Gordon L.J. Paterson

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Patterns in polychaete abundance and diversity from the Madeira Abyssal Plain, northeast Atlantic

Polychaete abundance and diversity patterns from the Madeira Abyssal Plain (MAP) were studied together with data from three other sites on the northeastern Atlantic abyssal plains. Polychaete abundance at MAP was significantly lower than at any of the other sites, including those lying under comparable productivity regimes. Analysis of diversity, using rarefaction and species counts per unit area, suggests that MAP is extremely species poor and shows dominance by a few common species. The MAP site is characterised by a superficial layer of turbidite sediment, and the hypothesis is put forward that the unusual sediment characteristics at MAP have affected macrofaunal abundance over a vast area (>2000 km2). Analysis of species composition indicates that the MAP site is not faunistically unique; rather it contains a high proportion of widespread, abundant, cosmopolitan species. We suggest that these are the opportunists of the abyssal benthic habitat. Differences in abundance between the other abyssal sites are the result of both productivity and local environmental conditions. Equitability at the other north Atlantic sites is not affected by productivity, although the actual number of species per unit area is affected, showing a south–north gradient.

Using a forensic science approach to minimize environmental contamination and to identify microfibres in marine sediments

There is growing evidence of extensive pollution of the environment by microplastic, with microfibres representing a large proportion of the microplastics seen in marine sediments. Since microfibres are ubiquitous in the environment, present in the laboratory air and water, evaluating microplastic pollution is difficult. Incidental contamination is highly likely unless strict control measures are employed. Here we describe methods developed to minimize the amount of incidental post-sampling contamination when quantifying marine microfibre pollution. We show that our protocol, adapted from the field of forensic fibre examination, reduces fibre abundance by 90% and enables the quick screening of fibre populations. These methods therefore allow an accurate estimate of microplastics polluting marine sediments. In a case study from a series of samples collected on a research vessel, we use these methods to highlight the prevalence of microfibres as marine microplastics.

Patterns in deep-sea macrobenthos at the continental margin: standing crop, diversity and faunal change on the continental slope off Scotland

Depth-related patterns of macrobenthic community structure and composition have been studied from box-core samples from the Scottish continental slope where deep-sea trawling and oil exploration are becoming increasingly important. There is a strong pattern of declining biomass and faunal abundance with increasing depth, but results also indicate reduced biomass and numbers of macrobenthos in the shallowest samples from just below the shelf edge where there are coarse sediments and a regime of strong bottom currents. There is also reduced species diversity at the shallowest stations, probably caused by hydrodynamic disturbance, but no clear mid-slope peak in species diversity as described from the northwest Atlantic. Taxonomic composition of the macrobenthic community shows most change between about 1000 and 1200 m, expressed as a major dichotomy in multivariate analysis by cluster analysis and ordination. It also shows up as a step-like increase in the rate of accumulation of new macrofaunal species. This corresponds to a change in hydrodynamic regime, from a seabed rich in suspension- and interface-feeding epifauna, to one where biogenic traces from large, burrowing deposit feeders are well developed, and visible epifauna rare in seabed photographs. It also corresponds to the depth zone where earlier study of megafaunal echinoderms in trawl and epibenthic sled samples also shows a clear peak in across-slope rate of change in faunal composition.

Evidence for episodic recruitment in a small opheliid polychaete species from the abyssal NE Atlantic

Abstract The abundance and size spectra of an infaunal opheliid polychaete species was followed over a two year period (September 1996–October 1998) in meiofaunal—(32 μm–1 mm) and macrofaunal —(>250 μm) samples collected at an abyssal site (4850 m depth) in the NE Atlantic. The site, situated on the Porcupine Abyssal Plain (PAP), is characterised by the episodic deposition of aggregated phytodetritus. The response of the fauna to this seasonal food supply was addressed by time-series sampling within the MAST-III BENGAL programme. In autumn 1996, small opheliid juveniles (mean length: 281 μm in September and 254 μm in October) were sampled only in the meiofauna samples. In March 1997, juvenile specimens of the opheliid, which were on average nearly twice as large (mean length: 480 μm) as those collected in 1996 were sampled in both both meio- and macrofaunal samples. The occurrence of only small juvenile individuals in 1996 suggests that a synchronous recruitment event had taken place earlier during that year. Small juveniles (mean length: 252 μm) were also abundant in a sample collected at the PAP site in May 1991, immediately following the deposition of a pulse of phytodetritus. The opheliid population structure in 1997 and 1998 indicates the slow progression of the settled cohort, possibly supplemented by a further, but relatively minor recruitment event in March 1998. Size spectra analysis implies that either growth was slow or that immigration of larger juveniles had augmented the population. The PAP opheliid may be an opportunist, which waits for optimal conditions before converting its slowly accumulated energy into reproduction. In addition, this species can apparently maintain a stable pool of developing juveniles if the organic pulse fails to materialise. The present study also shows that a more holistic approach is necessary to investigate the life cycles of some organisms, which lie close to the boundary between the meiofauna and macrofauna.

Micro-computed X-ray tomography: a new non-destructive method of assessing sectional, fly-through and 3D imaging of a soft-bodied marine worm

The detailed examination of the internal and functional anatomy of soft‐bodied marine worms has, until now, only been possible using the time consuming and destructive techniques of dissection, histology and electron microscopy. This is the first description of soft body morphology in polychaetes (Nephtys hombergii) derived by means of a bench‐top X‐ray micro‐CT scanner. The data are augmented, for comparison, by dissections, microscopy and scanning electron microscopy of the same species to show how this non‐destructive technique can rapidly and reliably produce high‐quality morphological data. It can also be applied to rare or unique invertebrate soft tissue material from museum collections and also to large‐scale invertebrate comparative anatomical studies possibly leading to greater evolutionary and taxonomic understanding. High‐definition images were obtained without the use of special tissue enhancing stains or radio‐opaque fluids and it is believed that this is the first time the technique has been successfully applied to this group of invertebrates. Extrapolation of the sectional imaging of regions of the gut and the production of three‐dimensional rotating and ‘fly‐through’ imaging can assist in assessment of aspects of functional anatomy.

Deep-sea litter: A comparison of seamounts, banks and a ridge in the Atlantic and Indian Oceans reveals both environmental and anthropogenic factors impact accumulation and composition

Marine litter is a global challenge that has recently received policymakers’ attention, with new environmental targets in addition to changes to old legislation. There are no global estimates of benthic litter because of the scarcity of data and only patchy survey coverage. However, estimates of baseline abundance and composition of litter are vital in order to implement litter reduction policies and adequate monitoring schemes. Two large-scale surveys of submarine geomorphological features in the Indian and Atlantic Oceans reveal that litter was found at all locations, despite their remoteness. Litter abundance was patchy, but both surveyed oceans had sites of high litter density. There was a significant difference in the type of litter found in the two oceans, with the Indian Ocean sites being dominated by fishing gear, whereas the Atlantic Ocean sites displayed a greater mix of general refuse. This study suggests that seabed litter is ubiquitous on raised benthic features, such as seamounts. It also concludes that the pattern of accumulation and composition of the litter is determined by a complex range of factors both environmental and anthropogenic. We suggest that the tracing of fishing effort and gear type would be an important step to elucidate hotspots of litter abundance on seamounts, ridges and banks.

Performance of cages as large animal-exclusion devices in the deep sea

Sedimentary, deep-sea communities include megafaunal animals (e.g., sea cucumbers, brittle stars, crabs) and demersal fishes, collectively termed the large, motile epifauna (LME). Individuals of the LME are common, and their biomass approximates that of the macrofauna. Based on analogies with shallow-water animals, they are likely to be sources of mortality for the infauna and to create spatial and temporal heterogeneity in the community. Given present theories of deep-sea community organization, such effects could be important. Unfortunately, this hypothesis has not been tested because of the difficulty of conducting experiments in the deep sea and because tools for manipulating the LME have not been developed. We studied the suitability of exclusion cages for this purpose at 780 m depth in San Diego Trough. We placed 16 cages of two mesh sizes for 4.5 months over regions of the seafloor that appeared free of LME. Time-lapse photographs of a cage and a control plot coupled with observations of all cages at the end of the experiment indicated that small (1.27-cm X 1.27-cm square)-mesh cages were effective at excluding LME. Further, the cages were essentially free of cage artifacts that have been reported in shallow-water studies. Large, mobile and disruptive animals (e.g., fishes, crabs) did not establish long-term residence adjacent to or on the cages. Bio-fouling slightly reduced the open surface area of the cage mesh, potentially reducing flow through the cage, but the composition of surface sediments in terms of organic C and N, phytoplankton-derived pigments, and grain size was indistinguishable between cages and control areas. Activities of excess 234 Th were significantly higher (average = 37%) inside of small-mesh cages, which might suggest enhanced particulate deposition inside cages. However, this measurement was an artifact of experimental manipulation. Particles that accumulated on the cage during the experiment were dislodged and settled to the seafloor when the cage was opened just prior to sampling. These particles would have been highly enriched in 234 Th, and their inclusion in core samples artificially inflated the calculated sediment accumulation rates inside cages. Therefore, the cages performed well; they excluded the targeted LME without causing artifacts and thus should be useful for experimental study of a group of animals that may have substantial impact on the structure and organization of deep-sea communities.

The influence of life history traits on the phenological response of British butterflies to climate variability since the late‐19th century

Many species of plants and animals have advanced their phenology in response to climate warming in recent decades. Most of the evidence available for these shifts is based on data from the last few decades, a period coinciding with rapid climate warming. Baseline data is required to put these recent phenological changes in a long-term context. We analysed the phenological response of 51 resident British butterfly species using data from 83 500 specimens in the collections of the Natural History Museum, London, covering the period 1880–1970. Our analysis shows that only three species significantly advanced their phenology between 1880 and 1970, probably reflecting the relatively small increase in spring temperature over this period. However, the phenology of all but one of the species we analysed showed phenological sensitivity to inter-annual climate variability and a significant advancement in phenology in years in which spring or summer temperatures were warm and dry. The phenologies of butterfly species were more sensitive to weather if the butterfly species was early flying, southerly distributed, and a generalist in terms of larval diet. This observation is consistent with the hypothesis that species with greater niche breadth may be more phenologically sensitive than species with important niche constraints. Comparison of our results with post-1976 data from the UK Butterfly Monitoring Scheme show that species flying early in the year had a greater rate of phenological advancement prior to the mid-1970s. Additionally, prior to the mid-1970s, phenology was influenced by temperatures in March or April, whereas since 1976, February temperature had a stronger influence on the phenology. These results suggest that early flying species may be approaching the limits of phenological advancement in response to recent climate warming.

New Prionospio and Aurospio Species from the Deep Sea (Annelida: Polychaeta)

The number of records of the genus Prionospio Malmgren, 1867, from the deep sea (>2000 m) are relatively few and do not reflect the actual occurrence of species nor their potential ecological importance. In this paper we describe five new species of this genus (Prionospio amarsupiata sp. nov., P. vallensis sp. nov., P. branchilucida sp. nov., P. hermesia sp. nov. and P. kaplani sp. nov.) all of which are abundant members of the deep-sea community. We also describe two new species of the genus Aurospio Maciolek, 1981 (Aurospio abranchiata sp. nov. and A. tribranchiata sp. nov.) again common elements of the abyssal fauna. Two of the new species have characters which question the generic distinctiveness of Prionospio and Aurospio. The problems in differentiating these two genera are discussed.