Journal of Plankton Research plankt.oxfordjournals.org J. Plankton Res. (2013) 35(5): 939–956. First published online June 4, 2013 doi:10.1093/plankt/fbt056 Relationships between phytoplankton Downloaded from thin layers and the fine-scale vertical Featured Article distributions of two trophic levels of zooplankton http://plankt.oxfordjournals.org/ ADAM T.GREER1*, ROBERT K. COWEN1, CEDRIC M. GUIGAND1, MARGARETA. MCMANUS2, JEFF C. SEVADJIAN2 AND AMANDA H.V.TIMMERMAN2 1 ROSENSTIEL SCHOOL OF MARINE AND ATMOSPHERIC SCIENCE, MARINE BIOLOGY AND FISHERIES, UNIVERSITY OF MIAMI, 4600 RICKERBACKER CSWY, MIAMI, 2 FL 33149, USA AND DEPARTMENT OF OCEANOGRAPHY, UNIVERSITY OF HAWAII AT MANOA, 1000 POPE ROAD, HONOLULU, HI 96822, USA *CORRESPONDING AUTHOR: [email protected] by guest on August 28, 2013 Received February 19, 2013; accepted May 9, 2013 Corresponding editor: Roger Harris 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 simultan- eously 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 chlorophyll- a 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. available online at www.plankt.oxfordjournals.org # The Author 2013. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH VOLUME 35 NUMBER 5 PAGES 939–956 2013 j j j j KEYWORDS: plankton imaging; thin layers; ctenophores; copepods; appendicularians INTRODUCTION et al., 2005), thus their association with thin layers and Thin layers are dense aggregations of phytoplankton or grazers was not known prior to the present study. zooplankton spanning a few centimeters to meters in Although gelatinous zooplankton are known to aggre- depth and sometimes several kilometers horizontally gate within temperature discontinuities (Arai, 1976; (Dekshenieks et al., 2001; McManus et al., 2003). The Graham et al., 2001), field studies relating gelatinous zoo- concentrations of organisms within thin layers can be plankton distributions to the well-understood physical orders of magnitude greater than above or below the processes of thin layer formation are limited. The frontal layer (Donaghay et al., 1992), and persist on time scales of zone at the edge of the upwelling shadow has been impli- hours to days depending upon physical, chemical and cated as a retention mechanism for the large (30 cm bell biological conditions (Sullivan et al., 2010). Thin layers diameter) scyphomedusa Chrysaora fuscescens, with highest are of interest ecologically because they may serve as concentrations located near the thermocline (Graham, Downloaded from zones of enhanced biological interactions in the vertical 1993). Hydromedusae have been found to be abundant dimension (Alldredge et al., 2002), much like fronts do in in Monterey Bay (Raskoff, 2002) and consistently aggre- the horizontal, with the trophic impact of a thin layer in- gate in salinity discontinuities, regardless of whether or creasing in relation to its temporal persistence (Cowles not prey is present indicating that they may use physical et al., 1998). As thin layers can occur in a variety of cues to aggregate there (Frost et al., 2010). http://plankt.oxfordjournals.org/ marine systems including estuaries (Donaghay et al., In Monterey Bay, CA, USA, thin layers of phytoplank- 1992), coastal shelves (Cowles and Desiderio, 1993) and ton typically form during upwelling favorable (north- fjords (Holliday et al., 1998; Dekshenieks et al., 2001; westerly) winds when the northern (sheltered) region of Alldredge et al., 2002), they may be important con- the bay tends to be thermally stratified (Graham and tributors to community structure in shallow water Largier, 1997; McManus et al., 2008). The upwelling environments. season spans between the months of March–October Trophic interactions in relation to phytoplankton thin (Pennington and Chavez, 2000). During upwelling layers are influenced by the degree of spatial overlap events, cold, nutrient-rich filaments cross the mouth of between thin layers, grazers and zooplankton predators. the bay (Rosenfeld et al., 1994) and a cyclonic gyre, by guest on August 28, 2013 While it may seem that grazers would seek an aggregated known as the ‘upwelling shadow,’ forms in the north- food source within thin layers, several studies have pro- eastern part of the bay. When present, the upwelling duced counter-intuitive results where grazers were found shadow increases the surface water residence time in the to spend a majority of time just outside of a thin layer bay (Breaker and Broenkow, 1994; Graham and Largier, (Bochdansky and Bollens, 2004; Benoit-Bird et al., 2010; 1997). Water in the upwelling shadow is sheltered from Talapatra et al., 2013). One possible explanation for these the winds, which results in decreased mixing, and diurnal observations is that zooplankton predators (including gel- heating results in high thermal stratification (Graham, atinous zooplankton) may influence the distribution of 1993). These characteristics provide optimal conditions grazers through predation or modification of grazer be- for thin layer formation. Density discontinuities formed havior. Linking the distribution of phytoplankton, zoo- via thermal stratification may serve as a mechanism to plankton and gelatinous zooplankton aggregations is slow the sinking rate of particles, creating thin phyto- challenging due to sampling limitations. For example, the plankton layers of non-motile organisms such as diatoms relative positioning of different zooplankton taxa in rela- (MacIntyre et al., 1995; Alldredge et al., 2002). When the tion to phytoplankton thin layers is poorly described upwelling winds subside or reverse direction, i.e. ‘relax- (Holliday et al., 1998, 2003, 2010) because it is difficult or ation events,’ surface waters in the upwelling shadow impossible to distinguish acoustic returns from organisms zone are advected from the bay to the northwest within of similar acoustic impedance (typically similarly sized). 2–3 days if the event persists (Woodson et al., 2009). Further, common gelatinous zooplankton are extremely Under these conditions, California current waters, char- difficult to sample with traditional net sampling systems acterized by relatively warm temperatures, low salinity [e.g. MOCNESS (Wiebe et al., 1976)], which destroy and low nutrient concentrations (Rosenfeld et al., 1994; fragile gelatinous bodies. Gelatinous zooplankton are Ramp et al., 2005; Ryan et al., 2008, 2009), are advected also thought to have low acoustic detectability, except for towards shore to replace exiting waters, disrupting the large (.10 cm) specimens (Monger et al., 1998; Brierley stratified conditions favorable to thin layer formation. 940 A. T.GREER ET AL. THIN LAYER RELATIONSHIPS TO PRIMARY CONSUMERS AND JELLIES j To elucidate the trophic effects of phytoplankton thin Imaging system sampling layers and directly sample the gelatinous community, we The ISIIS contains a Piranha II line scan camera from deployed a towed In Situ Ichthyoplankton Imaging Dalsa with 68 mm pixel resolution, imaging plankton in System (ISIIS) (Cowen and Guigand, 2008) to synoptical- the size range of 680 mm to 13 cm. The ISIIS uses a ly sample zooplankton abundance and related environ- shadowgraph imaging technique, in which a collimated mental parameters (including chlorophyll-a fluorescence) light source is projected across a sampled parcel of water, in northern Monterey Bay. The goals of this study were and the silhouettes created by the plankton blocking the (i) to describe the environmental conditions and their re- light source are then captured by the camera (Cowen and lationship to thin layers, (ii) to relate fine scale changes in Guigand, 2008). The ISIIS line scan camera shoots a abundance of different zooplankton taxa to environmen- continuous image at 36 000 scan lines per second, but tal conditions and (iii) to compare and contrast the parses the image into frames that correspond to a 13 fine-scale vertical distributions of three distinct planktonic 13 cm area of view with a depth of field of ca. 35 cm, trophic levels (phytoplankton, primary consumers and giving an individual image volume of 6.4 L. At the usual gelatinous zooplankton), their relationship to physical tow speed (2.5 ms21), 1 m3 of water is sampled