania kiliani (UFPEPOR2999) growing on the fronds of the fern Actinostachys pennula (UFP89884); B - Metania kiliani in detail; C - Gemmules of M. kiliani in detail. Scale bars = 1 cm (B); 5 cm (A,C).

The material was collected in Caracaraí, Roraima state, Brazil (0º54’01”S, 62º16’48”W) (Figure 2), on February 6^th, 2018, in a seasonally flooded campinarana area, as indicated on the specimen label. The climate in the collection area type AF (Köppen classification), with average annual temperature >26°C and rainfall of 2500-2800 mm (Alvarez et al. 2013). The soil is dystrophic Tb gleysol (IBGE 2006), and the area of the Rio Branco-Rio Negro Domain in Holocene alluvial deposits (IBGE 2005).

Figure 2
Distribution of Metania kiliani in Amazonas and Roraima states (Brazil) Black circle = type locality; black star = new record presented here.

The fern and the sponge were identified with the aid of specialized literature (Santiago and Almeida 2023; Volkmer-Ribeiro and Costa 1992). Spicule slides and preparations of spicules for scanning electron microscopy (SEM) were made following Hajdu et al. (2011). Spicules were viewed on Tabletop SEM Hitachi TM4000PLUSII at the Zoology Department at UFPE.

Description: The sponge formed small, thin, fragile crusts with a reticulated skeleton and brown color. Gemmules aligned side by side near the fronds (Figure 1b-c). Spicules: Alpha-megascleres (Figure 3a) smooth, short, stout, straight or slightly curved oxea with abruptly pointed extremities. Beta-megascleres (Figure 3b) short, stout, spined, straight to curved oxea with abruptly pointed extremities. Spines more concentrated in the middle part of the spicules. Microscleres minute anisochelaes (Figure 3c-e). Microscleres acanthomicroxea not present. In the original description, Volkmer-Ribeiro and Costa (1992) mentioned that they are rare and restricted to the pinacoderm. The present material was collected dry and probably lost part of the pinacoderm. Gemmoscleres (Figure 3f-g) short, stout, boletiform. Shafts straight or slightly curved with a typical collar of spines under the lower rotule or for one or two spines close to the upper rotule. Lower rotule small, thick, slightly umbonate, conspicuously polygonal, and with reduced margins. Upper rotule usually well-formed and bearing at its border six large, regular, incurved hooks. Gemmules abundant (Figures 1b-c; 3h-j), free, large, cocoon-shaped, forming a basal layer one gemmule thick. Micropile long but always sunken in a very thick pneumatic coat. First layer of gemmoscleres radially arranged around the inner coat with the lower rotules setting in this coat and the upper ones embedded in the pneumatic coat. Some upper rotules protruding from the outer gemmular coat (Figure 3i-j). The sponge was found in the budding phase.

Figure 3
SEM images of the spicules of Metania kiliani (UFPEPOR2999). A - Alpha-megasclere; B - Beta-megascleres; C-E - Anisochelaes gemoscleres; F-G - Boletiform gemmocleres; H-J - Gemmule. Scale bar = 10 μm (A-B); 5 μm (C-G); 100 μm (H); 10 μm (I); 20 μm (J).

Until now, M. kiliani had only been recorded in its original description for the Cuieiras River in the state of Amazonas (Brazil), encrusted “on leaves or around twigs reached by flood waters”, as stated in the original description by Volkmer-Ribeiro and Costa (1992). Therefore, this is the second record of the species and the first for the state of Roraima (Figure 2). The lack of previous records of M. kiliani on this or another fern may indicate that A. pennula was only a random support for the sponge. One association is known of an Amazonian moss, Fissidens brachypus Mitt. (Fissidentaceae) that uses a freshwater sponge of the genus Metania as a growth substrate when the water level is low (Buck and Pursell 1980).

The fronds of Actinostachys are peculiar, being undivided, narrow, linear, axis-like, photosynthetic, and with stomata arranged in two lines along its length (Salino et al. 2023), with sporangia at the apex (Figure 1). It occurs preferentially in sandy or rocky soils (Takeuchi 1960). There was no published record of this species being able to withstand flooding, although field observations show Schizaeaceae growing in periodically flooded areas in the states of Amazonas, Pará, and Roraima (T.E. Almeida, pers. comm.). In campinaranas of central Amazonia, A. pennula was one of the most abundant species within the shrubby group (open savannah), a functional group in which there are flood-tolerant species (Nogueira 2014). Few studies have examined morphophysiological adaptations of ferns to flooding in Brazil, with a conspicuous gap, particularly in the Amazon, where flooded areas are common. As the sponge needs some weeks to establish itself on the substrate (Calheira et al. 2019), the presence of M. kiliani indicates that A. pennula has the potential to survive for a long period submerged, although it is not known whether the fronds are long-lived and can withstand more than one flooding season.

The use of plants as growth support by sponges is common in Amazonian flooded areas, where it is usually possible to observe sponge remnants on trees after the water levels drop (Volkmer-Ribeiro and Parolin 2010). Sponges have even been used as indicators of the water level during the flood season (Keel and Prance 1979). However, it should be noted that sponges are generally found on trees that occur in floodplain areas and are physiologically adapted to withstand the flooding period (Prance 1979). In this context, it is important to study the life cycle and phenology of ferns in seasonal climates to understand their responses to abiotic factors such as temperature and rainfall (Sharpe and Mehltreter 2010). Climatic seasonality can influence the phenological patterns of ferns, as well as their fertility and growth patterns (Mehltreter and Palacios-Rios 2003; Sharpe and Mehltreter 2010), while some species are more resilient to seasonality (Muller and Schmitt 2019). Future studies should address the morphophysiological adaptations of ferns like A. pennula to flooding, as well as the conditions that facilitate sponge colonization, to improve our understanding of the biology of these species.

ACKNOWLEDGMENTS

We thank Conselho Nacional de Desenvolvimento Científico for the grants awarded to TEA (proc. # 317091/2021-2) and UP (proc. # 310914/2021-3). We thank the editors and two anonymous reviewers for their contributions. The Advanced Laboratory of Microscopy and Image, Nucleus for Prospecting and Management of Biodiversity in the Northeast-NPGBio at Universidade Federal de Pernambuco (LAMI-UFPE); the Zoology Museum, Department of Zoology at UFPE; and Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco (proc. # APQ-0522-2.04/19).

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• CITE AS:
  Sousa, C.V.M.; Lima, K.S.; Pinheiro, U.; Almeida, T.E. 2025. Rediscovery after three decades of the freshwater sponge Metania kiliani on a terrestrial fern. Acta Amazonica 55: e55bc23398.

Data availability

The data that support the findings of this study were published in this article.

Edited by

• ASSOCIATE EDITOR:
  Bruno Spacek Godoy

Data availability

Data citations

de Voogd, N.J.; Alvarez, B.; Boury-Esnault, N.; Carballo, J.L.; Cárdenas, P.; Díaz, M.-C.; et al 2023. World Porifera Database. ( (https://www.marinespecies.org/porifera ). Accessed on 04 Apr 2023.

Publication Dates

• Publication in this collection
  26 May 2025
• Date of issue
  2025

History

• Received
  22 Nov 2023
• Accepted
  03 Dec 2024