Introduction
Bryophytes are considered the descendants of the earliest forms of plants on Earth and are found anywhere from the tundra to the tropical rainforest. However, they are typically associated with temperate forests, peatlands, tundra, and alpine regions (Goffinet et al., 2012). With climate change as a growing concern for high-elevation and high-latitude habitats, and the large proportion of bryophyte endemism in high latitude regions (Rozzi et al., 2008), it is important to understand the dispersal mechanisms and potential for bryophytes to colonize new habitats. According to Urban (2015), if the Earth’s temperature increases by 3 °C, South America will be one of three regions where extinction risks of species will be highest (23%), followed by Australia and New Zealand (14%). Additionally, climate change is causing an upslope shift in montane plant and animal communities (Elsen & Tingley, 2015; Freeman et al., 2018) that is driven by niche conservatism, which is the retention of ancestral ecological characteristics, such as a habitat, by a species. Faced by climate change, species are more likely to respond by “following” their niches or ancestral climate regime rather than adapting their climatic tolerances (Wiens & Graham, 2005), which may represent a challenge for sessile organisms such as mosses.
The ability of bryophytes to disperse and establish in new areas is fundamental to their survival in a changing planet. This is made possible through anemophily, or wind dispersal facilitated by sexual reproduction morphological features such as exposed spores, tall sporophytes, or the production of a large number of spores (Muñoz, 2004; Barbé et al., 2016), or via water, such as gemma or splash cups (Glime, 2017a; Glime, 2017b; Zanatta et al., 2018). Some species, likeTayloria dubyi , have even been known to have sticky spores and brightly colored sporophytes, that emit a strong odor, mimicking decomposing organic matter, to attract flies as potential dispersal vectors (Jofre et al., 2011). Bryophyte dispersal and colonization is also facilitated by bryophyte cell totipotency, an asexual reproduction mechanism able to regrow the entire gametophyte from tissue fragments (Anderson, 1963; Longton, 1997; Cleavitt, 2002; Proctor et al., 2007; Zhang et al., 2003). However, because some birds and bryophytes share the same habitats, these birds may serve as animal vectors that allow these small plants to reach areas that they would not reach otherwise, or help reach them quicker. The behavior of birds can aid in directed and long-distance movement of bryophytes as they may act as dispersers in local sites through foraging and nesting (Calvelo et al., 2006; Parnikoza et al., 2012; Amélio et al., 2017; Parnikoza et al., 2018), and transcontinentally through migratory movements (Chmielewski & Eppley, 2019). Birds can disperse bryophytes long distances via ectozoochory, by external transportation (Lewis et al., 2014), and may be able to do this via endozoochory, through internal ingestion, as has also been shown with ferns and other herbs (Lovas-Kiss et al., 2018; Blanco et al., 2019; Hervías-Parejo et al., 2019; Silva et al., 2020).
The upland goose (Chloephaga picta , order Anseriformes, family Anatidae (Carboneras & Kirwan, 2020)) and the white-bellied seedsnipe (Attagis malouinus , order Charadriiformes, family Thinocoridae (del Hoyo et al., 1996)) are two herbivorous bird species that inhabit sub-Antarctic South America and could be potential vectors for bryophyte dispersal. A. malouinus is an altitudinal migratory shorebird that moves downwards from its upland habitats to lowland flats during the harsh winters (Fjeldså & Krabbe, 1990; del Hoyo et al., 1996; Jaramillo et al., 2003; “e-Bird: White-bellied Seedsnipe Attagis malouinus ”, n.d.) and has occasionally been known to leave Patagonia to the Falkland Islands (Hayman et al., 1986). C. picta is a migratory goose that is known to have larger movements through South America, migrating between breeding and wintering grounds. Pedrana et al. (2015) tracked the migratory route of a male C. picta and found that he migrated a minimum distance of 1485 km from Buenos Aires (the wintering grounds) to Santa Cruz province, Patagonia (the breeding grounds). This species also migrates altitudinally, as the same study found that the individual moved to lower than 100 masl on the wintering ground and between 1000-1500 masl on the breeding ground. Upland geese tagged on Navarino Island have been observed some 400 km north near Rio Gallegos in Argentina and some geese perform daily altitudinal migration from sea level up to over 700 masl there (J. Jiménez, 2020, pers. comm.).
Previous research suggests that birds, such as mallard ducks (Anas platyrhynchos ) and sub-Antarctic geese and shorebirds, might be capable of dispersing bryophytes through endozoochory (Wilkinson et al., 2017; Russo et al., 2020). Additional evidence of bryophyte dispersal through endozoochory has been reported in spectacled flying foxes (Pteropus conspicillatus ) (Parsons et al., 2007) and freshwater fish (Boedeltje et al., 2019). To our knowledge, the first observations of the consumption of bryophytes by C. picta and A. malouinus in sub-Antarctic South America were made by Behling et al. (2016). More recently, Russo et al. (2020) observed that fecal samples collected on a drying snowmelt bed were comprised of about 50-80% sporophyte fragments from the moss family Polytrichaceae, and those collected on flooded meadows were comprised of about 80-100% bryophyte sporophytes. Of all fecal samples the authors uncovered, 91% ofC. picta and 85% of A. malouinus samples contained bryophyte fragments, including fragments identified asPolytrichum sp., with at least one generating new growth.
Even though viable bryophyte gametophyte fragments have been recovered from avian species that feed on these plants, previous research has attempted to cultivate or regenerate these fragments with little success (Parsons et al., 2007; Wilkinson et al., 2017; Russo et al., 2020). Given that the dispersal and establishment of plants involves sequential and interdependent steps to be successful under field conditions, it is inappropriate to assume that finding bryophyte fragments in bird feces is directly correlated with successful dispersal. Thus, we cannot conclude that these fragments successfully propagate after passing through the bird’s digestive system. For these reasons, together with the search of viable fragments in bird feces, it was necessary to first test if the bryophyte fragments found in bird feces were capable of regenerating when grown under lab conditions. Here, we make observations of the potential role of two herbivorous bird species, C. pictaand A. malouinus , as endozoochorous bryophyte dispersers by testing the viability and regenerative capabilities of fragmented bryophyte gametophytes retrieved from their feces. We propose that both avian species have the potential to serve as dispersal vectors for bryophytes in the sub-Antarctic through endozoochory. Our prediction is that after being ingested, defecated and cultivated under the proper conditions, the bryophyte fragments will have the totipotence to regenerate a new individual. Endozoochory is likely to be a widespread phenomenon. Therefore, our findings could be applicable to regions beyond sub-Antarctic Chile, like the Arctic, where birds also feed on mosses (Fox & Bergersen, 2005) and climate change is altering the vegetation communities and plant-herbivore relations (Klein et al., 2008; Bjorkman et al., 2018).