Abundance and seasonal growth of epiphytic ferns at three sites along a rainfall gradient in Western Europe

Highlights

• Epiphytic Polypodium were studied at three sites along a rainfall gradient

• The frequency of epiphytes strongly increased with precipitation

• Growth, mortality and reproduction were highly seasonal at all sites

• Growth patterns over two years did not explain the site differences in abundance

Abstract

Vascular epiphytes in temperate zones are allegedly rare due to climatic constraints, such as drought and freezing temperatures during winter. Here, we investigate how abundance and seasonal growth of epiphytic polypod ferns in Western Europe are influenced by annual rainfall and temperature. We recorded abundances and growth of epiphytic polypod ferns over two years at three sites along a rainfall gradient from Southwest Ireland to Northwest Germany, spanning a two-fold difference in annual rainfall. We also investigated plant maturation and recorded key climate characteristics (rainfall and temperature). Abundance of epiphytic polypod ferns strongly decreased from the wetter end of the rainfall gradient in Ireland towards the drier end in Germany. Yet, frond turnover was equally high at all study sites during summer months, and equally low during winter. Plants showed only little to no expansive growth during the study period, except for the study site in France in the middle of the gradient, where the total number of fronds strongly increased. Similarly, we found an increase in the proportion of spore-bearing fronds at the French study site, whereas there was hardly any change between years at the other two sites. The observed growth patterns are inconsistent with the current differences in abundance of epiphytic ferns. We suggest that these differences are due to poor germination of spores under drier conditions and that small differences in annual growth have contributed to the current abundances over an extended time period. Surprisingly, seasonal frond productivity appeared to be unaffected by the amount of annual rainfall and average temperatures, although it seems likely that these factors do play a role during gametophyte establishment.

Introduction

Epiphytes are defined as plants that grow non-parasitically on other plants, usually trees. Since the equivalent of soil, i.e. accumulations of organic material, is typically rare in this habitat, poor water availability is assumed to be the main limiting abiotic factor for epiphyte growth (Zotz and Hietz, 2001).

Globally, vascular epiphyte species richness and abundance show a strong bias towards tropical regions, which is also reflected in the focus of ecological studies on tropical epiphytes, but vascular epiphytes also occur in temperate regions in both hemispheres. While orchids and other angiosperm taxa such as (neotropical) Bromeliaceae, Ericaceae or Piperaceae are the most important components of tropical epiphyte floras, ferns dominate in the temperate zones (Zotz, 2005, 2016). Temperate zone epiphytes and their ecology have already been discussed well over a century ago by Schimper (1888). Yet, due to the lack of quantitative studies, we are still missing an evidence-based understanding of the key factors determining growth and survival of temperate zone epiphytes. Studies from New Zealand, Chile, the Pacific Northwest of the USA or the Himalayas revealed that epiphytism in temperate zones is more common than typically appreciated (e.g. Arroyo et al., 1995; Burns, 2008; Sillett and Bailey, 2003; Singh and Chaturvedi, 1982). Surprisingly, quantitative studies on vascular epiphytes from Europe are very rare in the literature, although there are numerous anecdotal accounts from this continent (e.g. Berdrow, 1894; Beyer, 1895; Loew, 1891; Stäger, 1908), but see Hoeber et al. (2019).

So far, it has been suggested that growth of vascular epiphytes in temperate regions is mainly limited by an overall drier climate or frequent occurrences of frost, but neither factor, let alone both in combination, have been studied in detail (Zotz, 2003). While the occurrence of epiphytic angiosperms appears rather fortuitous in Europe, there are a few reports on local occurrences of epiphytic ferns from the genus Polypodium, suggesting that their epiphytic growth is not that uncommon (e.g. Büttner, 2012; Garretas and Salvo-Tierra, 1979; Kelly, 1981; Moe and Botnen, 1997; Zotz, 2002).

Although quantitative studies on epiphytic ferns from the temperate zones are scarce, the frost and drought tolerance of some terrestrial fern species have been studied, providing potential approaches for studying epiphytic ferns. For example, demographic studies performed on terrestrial ferns showed that severe winters had a negative impact on plant growth and survival in Dutch populations of Polystichum setiferum, Asplenium scolopendrium and A. trichomanes (Bremer, 1995, 2004; Bremer and Jongejans, 2010). In contrast, the frost tolerance of Blechnum penna-marina is fairly high and even more so in the case of desiccated plants (Bannister and Fagan, 1989). A very high drought and frost tolerance were also evident in sporophytes of Polypodium vulgare, which endured temperatures of -18°C and tolerated relative humidities as low as 40% for extended periods (Kappen, 1964). Similar results were obtained for conspecific gametophytes, which also showed a pronounced tolerance towards low humidity of 40% and tolerated freezing temperatures of -10°C after hardening at 6°C (Kappen, 1965). Additionally, tolerance towards freezing temperatures was investigated in gametophytes and sporophytes of several fern species in Japan. Noteworthy, epiphytic ferns survived much lower temperatures (between -20°C and -40°C) than terrestrial ferns in the understory (between -5°C and -17.5°C) (Sato, 1982). The role of prolonged freezing events was also discussed for Polypodium vulgare in an alpine deciduous forest in Switzerland (Zotz, 2002).

Ferns from the Polypodium vulgare complex are quite common in central and western Europe and are arguably the most abundant vascular epiphytes there (Zotz, 2005). In the present study, we investigated the abundance and growth patterns of local polypod communities along a rainfall and temperature gradient. In Europe, the Polypodium vulgare complex comprises up to six closely related species with different ploidy levels: the diploid Polypodium cambricum L., the triploid P. × font-queri Rothm. in Cadev. & Font Quer (P. cambricum × P. vulgare), the tetraploid P. vulgare L., the tetraploid P. × shivasiae Rothm. (P. cambricum × P. interjectum), the pentaploid P. × mantoniae Shivas (P. vulgare × P. interjectum) and the hexaploid P. interjectum Shivas (Haufler et al., 1995b; Page, 1997). While the hybridized species are apparently rarer (i.e. less well documented in publications) and allegedly show reduced fertility (Helánová et al., 2004; Manton, 1950; Neuroth, 1996), P. cambricum, P. vulgare and P. interjectum are quite common in most parts of Central and Western Europe (Page, 1997).

Here, we describe the frequency and seasonal growth patterns of epiphyte communities formed by species of the Polypodium vulgare complex in the temperate zone at three sites along a rainfall and temperature gradient in Western Europe spanning from Ireland to Germany. While annual rainfall decreased from Ireland to Germany, the number of freezing days with a mean daily temperature below 0°C increased. With uniquely marked fronds, we were able to closely follow frond productivity and mortality. These measurements allowed us to determine the net growth of plants, thus assessing the overall site performance and providing insights into leaf turnover rates of temperate zone epiphytes. Results are discussed with respect to potential climatic drivers. We hypothesized that frond productivity would be higher in locations with more rainfall and fewer freezing events. Also, we expected plants in warmer and wetter sites to exhibit greater expansive growth and to produce more spore-bearing fronds than in colder and drier sites.