Relationships between phytoplankton thin layers and the fine-scale vertical distributions of two trophic levels of zooplankton

Thin layers of phytoplankton are well documented, common features in coastal areas globally, but little is known about the relationships of these layers to higher trophic levels. We deployed the In Situ Ichthyoplankton Imaging System (ISIIS) to simultaneously quantify the three trophic levels of plankton, including phytoplankton, primary consumers (copepods and appendicularians) and secondary consumers (gelatinous zooplankton). Over a 2-week sampling period, phytoplankton thin layers, primarily composed of Pseudo-nitzschia spp., were common on two of the five sampling days. Imagery showed copepods aggregating in zones of lower chlorophyll-a fluorescence, while appendicularians were more common at greater depths and higher chlorophylla levels. All gelatinous zooplankton generally increased in abundance with depth. Bolinopsis spp. ctenophores underwent a ‘bloom,’ and they were the only species observed to aggregate within phytoplankton thin layers. The vertical separation between copepods, phytoplankton and gelatinous zooplankton suggests that copepods may use the surface waters as a predation refuge, only performing short migrations into favorable feeding zones where gelatinous predators are much more abundant. Thin layers containing dense diatom aggregates obstruct light reaching deeper waters (.10 m), which may allow gelatinous zooplankton to avoid visual predation as well as improve the effectiveness of contact predation with copepod prey.

[1]  M. Walter,et al.  Growth, food, and vulnerability to damage of the ctenophore Mnemiopsis mccradyi in its early life history stages , 1981 .

[2]  Piotr Dawidowicz,et al.  Vertical migration of Chaoborus larvae is induced by the presence of fish , 1990 .

[3]  Mary-Elena Carr,et al.  SMALL-SCALE PLANKTONIC STRUCTURE: PERSISTENCE AND TROPHIC CONSEQUENCES , 1998 .

[4]  Ph Wiebe,et al.  A multiple opening/Closing net and environment sensing system for sampling zooplankton , 1976 .

[5]  A. Herman.  Vertical distribution patterns of copepods, chlorophyll, and production in northeastern Baffin Bay , 1983 .

[6]  J. Link,et al.  Widespread and persistent increase of Ctenophora in the continental shelf ecosystem off NE USA , 2006 .

[7]  B. Monger,et al.  Foraging Behavior and Prey Selection by the Ambush Entangling Predator Pleurobrachia Bachei , 1986 .

[8]  E. Berdalet,et al.  Harmful algal blooms in stratified systems , 2014 .

[9]  G. Hays,et al.  Individual variability in diel vertical migration of a marine copepod: Why some individuals remain at depth when others migrate , 2001 .

[10]  Francisco P. Chavez,et al.  Seasonal fluctuations of temperature, salinity, nitrate, chlorophyll and primary production at station H3/M1 over 1989-1996 in Monterey Bay, California , 2000 .

[11]  J. Purcell.  A review of cnidarians and ctenophores feeding on competitors in the plankton , 1991, Hydrobiologia.

[12]  P. Donaghay,et al.  Thin layers and species-specific characterization of the phytoplankton community in Monterey Bay, California, USA. , 2010 .

[13]  J. Largier,et al.  Upwelling shadows as nearshore retention sites: the example of northern Monterey Bay , 1997 .

[14]  Michael S. Twardowski,et al.  Temporal and spatial occurrence of thin phytoplankton layers in relation to physical processes , 2001 .

[15]  L. C. Breaker,et al.  The circulation of Monterey Bay and related processes , 1989 .

[16]  James M. Sullivan,et al.  Occurrence and mechanisms of formation of a dramatic thin layer of marine snow in a shallow Pacific fjord , 2002 .

[17]  T. F. Hansen,et al.  Annual assessment of the predation of Mnemiopsis leidyi in a new invaded environment, the Kiel Fjord (Western Baltic Sea): a matter of concern? , 2009 .

[18]  T. Toda,et al.  Direct observations of a dense occurrence of Bolinopsis infundibulum (Ctenophora) near the seafloor under the Oyashio and notes on their feeding behavior , 2003 .

[19]  Percy L. Donaghay,et al.  Acoustic scattering in the coastal ocean at Monterey Bay, CA, USA: Fine-scale vertical structures , 2010 .

[20]  C. Oviatt,et al.  Predation on the ctenophore,Mnemiopsis leidyi, by butterfish,Peprilus triacanthus, in Narragansett Bay, Rhode Island , 1977 .

[21]  D. Holliday,et al.  Acoustical Sensing of Small-Scale Vertical Structures in Zooplankton Assemblages , 1998 .

[22]  James M. Sullivan,et al.  Coastal thin layer dynamics: Consequences to biology and optics , 2010 .

[23]  Mark A. Moline,et al.  Integrated measurements of acoustical and optical thin layers I: Vertical scales of association , 2010 .

[24]  R. Harris,et al.  Temperature effects on Calanus helgolandicus (Copepoda: Calanoida) development time and egg production , 2008 .

[25]  M. Norrbin,et al.  Fine-scale layer of hydromedusae is revealed by video plankton recorder (VPR) in a semi-enclosed bay in northern Norway , 2009 .

[26]  D. L. Aksnes,et al.  Predation efficiency in visual and tactile zooplanktivores , 2004 .

[27]  J. Costello,et al.  Seasonal refugia, shoreward thermal amplification, and metapopulation dynamics of the ctenophore Mnemiopsis leidyi in Narragansett Bay, Rhode Island , 2006 .

[28]  M. Silver,et al.  Effect of dissolved domoic acid on the grazing rate of krill Euphausia pacifica , 2006 .

[29]  R. Kudela,et al.  Hidden thin layers of toxic diatoms in a coastal bay , 2014 .

[30]  M. McManus,et al.  Physical and biological controls on the maintenance and dissipation of a thin phytoplankton layer , 2009 .

[31]  A review of cnidarians and ctenophores feeding on competitors in the plankton , 1991 .

[32]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[33]  K. A. Raskoff.  Foraging, prey capture, and gut contents of the mesopelagic narcomedusa Solmissus spp. (Cnidaria: Hydrozoa) , 2002 .

[34]  James M. Sullivan,et al.  Advances in defining fine- and micro-scale pattern in marine plankton , 2003 .

[35]  A. Leising,et al.  SIMULTANEOUS IMAGING ZOOPLANKTON OF PHYTOPLANKTON DISTRIBUTIONS AND By , 2007 .

[36]  T. Cowles,et al.  Resolution of Biological Microstructure Through In Situ Fluorescence Emission Spectra: An Oceanographic Application Using Optical Fibers , 1993 .

[37]  Claudia E. Mills,et al.  Pacific Coast Pelagic Invertebrates: A Guide to the Common Gelatinous Animals , 1998 .

[38]  Jiarong Hong,et al.  Characterization of biophysical interactions in the water column using in situ digital holography , 2013 .

[39]  W. E. Neill.  Induced vertical migration in copepods as a defence against invertebrate predation , 1990, Nature.

[40]  R. Cowen,et al.  In situ ichthyoplankton imaging system (ISIIS): system design and preliminary results , 2008 .

[41]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[42]  M. Youngbluth,et al.  Behavior of Nemopsis bachei L. Agassiz, 1849 medusae in the presence of physical gradients and biological thin layers , 2010, Hydrobiologia.

[43]  C. Storlazzi,et al.  Effects of physical processes on structure and transport of thin zooplankton layers in the coastal ocean , 2005 .

[44]  Peter H. Wiebe,et al.  Sound scattering by the gelatinous zooplankters Aequorea victoria and Pleurobrachia bachei , 1998 .

[45]  Rachel M. Jeffreys,et al.  Deep-Sea Research II , 2008 .

[46]  G. Mackie.  Coelenterate Ecology and Behavior , 1976, Springer US.

[47]  C. Williamson,et al.  Estimating predation risk in zooplankton communities: the importance of vertical overlap , 1990, Hydrobiologia.

[48]  A. Brierley,et al.  Towards the acoustic estimation of jellyfish abundance , 2005 .

[49]  T. Ikeda,et al.  Laboratory studies of ingestion and food utilization in lobate and tentaculate ctenophores 1 , 1978 .

[50]  L. Baker,et al.  Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity , 1974 .

[51]  S. Bollens,et al.  Relevant scales in zooplankton ecology: Distribution, feeding, and reproduction of the copepod Acartia hudsonica in response to thin layers of the diatom Skeletonema costatum , 2004 .

[52]  Franklin B. Schwing,et al.  Bifurcated flow from an upwelling center: a cold water source for Monterey Bay , 1994 .

[53]  S. Bates,et al.  Feeding, egg production, and egg hatching success of the copepods Acartia tonsa and Temora longicornis on diets of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia pungens , 2001, Hydrobiologia.

[54]  John P. Ryan,et al.  Phytoplankton thin layers caused by shear in frontal zones of a coastal upwelling system , 2008 .

[55]  Francisco P. Chavez,et al.  Observations of upwelling and relaxation events in the northern Monterey Bay during August 2000 , 2005 .

[56]  Feeding, egg production, and egg hatching success of the copepods Acartia tonsa and Temora longicornis on diets of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia pungens , 2001 .

[57]  M. Reeve.  POPULATION DYNAMICS OF CTENOPHORES IN LARGE SCALE ENCLOSURES OVER SEVERAL YEARS , 1980 .

[58]  Torkel Gissel Nielsen,et al.  Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community , 1990 .

[59]  W. M. Graham.  Spatio-temporal scale assessment of an “upwelling shadow” in Northern Monterey Bay, California , 1993 .

[60]  S. MacIntyre,et al.  Accumulation of marines now at density discontinuities in the water column , 1995 .

[61]  William M. Hamner,et al.  A physical context for gelatinous zooplankton aggregations: a review , 2001 .

[62]  Aaron M. Ellison,et al.  A Primer of Ecological Statistics , 2004 .

[63]  Claudia E. Mills,et al.  DENSITY IS ALTERED IN HYDROMEDUSAE AND CTENOPHORES IN RESPONSE TO CHANGES IN SALINITY , 1984 .

[64]  Scale-Dependent Dispersion within the Stratified Interior on the Shelf of Northern Monterey Bay , 2014 .

[65]  John P. Ryan,et al.  Northern Monterey Bay upwelling shadow front : observations of a coastally and surface-trapped buoyant plume , 2009 .

[66]  W. Greve.  Cultivation experiments on North Sea ctenophores , 1970, Helgoländer wissenschaftliche Meeresuntersuchungen.

[67]  M. Arai,et al.  Behaviour of Planktonic Coelenterates in Temperature and Salinity Discontinuity Layers , 1976 .

[68]  R. Kudela,et al.  Cryptic Blooms: Are Thin Layers the Missing Connection? , 2008 .

[69]  J. S. Suffern,et al.  Vertical migration in zooplankton as a predator avoidance mechanism1 , 1976 .

[70]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[71]  David C. Smith,et al.  Characteristics, distribution and persistence of thin layers over a 48 hour period , 2003 .

[72]  Hadley Wickham,et al.  The Split-Apply-Combine Strategy for Data Analysis , 2011 .

[73]  Andrew M. Fischer,et al.  Influences of upwelling and downwelling winds on red tide bloom dynamics in Monterey Bay, California , 2009 .

[74]  Jules S. Jaffe,et al.  Simultaneous Imaging of Phytoplankton and Zooplankton Distributions , 1998 .