Abstract
Frequent sampling of zooplankton is essential to understand their annual dynamics. However, in polar and subpolar ecosystems, such sampling is rare. This study comparatively analysed, for the first time, the annual mesozooplankton succession in the northwest nearshore and external zones of Ushuaia Bay in the sub-Antarctic Beagle Channel by monthly sampling over two years. The nearshore zone, with shallow waters and strong continental and anthropogenic influence, was characterised by the year-round occurrence of the euryhaline copepod Eurytemora americana and adventitious taxa. The mesozooplankton community exhibited pronounced monthly and year-to-year variability but, as a general seasonal trend, winter assemblages were dominated by the copepod Oithona similis and adventitious nematodes, whereas the spring–summer ones were dominated by E. americana, the cladoceran Podon leuckarti and Cirripedia nauplii. In the external zone, the copepods Drepanopus forcipatus and Ctenocalanus citer were found throughout the year. The annual succession showed a clearer seasonal pattern. Main shifts in community structure occurred in late winter–spring and late summer–autumn, when a high representation of meroplankton and appendicularians was closely associated with phytoplankton blooms. The higher temporal variability in the nearshore community was partially related to variable contributions of adventitious taxa to assemblage composition and may be also reflecting stressful conditions for plankton species linked to freshwater and urban discharges reported within the bay. This study allowed filling the temporal gaps in previous research and providing a more complete picture of the annual mesozooplankton dynamics in the Beagle Channel, generating hypotheses at the community and population levels for future research.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adami ML, Gordillo S (1999) Structure and dynamics of the biota associated with Macrocystis pyrifera (Phaeophyta) from the Beagle Channel, Tierra delFuego. Sci Mar 63:183–191. https://doi.org/10.3989/scimar.1999.63s1183
Aguirre GE, Capitanio FL, Lovrich GA, Esnal GB (2012) Seasonal variability of metazooplankton in coastal sub-Antarctic waters (Beagle Channel). Mar Biol Res 8:341–353. https://doi.org/10.1080/17451000.2011.627922
Almandoz GO, Hernando MP, Ferreyra GA, Schloss IR, Ferrario ME (2011) Seasonal phytoplankton dynamics in extreme southern South America (Beagle Channel, Argentina). J Sea Res 66:47–57. https://doi.org/10.1016/j.seares.2011.03.005
Amin O, Comoglio L, Spetter C, Duarte C, Asteasuain R, Freije RH, Marcovecchio J (2011) Assessment of land influence on a high-latitude marine coastal system: Tierra del Fuego, southernmost Argentina. Environ Monit Assess 175:63–73. https://doi.org/10.1007/s10661-010-1493-5
Antacli JC, Hernández D, Sabatini ME (2010) Estimating copepods' abundance with paired nets: implications of mesh size for population studies. J Sea Res 63:71–77. https://doi.org/10.1016/j.seares.2009.09.004
Antacli JC, Sabatini ME, Silva RI, Hernández DR, Jaureguizar AJ, Akselman R (2014) Feeding and reproductive activity of the copepods Drepanopus forcipatus and Calanus australis during late summer on the southern Patagonian shelf (Argentina, 47°-55° S). Braz J Oceanogr 62:295–314. https://doi.org/10.1590/s1679-87592014073406204
Arendt KE, Juul-Pedersen T, Mortensen J, Blicher ME, Rysgaard S (2013) A 5-year study of seasonal patterns in mesozooplankton community structure in a sub-Arctic fjord reveals dominance of Microsetella norvegica (Crustacea, Copepoda). J Plankton Res 35:105–120. https://doi.org/10.1093/plankt/fbs087
Avent SR (1998) Distribution of Eurytemora americana (Crustacea, Copepoda) in the Duwamish River Estuary. Report of Project results, School of Oceanography, University of Washington, Washington
Balestrini C, Manzella G, Lovrich GA (1998) Simulación de corrientes en el Canal Beagle y Bahía Ushuaia, mediante un modelo bidimensional. Servicio de Hidrografía Naval Departamento de Oceanografía Technical Report 98:1–58
Bell SS, Walters K, Hall MO (1987) Habitat utilization by harpacticoid copepods: a morphometric approach. Mar Ecol Prog Ser 35:59–64
Berasategui AA, Hoffmeyer MS, Biancalana F, Severini MF, Menendez MC (2009) Temporal variation in abundance and fecundity of the invading copepod Eurytemora americana in Bahía Blanca Estuary during an unusual year. Estuar Coast Shelf Sci 85:82–88. https://doi.org/10.1016/j.ecss.2009.03.008
Biancalana F, Torres AI (2011) Variations of mesozooplankton composition in a eutrophicated semi-enclosed system (Encerrada Bay, Tierra del Fuego, Argentina). Braz J Oceanogr 59:195–199. https://doi.org/10.1590/S1679-87592011000200008
Biancalana F, Barría de Cao MS, Hoffmeyer MS (2007) Micro and mesozooplankton composition during winter in Ushuaia and Golondrina Bays (Beagle Channel, Argentina). Braz J Oceanogr 55:83–95. https://doi.org/10.1590/S1679-87592007000200002
Biancalana F, Diodato SL, Hoffmeyer MS (2012a) Seasonal and spatial variation of mesozooplankton biomass in Ushuaia and Golondrina Bays (Beagle Channel, Argentina). Braz J Oceanogr 60:99–106. https://doi.org/10.1590/S1679-87592012000100010
Biancalana F, Menéndez MC, Berasategui AA, Fernández-Severini MD, Hoffmeyer MS (2012b) Sewage pollution effects on mesozooplankton structure in a shallow temperate estuary. Environ Monit Assess 184:3901–3913. https://doi.org/10.1007/s10661-011-2232-2
Biancalana F, Dutto MS, Berasategui AA, Kopprio G, Hoffmeyer MS (2014) Mesozooplankton assemblages and their relationship with environmental variables: a study case in a disturbed bay (Beagle Channel, Argentina). Environ Monit Assess 186:8629–8647. https://doi.org/10.1007/s10661-014-4032-y
Boltovskoy D (1981) Características biológicas del Atlántico Sudoccidental. In: Boltovskoy D (ed) Atlas del zooplancton de Atlántico Sudoccidental y métodos de trabajo con el zooplancton marino. Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Mar del Plata, pp 239–248
Breckenridge JK, Bollens SM, Rollwagen-Bollens G, Roegner GC (2015) Plankton assemblage variability in a river-dominated temperate estuary during late spring (high-flow) and late summer (low-flow) periods. Estuar Coast 38:93–103. https://doi.org/10.1007/s12237-014-9820-7
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, Plymouth
Diodato SL, Hoffmeyer MS, Biancalana F (2009) Grazing pressure of mesozooplankton under anthropogenic impact in Ushuaia Bay, Argentina. ICES Website. https://www.ices.dk/sites/pub/CM%2520Doccuments/CM-2009/P/P0909.pdf. Accessed 24 April 2020
Fernández-Severini MD, Hoffmeyer MS (2005) Mesozooplankton assemblages in two bays in the Beagle Channel (Argentina) during January 2001. Sci Mar 69:27–37. https://doi.org/10.3989/scimar.2005.69s227
Finni T, Laurila S, Laakkonen S (2001) The history of eutrophication in the sea area of Helsinki in the 20th century. Ambio 30:264–272. https://doi.org/10.1579/0044-7447-30.4.264
Freije RH, Spetter CV, Marcovecchio JE, Popovich CA, Botté SE, Negrin V, Arias A, Delucchi F, Asteasuain RO (2008) Water chemistry and nutrients of the Bahía Blanca Estuary. In: Neves R, Barretta J, Mateus M (eds) Perspectives on integrated coastal zone management in South America. IST Press, Lisbon, pp 241–254
Giesecke R, Höfer J, Vallejos T, González HE (2019) Death in southern Patagonian fjords: copepod community structure and mortality in land-and marine-terminating glacier-fjord systems. Prog Oceanogr 174:162–172. https://doi.org/10.1016/j.pocean.2018.10.011
Gil MN, Torres AI, Amin O, Esteves JL (2011) Assessment of recent sediment influence in an urban polluted subantarctic coastal ecosystem. Beagle Channel (Southern Argentina). Mar Pollut Bull 62:201–207. https://doi.org/10.1016/j.marpolbul.2010.10.004
Gislason A, Astthorsson OS (1998) Seasonal variations in biomass, abundance and composition of zooplankton in the subarctic waters north of Iceland. Polar Biol 20:85–94. https://doi.org/10.1007/s003000050280
González HE, Castro L, Daneri G, Iriarte JL, Silva N, Vargas CA, Giesecke R, Sánchez N (2011) Seasonal plankton variability in Chilean Patagonia fjords: carbon flow through the pelagic food web of Aysen Fjord and plankton dynamics in the Moraleda Channel basin. Cont Shelf Res 31:225–243. https://doi.org/10.1016/j.csr.2010.08.010
Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland Roads meso-and macrozooplankton time-series 1974 to 2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island of the North Sea. Helgol Mar Res 58:274–288. https://doi.org/10.1007/s10152-004-0191-5
Grice GD (1971) The developmental stages of Eurytemora americana Williams, 1906, and Eurytemora herdmani Thompson & Scott, 1897 (Copepoda, Calanoida) 1. Crustaceana 20:145–158. https://doi.org/10.1163/156854069X00178
Heron GA, Bowman TE (1971) Postnaupliar developmental stages of the copepod crustaceans Clausocalanus laticeps, C. brevipes, and Ctenocalanus citer (Calanoida: Pseudocalanidae). In: Llano GU, Wallen IE (eds) Biology of the Antarctic seas IV, Antarctic Research Series, vol 17. American Geophysical Union, Washington, pp 141–165
Holm-Hansen O, Riemann B (1978) Chlorophyll-a determination: improvements in methodology. Oikos 30:438–447. https://doi.org/10.2307/3543338
Howe JA, Austin WEN, Forwick M, Paetzel M, Harland R, Cage AG (2010) Fjord systems and archives: a review. In: Howe JA, Austin WEN, Forwick M, Paetzel M (eds) Fjord systems and archives. The Geological Society, London, pp 5–17
Hulsemann K (1991) The copepodid stages of Drepanopus forcipatus Giesbrecht, with notes on the genus and a comparison with others members of the family Clausocalanidae (Copepoda Calanoida). Helgol Meeresunters 45:199–224. https://doi.org/10.1007/BF02365642
Isinibilir M, Kideys AE, Tarkan AN, Yilmaz IN (2008) Annual cycle of zooplankton abundance and species composition in Izmit Bay (the northeastern Marmara Sea). Estuar Coast Shelf Sci 78:739–747. https://doi.org/10.1016/j.ecss.2008.02.013
Isla F, Bujalesky G, Coronato A (1999) Procesos estuarinos en el Canal Beagle, Tierra del Fuego. Rev Asoc Geol Argent 54:307–318
Ji R, Edwards M, Mackas DL, Runge JA, Thomas AC (2010) Marine plankton phenology and life history in a changing climate: current research and future directions. J Plankton Res 32:1355–1368. https://doi.org/10.1093/plankt/fbq062
Kenitz KM, Visser AW, Mariani P, Andersen KH (2017) Seasonal succession in zooplankton feeding traits reveals trophic trait coupling. Limnol Oceanogr 62:1184–1197. https://doi.org/10.1002/lno.10494
Kwasniewski S, Walkusz W, Cottier FR, Leu E (2013) Mesozooplankton dynamics in relation to food availability during spring and early summer in a high latitude glaciated fjord (Kongsfjorden), with focus on Calanus. J Mar Syst 111:83–96. https://doi.org/10.1016/j.jmarsys.2012.09.012
Landry MR, Lorenzen CJ, Peterson WK (1994) Mesozooplankton grazing in the Southern California Bight. II. Grazing impact and particulate flux. Mar Ecol Prog Ser 115:73–85
Melo XF, Martín J, Kerdel L, Bourrin F, Colloca CB, Menniti C, de Madron XD (2020) Particle dynamics in Ushuaia Bay (Tierra del Fuego)-potential effect on dissolved oxygen depletion. Water. https://doi.org/10.3390/w12020324
Mozetĭc P, Umani SF, Cataletto B, Malej A (1998) Seasonal and inter-annual plankton variability in the Gulf of Trieste (northern Adriatic). ICES J Mar Sci 55:711–722. https://doi.org/10.1006/jmsc.1998.0396
Niehoff B, Schnack-Schiel S, Cornils A, Brichta M (2002) Reproductive activity of two dominant Antarctic copepod species, Metridia gerlachei and Ctenocalanus citer, in late autumn in the eastern Bellingshausen Sea. Polar Biol 25:583–590. https://doi.org/10.1007/s00300-002-0378-7
Pachiappan P, Santhanam P, Begum A, Prasath BB (2019) An introduction to plankton. In: Santhanam P, Begum A, Pachiappan P (eds) Basic and applied phytoplankton biology. Springer, Singapore, pp 1–24
Presta ML, Capitanio FL, Hoffmeyer MS (2019) Spatio-temporal dynamics of mesozooplankton in the subantarctic Beagle Channel: The case of Ushuaia Bay (Argentina). Reg Stud Mar Sci. https://doi.org/10.1016/j.rsma.2019.100546
Primo AL, Azeiteiro UM, Marques SC, Martinho F, Pardal MÂ (2009) Changes in zooplankton diversity and distribution pattern under varying precipitation regimes in a southern temperate estuary. Estuar Coast Shelf Sci 82:341–347. https://doi.org/10.1016/j.ecss.2009.01.019
Racault M-F, Le Quéré C, Buitenhuis E, Sathyendranath S, Platt T (2012) Phytoplankton phenology in the global ocean. Ecol Indic 14:152–163. https://doi.org/10.1016/j.ecolind.2011.07.010
Sabatini M, Escribano R, Hidalgo P (2009) Mesozooplancton. In: Alder VA, Morales C (eds) Manual de métodos para el estudio de los sistemas planctónicos marinos. EUDEBA, Buenos Aires, pp 65–94
Sabatini ME, Reta R, Lutz VA, Segura V, Daponte C (2016) Influence of oceanographic features on the spatial and seasonal patterns of mesozooplankton in the southern Patagonian shelf (Argentina, SW Atlantic). J Mar Syst 157:20–38. https://doi.org/10.1016/j.jmarsys.2015.12.006
Siokou-Frangou I (1996) Zooplankton annual cycle in a Mediterranean coastal area. J Plankton Res 18:203–223. https://doi.org/10.1093/plankt/18.2.203
Siokou-Frangou I, Papathanassiou E (1991) Differentiation of zooplankton populations in a polluted area. Mar Ecol Prog Ser 76:41–51
Siokou-Frangou I, Shiganova T, Christou ED, Kamburska L, Gubanova A, Konsulov A, Musaeva E, Skryabin V, Khoroshilov V (2004) Mesozooplankton communities in the Aegean and Black Seas: a comparative study. Mar Biol 144:1111–1126. https://doi.org/10.1007/s00227-003-1277-3
Sommer U, Adrian R, De Senerpont DL, Elser JJ, Gaedke U, Ibelings B, Jeppesen E, Lürling M, Molinero JC, Mooij WM, van Donk E, Winder M (2012) Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst 43:429–448. https://doi.org/10.1146/annurev-ecolsys-110411-160251
Starr M, Himmelman JH, Therriault JC (1991) Coupling of nauplii release in barnacles with phytoplankton blooms: a parallel strategy to that of spawning in urchins and mussels. J Plankton Res 13:561–571. https://doi.org/10.1093/plankt/13.3.561
Steinberg DK, Landry MR (2017) Zooplankton and the ocean carbon cycle. Annu Rev Mar Sci 9:413–444. https://doi.org/10.1146/annurev-marine-010814-015924
Takahashi K, Kuwata A, Saito H, Ide K (2008) Grazing impact of the copepod community in the Oyashio region of the western subarctic Pacific Ocean. Prog Oceanogr 78:222–240. https://doi.org/10.1016/j.pocean.2008.06.002
Tommasi D, Hunt BP, Pakhomov EA, Mackas DL (2013) Mesozooplankton community seasonal succession and its drivers: Insights from a British Columbia, Canada, fjord. J Mar Syst 115:10–32. https://doi.org/10.1016/j.jmarsys.2013.01.005
Torres AI, Gil MN, Amín OA, Esteves JL (2009) Environmental characterization of a eutrophicated semi-enclosed system: nutrient budget (Encerrada Bay, Tierra del Fuego Island, Patagonia, Argentina). Water Air Soil Pollut 204:259–270. https://doi.org/10.1007/s11270-009-0042-8
Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool Stud 43:255–266
Varpe Ø (2012) Fitness and phenology: annual routines and zooplankton adaptations to seasonal cycles. J Plankton Res 34:267–276. https://doi.org/10.1093/plankt/fbr108
Viñas MD, Ramírez FC, Santos BA, Marrari M (2007) Spatial and temporal distribution patterns of Cladocera in the Argentine Sea. Hydrobiologia 594:59–68. https://doi.org/10.1007/s10750-007-9077-2
Viñas MD, Negri RM, Cepeda GD, Hernández D, Silva R, Daponte MC, Capitanio FL (2013) Seasonal succession of zooplankton in coastal waters of the Argentine Sea (Southwest Atlantic Ocean): prevalence of classical or microbial food webs. Mar Biol Res 9:371–382. https://doi.org/10.1080/17451000.2012.745003
Zervoudaki S, Nielsen TG, Carstensen J (2009) Seasonal succession and composition of the zooplankton community along an eutrophication and salinity gradient exemplified by Danish waters. J Plankton Res 31:1475–1492. https://doi.org/10.1093/plankt/fbp084
Acknowledgements
We are very grateful to Ignacio Chiesa, Cristina Daponte, Daniel Nahabedian and Sofia Dutto for helping us with the taxonomic determinations. We are indebted to the Centro Austral de Investigaciones Científicas (CADIC), Ushuaia, Argentina, and especially to the people who participated in project GEF-PNUD Arg. 2/18 “Coastal pollution prevention and management of marine biodiversity”. We would also like to thank the reviewer Dr. Danilo L. Calliari and the two anonymous reviewers for their constructive criticism and valuable suggestions that notably improved an earlier version of this manuscript. This study was partially supported by PIP CONICET 2012–2014 grant to F. Capitanio. M. L. Presta was funded by a doctoral fellowship of the Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Presta, M.L., Hoffmeyer, M.S. & Capitanio, F.L. Mesozooplankton succession in a sub-Antarctic bay (Beagle channel, Southern tip of South America): distinctive annual patterns between two environmentally different zones. Polar Biol 43, 1175–1191 (2020). https://doi.org/10.1007/s00300-020-02698-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-020-02698-z