Abstract

The Antarctic Peninsula has experienced some of the most accelerated warming worldwide, resulting in the retreat of glaciers and creation of new areas for plant development. Information regarding the plant dispersal processes to these new niches is scarce in Antarctica, despite birds being important vectors elsewhere. Many bird pellets (with feed remains such as bones and feathers) are generated annually in Antarctica, which are light and easily transported by the wind and include vegetation that is accidentally or purposely swallowed. The aim of this study was to analyze the presence of plant fragments within skua (Stercorarius/Catharacta spp.) pellets collected from two sampling areas in the Maritime Antarctic: Stinker Point (Elephant Island, 17 samples) and Byers Peninsula (Livingston Island, 60 samples), in the South Shetland Archipelago, during the austral summers of 2018 and 2020. In both study areas, five species of Bryophyta were found that were associated with the pellets and viable in germination tests in a humid chamber. The ingestion of Bryophyta for the skuas contribute to the dispersion of different moss species, including to areas recently exposed by the ice retreat. This is the first demonstration that skua pellets effectively act in the dispersion of Antarctic mosses.

Key words
Antarctica; birds; propagation; vegetation

INTRODUCTION

The warming of the Antarctic Peninsula over the last 50 years has been greater than any other terrestrial ecosystem in the Southern Hemisphere, with consequences being observed in the cryosphere and biology of species. The most affected regions are the Antarctic Peninsula, Maritime Antarctic, and the majority of western Antarctic (Bromwich et al. 2013BROMWICH DH, NICOLAS JP, MONAGHAN AJ, LAZZARA MA, KELLER LM, WEIDNER GA & WILSON AB. 2013. Central West Antarctica among the most rapidly warming regions on Earth. Nat Geosci 6: 139-145. doi: 10.1038/NGEO1671., Siegert et al. 2019SIEGERT M ET AL. 2019. The Antarctic Peninsula under a 1.5°C global warming scenario. Front Environ Sci 7: 102. doi: 10.3389/fenvs.2019.00102.). This warming has resulted in the loss of ice and glaciers, with exposure of soil and rocks (Cook et al. 2014COOK A, VAUGHAN D, LUCKMAN A & MURRAY T. 2014. A new Antarctic Peninsula glacier basin inventory and observed area changes since the 1940s. Antarct Sci 26(6): 614-624. doi: 10.1017/S0954102014000200., Convey & Lewis Smith 2006CONVEY P & LEWIS SMITH RIL. 2006. Responses of terrestrial Antarctic ecosystems to climate change. Plant Ecol 182: 1-10., Thomazini et al. 2014THOMAZINI A, TEIXEIRA DB, TURBAY CVG, LA SCALA JRN, SCHAEFER CEGR & MENDONÇA ES. 2014. Spatial variability of CO2 emissions from newly exposed paraglacial soils at a glacier retreat zone on King George Island, Maritime Antarctica. Permafr Periglac Process 25: 233-242.). This ice cover retreat provides new habitats for the colonization of plants, animals, and microorganisms (Parnikoza et al. 2009PARNIKOZA I, CONVEY P, DYKYY I, TRAKHIMETS V, MILINEVSKY G, TYSCHENKO O, INOZEMTSEVA D & KOZERETSKA I. 2009. Current status of the Antarctic herb tundra formation in the Central Argentine Islands. Glob Chang Biol 15(7): 1685-1693., Siegert et al. 2019SIEGERT M ET AL. 2019. The Antarctic Peninsula under a 1.5°C global warming scenario. Front Environ Sci 7: 102. doi: 10.3389/fenvs.2019.00102.), but the widely reported warming trend has paused since the late 1990s (Turner et al. 2016TURNER J, LU H, WHITE I, KING JC, PHILLIPS T, HOSKING JS, BRACEGIRDLE TJ, MARSHALL GJ, MULVANEY R & DEB P. 2016. Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535: 411-415.).

Antarctic terrestrial vegetation is restricted to ice-free areas, occurring directly on rocks or soil at different developmental stages. The main plant formations are composed of bryophytes (116 species), lichens (ca. 400 species), macroscopic terrestrial algae (four species), and two species of native vascular plants, Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth.) Bartl. (Caryophyllaceae) and the invasive Poa annua L. (Øvstedal & Lewis Smith 2001ØVSTEDAL DO & LEWIS SMITH RI. 2001. Lichens of Antactica and South Georgia: A guide to their identification and ecology. Cambridge, Cambridge University Press, 411 p., Putzke & Pereira 2001PUTZKE J & PEREIRA AB. 2001. The Antarctic mosses with special reference to the South Shetland Islands. Canoas: Ed. ULBRA, 196 p., Ochyra et al. 2008OCHYRA R, LEWIS SMITH RI & BEDNAREK-OCHYRA H. 2008. The illustrated moss flora of Antarctica. Cambridge University Press, Cambridge, 685 p., Pereira & Putzke 2013PEREIRA AB & PUTZKE J. 2013. A pesquisa brasileira contribui para o conhecimento das comunidades vegetais das áreas livres de gelo na Antártica. An Acad Bras Cienc 85: 923-935., Câmara & Carvalho-Silva 2020CÂMARA PEAS & CARVALHO-SILVA M. 2020. 180 years of botanical investigations in Antarctica and the role of Brazil. Acta Bot Brasilica 34(2): 430-436.).

Information regarding the colonization of mosses in newly exposed areas is attributed to the dispersion of fragments of bryophytes or their spores by the wind (Seppelt et al. 2004SEPPELT RD, GREEN TGA, SCHWARZ AMJ & FROST A. 2004. Extreme southern locations for moss sporophytes in Antarctica. Antarct Sci 4(01): 37-39.). An increase in the frequency of sporophyte formation and, consequently, spores may be occurring and would likely be expected, according to more recent studies, which is probably associated with climatic changes (Convey & Lewis Smith 1993CONVEY P & LEWIS SMITH RI. 1993. Investment in sexual reproduction by Antarctic mosses. Oikos 68: 293-302., Lewis Smith & Convey 2002LEWIS SMITH RI & CONVEY P. 2002. Enhanced sexual reproduction in bryophytes at high latitudes in the maritime Antarctic. J Bryol 24: 107-117., Casanova-Katny et al. 2016CASANOVA-KATNY A, TORRES-MELLADO GA & EPPLEY SM. 2016. Reproductive output of mosses under experimental warming on Fildes Peninsula, King George Island, Maritime Antarctica. Rev Chil de Hist Nat 89(13): 1-9., Erin et al. 2017ERIN E, SHORTLIDGE S, EPPLEY M, KOHLER H, ROSENSTIEL TN, ZÚÑIGA GE & CASANOVA-KATNY A. 2017. Passive warming reduces stress and shifts reproductive effort in the Antarctic moss, Polytrichastrum alpinum. Ann Bot 119(1): 27-38.).

Animal-mediated dispersion of Bryophyta has been discussed in numerous works around the world, including studies with mammalians (Heinken et al. 2001HEINKEN T, LEES R, RAUDNITSCHKA D & RUNGE S. 2001. Epizoochorous dispersal of bryophyte stem fragments by roe deer (Capreolus capreolus) and wild boar (Sus scrofa). J Bryol 23: 293-300., Pauliuk et al. 2011PAULIUK F, MÜLLER J & HEINKEN T. 2011. Bryophyte dispersal by sheep on dry grassland. Nova Hedwigia 92: 327-341., Parsons et al. 2007PARSONS JG, CAIRNS A, JOHNSON CN, ROBSON SKA, SHILTON LA & WESTCOTT DA. 2007. Bryophyte dispersal by flying foxes: a novel discovery. Oecologia 152: 112-114., Barbé et al. 2016BARBÉ M, FENTON NJ & BERGERON Y. 2016. So close and yet so far away: long-distance dispersal events govern bryophyte metacommunity reassembly. J Ecol 104(4): 1707-1719.), ants (Rudolphi 2009RUDOLPHI J. 2009. Ant-mediated dispersal of asexual moss propagules. Bryologist 112: 73-79.), slugs (Kimmerer & Young 1995KIMMERER RW & YOUNG CC. 1995. The role of slugs in dispersal of the asexual propagules of Dicranum flagellare. Bryologist 98: 149-153.) and birds (Chmielewski & Eppley 2019CHMIELEWSKI MW & EPPLEY SM. 2019. Forest passerines as a novel dispersal vector of viable bryophyte propagules. Proc Royal Soc B 286: 1-8., Wilkinson et al. 2017WILKINSON DM, LOVAS-KISS A, CALLAGHAN DA & GREEN AJ. 2017. Endozoochory of large bryophyte fragments by waterbirds. Cryptogam Bryol 38: 223-228., Osorio-Zuñiga et al. 2014OSORIO-ZUÑIGA F, FONTÚRBEL FE & RYDIN H. 2014. Evidence of mutualistic synzoochory between cryptogams and hummingbirds. Oikos 123: 553-558., Breil & Moyle 1976BREIL DA & MOYLE SM. 1976. Bryophytes used in construction of bird nests. Bryologist 79: 95-98.), but only recently were studied in Antarctica.

In some regions of Maritime Antarctic, birds have been described as important vectors for the dispersion of plants and the transportation of seeds and plant fragments during nesting activity (Marshall & Convey 1997MARSHALL W & CONVEY P. 1997. Dispersal of moss propagules on Signy Island, maritime Antarctic. Polar Biol 18: 376-383., Vera 2011VERA ML. 2011. Colonization and demographic structure of Deschampsia antarctica and Colobanthus quitensis along an altitudinal gradient on Livingston Island, South Shetland Islands, Antarctica. Polar Res 30: 1. doi: 10.3402/polar.v30i0.7146., Parnikoza et al. 2012PARNIKOZA I, DYKYY I, IVANETS V, KOZERETSKA I, KUNAKH V, ROZHOK R, OCHYRA R & CONVEY P. 2012. Deschampsia antarctica for nest building by the kelp gull in the Argentine Islands area (maritime Antarctica) and its possible role in plant dispersal. Polar Biol 35: 1753-1758. https://doi.org/10.1007/s00300-012-1212-5.
https://doi.org/10.1007/s00300-012-1212-... ). Birds of the Stercorarius genus (Antarctic skuas) are an example, as they use different types of substrates to build their nests, including mosses, lichens, and angiosperms (Albuquerque et al. 2012ALBUQUERQUE MP, VICTORIA FC, SCHUNEMANN AL, PUTZKE J, GUNSKI RJ, SEIBERT S, PETRY MV & PEREIRA AB. 2012. Plant composition of skuas nests at Hennequin Point, King George Island, Antarctica. Am J Plant Sci 3: 688-692., Costa & Alves 2008COSTA ES & ALVES MAS. 2008. The breeding birds of Hennequin Point: An icefree area of Admiralty Bay (Antarctic Specially Managed Area), King George Island, Antarctica. Rev Bras Ornitol 16(2): 137-141., Parnikoza et al. 2009PARNIKOZA I, CONVEY P, DYKYY I, TRAKHIMETS V, MILINEVSKY G, TYSCHENKO O, INOZEMTSEVA D & KOZERETSKA I. 2009. Current status of the Antarctic herb tundra formation in the Central Argentine Islands. Glob Chang Biol 15(7): 1685-1693.). However, the participation of these transporting plant propagules in the Antarctic requires better evaluation (Parnikoza et al. 2012PARNIKOZA I, DYKYY I, IVANETS V, KOZERETSKA I, KUNAKH V, ROZHOK R, OCHYRA R & CONVEY P. 2012. Deschampsia antarctica for nest building by the kelp gull in the Argentine Islands area (maritime Antarctica) and its possible role in plant dispersal. Polar Biol 35: 1753-1758. https://doi.org/10.1007/s00300-012-1212-5.
https://doi.org/10.1007/s00300-012-1212-... ).

Evaluating hummingbird nests, it was found that incorporated bryophyte leaves and stems established and grew, suggesting that nesting behavior can disperse bryophytes (Osório-Zuñiga et al. 2014). Some experiments have demonstrated that waterfowl may be able to vector bryophyte material (spores and plant fragments) internally (Proctor 1961PROCTOR VW. 1961. Dispersal of Riella spores by waterfowl. Bryologist 64: 58-61., Wilkinson et al. 2017WILKINSON DM, LOVAS-KISS A, CALLAGHAN DA & GREEN AJ. 2017. Endozoochory of large bryophyte fragments by waterbirds. Cryptogam Bryol 38: 223-228.). The presence of mosses associated with bird pellets has been also reported in the literature. The moss Aplodon wormskioldii (Hornem.) R.Br. (Splachnaceae), for example, grows in owl pellets, and uses this substrate for its growth and development in Alaska (Koponen 1990KOPONEN A. 1990. Entomophily in the Splachnaceae. J Lin Soc Bot 104: 115-127.).

Skuas from the Signy Islands were observed breaking up mosses, which were then blown by the wind. This type of action is common throughout the Antarctic, with the removal of mosses to make nests or for other reasons, which can contaminate feathers, legs, and beaks and with fragments ingested probably accidentally (Davis 1981DAVIS RC. 1981. Structure and function of two Antarctic terrestrial moss communities. Ecol Monogr 51: 125-143.). Skuas can feed on animals or their remains, including placentas and carrion from different marine mammals, fish, and krill, which are normally also consumed on ground sometimes covered by mosses (Carneiro et al. 2014CARNEIRO APB, MANICA A & PHILLIPS RA. 2014. Foraging behaviour and habitat use by brown skuas Stercorarius lonnbergi breeding at South Georgia. Mar Biol 161: 1755-1764. https://doi.org/10.1007/s00227-014-2457-z.
https://doi.org/10.1007/s00227-014-2457-... , Reinhardt et al. 2000REINHARDT K, HAHN S, PETER H-U & WEMHOFF H. 2000. A review of the diets of Southern Hemisphere skuas. Mar Ornithol 28: 7-19.).

Unlike other regions, in cold environments, animals ingest many mosses, which might be due to the presence of arachidonic acid that confers greater resistance to the cold environment (Prins 1982PRINS HHT. 1982. Why are mosses eaten in cold environments only? Oikos 38(3): 374-380.). However, some authors still believe that the ingestion of mosses by birds is incidental and do not play an important role in dietary requirements (Russo et al. 2020RUSSO NJ, ROBERTSON M, MACKENZIE R, GOFFINET B & JIMENEZ JE. 2020. Evidence of targeted consumption of mosses by birds in sub-Antarctic South America. Austral Ecol 45(3): 399-403.).

Using bryophytes as food or material to build their nests, birds can contribute to their dispersion. Spores and fragments use wind dispersal to reach other environments; however, attaching to the body of an animal may be another transport mechanism (Chmielewski & Eppley 2019CHMIELEWSKI MW & EPPLEY SM. 2019. Forest passerines as a novel dispersal vector of viable bryophyte propagules. Proc Royal Soc B 286: 1-8., Russo et al. 2020RUSSO NJ, ROBERTSON M, MACKENZIE R, GOFFINET B & JIMENEZ JE. 2020. Evidence of targeted consumption of mosses by birds in sub-Antarctic South America. Austral Ecol 45(3): 399-403.).

Pellets are the food remains of carnivorous birds, which are composed of nondigestible parts, mainly feathers and bones that will later be “vomited” in the form of pellets (Votier et al. 2003VOTIER SC, BERAHOP S, MACCORMICK A, RATCLIFFE N & FURNESS RW. 2003. Assessing the diet of great skuas, Catharacta skua, using five different techniques. Polar Biol 26: 20-26. doi 10.1007/s00300-002-0446-z.). Stercorarius spp. (former Catharacta) pellets as vectors of plant dispersion in the Antarctic have not yet been analyzed because most studies have focused on the type of diet and foraging of the species (Votier et al. 2003VOTIER SC, BERAHOP S, MACCORMICK A, RATCLIFFE N & FURNESS RW. 2003. Assessing the diet of great skuas, Catharacta skua, using five different techniques. Polar Biol 26: 20-26. doi 10.1007/s00300-002-0446-z., Borghello et al. 2019BORGHELLO P, TORRES DS, MONTALTI D & IBAÑEZ AE. 2019. Diet of the brown skua (Stercorarius antarcticus lonnbergi) at Hope Bay, Antarctic Peninsula: Differences between breeders and non-breeders. Polar Biol 42: 385-394. https://doi.org/10.1007/s00300-018-2429-8.
https://doi.org/10.1007/s00300-018-2429-... , Steele & Cooper 2012STEELE WK & COOPER J. 2012. Alguns itens alimentares do Polar Sul Skua Stercorarius maccormicki em locais no interior de Ahlmannryggen, Dronning Maud Land, Antártica. Mar Ornithol 40: 63-66., Mund & Miller 1995MUND MJ & MILLER GD. 1995. Diet of the south polar skua Catharacta maccormicki at Cape Bird, Ross Island, Antarctica. Polar Biol 15: 453-455. https://doi.org/10.1007/BF00239723.
https://doi.org/10.1007/BF00239723... , Malzof & Quintana 2008MALZOF SL & QUINTANA RD. 2008. Diet of the south polar skua Catharacta maccormicki and the brown skua C. antarctica lonnbergi at Cierva Point, Antarctic Peninsula. Polar Biol 31: 827. https://doi.org/10.1007/s00300-008-0421-4.
https://doi.org/10.1007/s00300-008-0421-... , Baker & Barbraud 2001BAKER S & BARBRAUD C. 2001. Foods of the South Polar skua Catharacta maccormicki on Ardery Island, Windmill Islands, Antarctica. Polar Biol 24: 59-61. https://doi.org/10.1007/s003000000163.
https://doi.org/10.1007/s003000000163... ).

The presence of mosses and other unidentified plant fragments in skua pellets found in the Antarctic has been mentioned, but only because they were ingested probably to clean the digestive tract of parasites (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). The marked change in the composition of S. maccormicki pellets from a predominance of penguin feathers at Potter Cove (King George Island) to mosses at Cierva Point (Antarctic Peninsula) suggests an alternative function of feather ingestion (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). The elimination of undigested material in pellets impedes the growth of gastric parasite populations in birds that feed on fishes (Piersma & Van Eerden 1989PIERSMA T & VAN EERDEN MR. 1989. Feather eating in great crested grebes Podiceps cristatus: A unique solution to the problems of debris and gastric parasites in fish-eating birds. Ibis 131: 477-486.).

Studying areas of recent ice retreat at Stinker Point (Elephant Island) and Byers Peninsula (Livingston Island), we found a large number of pellets partially covered by associated moss formations, indicating some relationship type. The influence of this form of dispersion and colonization by mosses in environments recently exposed to de-icing is analyzed and discussed here. The present study aimed to analyze skua (Stercorarius spp.) pellets as a source of moss inoculum for colonization of newly exposed areas in the Antarctic region.

MATERIALS AND METHODS

Study area

The Stinker Point (Elephant Island) and Byers Peninsula (Livingston Island), 340 km apart, where chosen among the South Shetland Archipelago to do this study due to the ease of access provided by the Brazilian Antarctic Program.

The Stinker Point region (61° 13’ S, 55° 21’W) is located on the southwest coast of Elephant Island, Antarctic (Figure 1), north of the South Shetland Archipelago, approximately 153 km from King George Island. Stinker Point has a coastline that is 4,300 m in length, with 13 beaches composed of sand, pebbles, and boulders. In addition to having plateau areas with steep cliffs and large fields of moss on top (Petry et al. 2018PETRY MV, VALLS F, PETERSEN E, FINGER J & KRÜGER L. 2018. Population trends of seabirds at Stinker Point, Elephant Island, Maritime Antarctica. Antarct Sci 30(4): 220-226. doi:10.1017/S0954102018000135.), it is rich in floristic diversity and is composed of two vascular plant species, D. antarctica Desv. (Poaceae) and C. quitensis (Kunth.) Bart. (Caryophyllaceae), 38 moss species, seven species of liverworts, 68 species of lichens, and four species of macroscopic fungi (Pereira & Putzke 1994PEREIRA AB & PUTZKE J. 1994. Floristic Composition of Stinker Point, Elephant Island, Antarctica. Korean J Polar Res 5: 37-47., Schmitz et al. 2020SCHMITZ D, VILLA PM, PUTZKE J, MICHEL RFM, CAMPOS PV, NETO JAAM & SCHAEFER CEGR. 2020. Diversity and species associations in cryptogam communities along a pedoenvironmental gradiente on Elephant Island, Maritime Antarctica. Folia Geobot 55: 211-224.).

The Byers Peninsula (62°34’35’S, 61°13’07’ W) is located at the western end of Livingston Island, and is the second largest island in the South Shetland Archipelago, Antarctic (Figure 2), comprising an area of ​​60,35 km². This area has extensive beaches, and is 12 km long and 900 m wide (Praia Sul), and is the most extensive in the South Shetland Archipelago (Ivanov 2015IVANOV L. 2015. General geography and history of Livingston Island. In: Pimpirev C & Chipev N (Eds), Bulgarian Antarctic Research: A Synthesis, 12 p.). The peninsula has a wide variety of periglacial relief forms, such as felsenmeers, terrains with patterns, rocky glaciers, and raised marine platforms (Quesada et al. 2009QUESADA A, CAMACHO A, ROCHERA C & VELÁZQUEZ D. 2009. Byers Peninsula: A reference site for coastal, terrestrial and limnetic ecosystem studies in maritime Antarctica. Polar Sci 3: 181-187. doi:10.1016/j.polar.2009.05.003.). During the summer, the peninsula contains many streams and more than 60 lakes and ponds (Toro et al. 2007TORO M ET AL. 2007. Limnological characteristics of the freshwater ecosystems of Byers Peninsula, Livingston Island, in maritime Antarctica. Polar Biol 30: 635. https://doi.org/10.1007/s00300-006-0223-5.
https://doi.org/10.1007/s00300-006-0223-... ). The vegetation cover consists of lichens that colonize inactive or weakly active periglacial landforms and rocky outcrops and moss carpets, which are abundant in poorly drained areas. There are two vascular plants, D. antarctica and C. quitensis, found in the highest marine terraces (Vera 2011VERA ML. 2011. Colonization and demographic structure of Deschampsia antarctica and Colobanthus quitensis along an altitudinal gradient on Livingston Island, South Shetland Islands, Antarctica. Polar Res 30: 1. doi: 10.3402/polar.v30i0.7146.). The peninsula was originally designated as a specially protected area because of its high Antarctic biodiversity levels (Toro et al. 2007TORO M ET AL. 2007. Limnological characteristics of the freshwater ecosystems of Byers Peninsula, Livingston Island, in maritime Antarctica. Polar Biol 30: 635. https://doi.org/10.1007/s00300-006-0223-5.
https://doi.org/10.1007/s00300-006-0223-... ).

Sample collections

During the southern summers of 2018 and 2020, Stercorarius spp. pellets were collected and analyzed in ice-free areas in the regions of Stinker Point, Elephant Island, and the Byers Peninsula, Livingston Island, approximately 340 km from each other.

The samples were collected and packed in paper bags and taken to the camp, where they were dehydrated and then transported to the Universidade Federal do Pampa laboratory in southern Brazil. They were analyzed under a magnifying glass (Olympus model SZ51), after each was disassembled in a Petri dish using tweezers and separating all the material found. The materials that adhered to the outside, including vegetal fragments, were discarded to avoid further contamination. The remains of prey, such as bones and feathers, were separated from the plant material found inside the pellet. The identification of plant species in the sampled material was based on the specific literature of Antarctic vegetation (Øvstedal & Lewis Smith 2001ØVSTEDAL DO & LEWIS SMITH RI. 2001. Lichens of Antactica and South Georgia: A guide to their identification and ecology. Cambridge, Cambridge University Press, 411 p., Ochyra et al. 2008OCHYRA R, LEWIS SMITH RI & BEDNAREK-OCHYRA H. 2008. The illustrated moss flora of Antarctica. Cambridge University Press, Cambridge, 685 p., Putzke & Pereira 2001PUTZKE J & PEREIRA AB. 2001. The Antarctic mosses with special reference to the South Shetland Islands. Canoas: Ed. ULBRA, 196 p.). All plant materials found inside each sample were assessed for their capacity to regenerate by the fragments being placed in a humid chamber. To this experiment the fragments isolated from each pellet were placed in Petri dishes upon several thicknesses of filter paper which had been saturated with distillated water and maintained at 25 (±2) °C and 12 h of continuous light. The experiment was weekly checked for regeneration of the fragments and maintained for three months.

A recent ice retreat area at Stinker Point (located at 61°13’36.06’ S and 55°21’15.68’ W) in an early stage of plant colonization was assessed for the presence of old pellets (that were at least partially buried in the sediment) and evaluated for the presence of associated plants. The area was entirely covered by a glacier when two of the authors (JP and ABP) visited it in 1990 and 1994, yet it was free of ice in 2012 and 2018. Pellets colonized by vegetation were counted, and the vegetation cover was estimated. Using the images captured by a Phantom 4 drone from the site (100 m high), a map was created, and three rectangles were identified to study the vegetation (Figure 1):

- Area 1: 8685.6 m², formed by a gentle slope facing southeast;

- Area 2: 5766.5 m², south of Area 1, created by a low elevation (with a top 4 m high in relation to the base);

- Area 3: 8361 m², east of Area 1, formed by an elevation with a southwest slope.

RESULTS

During field work there were collected 17 pellets in Stinker Point, Elephant Island (Figure 2) and 60 samples in Byers Peninsula, Livingston Island. The number of samples is different because the Livingston area was more protected from the direct wind interference, retaining more pellets. In all samples the plant material was restricted to small fragments (less than 1 cm long), being impossible to evaluate their proportion (or weight) in relation to the other components of the pellet. In Stinker Point 88% and Byers 91.6% of pellets presented plant fragments. One species of green algae (Prasiola crispa) and five moss species, Sanionia uncinata, S. georgico-uncinata, Warnstorfia sarmentosa, W. fontinaliopsis and Hennediella heimii were found (Figure 3). In Byers, only the green algae species was absent (Table I) being the mosses found the same.

In the wet chamber test, all moss samples regenerate (100%), forming new branches and demonstrating their ability to survive the digestive tract of the bird and the conditions of the interior of the regurgitate. After assessing the area where the ice retreat was most recent (last 20 years) at Stinker Point, Area 1 had more developed vegetation, forming a continuous carpet, especially of Sanionia uncinata, whereas the other areas did not have any apparent cover. In the count of the oldest pellets, 58 samples were found in the plant formation surroundings because in its interior the carpet of mosses prevented the visualization of older regurgitates (Figure 4).

In Area 2, no old pellets colonized by vegetation were found, perhaps because this area is at the top of an elevation, preventing the stabilization of pellets. In Area 3, 38 skua pellets were found, all presenting associated growing mosses and in places that held practically no vegetation (Figure 5). In the three areas, many scattered bones were observed, indicating that the pellets had been disintegrated by the time of exposure or that they had arrived at the site by the wind regardless of being integrated into the pellets.

DISCUSSION

During the summer period in the Maritime Antarctic region (November to March), after the melting of the ice deposited in the winter, birds migrate to the region in search of a place to rest, feed, and reproduce (Harris et al. 2011HARRIS CM, CARR R, LORENZ K & JONES S. 2011. Important bird areas in Antarctica: Antarctica Peninsula, South Shetland Islands, South Orkney Islands – Final Reports. Prepared for Bird Life International and the Polar Regions Unit of the UK Foreing & Commonwealth Office. Environmental Research & Assessment Ltd., Cambridge IBA, 226 p.). Among these, the skua (Catharacta/Stercorarius) has a regurgitating feeding habit because they are carnivorous birds and eliminate feathers and bones (in pellets) that are not digested (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). The kelp gull (Larus dominicanus) also regurgitates in Antarctica and could be investigated for plant dispersal too, despite eating more marine invertebrates (Coulson & Coulson 1993COULSON R & COULSON G. 1993. Diets of the Pacific Gull Larus pacificus and the Kelp Gull Larus dominicanus in Tasmania. Emu 93: 50-53., Lindsay & Meathrel 2008LINDSAY MCM & MEATHREL CE. 2008. Where, when and how? Limitations of the techniques used to examine dietary preference of Pacific Gulls (Larus pacificus) using non-consumed parts of prey and regurgitated pellets of prey remains. Waterbirds 31: 611-619.).

In the present study, we found the presence of fragments of different moss species in the pellets, which was previously noticed, but was associated with digestive tract cleaning (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). Another possibility is that during the reproductive period, these birds use plant species, such as mosses, lichens, and angiosperms to build their nests (Albuquerque et al. 2012ALBUQUERQUE MP, VICTORIA FC, SCHUNEMANN AL, PUTZKE J, GUNSKI RJ, SEIBERT S, PETRY MV & PEREIRA AB. 2012. Plant composition of skuas nests at Hennequin Point, King George Island, Antarctica. Am J Plant Sci 3: 688-692.), which is also undertaken by other birds, such as seagulls (Larus dominicanus) (Convey 2012CONVEY P. 2012. Use of Deschampsia antarctica for nest building by the kelp gull in the Argentine Islands area (Maritime Antarctica) and its possible role in plant dispersal. Polar Biol 35: 1753-1758.) and probably they accidentally ingest fragments of these plants. In the nest, plants serve as a protective barrier for climatic variations and are a more comfortable environment than rocks (Walsberg 1985WALSBERG GE. 1985. Physiological consequences of microhabitat selection. In: Cody ML (Ed), Habitat selection in birds, Academic Press, Florida, p. 389-413.).

The Antarctic birds are efficient in the dispersion of mosses, via the transport of vegetal fragments and spores adhered to their body (Lewis et al. 2014LEWIS LR, BEHLING E, GOUSSE H, QIAN E, ELPHICK CS, LAMARRE J, BÊTY J, LIEBEZEIT J, ROZZI R & GOFFINET B. 2014. First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ 2: e424., Schlichting et al. 1978SCHLICHTING H, SPEZIALE B & ZINK R. 1978. Dispersal of algae and protozoa by Antarctic flying birds. Antarct J U S [s. l.]13(4): 147-149.), disregarding the possibility of mosses being associated with regurgitated pellets. The results suggest that this association might imply another form of moss dispersion for areas exposed to melting in Antarctica. The implications of this association are unprecedented in studies of moss dispersion in this region, being the percentage of pellets with mosses considerable, with our findings (88 to 91,6%) similar to those found in literature (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). Migrant birds might just potentially also bring in pellets containing material of currently non-Antarctic plant species, for instance if they eliminate those pellets with any material foraged in Southern South America or subantarctic islands, when they first arrive at the beginning of the season. But this needs to be better investigated.

Despite being formed by a pile of remains of bones, hair, and feathers that are not used in digestion, the pellets constitute an excellent source of nutrients in areas recently devoid of ice, where rocks and sandy sediments predominate. Infiltrating a pellet can allow rapid plant development, once they are partially decomposed, after being expelled, providing essential nutrients to the mosses whose fragments are inside the pellet.

Cough pellets left by raptors, such as the common kestrel (Falco tinnunculus), are another likely mode of secondary dispersal of many organisms, including fungi (Watling 1963WATLING R. 1963. The fungal succession on hawk pellets. Trans Br Mycol Soc 6: 81-90.). Keratinophilic fungi are commonly isolated from regurgitated pellets, indicating a close relationship with the bird and this digestion mode (Bohacz et al. 2020BOHACZ J, KORNIŁŁOWICZ-KOWALSKAA T, KITOWSKIB I & CIESIELSKA A. 2020. Degradation of chicken feathers by Aphanoascus keratinophilus and Chrysosporium tropicum strains from pellets of predatory birds and its practical aspect. Intern Biodeterior & Biodegradation 151: 104968.). Therefore, the agents responsible for decomposition are also present in these pellets, accelerating the availability of nutrients.

Bryophytes are part of the diet of some high Andean birds and may disperse bryophytes internally, via endozoochory, in the sub-Antarctic zone, being present in 84.6% and 90.9% (white-bellied seedsnipe, Attagis malouinus, and Chloephaga spp. geese, respectively) of the fecal samples studied (Russo et al. 2020RUSSO NJ, ROBERTSON M, MACKENZIE R, GOFFINET B & JIMENEZ JE. 2020. Evidence of targeted consumption of mosses by birds in sub-Antarctic South America. Austral Ecol 45(3): 399-403.). This is also the case for Antarctic skuas, where mosses are used as gut-cleaning materials (Santos et al. 2012SANTOS MM, JUARES MA, ROMBOLA EF, GARCÍA ML, CORIA NR & DONCASTER CP. 2012. Over-representation of bird prey in pellets of South Polar Skuas. J Ornithol 153: 979-983. doi 10.1007/s10336-012-0840-4.). In this way, the ingestion of mosses, which allow the elimination of parasites, might include fragments of mosses in the pellets.

Animals that consume mosses in cold environments are related to high concentrations of arachidonic acid in Bryophyta, which gives them higher cold resistance (Prins 1982PRINS HHT. 1982. Why are mosses eaten in cold environments only? Oikos 38(3): 374-380.). The ingestion of arachidonic acid can benefit animals in several ways, including it being a precursor of some prostaglandin hormones; its low melting point (-49.5 °C) means that it might contribute to lowering the melting point of fats in the animal extremities; and it protects cell membranes against the effects of cold (Feng & Bai 2011FENG C & BAI XL. 2011. The bryophyte consumed by reindeers and species diversity of bryophyte in reindeer habitats (in Chinese). Acta Ecol Sin 31(13): 3830-3838.).

The presence of arachidonic acid is common in mosses, unlike other plants (Anderson et al. 1974ANDERSON WH, HAWKINS J, GELLERMAN JL & SCHLENK H. 1974. Fatty acid composition as a criterion in the taxonomy of mosses. J Hattori Bot Lab 38: 99-103.), and it has been found in three species of Antarctic mosses (Bryum pseudotriquetrum, Ceratodon purpureus, and Grimmia antarctici) (Wasley et al. 2006WASLEY J, ROBINSON SA, LOVELOCK CE & POPP M. 2006. Some like it wet – biological characteristics underpinning tolerance of extreme water events in Antarctic bryophytes. Funct Plant Biol 33(5): 443-455.). Thus, it is possible that the Antarctic skuas are making use of mosses as food, eliminating part of them in the regurgitates, and enabling the dispersion of this vegetation to new areas.

The weight of each pellet is small because they are dehydrated and formed mostly by feathers, allowing it to be carried easily by the wind. Therefore, it is highly unlikely that pellets at such concentrations were deposited directly in the area by birds, as they would be easily displaced by wind action. The pellets found partially buried in sediments must have been carried by winds to the glaciers and incorporated into the cracks, remaining stored for a long time until total melting in the area, when they grew back normally after being exposed. The Antarctic moss Chorisodontium acyphyllum remained alive after being frozen for more than 1500 years (Roads et al. 2014ROADS E, LONGTON RE & CONVEY P. 2014. Millennial timescale regeneration in a moss from Antarctica. Curr Biol 24(6): 222-223.). Mosses buried for more than 600 years by a glacier were re-exposed by the retreat of the ice, and parts of the moss could activate again and grow normally “in vitro” (Cannone et al. 2017CANNONE N, CORINTI T, MALFASI F, GEROLA P, VIANELLI A, VANETTI I, ZACCARA S, CONVEY P & GUGLIELMIN M. 2017. Moss survival through in situ cryptobiosis after six centuries of glacier burial. Sci Rep 7: 1-7.). Therefore, the resistance of these species is very high and they can remain viable for a long time, waiting for the right moment to colonize the pellet, which is its only source of nutrients.

The potential could also apply to native flowering plants, especially seeds of the grass Deschampsia antarctica, a species that skuas are also known to move around and incorporate in their nesting material, but this needs to be investigated (Parnikoza et al. 2009PARNIKOZA I, CONVEY P, DYKYY I, TRAKHIMETS V, MILINEVSKY G, TYSCHENKO O, INOZEMTSEVA D & KOZERETSKA I. 2009. Current status of the Antarctic herb tundra formation in the Central Argentine Islands. Glob Chang Biol 15(7): 1685-1693., 2012). It is also important not to let skuas scavenge around stations, since seeds of food plants can easily be ingested and eliminated in pellets later in the natural environment.

The occurrence of mosses in pellets, from the ingestion of these by the skuas, represents another way of dispersion of Bryophyta in the Antarctic region, associated to wind and uses for nest building, reinforcing similar findings already made for the Arctic.

ACKNOWLEDGMENTS

We acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, for concession the scholarship of the first author. This work is a contribution of the INCT-Criosfera TERRANTAR and PERMACLIMA projects, with financial support of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil.

REFERENCES

Publication Dates

History