High-frequency observations from a deep-sea cabled observatory reveal seasonal overwintering of Neocalanus spp. in Barkley Canyon, NE Pacific: Insights into particulate organic carbon flux
Introduction
Nearly 10,000 submarine canyons exist worldwide predominantly along continental margins, covering a total area of 4.4 million square kilometers, or 1.2% of the ocean seafloor (Harris et al., 2014a). These abrupt topographic features are key to connecting shallow coastal areas with the deep-sea, channeling and transporting sediments (Oliveira et al., 2007, Puig et al., 2014), organic matter (Vetter and Dayton, 1998, Vetter and Dayton, 1999, De Leo et al., 2010, De Leo et al., 2014), marine debris (Schlining et al., 2013) and pollutants (Paull et al., 2002). Canyons can focus kinetic energy of internal tides inducing vertical mixing (Zhao et al., 2012, Aslam et al., 2018), and also trigger upwelling through the topographic steering of along-shelf currents (Klinck, 1996, Hickey, 1997, Allen and De Madron, 2009) promoting enhancement of local primary productivity (Sobarzo et al., 2001, Ryan et al., 2005) and the concentration of zooplankton biomass (Greene et al., 1988, Macquart-Moulin and Patriti, 1996, Lavoie et al., 2000). Additionally, the topographic focusing of zooplankton and micronekton biomass in submarine canyons may enhance trophic subsidies to larger predatory fish, marine mammals and seabird species (Hooker et al., 1999, Genin, 2004, Moors-Murphy, 2014). Furthermore, due to high-localized productivity in concert with extremely heterogeneous and complex seafloor habitats, high benthic biomass and biodiversity have also been reported for a range of temperate and tropical submarine canyons (Schlacher et al., 2007, McClain and Barry, 2010, De Leo et al., 2010, De Leo et al., 2012, De Leo et al., 2014, Vetter et al., 2010).
For the Canadian NE Pacific, very little information exists on biological productivity and biodiversity of both pelagic and benthic habitats within submarine canyons, despite the fact that there are at least 40 canyons cutting across the Cascadia Margin north of the Juan de Fuca Strait (48°N) and towards the northern tip of the Haida Gwaii (Queen Charlotte) Islands, at 54°N (Harris et al., 2014a, Harris et al., 2014b). Barkley Canyon is perhaps one exception, where several studies have documented high pelagic productivity (Freeland and Denman, 1982) and zooplankton biomass associated with spring-summer upwelling season (Mackas et al., 1997, Allen et al., 2001). Under such conditions, analytical models show that stretching vorticity generated above the canyon topography is strong enough to produce closed cyclonic eddies around 200 m, the depth at which the canyon rim intersects with shelf, causing even strong swimmer macrozooplankton species such as Euphausia pacifica and Thysanoessa spinifera to be trapped and transported towards the shore (Allen et al., 2001). However, even though the concentration of zooplankton is relatively well-described for waters above 250 m in Barkley Canyon, no information exists on the potential for topography-induced transport and aggregation of deep-dwelling ontogenetically migrating zooplankton species. In particular, large calanoid copepod species characteristic of outer shelf waters in the NE Pacific, such as Neocalanus plumchrus, N. cristatus and N. flemingeri, which are known to undergo strong seasonal ontogenetic vertical migration (Miller et al., 1984, Mackas et al., 1998), have been reported in high densities at the head and near the walls of Barkley Canyon (Allen et al., 2001). Populations of N. plumchrus spend late summer through fall as nonfeeding fifth-stage (C5) copepodites in deep waters ranging from 200 to 2000 m, but are mostly concentrated between 400 and 800 m (Miller et al., 1984, Miller and Clemons, 1988). From late fall to early winter, they molt to the non-feeding adult stage (C6), mate and spawn at or near the overwintering depth, and remain there until they die (Miller et al., 1984). The nonfeeding nauplii then migrate upwards arriving at sea surface as late-stage N6 nauplii or first-stage (C1) copepodites (Miller et al., 1984).
Large-grazing and ontogenetically migrating calanoid copepods are the main components of the total zooplankton biomass in the NE Pacific during spring and early summer (Goldblatt et al., 1999, Mackas and Tsuda, 1999), with N. plumchrus comprising up to half of the mesozooplankton biomass in the Alaskan Gyre region (poleward from 45°N). Ontogenetically migrating copepods feed on a variety of food items ranging from diatoms, flagellates, microzooplankton, sinking aggregates, and feces, helping to connect the grazing and microbial food webs (Dagg, 1993, Gifford, 1993, Kobari et al., 2003, Steinberg et al., 2008). Also not surprisingly, large calanoids make up a great proportion of the diets of local salmon populations (Burgner, 1991), myctophids (Kawamura and Fujii, 1988), baleen whales (Kawamura, 1982) and seabirds (Hunt et al., 1993), and can therefore be considered keystone species in the trophodynamics of the NE Pacific pelagic ecosystem (Mackas et al., 1998). Additionally, some studies have shed light on the importance of the mass ontogenetic migration of large grazing calanoid copepods to the downward carbon flux into the mesopelagic zone, often not accounted for by traditional methods for measuring particulate organic carbon (POC) flux (Bradford-Grieve et al., 2001, Kobari et al., 2003, Kobari et al., 2008a, Kobari et al., 2008b, Steinberg et al., 2008). Furthermore, particularly in Barkley Canyon, recent findings of high concentrations of zooplankton-derived lipid biomarkers in deep-sea sediments at mid canyon depths (∼800–1000 m) suggest the canyon’s seafloor is being seasonally enriched by this highly labile organic material, and serving as food for and structuring the benthic communities (Campanyà-Llovet et al., this volume).
The motivation for the present study initiated by unexpected observations of dense aggregations of large calanoid copepods at 970 m depth in Barkley Canyon, only made possible by the high-definition seafloor video cameras installed and connected through the NEPTUNE cabled observatory (Ocean Networks Canada Data Archive, 2013). Bi-hourly observations of high densities of these large-bodied copepods (∼3–8 mm in prosome length) throughout the entire month of December of 2013, suggested we were observing the nonfeeding C5s and adult C6 stages of either one, or a combination of three Neocalanus species (i.e., N. plumchrus, N. cristatus, N. flemingeri - identified not only due to the relatively large prosome size, but also to its shape), passively drifting at their overwintering depth. We therefore aimed to test the hypothesis that these observations represented peak densities reached after the onset of overwintering migration by Neocalanus spp., and further to evaluate the seasonal and interannual variability in this downward ontogenetic migration. Additionally, we addressed the potential role of Barkley Canyon’s topography in concentrating this migrant biomass. We analyzed a ∼20-month time-series of bi-hourly video imagery combined with high-frequency acoustic Doppler current profiler (ADCP) data sampled at 0.1 Hz resolution from Barkley Canyon’s node of Ocean Networks Canada’s (ONC) NEPTUNE seafloor cabled observatory. To the best of our knowledge, the high temporal resolution of these observations is unprecedented for studies dealing with the seasonal dynamics of ontogenetically migrating zooplankton. The longest and most consistent sampling of the temporal and vertical distribution of Neocalanus spp. in offshore waters of Vancouver Island (NE Pacific) comes from the Line P and La Perouse bank long-term monitoring stations (Mackas et al., 2001). However, both programs rely on limited net-tow sampling at frequencies ranging from twice to three times per year (Mackas, 1992). In addition to our three main objectives, the present study aimed to further characterize the importance of ontogenetically migrating zooplankton species as sources of POC reaching Barkley Canyon’s seafloor and promoting a strong pelagic-benthic coupling.
Section snippets
Study area
Barkley Canyon is a highly sinuous shelf-incising submarine canyon located ∼100 km offshore Vancouver Island in the NE Pacific (Fig. 1A and B). It possesses multiple head branches intersecting the continental shelf edge, all discharging in the main canyon axis around mid-slope depths of 400–600 m (Fig. 1B). Storm and along-shelf current-induced sediment resuspension events over the shelf generate strong bottom and intermediate nepheloid layer flows, which transport and redistribute sediments
Barkley canyon current dynamics
Barkley Canyon exerts significant influence on the dynamics of the near bottom oceanic currents at our study site, BCA. These currents are aligned with the orientation of the local segment of the canyon thalweg (North–South) with the low-frequency non-tidal component directed downslope towards the south (Fig. 4A; also refer to map in Fig. 1C). This location is significantly removed from the canyon walls (>300 m) and other topography such that we expect it to be representative of flow along the
Temporal variability of Neocalanus spp. ontogenetic migration
Our study reports on an unprecedented high-resolution data time-series witnessing the seasonal timing and between year variability of the ontogenetic vertical migration of Neocalanus spp., a key mesozooplankton genus in the trophic dynamics, ecosystem function and carbon export into the mesopelagic zone of the subarctic NE Pacific (Mackas, 1992, Mackas et al., 1998, Mackas et al., 2001; Bradford-Grieve et al., 2001). The use of the NEPTUNE seafloor cabled observatory offered a novel and
Conclusions
We conclude that the high-frequency observations made possible by a seafloor cabled observatory offered an entirely novel approach for monitoring the seasonal and interannual variability in the deep water biomass of large ontogenetically migrating calanoid copepods, a key zooplankton functional group for the subarctic NE Pacific pelagic food-web. Previously, the developmental and reproductive cycle, migratory biomass and export flux by Neocalanus spp. (more comprehensively N. plumchrus, N.
Acknowledgements
We would like to thank Ocean Networks Canada’s Marine Operations team for onshore and at-sea support and maintenance of the NEPTUNE cabled observatory. We also extend our gratitude to ONC’s ‘Data’ and ‘Data Stewardship’ teams for ensuring data quality and curation of all observatory data streams utilized in this study. Special thanks to K. Douglas, in charge of curating ONC’s multibeam bathymetric database, who prepared Fig. 1 and 3D base maps for Fig. 12. We thank the Department of Fisheries
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