Reply to Haddock, S. H. D. Reconsidering evidence for potential climate-related increases in jellyfish

Following the publication of our paper (Attrill et al. 2007), we became quickly aware of a couple of errors. We have subsequently been collaborating with Dr. Chris Lynam (Lynam et al. 2004, 2005) to bring together our two datasets, explore the common patterns within our data, and attempt to provide a consensus on how climate is affecting gelatinous plankton in the North Sea. During this reanalysis, two errors within the data were discovered, one involving a transcription error of a column of residuals during de-trended analysis, the other a major data entry error deep in the Continuous Plankton Recorder (CPR) database for sector B2. Here we present a revised version of table 1 from Attrill et al. (2007) to incorporate corrections to these transcription and data entry errors. These corrections alter some of the results in our original data table, mainly to increase and strengthen the number of significant relations we found (e.g., for sector B2 and whole sea area); all previous main results remain robustly significant. Following discussions with Dr. Lynam, two clarifications of statements made in Attrill et al. (2007) are also required. Page 482, Results, last line of first column: ‘‘There were no...robust, consistent relations between jellyfish frequency and any environmental variables for B and D… contrary to the findings of previous shorter time series (Lynam et al. 2005).’’ The Lynam et al. (2004, 2005) papers presented no data for the D sector and found no link in the B sector, contrary to our revised results. Page 482, Discussion, paragraph 1, last sentence: ‘‘… positive association … North of Scotland (Lynam et al. 2005) … does not appear to be maintained.’’ Our paper did not report on any data that covered Lynam et al.’s (2005) North of Scotland area so the statement is not directly supported, although their positive relation North of Scotland, when considered in conjunction with inflow, may agree with the C2 and B2 results of Attrill et al. (2007).

The North Pacific Continuous Plankton Recorder Survey

The Continuous Plankton Recorder (CPR) survey of the North Pacific is a PICES project now in its ninth year and facing an uncertain future. CPRs have been towed behind commercial ships along two (north–south and east–west) transects for a total of ~ nine times per year. Samples are collected with a filtering mesh and are then microscopically processed for plankton abundance in the laboratory. The survey, so far, has accumulated 3,648 processed samples (with approximately three times as many archived without processing), each representing 18 km of the transect (Fig. 1) and containing an abundance of data on over 290 phytoplankton and zooplankton taxa. A CTD with a fluorometer has been attached to the CPR sampling at the east–west transect in more recent years to provide supplementary environmental data.

The Continuous Plankton Recorder: towards a global perspective

The Continuous Plankton Recorder (CPR) began its first routine deployment to collect plankton samples in the North Sea in 1931. The better part of a century after that event, the Recorder is used for sampling plankton widely in many oceans. The CPR is designed to be towed behind ships of opportunity (such as commercial and passenger vessels) and to collect plankton samples along the ship’s path. The samples provide information on the broad scale spatial distributions of larger hard-shelled phytoplankton and robust mesozooplankton organisms (Richardson et al., 2006). Changes in these distributions provide indices for the biological health of the ocean including those required for fisheries and for assessment of climate change impacts.

Effects of formalin preservation on stable carbon and nitrogen isotope signatures in Calanoid copepods: implications for the use of Continuous Plankton Recorder Survey samples in stable isotope analyses

Preserved and archived organic material offers huge potential for the conduct of retrospective and long-term historical ecosystem reconstructions using stable isotope analyses, but because of isotopic exchange with preservatives the obtained values require validation. The Continuous Plankton Recorder (CPR) Survey is the most extensive long-term monitoring program for plankton communities worldwide and has utilised ships of opportunity to collect samples since 1931. To keep the samples intact for subsequent analysis, they are collected and preserved in formalin; however, previous studies have found that this may alter stable carbon and nitrogen isotope ratios in zooplankton. A maximum ~0.9‰ increase of δ15N and a time dependent maximum ~1.0‰ decrease of δ13C were observed when the copepod, Calanus helgolandicus, was experimentally exposed to two formalin preservatives for 12 months. Applying specific correction factors to δ15N and δ13C values for similarly preserved Calanoid species collected by the CPR Survey within 12 months of analysis may be appropriate to enable their use in stable isotope studies. The isotope values of samples stored frozen did not differ significantly from those of controls. Although the impact of formalin preservation was relatively small in this and other studies of marine zooplankton, changes in isotope signatures are not consistent across taxa, especially for δ15N, indicating that species-specific studies may be required. Copyright © 2011 John Wiley & Sons, Ltd.

Temporal and spatial variability of Oithona spp. abundance and phenology in the North Atlantic, North Pacific and Southern Ocean using the CPR data

The genus Oithona is considered the most ubiquitous and abundant copepod group in the world oceans. Although they generally make-up a lower proportion of the total copepod biomass, because of their high numerical abundance, preferential feeding for microzooplankton and motile preys, Oithona spp. plays an important role in microbial food webs and can provide a food source for other planktonic organisms. Thus, changes in Oithona spp. overall abundance and the timing of their annual maximum (i.e. phenology) can have important consequences for both energy flow within marine food webs and secondary production. Using the long term data (1954-2005) collected by the Continuous Plankton Recorder (CPR), the present study, investigates whether global climate warming my have affected the long term trends in Oithona spp. population abundance and phenology in relation to biotic and abiotic variables and over a wide latitudinal range and diverse oceanographic regions in the Atlantic, Pacific and Southern Ocean.

Continuous Plankton Recorder Underestimates Zooplankton Abundance

A comparison between monthly mean ContinuousPlanktonRecorder (CPR) data and zooplankton data caught during winter and early spring with different sampling devices in the North Sea is presented to estimate the relative error in abundance of CPR measurements. CPR underestimates the abundance of zooplankton by a factor 25 during winter and early spring and by a factor 18 if Oithona spp. is not considered. This has serious implications for estimation of biomass as well as for modelling ecosystem dynamics.

Biologging, Remotely-Sensed Oceanography and the Continuous Plankton Recorder Reveal the Environmental Determinants of a Seabird Wintering Hotspot

Marine environments are greatly affected by climate change, and understanding how this perturbation affects marine vertebrates is a major issue. In this context, it is essential to identify the environmental drivers of animal distribution. Here, we focused on the little auk (Alle alle), one of the world’s most numerous seabirds and a major component in Arctic food webs. Using a multidisciplinary approach, we show how little auks adopt specific migratory strategies and balance environmental constraints to optimize their energy budgets. Miniature electronic loggers indicate that after breeding, birds from East Greenland migrate .2000 km to overwinter in a restricted area off Newfoundland. Synoptic data available from the Continuous Plankton Recorder (CPR) indicate that this region harbours some of the highest densities of the copepod Calanus finmarchicus found in the North Atlantic during winter. Examination of large-scale climatic and oceanographic data suggests that little auks favour patches of high copepod abundance in areas where air temperature ranges from 0uC to 5uC. These results greatly advance our understanding of animal responses to extreme environmental constraints, and highlight that information on habitat preference is key to identifying critical areas for marine conservation.

Can the Continuous Plankton Recorder (CPR) be used to infer sardine diet?

Knowledge on the impact of climate variability in the diet of planktivorous fish is limited by the laborious work involved in stomach content analysis, impractical for large scale studies. Routine measurements of plankton such as the Continuous Plankton Recorder (CPR) survey provide valuable information of the temporal variation of phyto- and zooplankton prey availability for higher trophic levels. Sardines are a world-wide distributed and commercially important planktivorous fish, at the basis of the pelagic marine food web. Being predominantly non-selective filter-feeders, their diets closely correspond to the water plankton species and a significant relationship was recently found between Sardina pilchardus feeding intensity and remotely sensed chlorophyll alpha . Data of sardine stomach prey composition and CPR were obtained during 2003 for the same location off the west coast of Portugal, an area characterised by strong seasonality of plankton abundance and composition, mainly governed by upwelling events. Phyto- and zooplankton prey in sardine stomachs were identified to the lowest possible taxa and their numerical and volumetric abundance was registered, as well as their contribution to the prey carbon content. The seasonal variation of the abundance and composition of sardine diet was then compared to the abundance and composition of the water plankton obtained with the CPR at the same time and for the same area where the fish were collected, in order to evaluate if CPR data can be used to proxy sardine prey availability and diet composition at large temporal scales.

Patterns of jellyfish abundance in the North Atlantic

A number of explanations have been advanced to account for the increased frequency and intensity at which jellyfish (pelagic cnidarians and ctenophores) blooms are being observed, most of which have been locally directed. Here, we investigate seasonal and inter-annual patterns in abundance and distribution of jellyfish in the North Atlantic Ocean to determine if there have been any system-wide changes over the period 1946–2005, by analysing records of the presence of coelenterates from the Continuous Plankton Recorder (CPR) survey. Peaks in jellyfish abundance are strongly seasonal in both oceanic and shelf areas: oceanic populations have a mid-year peak that is more closely related to peaks in phyto- and zooplankton, whilst the later peak of shelf populations mirrors changes in SST and reflects processes of advection and aggregation. There have been large amplitude cycles in the abundance of oceanic and shelf jellyfish (although not synchronous) over the last 60 years, with a pronounced synchronous increase in abundance in both areas over the last 10 years. Inter-annual variations in jellyfish abundance in oceanic areas are related to zooplankton abundance and temperature changes, but not to the North Atlantic Oscillation or to a chlorophyll index. The long-term inter-annual abundance of jellyfish on the shelf could not be explained by any environmental variables investigated. As multi-decadal cycles and more recent increase in jellyfish were obvious in both oceanic and shelf areas, we conclude that these are likely to reflect an underlying climatic signal (and bottom-up control) rather than any change in fishing pressure (top-down control). Our results also highlight the role of the CPR data in investigating long-term changes in jellyfish, and suggest that the cnidarians sampled by the CPR are more likely to be holoplanktic hydrozoans and not the much larger meroplanktic scyphozoans as has been suggested previously.

Monitoring changes in phytoplankton abundance and composition in the Northwest Atlantic: a comparison of results obtained by Continuous Plankton Recorder sampling and colour satellite imagery

Phytoplankton abundance in the NW Atlantic was measured by continuous plankton recorder (CPR) sampling along tracks between Iceland and the western Scotian Shelf from 1998 to 2006, when sea-surface chlorophyll (SSChl) measurements were also being made by ocean colour satellite imagery using the SeaWiFS sensor. Seasonal and inter-annual changes in phytoplankton abundance were examined using data collected by both techniques, averaged over each of four shelf regions and four deep ocean regions. CPR sampling had gaps (missing months) in all regions and in the four deep ocean regions satellite observations were too sparse between November and February to be of use. Average seasonal cycles of SSChl were similar to those of total diatom abundance in seven regions, to those of the phytoplankton colour index in six regions, but were not similar to those of total dinoflagellate abundance anywhere. Large inter-annual changes in spring bloom dynamics were captured by both samplers in shelf regions. Changes in annual (or 8 months) averages of SSChl did not generally follow those of the CPR indices within regions and multi-year averages of SSChl, and the three CPR indices were generally higher in shelf than in deep ocean regions. Remote sensing and CPR sampling provide complementary ways of monitoring phytoplankton in the ocean: the former has superior temporal and spatial coverage and temporal resolution, and the latter provides better taxonomic information.