Abstract
We set out to examine a postulated latitudinal trend in species richness within the Arctic Ocean. We compiled species records of tintinnid ciliates in the Arctic from the literature and added our own unpublished Chukchi Sea data to produce a database (available as an Online Resource data file) consisting of 1427 records of 89 species from 414 locations above 65°N sampled from 1885 to 2015. While there was no trend of species richness throughout the Arctic, there was a significant positive relationship between species richness and the number of sites sampled in a 2° band, suggesting a sampling effect. Plotting cumulative numbers of species and cumulative number of sites sampled by year, we found a linear relationship in log cumulative numbers of species and log sites sampled, and a lack of a plateau in the species accumulation trend. Species records are highly dominated by four species, accounting for 45% of the records: Acanthostomella norvegica, Parafavella denticulata, Ptychocylis obtusa and Sal**ella acuminata, all of which, except S. acuminata, have long been suspected to be morphologically variable, with different morphotypes given undue species status. Pooling all reported species of Acanthostomella, Parafavella and Ptychocylis yielded little qualitative differences but considerable quantitative differences. We found large discrepancies in geographic coverage. We conclude that many zones projected to experience large changes in sea ice coverage are under-sampled. Based on the historical trend, the list of Arctic tintinnid ciliate species will likely continue to grow with new sampling, regardless of changes in the Arctic Seas.
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References
Berline L, Siokou-Frangou I, Marasovic I, Vidjak O, Fernandez de Puelles ML, Mazzocchi MG, Assimakopoulou G, Zervoudaki S, Fonda-Umani S, Conversi A, Garcia-Comas C, Ibanez F, Gasparini S, Stemmann L, Gorsky G (2012) Intercomparison of six Mediterranean zooplankton time series. Prog Oceanogr 97–100:76–91
Bernstein T (1931) Protist plankton of the North-West part of the Kara Sea. Trans Arct Inst 3:1–23 (in Russian with English summary)
Boltovskoy D, Vivequin SM, Swanberg NR (1991) Vertical distribution of tintinnids and associated microplankton in the upper layer of the Barents Sea. Sarsia 76:141–151
Boltovskoy D, Vivequin SM, Swanberg NR (1995) Tintinnids and other microplankton from the Greenland Sea: abundance and distribution in the marginal ice zone (May–June 1989). PSZNI: Mar Ecol 16:117–131
Braarud T, Gaarder KR, Nordli O (1985) Seasonal changes at various points off the Norwegian west coast. 1958. Fisk Skr Ser Havunders 12:1–77
Burkovsky IV (1973) Variability of Parafavella denticulata in the White Sea. Zool Zhurnal 52:1277–1285 (in Russian with English summary)
Burkovsky IV (1976) New data on tintinnids (Ciliata) of the Arctic and revision of fauna. Zool Zhurnal 55:325–336 (in Russian with English summary)
Burkovsky IV, Zamyshlyak YY, Poskryakova NP (1974) Revision of the fauna of tintinnida (Ciliata) of the White Sea. Zool Zhurnal 53:1757–1776 (in Russian with English summary)
Bursa A (1963) Phytoplankton in coastal waters of the Arctic Ocean at Point Barrow Alaska. Arctic 16:239–262
Cardinal A, Lafleur P-E, Bonneau E (1977) Les tintinnides (Ciliata: tintinnida) des eaux marines et saumatres du Québec. I. Formes hyalines. Acta Protozool 16:15–22
Chaudary C, Saeedi H, Costello MJ (2016) Bimodality of latitudinal gradients in marine species richness. Trends Ecol Evol 31(9):670–676 in press
Chernova EN, Primako EM (2011) Distribution of zooplankton in the estuary of Keretskaya Guba (White Sea). Rus J Mar Biol 37:104–110
Cleve PT (1899) Plankton collected by the Swedish expedition to Spitzbergen in 1898, vol 32. Kongl Svenska Vetenskaps-Akademiens Handlingar, 51 pp
Daniëls FJA, Gillespie LJ, Poulin M et al (2013) Plants. In: Meltofte H (ed) Arctic biodiversity assessment. Status and trends in Arctic biodiversity. Conservation of Arctic Flora and Fauna, Akureyri, pp 311–353
Davis CC (1978) Variations of the lorica in the genus Parafavella (Protozoa: tintinnida) in northern Norway waters. Can J Zool 56:1822–1827
Davis CC (1981) Variations of lorica shape in the genus Ptychocylis (Protozoa: tintinnina) in relation to species identification. J Plank Res 3:433–443
Dickson I, Walker G, Pearce DA (2016) Microbes and the Arctic Ocean. In: Hurst CJ (ed) Their world: a diversity of microbial environments. Advances in environmental microbiology I, Springer, Zurich, pp 341–381
Dolan JR (2016a) Historical trends in the species inventory of tintinnids (ciliates of the microzooplankton) in the Bay of Villefranche (NW Mediterranean Sea): shifting baselines. Eur J Protistol. doi:10.1016/j.ejop.2016.10.004
Dolan JR (2016b) Planktonic protists: little bugs pose big problems for biodiversity assessments. J Plank Res 38:1044–1051. doi:10.1093/plankt/fbv079
Dolan JR, Pierce RW (2013) Diversity and distributions of tintinnid Ciliates. In: Dolan JR, Agatha S, Coats DW, Montagnes DJS, Stocker DK (eds) Biology and ecology of tintinnid ciliates: models for marine plankton. Wiley-Blackwell, Oxford, pp 214–243
Dolan JR, Ritchie MR, Ras J (2007) The neutral community structure of planktonic herbivores, tintinnid ciliates of the microzooplankton, across the SE Pacific Ocean. Biogeosciences 4:297–310
Dolan JR, Yang EJ, Kim TW, Kang S-H (2014) Microzooplankton in a warming Arctic: a comparison of tintinnids and radiolarians from summer 2011 and 2012 in the Chukchi Sea. Acta Protozool 52:101–113
Dolan JR, Yang EJ, Kang S-H, Rhee TS (2016) Declines in both redundant and trace species characterise the latitudinal diversity gradient in tintinnid ciliates. ISME J 10:2174–2183. doi:10.1038/ismej.2016.19
Eakins BW, Sharman GF (2010) Volumes of the World’s Oceans from ETOPO1. NOAA National Geophysical Data Center, Boulder. https://www.ngdc.noaa.gov/mgg/global/etopo1_ocean_volumes.html
Feng M, Zhang W, **ao T (2014) Spatial and temporal distribution of tintinnid (Ciliophora: tintinnida) communities in Kongsfjordn, Svalbard (Arctic), during summer. Polar Biol 37:291–296
Gaarder KR (1938) Phytoplankton studies from the Tromso district 1930-31. Tromso Mus Arsh Nat Avd NR 11(55):1–159
Glig O, Kovacs KM, Aars J et al (2012) Climate change and the ecology and evolution of Arctic vertebrates. Ann NY Acad Sci 1249:166–190
Gran HH (1900) Hydrographic-biological studies of the North Atlantic Ocean and the coast of Nordland. Rep Nor Fish Mar Investig 1:1–137
Heimdal B (1974) Composition and abundance of phytoplankton in the Ullsfjord area, North Norway. Astarte 7:17–42
Jedrzejek B, Drees B, Daniëls FJA, Hörtzel N (2012) Vegetation discontinuities and altitudinal indicator species in mountain of West Greenland: finding the best positions and traits to observe the impact of climate warming in the Arctic. Appl Veg Sci 15:432–448
Jensen F, Hansen BW (2000) Ciliates and heterotrophic dinoflagellates in the marginal ice zone of the central Barents Sea during spring. J Mar Biol Assoc UK 80:45–54
Jorgensen LL, Archambault P, Armstrong C et al (2016) Chapter 36G. Arctic Ocean. In: Innisss L, Simcock A (joint coordinators) The group of experts of the regular process. The first global integrated marine assessment. United Nations, New York, 47 pp
Kofoid CA, Campbell AS (1929) A conspectus of the marine and freshwater ciliata belonging to the suborder tintinnoinea, with despcriptions of new species principally from the Agassiz Expedition to the Eastern Tropical Pacific 1904–1905. Univ Calif Publ Zool 34:1–403
Kosobokova KN, Hopcroft RR, Hirche H-J (2010) Patterns of zooplankton diversity through the depths of the Arctic’s central basins. Mar Biodiv. doi:10.1007/s12526-010-0057-9
Kubiszyn AM, Piwosz K, Wiktor JM, Wiktor JM Jr (2014) The effect of inter-annual Atlantic water inflow variability on the planktonic protist community structure in the West Spitsbergen waters during the summer. J Plank Res 36:1190–1203
Lee K-H, Chung K-H, Soh HY, Lee W (2003) On the distribution of zooplankton in the southeaster Barents Sea during July 2002. Korean J Environ Biol 21:392–399
Levinsen H, Nielsen TG, Hansen BW (1999) Plankton community structure and carbon cycling on the western coast of Greenland during the stratified summer situation. II. Heterotrophic dinoflagellates and ciliates. Aquat Microb Ecol 16:217–232
Li WKW, McLaughlin FA, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539
Li H, Xu Z, Zhang W, Wang S, Zhang G, **ao T (2016) Boreal tintinnid assemblage in the Northwest Pacific and its connection with the Japan Sea in summer 2014. PLoS ONE 11:e0153379. doi:10.1371/journal.pone.0153379
Longhurst A (1998) Ecological geography of the sea. Academic Press, San Diego, pp 101–108
Lovejoy C (2014) Changing views of Arctic protists (marine microbial eukaryotes) in a changing Arctic. Acta Protozool 53:91–100
Lovejoy C, Legendre L, Martineau M-J, Bacle J, von Quillfeldt CH (2002) Distribution of phytoplankton and other protists in the north water. Deep-Sea Res II 49:5027–5047
Lutter S, Taasen J, Hopkins CCE, Smetacek V (1998) Phytoplankton dynamics and sedimentation processes during spring and summer in Balsfjord, Northern Norway. Polar Biol 10:113–124
Matsuno K, Ichinomiya M, Yamaguchi A, Imai I, Kikuchi T (2014) Horizontal distribution of microprotist community structure in the western Arctic Ocean during late summer and early fall of 2010. Polar Biol 37:1185–1195
McLaughlin F, Carmack E, O’Brien M et al (2009) Physical and chemical data from the Beaufort Sea and Western Canadian Arctic Archipelago, September 2–16, 2000. Canadian data report of hydrography and ocean science, vol 180, 167 pp
McManus GB, Santoferrara LF (2013) Tintinnids in microzooplankton communities. In: Dolan JR, Montagnes DJS, Agatha S, Stoecker DK (eds) The biology and bcology of tintinnid ciliates: models for marine plankton. Wiley-Blackwell, Oxford, U.K., pp 198–213
Melnikov IA, Kolosova EG, Welch HE, Zhitina LS (2002) Sea biological communities and nutrient dynamics in the Canada Basin of the Arctic Ocean. Deep-Sea Res. I 49:1623–1649
Meltofte H (2013) Arctic biodiversity assessment: status and trends in Arctic biodiversity. Conservation of Arctic Flora and Fauna, Akureyri
Meschkat A (1939) Untersuchung über das herbstplankton im Bereich des “Ostilandstromes”. Int Rev Hydrobiol Hydrogr 38:285–352
Michel C, Bluhm B, Gallucci V et al (2012) Biodiversity of Arctic marine ecosystems and responses to climate change. Biodiversity 13:200–214
Montagnes DJS (2013) Ecophysiology and behavior of tintinnids. In: Dolan JR, Montagnes DJS, Agatha S, Stoecker DK (eds) The biology and ecology of tintinnid ciliates: models for marine plankton. Wiley-Blackwell, Oxford, UK, pp 85–121
Monti M, Minocci M (2013) Microzooplankton along a transect from northern continental Norway to Svalbard. Polar Res 32:19306. doi:10.3402/polar.v32i0.19306
Nelson RJ, Ashjian CJ, Bluhm B, Conlan KE et al (2014) Biodiversity and biogeography of the lower trophic taxa of the Pacific Arctic region: sensitivities to climate change. In: Grebbmeier JM, Maslowski W (eds) The Pacific Arctic region: ecosystem status and trends in a rapidly changing environment. Springer, Dordrecht, pp 269–336
Ostenfeld H (1910) Marine plankton from the East-Greenland Sea (W. of 6°W. Long. and N. of 73°30′Lat.) collected during the Danmark Expedition” 1906-1908. II. Protozoa. Danmark-Ekspeditionen til Gronlands Nordostkyst 1906–1908 under ledelse af l. Mylius-Erichsen 3:288–299
Ostenfeld CH, Paulsen O (1911) Marine plankton from the East-Greenland Sea (W. of 6° W. Long. and N. of 73°30′Lat.) collected during the Danmark Expedition” 1906–1908. IV. General remarks on the microplankton. Danmark-Ekspeditionen til Gronlands Nordostkyst 1906–1908 under ledelse af l. Mylius-Erichsen 3:319–336
Paranjape MA (1987) The seasonal cycles and vertical distribution of tintinnines in Bedford Basin, Nova Scotia, Canada. Can J Zool 65:41–48
Pedros-Alio C, Potvin M, Lovejoy C (2015) Diversity of planktonic microorganisms in the Arctic Ocean. Prog Oceanogr 139:233–243
Pierce RW, Turner JT (1993) Global biogeography of marine tintinnids. Mar Ecol Prog Ser 94:11–26
Piontek J, Sperling M, Nöthig E-M, Engel A (2014) Regulation of bacterioplankton activity in fram strait (Arctic Ocean) during early summer: the role of organic matter supply and temperature. J Mar Syst 132:83–94
Preston FW (1962) The canonical distribution of commoness and rarity: part 1. Ecology 43:185–215
Ratkova TN, Wassmann P, Verity PG, Andreassen IJ (1998) Abundance and biomass of pico-, nano-, and microplankton on a transect across Nordvestbanken, north Norwegian shelf in 1994. Sarsia 84:213–225
Rossolimo LL (1927) Planktonic ciliates of the Kara Sea. Tr. Plavuch. morsk. n.-i. in-ta 2:63–77 (in Russian with German summary)
Santoferrara LF, Bachy C, Alder VA et al (2016) Updating biodiversity studies in loricate protists: the case of the tintinnids (Alveolata. J Eukaryot Microbiol, Ciliophora, Spirotrichea). doi:10.1111/jeu.12303
Schulz B, Wulff A (1927) Hydrographische und planktologische Ergebnisse der Fahrt Des Fischereischutzbootes “Zeiten” in das Barentsmeer im August–September 1926. Ber Dtsch Wiss Komm Meeresforsch 3:211–280
Scott RW, Barton DR, Evans MS, Keating JJ (2011) Latitudinal gradients and local control of aquatic insect richness in a large river system in northern Canada. J N Am Benthol Soc 30:621–634
Seuthe L, Iversen KR, Narcy F (2011) Microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): iI. Ciliates dinoflag Polar Biol 34:751–766
Sherr EB, Sherr BF, Hartz AJ (2009) Microzooplankton grazing impact in the Western Arctic Ocean. Deep-Sea Res II 56:1264–1273
Smayda TJ (1958) Phytoplankton studies around Jan Mayen Island. March–April, 1955. Nytt Mag Botanikk 6:75–96
Stecher A, Neuhaus S, Lange B, Frickenhaus S, Beszteri A, Kroth PG, Valentin K (2016) rRNA and rDNA based assessment of sea ice protist biodiversity from the central Arctic Ocean. Eur J Phycol 51:31–46
Tibbs JF (1967) On some planktonic protozoa taken from the track of drift station ARLISI, 1960–61. Arctic 20:247–254
Wassmann P (2011) Arctic marine ecosystems in an era of rapid climate change. Prog Oceanogr 9:1–17
Wassmann P, Kosobokova KN, Slagstad D et al (2015) The contiguous domains of Arctic Ocean advection: trails of life and death. Prog Oceanogr 139:42–65
WoRMS Editorial Board (2016) World register of marine species. doi:10.14284/170; http://www.marinespecies.org at VLIZ. Accessed 2016-07-14
Yang EJ, Choi JK, Kim SY, Chung KH, Shin H-C, Kim Y (2004) Spatial distribution and community structure of heterotrophic protists in the Central Barents Sea of Arctic Ocean during Summer. Ocean Polar Res 26:567–579
Yokoi N, Matsuno K, Ichinomiya M et al (2016) Short-term changes in a microplankton community in the Chukchi Sea during autumn: consequences of a strong wind event. Biogeosciences 13:913–923. doi:10.5194/bg-13-913-2016
Zhang W, Feng M, Yu Y, Zhang C, **ao T (2012) An illustrated guide to contemporary tintinnids in the world. Science Press, Bei**g, p 499
Acknowledgements
Marina Monti, Kohel Mastsuno, and Neil Swanberg supplied a substantial quantity of data. They kindly retrieved data from their own archives and sent us spreadsheets of species records from their oceanographic campaigns. We also appreciate the efforts of Kristian Seteras of the Institute of Marine Research Library in Bergen who sent us images of the many tables in Gran (1900), missing from copies available online, which provided the earliest Arctic records. We thank Sabine Agatha for providing copies of early Russian reports and Yana Eglit for hel** us decipher them. Comments on earlier drafts by Mark Costello, Dave Montagnes, three reviewers and the Editor led to significant improvements. Partial financial support was provided by grants from the ‘(K-AOOS KOPRI, PM16040)’, funded by the MOF, Korea.
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Dolan, J.R., Pierce, R.W. & Yang, E.J. Tintinnid ciliates of the marine microzooplankton in Arctic Seas: a compilation and analysis of species records. Polar Biol 40, 1247–1260 (2017). https://doi.org/10.1007/s00300-016-2049-0
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DOI: https://doi.org/10.1007/s00300-016-2049-0