Aquatic Hyphomycetes from streams on Madeira Island (Portugal)

Abstract Background Aquatic hyphomycetes are a phylogenetically heterogeneous group of fungi living preferentially in fast flowing, well-aerated forest streams. These fungi have worldwide distribution, but with the exception of Articulospora tetracladia, no aquatic hyphomycete taxon was previously recorded on Madeira Island. Aquatic hyphomycetes were sampled from 40 sites, distributed by 27 permanent streams in 2015, to provide the distribution of aquatic hyphomycetes in Madeira Island streams. New information In this study, a total of 21 species of aquatic hyphomycetes were recorded belonging to three classes of Ascomycota. All taxa are new records for Madeira Archipelago, except Articulospora tetracladia and four are reported for the first time in Macaronesian biogeographic region.


Introduction
Aquatic hyphomycetes, or Ingoldian fungi, are a phylogenetically heterogeneous group of fungi, composed mainly by the asexual stages of ascomycetes and basidiomycetes, living preferentially in fast flowing, well-aerated forest streams (Bärlocher 1992). Although aquatic fungi have been studied since the 1840s (Desmaziéres 1849), the knowledge of this fungal group is still scarce compared to their terrestrial counterparts. These fungi have worldwide distribution, but studies, so far, point to a higher species richness in temperate regions (Jones and Pang 2012, Duarte et al. 2016a, Seena et al. 2019. In fact, in temperate regions, they are the most important group of litter microbial decomposers in streams and rivers (Suberkropp and Klug 1974, Hieber and Gessner 2002, Gulis and Suberkropp 2003. Aquatic hyphomycetes play a fundamental role in the decomposition of plant litter of terrestrial origin, which is a key ecosystem process in forest streams that allows for the transfer of energy and nutrients to higher tropic levels, contributing to nutrient cycling (Wallace et al. 1997, Gessner et al. 2007, Gulis et al. 2019. Aquatic hyphomycetes colonise leaf litter soon after leaf immersion. They can promote litter mass loss directly by mineralising organic carbon and nutrients and by converting coarse into fine particulate organic matter (e.g. by the conidia production) Suberkropp 2003, Cornut et al. 2010) and indirectly by increasing litter palatability to shredders and facilitating physical fragmentation (Gulis et al. 2006, Graça andCressa 2010). Aquatic hyphomycetes can be particularly important on oceanic island streams, where macroinvertebrate detritivores can be scarce (Benstead et al. 2009, Raposeiro et al. 2014). In fact, fungal biomass, sporulation rates and litter decomposition by aquatic hyphomycetes in Atlantic islands was reported to be equivalent to those observed in temperate continental zones . Despite their importance, little is known about aquatic hyphomycetes in oceanic island systems (e.g. Ranzoni 1979).
Interest in Madeiran terrestrial fungi started almost two centuries ago with the work of Holl (1830) that recorded a dozen species belonging to different groups. During the 20 century, many mycological studies increased the number of records for Madeira Archipelago (North Atlantic), including numerous descriptions of species new to science (see Melo and Cardoso 2008 and references therein). According to Melo and Cardoso (2008), 743 fungal taxa were recorded for the Madeira Archipelago, with 99.3% occurring on Madeira Island. Despite their major relevance for the knowledge of Madeiran fungal biodiversity, these taxonomic studies focused on terrestrial ecosystems, whereas little is known about the aquatic habitat. The main objective of this paper is to provide the distribution of aquatic hyphomycetes in Madeira Island streams. th

Study area
Madeira Island is located 600 km off the Atlantic coast of North Africa (Fig. 1). It has an area of 742 km and a maximum altitude of 1861 m (Pico Ruivo). Lying in the subtropical region, Madeira's climate is influenced by winds from NE and the Canary Islands current. The Island has a mild oceanic climate, both in winter and summer with mild temperatures ranging from 15.9°C in February up to 22.3°C in August (average annual temperature of 18.7°C), relative humidity between 55 and 75% and annual rainfall between 500 and 1,000 mm (Santos et al. 2004).
Madeira Island comprises approximately 126 catchments and 200 streams (Marques 1994) ranging from 1st to 6th order. The radial drainage pattern of the watersheds is typical of oceanic islands as streams flow away from the island's mountainous central peaks (Hughes 2006). Madeira stream drainage networks are typically narrow and short with very steep, shallow channels often characterised by turbulent, torrential and seasonal flow. Substrates are predominantly coarse, comprising bedrock, boulders, cobbles and sand. Due to complex orography and the altitudinal span of the Island, the vegetation and land use are distributed along the altitudinal gradient. Forested areas (native laurel forest and commercial plantations) and less impacted areas occupy the higher reaches of most catchments, while agricultural and urban land uses characterise more accessible middle and lower lying areas. Other observed impacts include organic pollution, nutrient enrichment via diffuse pollution and physical disturbance (bank reinforcement or modification in the riparian corridor).
From the 21 species identified, none occurred in all 40 studied stream sites and only 8 taxa occurred in more than 50% of the stream sites: Articulospora tetracladia, Clavariopsis aquatica, Lemonniera aquatica, Lunulospora curvula, Tetrachaetum elegans, Tetracladium marchalianum, Tricladium chaetocladium and Triscelophorus monosporus, which were the most ubiquitous aquatic hyphomycetes in Madeira streams. Two taxa, Lemonniera sp. and Tetracladium furcatum, had a sporadic occurrence, being found at only one or two sampling sites. A maximum of 14 species was recorded in MAD15 and a minimum of one species in MAD13 and MAD20, with a mean richness of eight species per stream site. Higher altitude stream sites (> 800 m a.s.l.) in natural areas, such as MAD07, MAD08, MAD24 and MAD26, displayed higher taxa richness (11.0 ± 0.9, mean ± SE), compared with coastal (< 25 m a.s.l.) and urban stream sites, such as MAD13, MAD20, MAD32, MAD33, MAD37, MAD38, MAD39 and MAD40 (5.8 ± 1.2). All species, with the exception of Articulospora tetracladia reported by Seena et al. (2012), were new records for Madeira Archipelago and the following section provides brief notes on the records with information on their wider distribution patterns and habitat.

Discussion
Here we present the first study that explored the distribution of aquatic hyphomycetes in insular streams from Madeira Island. Twenty-one taxa are recorded for Madeira Island, which is lower than what is reported for the Azores archipelago (41 species; see , Balibrea et al. 2020). However, these numbers cannot be used to draw conclusions about aquatic hyphomycetes species richness in each archipelago since sampling has used different approaches and has been limited in both archipelagos: in Madeira, aquatic hyphomycetes were sampled on one occasion from water in a large number of streams spatially distributed to cover the entire island surface, while in the Azores, aquatic hyphomycetes have been sampled on multiple occasions from submerged litter in few streams in one of the nine islands (São Miguel) of the Archipelago. In this context, it is essential to increase the sampling effort for both archipelagos, as well as to survey multiple matrices (water, foam, different decomposing litter species and types) in order to find a greater diversity of aquatic hyphomycetes. To the best of our knowledge, no data of recorded species exist for the other Macaronesia archipelagos, such as Canary Islands and Cabo Verde Archipelago.
The aquatic hyphomycete assemblages of Madeira were composed mainly by ascomycetes with a cosmopolitan distribution (Duarte et al. 2016a, Seena et al. 2019 which are also known from other oceanic islands (Ranzoni 1979,Balibrea et al. 2020). In fact, other studies (Fenchel 1993, Finlay and Clarke 1999, Finlay 2002, Finlay and Fenchel 2004 suggested the high capacity of dispersal of microorganisms with few geographical barriers when compared to macroorganisms, such as freshwater macroinvertebrates (Hughes et al. 1998, Hughes and Malmqvist 2005, Raposeiro et al. 2012. While at the global scale, most of the aquatic hyphomycetes species have a cosmopolitan distribution (although some level of endemism was observed in some studies; see Duarte et al. 2016a, Seena et al. 2019, at a local scale, their assemblages are strongly influenced by environmental factors that dominate over the spatial processes (Barlocher and Graça 2002, Gulis and Suberkropp 2003, Rajashekhar and Kaveriappa 2003, Heino et al. 2004, Ferreira et al. 2006a, Cornut et al. 2012, Ferreira et al. 2016a, Duarte et al. 2017, which can explain the differences in the distribution of aquatic hyphomycetes species observed in Madeira streams. This is in line with the hypothesis of Baas-Becking (1934), which claims that "everything is everywhere", but microbial assemblages are controlled by environmental factors. However, we must have in mind that the actual knowledge on the global distribution of aquatic hyphomycetes is biased to certain geographical areas where the sampling efforts have been concentrated (Duarte et al. 2016a).
To better understand the complexity of these unique insular streams, further research on taxonomy, population dynamics, litter decomposition, sensitivity to environmental conditions, amongst others, need to be carried out. Additionally, replication and larger datasets are required to better understand insular aquatic hyphomycete communities and how they response to environmental changes.