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).