Correlations between transequatorial migratory bird routes and bipolar biogeographic disjunctions in bryophytes suggest that disjunctions between northern and southern high latitude regions may result from bird-mediated dispersal; supporting evidence is, however, exclusively circumstantial. Birds disperse plant units (diaspores) internally via ingestion (endozoochory) or externally by the attachment of diaspores to the body (ectozoochory). Endozoochory is known to be the primary means of bird-mediated dispersal for seeds and invertebrates at local, regional, and continental scales. Data supporting the role of bird-mediated endozoochory or ectozoochory in the long distance dispersal of bryophytes remain sparse, however, despite the large number of bryophytes displaying bipolar disjunctions. To determine if transequatorial migrant shorebirds may play a role in the ectozoochory of bryophyte diaspores, we developed a method for screening feathers of wild birds. We provide the first evidence of microscopic bryophyte diaspores, as well as those from non-bryophyte lineages, embedded in the plumage of long distance transequatorial migrant birds captured in their arctic breeding grounds. The number of diaspores recovered suggests that entire migratory populations may be departing their northern breeding grounds laden with potentially viable plant parts and that they could thereby play significant roles in bipolar range expansions of lineages previously ignored in the migrant bird dispersal literature.
References
[1]
Andres BA, Smith PA, Morrison RIG, Gratto-Trevor CL, Brown SC, Friis CA. 2012. Population estimates of North American shorebirds. Wader Study Group Bulletin 119:178-194
[2]
Bailey R, James P. 1979. Birds and the dispersal of lichen propagules. Lichenologist 11:105-106
[3]
Bednarek-Ochyra H, Vana J, Ochyra R, Lewis Smith RI. 2000. The liverwort flora of Antarctica. Poland: W. Szafer Institute of Botany, Polish Academy of Sciences.
[4]
Boch S, Berlinger M, Fischer M, Knop E, Nentwig W, Türke M, Prati D. 2013. Fern and bryophyte endozoochory by slugs. Oecologia 172:817-822
[5]
Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ. 2010. Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshwater Biology 55:1262-1273
[6]
Bruun HH, Lundgren R, Philipp M. 2008. Enhancement of local species richness in tundra by seed dispersal through guts of muskox and barnacle goose. Oecologia 155:101-110
[7]
Carlquist S. 1974. Island biology. New York & London: Columbia University Press.
[8]
Costa MJ, Ramos JA, da Silva LP, Timoteo S, Araújo PM, Felgueiras MS, Rosa A, Matos C, Encarnao P, Tenreiro PQ, Heleno RH. 2014. Endozoochory largely outweights epizoochory in migrating passerines. Journal of Avian Biology 45:59-64
[9]
Crandall-Stotler B, Stotler RE, Long DG. 2009. Morphology and classification of the Marchantiophyta. In: Goffinet B, Shaw AJ, eds. Bryophyte biology (2nd edition). Cambridge: Cambridge University Press. 1-54
[10]
Du Rietz GE. 1940. Problems of bipolar plant distribution. Acta Phytogeographica Suecica 13:215-282
Fernández-Mendoza F, Printzen C. 2013. Pleistocene expansion of the bipolar lichen Cetraria aculeata into the Southern hemisphere. Molecular Ecology 22:1961-1983
[13]
Figuerola J, Green AJ. 2002. Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biology 47:483-494
[14]
Goffinet B, Buck WR, Shaw AJ. 2009. Morphology and classification of Bryophyta. In: Goffinet B, Shaw AJ, eds. Bryophyte biology (2nd edition). Cambridge: Cambridge University Press. 55-138
[15]
Green AJ, Figuerola J. 2005. Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Diversity and Distributions 11:149-156
[16]
Hicklin P, Gratto-Trevor CL. 2010. Semipalmated sandpiper (Calidris pusilla) In: Poole A, ed. The birds of North America online. Ithaca: Cornell Lab of Ornithology.
[17]
Heinken T, Lees R, Raudnitschka D, Runge S. 2001. Epizoochorous dispersal of bryophyte stem fragments by roe deer (Capreolus capreolus) and wild boar (Sus scrofa) Journal of Bryology 23:293-300
[18]
Hyeong K, Park S, Yoo CH, Kim K. 2005. Mineralogical and geochemical compositions of the eolian dust from the northeast equatorial Pacific and their implications on paleolocation of the Intertropical Convergence Zone. Paleoceanography 20:PA1010
[19]
Johnson OW, Connors PG. 2010. American Golden-Plover (Pluvialis dominica) In: Poole A, ed. The birds of North America online. Ithaca: Cornell Lab of Ornithology.
[20]
Kreier HP, Feldberg K, Mahr F, Bombosch A, Schmidt AR, Zhu RL, von Konrat M, Shaw B, Shaw AJ, Heinrichs J. 2010. Phylogeny of the leafy liverwort Ptilidium: cryptic speciation and shared haplotypes between the Northern and Southern Hemispheres. Molecular Phylogenetics and Evolution 57:1260-1267
[21]
La Farge C, Williams KH, England JH. 2013. Regeneration of Little Ice Age bryophytes emerging from a polar glacier with implications of totipotency in extreme environments. Proceedings of the National Academy of Sciences of the United States of America 110:9839-9844
[22]
Mao K, Milne RI, Zhang L, Peng Y, Liu J, Thomas P, Mill RR, Renner SS. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proceedings of the National Academy of Sciences of the United States of America 109:7793-7798
[23]
Muoz J, Felicísimo AM, Cabezas F, Burgaz AR, Martínez I. 2004. Wind as a long-distance dispersal vehicle in the Southern Hemisphere. Science 304:1144-1147
[24]
Ochyra R. 1992. Amblyodon dealbatus (Musci, Meesiaceae)—a bipolar disjunct. Fragmenta Floristica et Geobotanica 37:251-259
[25]
Ochyra R, Smith L, Bednarek-Ochyra H. 2008. The illustrated moss flora of Antarctica. New York: Cambridge University Press.
[26]
Ochyra R, Buck WR. 2003. Arctoa fulvella, new to Tierra del Fuego, with notes on trans-American bipolar bryogeography. Bryologist 106:532-538
[27]
Osorio-Zuiga F, Fontúrbel FE, Hkan R. 2014. Evidence of mutualistic synzoochory between cryptogams and hummingbirds. Oikos 123:553-558
[28]
vstedal DO, Lewis Smith RI. 2001. Lichens of Antarctica and South Georgia: a guide to their identification and ecology. In: Studies in polar research. Cambridge: Cambridge University Press.
[29]
Parsons JG, Cairns A, Johnson CN, Robson SKA, Shilton LA, Westcot DA. 2007. Bryophyte dispersal by flying foxes: a novel discovery. Oecologia 152:112-114
[30]
Pauliuk F, Muller J, Heinken T. 2011. Bryophyte dispersal by sheep on dry grassland. Nova Hedwigia 92:327-341
[31]
Pieiro R, Popp M, Hassel K, Listl D, Westergaard KB, Flatberg KI, Stenien HK, Brochmann C. 2012. Circumarctic dispersal and long-distance colonization of South America: the moss genus Cinclidium. Journal of Biogeography 39:2041-2051
[32]
Popp M, Mirré V, Brochmann C. 2011. A single Mid-Pleistocene long-distance dispersal by a bird can explain the extreme bipolar disjunction in crowberries (Empetrum) Proceedings of the National Academy of Sciences of the United States of America 108:6520-6525
[33]
Proctor VW. 1961. Dispersal of Riella spores by waterfowl. Bryologist 64:58-61
[34]
Proctor VW. 1968. Long-distance dispersal of seeds by retention in digestive tract of birds. Science 160:321-322
[35]
Pyle P. 2008. Identification guide to North American birds, part II. Point Reyes Station, CA: Slate Creek Press.
[36]
Ridgeley RS, Allnutt TF, Brooks T, NcNicol DK, Mehlman DW, Young BE, Zook JR, BirdLife International. 2012. Digital distribution maps of the birds of the Western Hemisphere, version 5.0. In: BirdLife International & NatureServe Bird species distribution maps of the world (Version 2.0). Arlington: BirdLife International. Cambridge, UK and NatureServe
[37]
Ridley HN. 1930. The dispersal of plants throughout the world. Ashford: L. Reeve & Co. Ltd..
[38]
Sánchez MI, Hortas F, Figuerola J, Green AJ. 2012. Comparing the potential for dispersal via waterbirds of a native and an invasive brine shrimp. Freshwater Biology 57:1896-1903
[39]
Schuster RM. 1983. Phytogeography of the bryophyta. In: Schuster RM, ed. New manual of bryology. Nichinan, Miyazaki: Hattori Botanical Laboratory. Chapter 10
[40]
Shaw AJ. 1986. A new approach to the experimental propagation of bryophytes. Taxon 35:671-675
[41]
Sorensen AE. 1986. Seed dispersal by adhesion. Annual Review of Ecology and Systematics 17:443-463
[42]
Suthers HB. 1985. Ground-feeding migratory songbirds as cellular slime mold distribution vectors. Oecologia 65:526-530
[43]
Tracy DM, Schamel D, Dale J. 2002. Red Phalarope (Phalaropus fulicarius) In: Poole A, ed. The birds of North America online. Ithaca: Cornell Lab of Ornithology.
[44]
Traveset A, Riera N, Mas RE. 2001. Passage through bird guts causes interspecific differences in seed germination characteristics. Functional Ecology 15:669-675
[45]
van Leeuwen CHA, van der Velde G, van Groenendael JM, Klaassen M. 2012. Gut travellers: internal dispersal of aquatic organisms by waterfowl. Journal of Biogeography 39:2031-2040
[46]
Viana DS, Santamaria L, Michot TC, Figuerola J. 2013. Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms. Ecography 36:430-438
[47]
van Zanten BO. 1978. Experimental studies on trans-oceanic long-range dispersal of moss spores in the Southern Hemisphere. Journal of the Hattori Botanical Laboratory 44:455-482
[48]
Warner GM, French DW. 1970. Dissemination of fungi by migratory birds: survival and recovery of fungi from birds. Canadian Journal of Botany 48:907-910
[49]
Wen J, Ickert-Bond SM. 2009. Evolution of the Madrean-Tethyan disjunctions and the North and South American amphitropical disjunctions in plants. Journal of Systematics and Evolution 47:331-348
[50]
Wilkinson DM. 2010. Have we underestimated the importance of humans in the biogeography of free-living terrestrial microorganisms? Journal of Biogeography 37:393-397
[51]
Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I. 2012. Modelling the effect of size on the aerial dispersal of microorganisms. Journal of Biogeography 39:89-97
[52]
Wirtz N, Printzen C, Lumbsch HT. 2008. The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycological Research 112:472-484
