Reply to Smith et al .: Network analysis reveals connectivity patterns in the continuum of reducing ecosystems
2017; Royal Society; Volume: 284; Issue: 1863 Linguagem: Inglês
10.1098/rspb.2017.1644
ISSN1471-2954
Autores Tópico(s)Coral and Marine Ecosystems Studies
ResumoYou have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Kiel Steffen 2017Reply to Smith et al.: Network analysis reveals connectivity patterns in the continuum of reducing ecosystemsProc. R. Soc. B.2842017164420171644http://doi.org/10.1098/rspb.2017.1644SectionYou have accessInvited replyReply to Smith et al.: Network analysis reveals connectivity patterns in the continuum of reducing ecosystems Steffen Kiel Steffen Kiel http://orcid.org/0000-0001-6281-100X [email protected] Google Scholar Find this author on PubMed Search for more papers by this author Steffen Kiel Steffen Kiel http://orcid.org/0000-0001-6281-100X [email protected] Google Scholar Find this author on PubMed Search for more papers by this author Published:27 September 2017https://doi.org/10.1098/rspb.2017.1644The role of whale falls in the connectivity among, and adaptation to, reducing ecosystems in the deep sea has been the matter of a long debate [1,2]. Hydrothermal vents are the most extreme among the reducing habitats in terms of temperature, metal concentrations and in their geographical isolation, and it is hence thought that stepping stones are needed to reach them. As new types of reducing habitats are being discovered, they are now increasingly seen as a ‘continuum of reducing ecosystems’ [3]. Taking this concept seriously implies that any habitat type within this continuum could provide connectivity to any other. Thus rather than focusing just on whales, I will address the issues raised by Smith et al. [4] in the context of the question ‘who provides connectivity with whom, and to which extent?’Smith et al. point out that whale falls are severely undersampled and unevenly sampled (i.e. missing the infauna) in most of the world's oceans and that this would be the main reason for the lack of connectivity between whale falls, vents and seeps found in my original study [5]. Here I present a new analysis with the aim to reduce the impact of sampling biases.Two measures were taken to reach this aim: first, the new dataset consists of only the sites along the margin of the northeast Pacific Ocean from my original dataset [5], where all ecosystems types occur and especially the whale falls are well sampled, and includes bare-rock vents (hereafter referred to simply as vents), sedimented vents, whale falls, seeps and a hydrothermal seep (table 1). The following updates to the dataset were made: the whale-fall fauna in 2890 m depth in Monterey Canyon (MontereyWhale) now includes Pliocardia_I and Calyptogena, and Archivesica was removed, following new data presented in a recent study on vesicomyid phylogeny [6]. I also added the molluscan fauna of a grey-whale carcass implanted at 1675 m depth in the Santa Cruz Basin on the California margin (as ‘SantaCruzWhale’ in table 1), which consists of the genera Hyalogyrina, Idas, Archivesica, Pliocardia_I and Calyptogena [7]. Although Smith et al. warned that even including these new data would be insufficient to yield reliable results, I think that by restricting the analysis to the northwestern Pacific margin and by employing the subsampling approach outlined below, network analysis will provide meaningful new insight into the question of connectivity among reducing ecosystems. Table 1.The sites used in this analysis, their habitat types and average betweenness centrality values from 100 000 iterations of the subsampling procedure; see the original study for details on site names. (sed.vent, sedimented vent; hydro.seep, hydrothermal seep.) Collapse site (m depth)ecosystem typebetweenness centralityGuaymas (2020–2033)sed.vent14.24NicolasWhale (960)whale fall7.94Gorda (2700–3271)sed.vent7.68SantaCruzWhale (1675)whale fall7.38Sonora (1550)seep6.77JdFMV (2423)vent4.87JdFAx (1500–1600)vent4.39JaliscoBlock (3800)seep4.02CostaRicaU (741–997)seep2.98MontereyWhale (2893)whale fall2.87JacoScar (1752–1805)hydro.seep2.52JdFExplorer (1762)vent2.35CostaRicaM (1007–1854)seep2.23HydrateRidge (770)seep2.08MontereyShallow (635–1000)seep1.76JdFEndeavour (2200–2400)vent1.06CatalinaWhale (1240)whale fall1.04AleutianT (4800–4960)seep0.26Second, to simulate more even sampling, an iterative subsampling procedure was applied that randomly choose five taxa from each site in the new dataset to construct the network (five was the lowest number of taxa present at any of the whale-fall sites). This subsampling procedure was repeated 100 000 times to calculate averages of the following values: first, as an indicator for the overall connectedness of each site, its betweenness centrality was computed. The general concept of betweenness centrality is illustrated in figure 1a, though in the present analysis also the weights of the links were taken into account (see [8] for the algorithm). Second, to assess the degree of connectivity of each habitat type, for each site the average weights of its links to each habitat type were calculated (figure 1b for an illustration of this approach). All analyses were performed in the statistical computing language R [9], using the packages ‘igraph’ v. 1.01 [10] and ‘vegan’ v. 2.4-2 [11]. The complete R code is provided in the electronic supplementary material. Figure 1. Illustration of the measures for connectivity used herein. (a) Betweenness centrality: the numbers at each node indicate the number of shortest paths going through them. The shortest paths from node A to nodes C and D are via node B; all other shortest paths between the nodes in this network are direct links. (b) Weights of links by habitat type; consider the red node: it is linked to two blue habitats at an average weight of 0.5, and to only one yellow habitat, though at a weight of 0.8. The red habitat provides connectivity between the yellow and blue habitats, but the yellow habitat plays no role in connecting the blue and the red habitat; and neither does the blue habitat connect the red and the yellow habitat.Download figureOpen in new tabDownload PowerPointThe betweenness centrality values (table 1) indicate that the Guaymas sedimented vent site has by far the highest connectivity within the continuum of reducing ecosystems along the northeastern Pacific margin. Also the well-sampled Nicolas and Santa Cruz whale falls show high connectivity, as does the Gorda Ridge sedimented vent site. The ‘average link weights by habitat’ (figure 2) provide more detailed insights into the patterns of connectivity: vents are strongly linked to other vents, and show low connectivity to seeps and whale falls. Also whale falls are strongly linked among themselves, and show mostly low to moderate connectivity to the other ecosystems. Seeps show an overall low connectivity. Sedimented vents show moderate connectivity to all ecosystem types and have overall the most balanced connectivity, as they lack the very high or low values seen at the other habitat types (figure 2). Figure 2. Connectivity within the continuum of reducing ecosystems, as indicated by the weights of the links of each site, averaged by habitat type. Red, vent; purple, sedimented vent; yellow, whale fall; blue, seep. Note that for clarity the Jaco Scar hydrothermal seep is not included in this figure, and that the inverse value of the actual weights of the links is shown, so that a high value indicates high connectivity. See the electronic supplementary material, table S1 for the complete results.Download figureOpen in new tabDownload PowerPointThe potential impacts of various other variables in shaping connectivity pattern, including water depth and geographical proximity, were ignored. The analysed seeps had by far the widest depth range, which could potentially have contributed to their low overall connectivity. Geographical proximity could have contributed to the high connectivity among vents because they are all located along the Juan de Fuca Ridge, and among whale falls because the two best-sampled sites are located not far from each other just offshore California.My interpretation of these results is that while sedimented vents provide connectivity across all investigated ecosystem types, vents and whale falls are highly connected among themselves, but their importance in connecting different ecosystem types does not match that of sedimented vents. The low-moderate connectivity of whale falls to seeps and sedimented vents supports the claim of Smith and co-workers that ‘whale falls may well represent an intermediate habitat type between soft sediment vents and seeps’ [4,12]. The connectivity between whale falls and bare-rock vents, however, appears to be low (figure 2). Thus, the claim that whales provide ‘stepping stones to deep-sea vents’ seems to hold only for sedimented vents, but not for bare-rock vents, at least not in a straight forward way.Another aspect of the stepping stone hypothesis put forward by Smith and colleagues poses that the appearance of whales in the early Cenozoic Era ‘could have driven evolution by providing ecological stepping stones to isolated habitats for which a species was already adapted, expanding its geographic range and facilitating speciation in remote locations' [13, p. 583]. On higher taxonomic level, many clades inhabiting vents and seeps have a nearly global distribution [14], so the globally distributed whales could indeed have facilitated their radiation and dispersal. However, a nearly globally distributed seep fauna can now be traced into the Earth's history to the Triassic Period (approx. 230 Ma [15]) and has thus existed much longer than whales. Cretaceous plesiosaurs hosted a seep-like fauna [16], so one might argue that instead of whales, large marine reptiles facilitated dispersal and evolution during the Mesozoic Era. However, invertebrate animals have colonized hydrothermal vents already during the Silurian Period (more than 420 Ma [17]), long before the advent of aquatic tetrapods, showing that adaptation to, and dispersal between, these extreme environments is possible also in the absence of putative sulfide-emitting carcasses.The onset of modern plate tectonics, including the development of back-arc basins with sedimented vents, dates back to 2 to 3 billion years ago [18]. Thus while marine tetrapods had waxing and waning abundances through the Earth's history and occasionally disappeared altogether owing to mass extinction events, the habitat type identified here as the most important link between vents and seeps has continuously existed since the origin of animals, and probably provided stepping stones throughout the continuum of reducing ecosystems. Therefore, despite the higher connectivity of whale falls shown in my new analysis compared to my original study, I remain sceptical that whales have played the major role in the evolution of the deep-sea chemosynthetic fauna that Smith et al. attribute to them.In summary, based on my new analysis: — I agree with Smith et al. that the role of whale falls in connecting reducing ecosystems was underestimated in my original study, owing to the sampling biases pointed out by them;— sedimented vents do indeed provide the strongest link between vents and seeps, and are overall the most important habitat type for providing connectivity within the continuum of reducing ecosystems; and— I maintain my point that network analysis is a viable and promising tool to investigate connectivity patterns among reducing habitats.Lastly, it should be pointed out that this analysis is based exclusively on molluscs, and that other clades might have different connectivity patterns, as shown previously [19].Data accessibilityAll data and computer code associated with this manuscript are available as the electronic supplementary material to either this or the original manuscript (doi:10.1098/rspb.2016.2337 [5]).Competing interestsI have no competing interests.FundingWe received no funding for this study.FootnotesThe accompanying comment can be viewed at http://dx.doi.org/10.1098/rspb.2017.1281.Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3889087.© 2017 The Author(s)Published by the Royal Society. 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