Spatial structuring of zooplankton communities through partitioning of habitat and resources in the Bay of Bengal during spring intermonsoon
Despite advances in oceanographic investigations in the Indian Ocean, zooplankton ecology is still poorly known from the open waters of the Bay of Bengal. In order to understand the vertical and horizontal distribution of zooplankton in the Bay of Bengal during spring intermonsoon, stratified sampling was conducted using a multiple plankton net. We found that higher zooplankton biomass was often associated with mesoscale cold-core eddies. The biomass in the mixed layer was less in the central bay and the near absence of organisms beneath this layer was attributed to the very low dissolved oxygen levels, including suboxia in the northern extent. The copepod diversity was severely reduced here and only a few species specialized to thrive in minimum oxygen concentrations were found in this zone. However, Pleuromamma indica is another copepod that seems to have adapted to the oxygen minimum zone, as seen from its increased numbers and its strong vertical migrating ability to cross the low oxygen barrier. Highly diverse copepod assemblages comprising 129 identified species were found to be vertically structured, mostly through partitioning of habitat and food resources.
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- Acuna JL, Deibel D, Saunders PA, Booth B, Hatfield E, Klein
B, Mei ZP, Rivkin RB (2002). Phytoplankton ingestion by
appendicularians in the North Water. Deep-Sea Res II 49:
5101-5115.
- Auel H, Verheye HM (2007). Hypoxia tolerance in the copepod
Calanoides carinatus
and the effect of an intermediate oxygen
minimum layer on copepod vertical distribution in the
northern Benguela Current upwelling system and the Angola-
Benguela Front
.
J Exp Mar Biol Ecol 352: 234-243.
- Banse K (1964). On the vertical distribution of zooplankton in the
sea. Prog Oceanogr 2: 53-125.
- Beckmann W, Auras A, Hemleben Ch (1987). Cyclonic cold-core
eddy in the eastern North Atlantic. 111. Zooplankton. Mar
Ecol Prog Ser 39: 65-173.
- Boxshall GA (1985). The comparative anatomy of two copepods,
a predatory calanoid and a particle-feeding mormonilloid.
Philos T R Soc B 311: 303-377.
- Boyd SH, Ortner PB, Cox JL (1976). Gulf Stream cold core rings:
large-scale interaction sites for open ocean plankton
communities. Deep-Sea Res 23: 685-710.
- Briggs JC (1974). Marine Zoogeography. New York, NY, USA:
McGraw-Hill.
- Brodeur RD, Sugisaki H, Hunt GL (2002). Increases in jellyfish
biomass in the Bering Sea: implications for the ecosystem. Mar
Ecol Prog Ser 233: 89-103.
- Cass CJ (2011). A comparative study of eucalanoid copepods residing
in different oxygen environments in the Eastern Tropical North
Pacific: an emphasis on physiology and biochemistry. Tampa,
FL, USA: University of South Florida.
- Cass CJ, Daly KL (2014). Eucalanoid copepod metabolic rates in the
oxygen minimum zone of the eastern tropical North Pacific:
effects of oxygen and temperature. Deep-Sea Res I 94: 137–149.
- Cass CJ, Daly KL, Wakeham SG (2014). Assessment of storage lipid
accumulation patterns in eucalanoid copepods from the eastern
tropical Pacific Ocean. Deep-Sea Res I 93: 117-130.
- Checkley DM Jr (1980). Food limitation of egg production by a marine
planktonic copepod in the sea off southern California. Limnol
Oceanogr 25: 991-998.
- Childress JJ, Seibel BA (1998). Life at stable low oxygen levels:
adaptations of animals to oceanic oxygen minimum layers. J Exp
Biol 201: 1223-1232.
- Clarke KR, Warwick RM (2001). Change in Marine Communities:
An Approach to Statistical Analysis and Interpretation, 2nd ed.
Plymouth, UK: PRIMER-E.
- Conover RJ, Lalli CM (1972). Feeding and growth in
Clione limacina
(Phipps), a pteropod mollusc. J Exp Mar Biol Ecol 9: 279-302.
- Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences
for marine ecosystems. Science 321: 926-929.
- Ekau W, Auel H, Portner HO, Gilbert D (2010). Impacts of hypoxia
on the structure and processes in pelagic communities
(zooplankton, macro-invertebrates and fish). Biogeosciences 7:
1669-1699.
- Escribano R, Hidalgo P, Krautz C (2009). Zooplankton associated with
the oxygen minimum zone system in the northern upwelling
region of Chile during March 2000. Deep-Sea Res II 56: 1049-
1060.
- Falkowski PG, Ziemann D, Kolber Z, Bienfang PK (1991). Role of
eddy pumping in enhancing primary production in the ocean.
Nature 352: 55-58.
- Fernandes V (2008). The effect of semi-permanent eddies on the
distribution of mesozooplankton in the central Bay of Bengal.
J Mar Res 66: 465-488.
- Fernandes V, Ramaiah N (2009). Mesozooplankton community in
the Bay of Bengal (India): spatial variability during the summer
monsoon. Aquat Ecol
43: 951-963.
- Fernandes V, Ramaiah N (2013). Mesozooplankton community
structure in the upper 1,000 m along the western Bay of Bengal
during the 2002 fall intermonsoon. Zool Stud 52: 31.
- Fogg GE, Egan B, Floodgate GD, Jones DA, Kassab JY, Lochte K, Rees
EIS, Scrope-Howe S, Turley CM (1985). Biological studies in
the vicinity of a shallow sea tidal mixing front. VII. The frontal
ecosystems. Philos T R Soc B 310: 555-571.
- Frost BW (1972. Effects of size and concentration of food particles
on the feeding behaviour of the marine planktonic copepod
Calanus pacificus
. Limnol Oceanogr 17: 805-815.
- Frost BW, Fleminger A (1968). A revision of the genus
Clausocalanus
(Copepoda: Calanoida) with remarks on distributional patterns
in diagnostic characters. Bull Scripps Inst Oceanogr 12: 1-235.
- Gonzalez RR, Quinones RA (2002).
Ldh
activity in Euphausia
mucronata and
Calanus chilensis
: implications for vertical
migration behaviour. J Plankton Res 24: 1349-1356.
- Gooday AJ, Levin LA, Aranda da Silva A, Bett BJ, Cowie GL,
Dissard D, Gage JD, Hughes DJ, Jeffreys R, Lamont PA et al
(2009). Faunal response to oxygen gradients on the Pakistan
Margin: a comparison of foraminiferans, macrofauna and
megafauna. Deep Sea Res II 56: 488-502.
- Goswami SC, Gajbhiye SN, Padmavati G (1992). Distribution of
Pleuromamma
(Copepoda: Metridinidae) along a north-south
transect in the Indian Ocean. In:
Desai BN, editor. Oceanography
of the Indian Ocean. Oxford, UK: IBH, pp. 159-166.
- Grasshoff K, Ehrhardt M, Kremling K (1983). Methods of Seawater
Analysis. Second Revised, Extended Edition. Weinheim,
Germany: Verlag Chemie.
- Harris RP, Wiebe P, Lenz J, Skjoldal HR, Huntley M (2000). ICES
Zooplankton Methodology Manual.
San Diego, CA, USA:
Academic Press.
- Hulsizer EE (1976). Zooplankton of lower Narragansett Bay, 1972-
1973. Ches Sci 17: 260-270.
- Huntley ME, Zhou M, Nordhausen W (1995). Mesoscale distribution
of zooplankton in the California Current in late spring, observed
by optical plankton counter. J Mar Res 53: 647-674.
- Ishii H, Tanaka F (2001). Food and feeding of
Aurelia aurita
in Tokyo
Bay with an analysis of stomach contents and a measurement of
digestion times. Hydrobiologia 451: 311-320.
- Jagadeesan L, Jyothibabu R, Anjusha A, Mohan AP, Madhu NV,
Muraleedharan KR, Sudheesh K (2013). Ocean currents
structuring the mesozooplankton in the Gulf of Mannar and the
Palk Bay, southeast coast of India. Prog Oceanogr 110: 27-48.
- Jyothibabu R, Madhu NV, Maheswaran PA, Jayalakshmya KV,
Nair KKC, Achuthankutty CT (2008). Seasonal variation of
microzooplankton (20–200 mm) and its possible implications
on the vertical carbon flux in the western Bay of Bengal. Cont
Shelf Res 28: 737-755.
- Jyothibabu R, Maheswaran PA, Madhu NV, Mohammed Ashraf TT,
Gerson VJ, Haridas PC, Venugopal P, Revichandran C, Nair
KKC, Gopalakrishnan TC (2004). Differential response of
winter cooling on biological production in the northeastern
Arabian Sea and northwestern Bay of Bengal. Curr Sci 87: 783-
791.
- Karati KK, Vineetha G, Raveendran TV, Muraleedharan KR,
Achuthankutty CT (2017). Plankton and the invisible barriers in
the tropical ocean. J Aquac Mar Biol 6: 00162.
- Karati KK, Vineetha G, Raveendran TV, Muraleedharan KR,
Habeebrehman H, Philson KP, Achuthankutty CT (2018).
River plume fronts and their implications for the biological
production of the Bay of Bengal, Indian Ocean. Mar Ecol Prog
Ser 597: 79-98.
- Kasturirangan LR (1963). A Key for the Identification of the More
Common Planktonic Copepoda of Indian Coastal Waters. New
Delhi, India: Indian National Committee on Oceanic Research,
Council of Scientific and Industrial Research.
- Lampitt RS, Gamble JC (1982). Diet and respiration of the small
planktonic marine copepod
Oithona nana.
Mar Biol 66: 185-
190.
- Li K, Yin J, Huang L, Tan Y, Lin Q (2017). A comparison of the
zooplankton community in the Bay of Bengal and South China
Sea during April-May, 2010. J Ocean U China 16: 1206-1212.
- Loick N, Ekau W, Verheye HM (2005). Water body preferences of
dominant calanoid copepod species in the Angola-Benguela
frontal zone. Afr J Mar Sci 27: 597-608.
- Longhurst AR (1976). Interactions between zooplankton and
phytoplankton profiles in the eastern tropical Pacific Ocean.
Deep-Sea Res 23: 729-775.
- Longhurst AR (2007). Ecological Geography of the Sea. London, UK:
Academic Press.
- Maas AE, Frazar SL, Outram DM, Seibel BA, Wishner KF (2014). Fine-
scale vertical distribution of macroplankton and micronekton
in the Eastern Tropical North Pacific in association with an
oxygen minimum zone. J Plankton Res 36: 1557-1575.
- Madhupratap M (1987). Status and strategy zooplankton of tropical
Indian estuaries: a review. Bull Plankton Soc Japan 34: 65-81.
- Madhupratap M, Achuthankutty CT, Nair VR (1981). Zooplankton
abundance of the Andaman Sea. Indian J Mar Sci 10: 258-261.
- Madhupratap M, Haridas P (1990). Zooplankton, especially calanoid
copepods, in the upper 1000 m off the Southeast Arabian Sea. J
Plankton Res
12: 305-321.
- Madhupratap M, Nair SRS, Haridas P, Padmavati G (1990). Response
of zooplankton to physical changes in the environment: coastal
upwelling along the central West coast of India. J Coast Res 6:
413-426.
- Madhupratap M, Nair KNV, Gopalakrishnan TC, Haridas P, Nair
KKC, Venugopal P, Gauns M (2001). Arabian Sea oceanography
and fisheries of the west coast of India. Curr Sci 81: 355-361.
- Madin LP, Horgan EF, Steinberg DK (2001). Zooplankton at the
Bermuda Atlantic Time-series Study (BATS) station: diel,
seasonal and interannual variation in biomass, 1994-1998.
Deep-Sea Res
II 48: 2063-2082.
- Marcus NH, Richmond C, Sedlacek C, Miller GA, Oppert C (2004).
Impact of hypoxia on the survival, egg production and
population dynamics of
Acartia tonsa
Dana. J Exp Mar Biol
Ecol
301: 111-128.
- McGowan JA (1990). Species dominance-diversity patterns in
oceanic communities. In: Woodwell GM, editor. The Earth in
Transition. New York, NY, USA: Cambridge University Press,
pp. 395-421.
- Miyashita LK, de Melo JM, Lopes RM (2009). Estuarine and oceanic
influences on copepod abundance and production of a
subtropical coastal area. J Plankton Res 31: 815-826.
- Moodley L, Van der Zwaan GJ, Herman PMJ, Kempers L,Van Breugel
P (1997).
- Differential response of benthic meiofauna to anoxia with special
reference to foraminifera (Protista: Sarcodina). Mar Ecol Prog
Ser 158: 151-163.
- Mukherjee J, Naidu SA, Sarma VVS S, Ghosh T (2018). Influence of
river discharge on zooplankton diet in the Godavari estuary
(Bay of Bengal, Indian Ocean). Adv Oceanogr Limnol 9: 1-12.
- Nakamura Y, Turner JT (1997). Predation and respiration by the
small cyclopoid copepod
Oithona similis
: how important is
feeding on ciliates and heterotrophic flagellates? J Plankton Res
19: 1275-1288.
- Nuncio M, Prasanna Kumar S (2012). Life cycle of eddies along the
western boundary of the Bay of Bengal and their implications.
J Mar Syst 94: 9–17.
- Omori M, Ishii H, Fujinaga AI (1995). Life history strategy of
Aurelia aurita
(Cnidaria, Scyphomedusae) and its impact on
the zooplankton community of Tokyo Bay. ICES
J Mar Sci 52:
597-603.
- Padmavati G, Haridas P, Nair KKC, Gopalakrishnan TC,
Shiney P, Madhupratap M (1998). Vertical distribution of
mesozooplankton in the central and eastern Arabian Sea
during the winter monsoon. J Plankton Res 20: 343-354.
- Paffenhöfer GA (1993). On the ecology of marine cyclopoid
copepods (Crustacea, Copepoda). J Plankton Res 15: 37-55.
- Paffenhöfer GA, Mazzocchi MG (2003). Vertical distribution of
subtropical epiplanktonic copepods. J Plankton Res 25: 1139-
1156.
- Panikkar NK, Rao TSS (1973). Zooplankton Investigation in Indian
Waters and the Role of the Indian Ocean Biological Centre.
Handbook to the International Zooplankton Collections
Volume V. Cochin, India: National Institute of Oceanography.
- Parker-Stetter SL, Horne JK (2009). Nekton distribution and
midwater hypoxia: a diel, seasonal prey refuge? Est Coast Shelf
Sci 81: 13-18.
- Paul JT, Ramaiah N, Sardessai S (2008). Nutrient regimes and their
effect on distribution of phytoplankton in the Bay of Bengal.
Mar Environ Res 66: 337-344.
- Pielou EC (1977). Mathematical Ecology. New York, NY, USA: Wiley.
Piontkovski SA, Landry MR, Finenko ZZ, Kovalev AV, Williams
R, Gallienne CP, Mishonov AV, Skryabin VA, Tokarev YN,
Nikolsky VN (2003). Plankton communities of the South
Atlantic anticyclonic gyre. Oceanol Acta 26: 255-268.
- Piontkovski SA, Williams R, Melnik TA (1995). Spatial heterogeneity,
biomass and size structure of plankton of the Indian Ocean:
some general trends. Mar Ecol Prog Ser 117: 219-227.
- Piontkovski SA, Williams R, Peterson W, Kosnirev VK (1995).
Relationship between oceanic mesozooplankton and energy of
eddy fields. Mar Ecol Prog Ser 128: 35-41.
- Poulet SA, Oullet G (1982). The role of amino acids in the
chemosensory swarming and feeding of marine copepods. J
Plankton Res 4: 341-361.
- Prasanna Kumar S, Nuncio M, Narvekar J, Kumar A, Sardessai S,
DeSouza SN, Gauns M, Ramaiah N, Madhupratap M (2004).
Are eddies nature’s trigger to enhance biological productivity
in the Bay of Bengal? Geophys Res Lett 31: L07309.
- Prasanna Kumar, S, Nuncio M, Narvekar J, Ramaiah N, Sardessai S,
Gauns M, Fernandes V, Paul JT, Jyothibabu R, Jayraj KA (2010).
Seasonal cycle of physical forcing and biological response in
the Bay of Bengal. Indian J Mar Sci 39: 388-405.
- Prasanna Kumar S, Nuncio M, Ramaiah N, Sardessai S, Narvekar
J, Fernandes V, Paul JT (2007). Eddy-mediated biological
productivity in the Bay of Bengal during fall and spring
intermonsoons. Deep-Sea Res I 54: 1619-1640.
- Ramaiah N, Fernandes V, Paul JT, Jyothibabu R, Gauns M, Jayraj
KA (2010). Seasonal variability in biological carbon biomass
standing stocks and production in the surface layers of the Bay
of Bengal. Indian J Mar Sci 39: 369-379.
- Riandey V, Champalbert G, Carlottia F, Taupier-Letage I, Thibault-
Bothac D (2005). Zooplankton distribution related to the
hydrodynamic features in the Algerian Basin (western
Mediterranean Sea) in summer 1997. Deep-Sea Res I 52: 2029-
2048.
- Roff JC, Turner JT, Webber MK, Hoppcroft RR (1995). Bacterivory
by tropical copepod nauplii: extent and possible significance.
Aquat Microb Ecol 9: 165-175.
- Roman MR, Dam HG, Gauzens AL, Urban-Rich, J, Foley DG, Dickey
TD (1995). Zooplankton variability on the equator at 140ºW
during the JGOFS EqPac study. Deep-Sea Res II 42: 673-693.
- Roy K, Jablonski D, Valentine JW, Rosenberg G (1998). Marine
latitudinal diversity gradients: tests of causal hypotheses. P Natl
Acad Sci USA 95: 3699-3702.
- Rutherford S, D’Hondt S, Prell W (1999). Environmental controls on
the geographic distribution of zooplankton diversity. Nature
400: 749-753.
- Saltzman J, Wishner KF (1997). Zooplankton ecology in the eastern
tropical Pacific oxygen minimum zone above a seamount: 2.
Vertical distribution of copepods. Deep-Sea Res 44: 931-954.
- Saraswathy M (1986). Pleuromamma (Copepoda-Calanoida) in the
Indian Ocean. Mahasagar Bulletin of the National Institute of
Oceanography 19: 185-201.
- Saraswathy M, Iyer H (1986). Ecology of
Pleuromamma indica
Wolfenden (Copepoda-Calanoida) in the Indian Ocean.
Indian J Mar Sci
15: 219-222.
- Sen Gupta R, Naqvi SWA (1984). Chemical oceanography of the
Indian Ocean, north of the equator, Deep-Sea Res 31: 671-706.
- Smith SL (1998). 1994–1996 Arabian Sea Expedition: Oceanic
response to monsoonal forcing Part 1. Deep-Sea Res II
45:1905-2501.
- Spindler M, Hemleben C, Salomons J, Smit L (1984). Feeding
behavior of some planktonic foraminiferas in laboratory
cultures. J Foramin Res 14: 1-3.
- Steinberg DK, Silver MW (1994). Midwater zooplankton
communities on pelagic detritus (giant larvacean houses) in
Monterey Bay, California. Limnol Oceanogr 39: 1606-1620.
- Stephen R (1988). Oncaeidae (Copepoda: Poecilostomatoida) in the
Indian Ocean with comments on the species of
Lubbockia
and
Conaea
. Mahasagar 21: 35-43.
- Stephen R, Saraladevi K, Meenakshikunjamma PP, Gopalakrishnan
TC, Saraswathy M (1992). Calanoid copepods of the
International Indian Ocean Expedition collections. In: Desai
BN, editor. Oceanography of the Indian Ocean. Oxford, UK:
IBH Publishing Company, pp. 143-156.
- Tanaka O (1956). The Pelagic Copepods of the Izu Region,
Middle Japan. Systematic Account I. Families Calanidae
and Eucalanidae. Publications of the Seto Marine Biological
Laboratory, Volume V (2). Shirahama, Japan: Seto Marine
Biological Laboratory.
- Terazaki M (1996). Vertical distribution of pelagic chaetognaths and
feeding of
Sagitta enflata
in the Central Equatorial Pacific. J
Plankton Res 18: 673-682.
- Turner JT (2004). The importance of small planktonic copepods and
their roles in pelagic marine food webs. Zool Stud
43: 255-266.
- UNESCO (1968). Zooplankton Sampling. Monographs on
Oceanographic Methodology. Paris, France: UNESCO.
- UNESCO (1994). Protocols for the Joint Global Ocean Flux Study
(JGOFS). Manual and Guides 29. Paris, France: UNESCO.
- Vaillancourt RD, Marra J, Barber
RT, Smith WO Jr. (2003). Primary
productivity and in situ quantum yields in the Ross Sea and
Pacific Sector of the Antarctic Circumpolar Current. Deep-Sea
Res II 50: 559-578.
- Vinogradov ME (1997). Some problems of vertical distribution of
meso- and macroplankton in the ocean. Adv Mar Biol
32: 1-92.
- Vinogradov ME, Voronina NM (1962). The influence of oxygen
deficit upon the plankton distribution in the Arabian Sea.
Okeanologiat 1: 670-678 (in Russian).
- Wiebe PH (1976). The biology of cold-core rings. Oceanus
19: 69-76.
- Wishner KF, Gelfman C, Gowing MM, Outram DM, Rapien M,
Williams RL (2008). Vertical zonation and distributions of
calanoid copepods through the lower oxycline of the Arabian
Sea oxygen minimum zone. Prog Oceanogr 78: 163-191.
- Woodd-Walker RS, Ward P, Clarke A (2002). Large-scale patterns in
diversity and community structure of surface water copepods
from the Atlantic Ocean. Mar Ecol Prog Ser 236: 189-203.
- Wyrtki K (1971). Oceanographic Atlas of the International Indian
Ocean Expedition. Alexandria, VA, USA: National Science
Foundation.