Research Article |
Corresponding author: Saskia Brix ( sbrix@senckenberg.de ) Academic editor: Jörundur Svavarsson
© 2018 Saskia Brix, Anne-Nina Lörz, Anna M. Jażdżewska, Lauren Hughes, Anne Helene S. Tandberg, Krzysztof Pabis, Bente Stransky, Traudl Krapp-Schickel, Jean Claude Sorbe, Ed Hendrycks, Wim Vader, Inmaculada Frutos, Tammy Horton, Krzysztof Jażdżewski, Rachael Peart, Jan Beermann, Charles Oliver Coleman, Lene Buhl-Mortensen, Laure Corbari, Charlotte Havermans, Ramiro Tato, Anali Jimenez Campean.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Brix S, Lorz A-N, Jazdzewska AM, Hughes L, Tandberg AHS, Pabis K, Stransky B, Krapp-Schickel T, Sorbe JC, Hendrycks E, Vader W, Frutos I, Horton T, Jazdzewski K, Peart R, Beermann J, Coleman CO, Buhl-Mortensen L, Corbari L, Havermans C, Tato R, Campean AJ (2018) Amphipod family distributions around Iceland. In: Brix S, Lorz A-N, Stransky B, Svavarsson J (Eds) Amphipoda from the IceAGE-project (Icelandic marine Animals: Genetics and Ecology). ZooKeys 731: 1-53. https://doi.org/10.3897/zookeys.731.19854
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Amphipod crustaceans were collected at all 55 stations sampled with an epibenthic sledge during two IceAGE expeditions (Icelandic marine Animals: Genetics and Ecology) in 2011 and 2013. In total, 34 amphipod families and three superfamilies were recorded in the samples. Distribution maps are presented for each taxon along with a summary of the regional taxonomy for the group. Statistical analyses based on presence/absence data revealed a pattern of family distributions that correlated with sampling depth. Clustering according to the geographic location of the stations (northernmost North Atlantic Sea and Arctic Ocean) can also be observed. IceAGE data for the Amphilochidae and Oedicerotidae were analysed on species level; in case of the Amphilochidae they were compared to the findings from a previous Icelandic benthic survey, BIOICE (Benthic Invertebrates of Icelandic waters), which also identified a high abundance of amphipod fauna.
Amphipoda , benthos, deep sea, distribution, Greenland-Iceland-Faroe Ridge, subarctic, taxonomy
The international IceAGE project (Icelandic marine Animals: Genetics and Ecology) focuses on the climatic sensitive region at the northernmost part of the North Atlantic and the Nordic Seas (Greenland, Iceland and Nordic Seas reaching to the North Sea). The study area is characterised by a steep temperature gradient (< -0.9 °C to 14 °C) as well as several shallow (<800 m) submarine ridges which define distinct deep marine basins and host cold-water coral reefs along their slopes (
Despite amphipods being the most common peracarid crustacean order within the IceAGE samples, prior to this study, amphipod crustaceans were underrepresented in project research outputs. The lack of scientific focus on this group was largely due to the large amounts of time and specialised expertise required to process the volume of material. At the beginning of the project, more than 66,000 amphipod specimens had been collected and were available for further identification (DZMB database, unpublished data).
Identifying amphipods is a complex task and owing to the "taxonomic impediment" the number of amphipod experts worldwide is in decline (
Here the results from two such workshops are presented. These results show the distribution patterns for amphipod families identified from IceAGE samples. For two abundant families, Amphilochidae and Oedicerotidae, species level identification is also presented.
The IceAGE project and the expeditions were initiated and coordinated by Senckenberg am Meer (http://www.iceage-project.org), part of the Senckenberg Forschungsinstitut und Naturmuseum that serves to link scientists to samples collected by German research vessels and to make this material available. All sorting was handled according to
During both identification workshops, sample processing concentrated on amphipods collected with the epibenthic sledge (EBS). It should be noted that three types of gear were used during the IceAGE expeditions: RP sled (
For the families Amphilochidae and Oedicerotidae, all identified specimens have been registered in the permanent zoological collection at either Senckenberg (Frankfurt), the Naturkundemuseum Berlin or the Zoological Museum Hamburg (ZMH), Centrum fur Naturkunde (CeNak). All specimens selected as molecular vouchers (
Due to the "expert-bias" of participants at our two workshops and the incomplete sorting at family level, small families often received a more detailed treatment, while some larger taxa such as the Lysianassoidea or Phoxocephalidae were dealt with quite cursorily. Families that are known to be very abundant in Icelandic waters, including e.g., the Ampeliscidae (
Certain findings of singletons or rarer taxa are important for particular families, i.e., the Sicafodiidae (
Distribution maps were created for the amphipod families, one superfamily (Lysianassoidea) and one infraorder (Corophiida) occurring at more than two stations using the freeware QGIS, and were assembled using Photoshop CS6. Multivariate analyses were performed on samples where more than 40% of the individuals were identified to family level (76-100%: 14 samples, 51-75%: 5 samples, 41-50%: 14 samples). As a result of this processing methodology we readily acknowledge possible underestimations and restrictions within the dataset. Data were presence/absence transformed before the analysis. Hierarchical agglomerative clustering was based on Bray-Curtis similarity formula (
Additional multivariate analyses (Bray-Curtis formula, group average grouping method, SIMPROF test with 1% significance level) were also carried out for the two families whose specimens were identified to species level (Amphilochidae - 32 samples and Oedicerotidae -25 samples). Here, abundance data (number of individuals per station) were standardised and square root transformed prior to analysis (
Amphipod crustaceans were collected at all 55 stations analysed; however, identification to the family level was only possible for 40 of them (see Figure
Family distribution at all IceAGE stations ordered by transect. Within each transect (1: Norwegian Channel, 2: Iceland-Faroe Ridge, 3: Iceland Basin, 4: Irmninger Basin, 5: Denmark Strait, 6: Norwegian Sea), stations are ordered by depth. The upper graph (black bars) indicates the absolute number of amphipod individuals per station. The lower graph indicates the amphipods sorted to families per station (legend by colours shown on the right side).
In numerical order, the most abundant taxa were the Dulichiidae, Oedicerotidae, Phoxocephalidae, and Lysianassoidea followed by the Amphilochidae (Figure
Figure
In the present study, the family was recorded at two of the 40 stations from ca. 600 m north of Faroe Islands, with a total of ten specimens. In a revision of the Iphimediidae and related families,
Figure
In total, 50 amathillopsid individuals were reported from 12 stations, most from the two upper bathyal stations just South of Iceland. Cleonardopsis was found at stations west of Iceland whereas Amathillopsis is reported from the eastern stations. Forty-six specimens of Cleonardopsis were recorded, distributed in the Iceland Basin (eight stations) and the Irminger Basin (one station). The Amathillopsidae consists of a few little known, but morphologically spectacular, large amphipods, which lead a pelagic or bentho-pelagic life. Amathillopsids are found from the Arctic to the Antarctic. In the North Atlantic, the most commonly reported species is Amathillopsis spinigera Heller, 1875, with the lesser cited A. affinis Miers, 1881 possibly also present. In the present study, four specimens of this genus were recorded at three deep stations in the Norwegian Sea. The genus Cleonardopsis was reassigned to the Amathillopsidae in the new subfamily Cleonardopsinae (
Figure
Ampeliscidae were reported from 23 of the 40 stations studied, with a total of 492 specimens. The Ampeliscidae are a benthic, soft sediment, generally tube-dwelling family. This group has strong grain-size and depth constraints (
Figure
Amphilochids were reported from 33 of the 40 stations studied, with a total of 1110 specimens. The family Amphilochidae is cosmopolitan and interestingly includes one species (Gitanopsis alvina Bellan-Santini and Thurston, 1996) from hydrothermal vents at the Mid-Atlantic Ridge (
Figure
Argissids were collected at three of the 40 sampling stations, all located south of Iceland, at 686-2749 m, with a total of six specimens. The family Argissidae comprises the single species Argissa hamatipes (Norman, 1869), originally described from shallow water in St. Magnus Bay, Shetland Islands, Scotland. Another species, A. stebbingi Bonnier, 1896, described from bathyal muddy bottoms of the southern Bay of Biscay, is currently considered a junior synonym of A. hamatipes. However,
Figure
Atylidae occurred in samples from the Denmark Strait and the Faroe Channel at stations associated with strong bottom currents, in six of the 40 stations studied, with a total of 20 specimens.
Figure
The family was present at 24 of the 40 stations studied, with a total of 470 specimens indicating its relative importance in this cold-water area. The relatively speciose family Calliopiidae is represented in the north east Atlantic by 39 species from 12 genera (Vader and Tandberg, unpublished data) which accounts for almost 50% of the known Calliopiidae in the world (
Figure
The family Cressidae was reported from 14 of the 40 stations studied, with a total of 190 specimens. Cressids have a compact body, specialised mandible and an extremely lengthened mandibular palp (
Figure
Cyproideidae was reported from three of the 40 stations studied. Twenty-four cyproideid specimens were recorded in the IceAGE material, mainly on the upper slope in both Irminger and Iceland basins (13 and ten individuals, respectively). A single specimen was also recorded from a northern Faroe station (station 879). The Cyproideidae are characterised by immensely broadened coxae 3/4 with contiguous abutting margins and overlapping coxae 1/2. The Cyproideidae includes 20 genera with 46 species (
Figure
Dexaminids were found at four of the 40 stations studied in shallow areas east of Faroe Islands, Iceland Basin and Denmark Strait and at one deep station (2749 m) in the Iceland Basin, with a total of 14 specimens. Four species of the family Dexaminidae have been reported in the North-Atlantic (
Figure
Epimeriidae were reported from five of the 40 stations studied, with a total of 55 specimens, in the area of Iceland-Faroe Ridge, at depths less than 1600 m. This family usually feature prominent teeth carinae (
Figure
Eusiridae were reported from 27 of the 40 stations studied with representatives in all sampling areas and depth zones. A total of 775 specimens of Eusiridae have so far been identified from the IceAGE samples. Eusirids are abundant members of the deep-sea fauna off Iceland (
Figure
Lepechinellids were reported from ten of the 40 stations studied, with a total of 103 specimens. The lepechinellids are well adapted to a demersal or epibenthic lifestyle on soft substrates in deeper waters (
Figure
Leucothoids were reported from nine of the 40 stations studied, with a total of 35 specimens. The Leucothoidae are well represented within the Atlantic Ocean, though mainly in warmer regions. The documented Atlantic Ocean leucothoids have broad shared distributions with eight species also known from South and West Africa, 13 from the Caribbean and Gulf of Mexico, five from Brazil, three species from the Azores, Biscay, and Mid-Atlantic Ridge near Santa Cruz das Flores, and seven species from United Kingdom waters to the central and northern Atlantic. A new species of leucothoid is described based on specimens collected during the IceAGE expedition (
Figure
Three hundred eleven liljeborgiid specimens were collected from 20 of the 40 stations studied and covering a range of depths and distinct hydrological features. The Liljeborgiidae are micropredators, with some being known associates of other invertebrates, including hermit crabs (
Figure
A total of 2008 specimens of lysianassoids and allied taxa was reported from 38 of the 40 stations studied occurring at depths from 169 to 2743 m. This superfamily is an incredibly large, diverse group of amphipods, which includes scavengers, predators, ectoparasites, obligate associates, and inquilines (e.g.,
Figure
In total, 254 melphidippid specimens were recorded from 16 of the 40 stations. Melphidippids have elaborate spination and elongate slender legs and are, at least partially, epifaunal. Several studies have indicated that the normal orientation is upside down in a sling created by the elongate pereopods V to VII (
Figure
Oedicerotids were present and often the most abundant family at 35 of the 40 stations and occurred alongside other fossorial amphipod families including the Phoxocephalidae and Urothoidae. A total of 3569 specimens was reported; nine genera and 21 species were identified from the material. Among amphipods, the Oedicerotidae are a dominant part of the North Atlantic benthic fauna. Oedicerotids live within the surface sediment of the seafloor and are deposit feeders (
Figure
Pardaliscids occurred at 26 of the 40 stations studied, with a total of 327 specimens, suggesting that the family is well represented in the North Atlantic. Pardaliscids contain approximately 80 species worldwide (
Figure
Phoxocephalidae were reported from 39 of the 40 stations studied, with a total of 2134 specimens. The family Phoxocephalidae contains 375 species (
Figure
Pleustidae were reported from 16 of the 40 stations studied, with a total of 594 specimens. The family Pleustidae currently contains 241 species worldwide (
Figure
In total, 1552 stegocephalids were found at 29 of 40 stations studied. Four of these stations reported more than 100 specimens, including one with 704 individuals (station 870). Stegocephalidae have been found at all depths and temperature ranges in the IceAGE material which aligns with the findings of the BIOICE expedition (
Figure
A total of 500 stenothoid specimens were recorded from 39 of the 40 stations. Stenothoids are well known associates of molluscs, sponges, or coelenterates (
Figure
A total of 30 stilipedids was sampled from ten of the 40 stations studied. The family Stilipedidae is divided into three subfamilies and comprises six genera (Alexandrella, Astyra, Astyroides, Bathypanoploea, Eclysis and Stilipes) (
Figure
Synopiidae were sampled at 19 of the 40 stations studied, with a total of 676 specimens. The Synopiidae are a typical deep-sea family distributed worldwide (
Figure
A total of 138 individuals were present at 12 of the 40 stations examined, all situated south of Iceland (but were not found in the Norwegian Sea). This family comprises amphipods with small body size, 2 mm to 10 mm, which are highly adapted to a fossorial lifestyle (
Taking into account frequent damage of fragile Amphipoda belonging to the infraorder Corophiida, individuals with uncertain family assignation, are presented in Figure
Figure
Aorids were collected at 12 of the 40 stations, located east, south and west of Iceland (apparently absent at the northern stations), at depths between 168 and 2750 m, with a total of 105 specimens. The family Aoridae contains 250 known species world-wide belonging to 25 genera. According to
Figure
Caprellidae occurred at half of the stations sampled (18 of 40 stations), between 168 and 2747 m, with a total of 1052 specimens. The family Caprellidae is large with 91 genera and more than 400 species. Species are often epibionts, associated with other organisms such as algae, hydrozoans, bryozoans (
Figure
Dulichiids were moderately abundant at more than half the stations in all areas studied and were found in very large numbers (thousands of individuals) at two stations in the Iceland Basin. They were reported from 24 of the 40 stations studied, with a total of 6547 specimens. In our material, Dulichiidae are represented by the genus Dulichiopsis, and mainly by the species Dulichiopsis macera (Sars, 1879). It is one of the most abundant groups, dominating at stations in the Iceland Basin. The Dulichiidae currently comprises six genera (
Figure
Ischyrocerids were reported from 20 of the 40 stations studied, with a total of 731 specimens. The family Ischyroceridae is a diverse group with 269 described species worldwide (
Figure
In this study, 638 podocerids were identified from 11 of the 40 stations studied, with clusters in the waters south-west and south-east of Iceland. This diversity is almost certainly underrepresented, as some specimens were most likely identified as corophiids. The Podoceridae have undergone major changes due to the work of
Figure
Photids were collected at 12 of the 40 stations studied located all around Iceland, excluding the Irminger Basin, at depths between 118 and 2749 m, with a total of 454 specimens. Worldwide, the Photidae contain 163 known species belonging to 17 genera (
Figure
A total of 155 specimens of the family Unciolidae was recovered from ten of the 40 stations studied, in all areas and with a very wide depth range (118-2749 m). Unciolidae are comprised of 18 genera and are distributed worldwide in both cold and warm waters. There are two genera in the subfamily Unciolinae present in Nordic Seas, Neohela and Unciola. One of the largest and most conspicuous species is Neohela monstrosa (Boeck, 1861). It is common in the cold and deep waters of the Norwegian Sea from 300 to 2000 m, and is known to create burrows 10 cm deep and form dense populations on soft deep-sea sediments (
Figure
Hyperiids were reported from 22 of the 40 stations studied, with a total of 134 specimens. The Hyperiidea is a diverse planktonic suborder of amphipods comprising almost 300 species in 76 genera (
Within the benthic deep-sea invertebrate assemblages, amphipods are an abundant and diverse group. Worldwide around 10,000 species are described, about 80% of which are marine (
Similarity analysis yielded two larger groups of samples, of which one (A) is further divided into two subclusters (Figure
Dendrogram of samples for the family level data (Bray-Curtis similarity, group average grouping method and presence/absence transformed data). Abbreviations: RR - Reykjanes Ridge, NS - Norwegian Sea, DS - Denmark Strait, IB - Iceland Basin, IrmB - Irminger Basin, WFI - west off Faroe Islands, EFI - east off Faroe Islands, SFI - South of Faroe Islands, NFI - North of Faroe Islands. (Grey spotted lines indicate the samples that cannot be significantly differentiated by SIMPROF.) Regions are named based on the habitats defined by
The second major group, cluster B (Figure
Differences in family richness are also observed between cluster A1 and B. The mean number of families per sample is significantly higher in cluster A1 (Z = 3.951, p=0.00007; 21.4 ± 3.6, min = 17, max = 30) compared to cluster B (11.2 ± 1.8, min = 9, max = 14).
The spatial distribution of the clusters (Figure
Figure
For the IceAGEAmphilochidae, similarity analysis demonstrated two larger groups of samples both at relatively low levels of similarity (Figure
Dendrogram of samples for the Amphilochidae (Bray-Curtis similarity, group average grouping method standardised and square root transformed data). RR - Reykjanes Ridge, NS - Norwegian Sea, DS - Denmark Strait, IB - Iceland Basin, IrmB - Irminger Basin, WFI - west off Faroe Islands, EFI - east off Faroe Islands, SFI - South of Faroe Islands, NFI - North of Faroe Islands. Grey spotted lines indicate the samples that cannot be significantly differentiated by SIMPROF.
In the analysis of Amphilochidae from BIOICE (Figure
AmphilochidaeBIOICE Dendrogram of samples for the Amphilochidae collected during BIOICE project (Bray-Curtis similarity, group average grouping method standardised and square root transformed data). Grey spotted lines indicate the samples that cannot be significantly differentiated by SIMPROF.
Although Gitana was recorded as a deep and cold-water associated genus in the IceAGE samples, it is known to occur commonly at shallow depths in the North Sea (
More detailed analysis of the family Oedicerotidae yields two weakly marked clusters at low levels of similarity (cluster C -19%, cluster D - 4%; Figure
Dendrogram of samples for the Oedicerotidae (Bray-Curtis similarity, group average grouping method standardised and square root transformed data). Abbreviations: RR - Reykjanes Ridge, NS - Norwegian Sea, DS - Denmark Strait, IB - Iceland Basin, IrmB - Irminger Basin, WFI - west off Faroe Islands, EFI - east off Faroe Islands, SFI - South of Faroe Islands, NFI - North of Faroe Islands. Grey spotted lines indicate the samples that cannot be significantly differentiated by SIMPROF.
In assessing the Oedicerotidae species distribution patterns within the IceAGE material (for examples see Figure
Oedicerotidae genera and species have the highest diversity in the North Atlantic. As the family has not received intensive study in other regions, with the exception of the north east Pacific, it is difficult to know if this is a biodiverse region for Oedicerotidae or an artefact of taxonomic treatment. Generic level review would be meaningful to address the taxonomic errors in the literature and to better understand relationships where few characters separate groups (
The shelf-edge, especially in the Norwegian Channel, is particularly diverse. One possibility for this might be that the two northbound water masses (deep and cold, shallow and warm) mix in this zone, making possible habitats and more abundant food sources for a larger and more diverse set of species. The diversity maximum for gastropod molluscs was found to be between 400 and 450 m (
While substantial parts of Arctic waters north of Iceland, as well as the North Atlantic south of Iceland, belong to the deep sea, reaching below 3000 m on the abyssal plains, the BIOICE dataset includes only a few stations at these depths. The dataset used here contains several samples below 1000 m. The Icelandic shallow water fauna is well documented, particularly for crustaceans (Sars 1890-1895,
Other groups show similar depth patterns. In the case of deep-sea prosobranchs from the North Atlantic (Porcupine Seabight and Abyssal Plain)
The sorting effort of two workshops on IceAGE expedition material has enabled the identification of more than 20,000 amphipod specimens to the family level from Icelandic and adjacent waters. Several families were identified further to species level. Distribution maps of occurrences have been provided in a preliminary investigation of regional amphipod family distributions. Statistical analyses at the family level revealed a depth related pattern, which was supported by species level data for two abundant families in the samples, the Amphilochidae and Oedicerotidae. In all three datasets (family level, Oedicerotidae and Amphilochidae) diversity was highest at slope depths where due to upwelling effects, cold water mixes with warmer water and phytoplankton/zooplankton are more abundant, supporting previous hypotheses that thermoclines play an important role in shaping species diversity and distribution patterns in the Icelandic benthic ecosystem (
Financial support was given from the Volkswagenstiftung "Forschung in Museen" to organise the first sorting workshop in Wilhelmshaven July 2016. The second workshop in Spala (Poland) was organised with the support from the internal funds of the University of Lodz and the enthusiasm of all travelling experts. This paper would not be in this special Issue of ZooKeys without the support of the Volkswagenstiftung. Special thanks go to Antje Fischer, who always offered her technical support to solve all issues looking out for vials in the storage rooms and made specimens available to all experts involved at any time. Technical help was also provided by Karen Jeskulke solving all database issues and requests. Leon Kobe did his school practical days during the workshop in Wilhelmshaven and was a great help organizing the workshop as well as Charlotte Brenneken, who provided her student helper assistance in database entries of sorting protocols during this workshop. We thank all workshop participants who could not contribute to paper writing for their participation and sorting effort during the workshops, namely Stas Malavin, Paulina Debiec and Josh Hatton. Without the enthusiasm of Magda Blazewicz and her team the second workshop in Spala would not have been possible. Species level identification for Oedicerotidae and Amphilochidae was enabled by the Volkswagenstiftung allowing Anne-Nina Lorz, Bente Stransky, and Saskia Brix to invite the specialists for these groups to the DZMB Hamburg for research visits in April 2017 (Lauren Hughes and Ed Hendrycks) and June and August 2017 (Anne Helene S. Tandberg). Travel funds for Tammy Horton were provided by the EU ATLANTOS program. This project has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement no 633211. Alan Myers is thanked for his helpful and constructive review comments on our manuscript.
Table 1. Samples used for present study.
Data type: occurence
Explanation note: Stations are organised according to the percentage of amphipods identified to the family level. Only the stations marked in green were used for primer analysis, while all were the basis for map preparation. Amphipod taxa are presented from the most to the least abundant in all samples.
Table 2. BIOICE and IceAGE stations used for Primer analysis of Amphilochidae including information about species distribution/number of specimens per station.
Data type: occurence
Table 3. IceAGE stations used for Primer analysis of Oedicerotidae including information about species distribution/number of specimens per station.
Data type: occurence