Ecosystem Status Report for the Northeast Large Marine Ecosystem
4. Primary and Secondary Production
4.1 Primary Production
Ecosystem productivity ultimately depends on the amount of production at the base of the food web. Such production is determined by the amount of photosynthesis from plants, algae and other photosynthetic organisms. Single-celled microscopic algae, collectively known as phytoplankton, are responsible for nearly all of the primary production in marine ecosystems and almost half of the total photosynthesis on the planet (Falkowski et al. 1998; Morel and Antoine 2002). Measurements of the primary photosynthetic pigment, chlorophyll a (CHL), are commonly used as a proxy for phytoplankton biomass. Pigment concentrations can be extracted and measured directly from water samples or measured remotely by observing the ‘color’ of the water. Ocean color remote sensors on satellites measure the spectrum (color) of the water, or rather the water-leaving radiances, at a number of visible and near-infrared wavelengths. These radiance measurements are then used to estimate the near-surface concentration of CHL primarily by comparing the reflectance from the blue and green wavelengths. Satellite estimates of CHL complement those obtained by in situ shipboard sampling and provide increased spatial and temporal coverage of phytoplankton dynamics that are not attainable by ship-based sampling alone. Satellite measurements of CHL and other parameters such as photosynthetic available radiation (PAR) and sea surface temperature (SST) can also be incorporated into integrated primary productivity (PP) models at the same scale and resolution as the CHL data.
In addition to being a primary food source for marine food webs, phytoplankton are also a fundamental biological component of the global carbon cycle and can significantly influence trophic food-web dynamics and ecosystem health (Falkowski et al. 1998; Morel and Antoine 2002). Furthermore, the amount of phytoplankton biomass in the water column, particularly during seasonal bloom events, can be a useful indicator of the amount of organic carbon exported from the pelagic zone to the benthos. In the NES LME, the annual mean surface CHL concentration is 0.75 (mg m-3) and the mean daily integrated PP rate is 0.55 (gC m-2 d-1) (Figure 4.1). Note, the satellite CHL values were derived from a regionally tuned algorithm (Pan et al., 2008), which results in lower CHL concentrations and PP rates compared to previous editions of the Ecosystem Status Report.
There are large regional differences in PP and CHL in the NES LME (Figure 4.1). The most obvious pattern is the general onshore-offshore decrease in both PP and CHL, from the coast to the shelf break. This pattern, as well as the seasonal changes derived from the satellite data and model estimates of PP, agrees well with patterns revealed during earlier shipboard surveys (O'Reilly et al. 1987; O'Reilly and Zetlin 1998), which found that the overall high levels of PP in the NES LME place it among the most productive continental shelf systems in the world.
The highest levels of PP are found on Georges Bank and in the immediate near-shore areas (particularly in the Mid-Atlantic Bight) and in the major estuaries where terrestrial derived nutrient concentrations are high. Elevated levels of PP (1-2 gCm-2d-1) are evident in the coastal waters adjacent to and generally south of the mouths of the Hudson, Delaware and Chesapeake Bays. Intermediate levels are found on the mid-shelf region of the Mid-Atlantic Bight, and in coastal areas of the Gulf of Maine. The lowest production rates in the NES LME (approximately 0.35 gCm-2d-1) are over the deep basins in the Gulf of Maine. PP in the deep outer shelf Georges Bank and Mid-Atlantic Bight water is low and similar to the levels in the deep basins of the Gulf of Maine. Note, however, that along the outer shelf the mean PP decreases along the 100m isobath from the southern flank of Georges Bank through the Mid-Atlantic Bight to Cape Hatteras. Of the four eco-regions, Georges Bank has the greatest mean annual CHL concentration, whereas the highest PP rates are found in the Mid-Atlantic Bight. The major temporal trends evident in both the CHL and PP time series are the minimums in 2004 and an increase in primary production over the past eight years.
In addition to the mean and anomalies, the span is a good indicator of how much the phytoplankton biomass and production rates vary throughout the year in a given location. For example, in 2012 the CHL concentration was highly variable in the Mid-Atlantic bight, yet there was a small range of PP in the same region (Figure 4.2). The large PP span in the Gulf of Maine compared to the Mid-Atlantic Bight is due to the greater variability in photosynthetic available solar radiation in the Gulf of Maine.
Interannual variability of CHL in the NES is also quite substantial. The first spatial mode of interannual CHL variability during the spring in the NES shows that part of the northern flank of Georges Bank, the Great South Channel, and the southern Gulf of Maine have synchronous interannual variability of CHL as opposed to the rest of the NES (Figure 4.3) (Saba et al. 2015). This is based on an empirical orthogonal function analysis of satellite derived CHL from the MODIS sensor from 2002 to 2012.
In addition to the satellite time series that begins in September, 1997, the NEFSC also uses volunteer merchant ships to collect phytoplankton data using the Continuous Plankton Recorder (CPR). These monthly transects, one of which crosses the Gulf of Maine from Cape Sable Island, NS to Boston, MA and the second crosses the Mid-Atlantic Bight from New York toward Bermuda, help extend the phytoplankton record back to the late 1970s. The CPR is a mechanical device that is towed behind a vessel. Water passing through an opening in the nose as it is towed is filtered by a silk sampling mesh that is continuously wound onto a spool where it is preserved for later analysis. The phytoplankton cells are identified and enumerated in the laboratory. The relative greenness of the silk is also recorded to generate a phytoplankton color index (PCI), which serves as an indicator of overall phytoplankton abundance.
The annual mean of the monthly standardized anomalies for the CPR phytoplankton color index were calculated for the continental shelf along both CPR transects (Figure 4.4). The PCI in the Gulf of Maine were generally higher in the late 1980s and late 1990s, while values were lower in the 2000s driving an overall long term decreasing trend. There was also a decline in the PCI in the Mid-Atlantic Bight, with the highest values generally occurring prior to 1985. The declines in PCI suggest a decrease in the abundance of the larger phytoplankton cells that are sampled more effectively by the CPR filtering mesh.
The abundance of phytoplankton and the rates of productivity change seasonally and vary from year to year in response to the physical environment, the availability of nutrients and sunlight, and grazing pressures. In general, CHL concentrations are greatest in the spring (March, April and May) and the fall (September, October and November) and lowest in winter (December, January and February) and summer (June, July and August). In contrast, the highest rates of primary productivity are during the summer months when solar radiation is at its maximum. The annual cycle of PP differs from CHL in that PP reflects changes in phytoplankton photosynthesis rather than changes in phytoplankton biomass.
Phytoplankton blooms are characterized by a rapid increase in biomass lasting from a few days to several weeks. Spatially, the blooms can be small (due to localized features, e.g. upwelling or frontal structures), regional or basin-wide. In 2014, the spring bloom started developing in the shallow portions of Georges Bank and Nantucket Shoals. Shorter term blooms are also evident along the Mid-Atlantic coast at this time. The bloom progressed in the western Gulf of Maine and reached its peak in mid April. By mid-May, most of the bloom had subsided, although smaller scale blooms continued to develop in the portions of the Gulf of Maine (see Figure 4.5, chlorophyll animation).
In the NES LME, there are regional differences in the timing and magnitude of the spring and fall blooms in additional to inter-annual variability (Figure 4.6). The spring and fall phytoplankton blooms typically consist of larger phytoplankton species (microplankton, > 20 µm) and can be quite variable in the initiation, peak concentration, duration, and species composition. This variability can affect the food availability for zooplankton grazers and the trophic transfer efficiency from phytoplankton to pelagic and benthic resources. The spring bloom period is a dominant feature of the phytoplankton cycle over most of the NES LME. Though the duration is short (~1-2 months), the timing of the bloom provides a major food resource for marine grazers. Furthermore, the bloom often produces phytoplankton concentrations in excess of what can be used in the water column, thus providing surplus material that can be exported to the benthos.
The summer period is characterized by relatively low phytoplankton biomass, but high photosynthetic rates. The summer has the greatest amount of available sunlight, so despite lower chlorophyll concentrations, it is the period of highest PP. The fall bloom period is an important and sometimes overlooked part of the phytoplankton cycle that is affected by many factors, including weather events that mix nutrients into the well lit euphotic zone. There is considerable inter-annual variability in the timing, duration and magnitude of the fall bloom and in some years, the fall bloom is a distinct event of equal or greater magnitude than the spring bloom. In other years, however, the physical drivers do not produce favorable conditions for rapid phytoplankton growth and the fall bloom does not fully develop.
Phytoplankton communities in the NES LME are highly diverse and variable, changing at diel, seasonal, annual and inter-decadal timescales. Within a community, individual phytoplankton species vary considerably in size (<1 µm to >100 µm) and include a broad suite of taxa, from prokaryotic cyanobacteria to eukaryotic protists, each of which differentially affect biogeochemical cycling, export flux, and secondary production. Among the common taxa in the NES LME are diatoms, dinoflagellates, microflagellates and cyanobacteria. Phytoplankton are commonly grouped into size classes (PSCs) because several physiological and ecological processes, including nutrient uptake, light absorption, sinking, and export are related to cell size (Brewin et al. 2011 and references within). Microplankton (> 20 µm), represented primarily by diatoms and dinoflagellates, are more common in nutrient-rich waters in the NES LME and dominate during the spring and fall blooms (Figure 4.7) (Aiken et al. 2008). Microplankton are grazed on by larger zooplankton or sink to the benthos, often providing a direct transfer of energy up the food chain. In contrast, smaller nanoplankton (2-20 µm) and picoplankton (< 20 µm) (Sieburth et al. 1978) dominate the community composition in the summer months when nutrient concentrations are low. The production generated by the smaller nano- and picoplankton is primarily consumed within the microbial community and remineralization within the euphotic zone before it can reach higher trophic levels (Calbet and Landry 2004).
Using the Continuous Plankton Recorder (CPR) phytoplankton abundance for the Gulf of Maine and Mid-Atlantic Bight shelf regions, the ratio of diatoms to total phytoplankton and ratio of dinoflagellates to total phytoplankton were calculated for both regions (Figure 4.8). The ratio of total diatoms to total phytoplankton in the Gulf of Maine has generally decreased, while the ratio of dinoflagellates to total phytoplankton has generally increased. This suggests an ecological shift favoring dinoflagellates relative to diatoms within the Gulf of Maine. This same pattern is not evident in the Mid-Atlantic Bight, with diatoms increasing and dinoflagellates decreasing as a fraction of total phytoplankton in the 2000s relative to the 1990s. The long-term trend in the relative diatom abundance is also not well-defined due to significant inter-annual variability.
4.2. Secondary Production
The energy produced by phytoplankton can be divided among three fluxes; remineralization within the euphotic zone (the "microbial loop"), export (sinking) to depth, and food web transfer (grazing) (Legendre and Rassoulzadegan 1996). In the microbial loop, decomposing bacteria consume particulate and organic material from phytoplankton and other organisms. These bacteria feed nanoplanktonic heterotrophs, which are then preyed upon by microzooplankton. Larger zooplankton graze on both microzooplankton and larger phytoplankton species; however the energy transferred through microbial loop is considered less efficient as it must travel through at least two additional trophic levels prior to becoming part of the secondary production pool. Phytoplankton that are not grazed or remineralized in the upper water column are exported to the benthos where they fuel benthic production. Large diatom blooms associated with the spring and fall blooms are the primary source of exported production. Zooplankton grazing on microphytoplankton is the most direct energy pathway to transfer primary production up the food web. Zooplankton in the NES LME are routinely monitored by deploying small (61 cm diameter), fine meshed (333 µm) nets at numerous locations throughout the ecosystem. The net is deployed from the surface to near the bottom, providing an integrated sample through the entire water column. Currently, the NEFSC’s sampling includes six surveys per year with approximately 120 stations over the whole ecosystem; these surveys are designed to capture seasonal and annual trends, but not smaller-scale variability. Zooplankton are also monitored monthly using a Continuous Plankton Recorder (CPR) along two transects in the NES LME: One crossing the Gulf of Maine and one crossing the Mid-Atlantic Bight from New York toward Bermuda towed by volunteer merchant vessels. The CPR is a mechanical device that is towed behind a vessel. Water passing through an opening in the nose as it is towed is filtered by a silk sampling mesh that is continuously wound onto a spool where it is preserved for later analysis. Zooplankton on the CPR silk are then identified and enumerated in the laboratory.
One simple indicator of zooplankton biomass/abundance is the volume of material collected in the net, termed zooplankton biovolume. The time series of zooplankton biovolume among the Georges Bank, Mid-Atlantic, and western Gulf of Maine ecoregions are relatively consistent suggesting large‐scale coherence in zooplankton throughout much of NES LME (Figure 4.9). The trends in the eastern Gulf of Maine/western Scotian Shelf are somewhat different with lower biovolumes through the 1990s. In the early years of the time series, there was a marked drop and recovery in zooplankton abundance, with variable but near constant values through the late 1980s, 1990s, and 2000s. Data from 2010 to present are low and approaching the minimums observed in the early 1980s.
Another indicator of zooplankton abundance is the total zooplankton along repeated continuous plankton recorder (CPR) transects. The NEFSC conducts two Continuous Plankton Recorder (CPR) transects in the United States Northeast Shelf Ecosystem: One crossing the Gulf of Maine and one crossing the Mid-Atlantic Bight from New York toward Bermuda using volunteer merchant vessels. The CPR is a mechanical device that is towed behind a vessel. Water passing through an opening in the nose as it is towed is filtered by a silk sampling mesh that is continuously wound onto a spool where it is preserved for later analysis. Zooplankton on the CPR silk are then identified and enumerated in the laboratory. The total CPR mesozooplankton abundance in the Gulf of Maine had generally higher values in the 1990s and lower values in the 2000s. The lowest values of the time series occurred in the late 1970s and early 1980s so overall there has been an increase in mesozooplankton since 1978. Similarly, the lowest mesozooplankton abundance in the Mid-Atlantic Bight occurred in the 1970s and 1980s and has been generally higher since (Figure 4.10).
Another measure related to secondary production is the number of copepods in the ecosystem. Copepods are microscopic animals related to lobsters and crabs and are the primary grazers of phytoplankton and microzooplankton. These small animals are the primary food source for forage fishes (e.g. herring and mackerel) and young groundfishes (e.g., cod, haddock). They are also an important food source for many baleen whales including the endangered North Atlantic right whale (Eubalaena japonica), which feeds primarily on a lipid rich copepod species – Calanus finmarchicus. The relative number of nine copepod species in the NES LME is largely coherent across the 4 EPUs, with the Mid-Atlantic the most different (Figure 4.11). There are some similarities with the biovolume estimates, but also some important differences. Similarities include low values in the mid-1980s, high values in the 1990s, and decreasing values in the early 2000s. Differences include low values at the beginning of the time series and increasing value later in the 2000s. The recent uptick in copepod abundance is more pronounced in the Gulf of Maine compared to Georges Bank and the Mid-Atlantic.
Recent work has found that the composition of the zooplankton community has changed over time. Specifically, several species of small copepods increased in abundance in the 1990s resulting in an increase in total copepod abundance. The community composition changed again around 2000, consistent with the drop in total copepod abundance. Individual copepod species can serve as indicators of these broader changes in overall species composition. As an example, in the Gulf of Maine, Pseudocalanus spp., Temora longicornis, Centropages typicus, and Centropages hamatus were all more abundant in the 1990s compared to the 1980s and the 2000s. Calanus finmarchicus was more abundant during the 1980s and 2000s compared to the 1990s (Figure 4.12). There is evidence of a changing community, with smaller zooplankton becoming more abundant in recent years. These changes in community composition are also represented in more statistical analyses of the zooplankton community composition. A multivariate statistical measure of zooplankton community composition shows a similar trend as the difference between small and large zooplankton (Figure 4.13). Interestingly, a similar analysis of phytoplankton community composition derived from the Continuous Plankton Recorder (CPR) shows very similar trends to zooplankton community composition indicating that there were marked changes in lower-trophic levels in the 1990s compared to the 1980s and 2000s (Figure 4.10).
Zooplankton sampling conducted by the NEFSC includes gelatinous zooplankton (including salps, siphonophores, and ctenophores). Salps and siphonophores, filter-feeding gelatinous zooplankton, were caught most frequently during sampling with bongo nets. Ctenophore occurrence on the shelf can be estimated by gut content analysis of the top predator for ctenophores, the spiny dogfish, Squalus acanthias (Link and Ford 2006). Salp, siphonophore, and ctenophore populations can react quickly to changes in food availability such as when water masses intrude on the shelf. When concentrations are high, increased grazing can reduce copepod populations and fishing nets can become clogged with gelatinous plankton (Mills 1995; Madin et al. 2006). These gelatinous zooplankton metrics allow tracking of three zooplankton groups with significant potential to alter mesozooplankton populations and interact with larval fish.
In the Georges Bank, Gulf of Maine, and the Scotian Shelf ecoregions the siphonophore and salp populations have remained below the historical mean for the last three years (Figure 4.14). This follows a period between 2007 and 2008 where this region experienced the largest increase in salp population from this survey (Figure 4.14A). In the Middle Atlantic Bight ecoregion, salps and siphonophores return to levels close to the historical mean after a salp increase in 2010 (Figure 4.14B). The percent frequency of occurrence of ctenophores across all ecoregions held at approximately 6.5% in 2012, down slightly from 7.9% in 2011. Both of these recent observations are lower than the historical average of 11.9%, which peaked in 1996 (Figure 4.15).
Other species of macrozooplankton are routinely monitored by NEFSC. Trends in abundance of arrow worms (chaetognaths), krill (euphausiids), sand fleas (amphipods), and planktonic sea squirts (appendicularians or larvaceans), indicate generally increasing trends over time (Figure 4.16). Of note are the large increases in the eastern and western Gulf of Maine over the last few years. Chaetognaths are predators of other zooplankton species (including some fish larvae) while euphausiids and amphipods are important prey of a number of species including fish, marine mammals, and seabirds.