Abstract
Oceanic islands, characterized by high levels of endemism and distinct faunas when compared to neighbouring continents, represent natural evolutionary laboratories for biologists to understand ecological and evolutionary processes. However, most studies on oceanic islands have focused on terrestrial and marine macrofaunal organisms, and ignored microscopic animals. We present here an inventory of all soft-bodied meiofaunal organisms collected during a 2-week workshop on the oceanic island of Lanzarote, Canary Islands. Our checklist included 239 species, with 88 of them endemic to the archipelago. The number of endemic species was lower in groups with a higher proportion of parthenogenetic species, while it was not significantly affected by body size and percentage of species with dispersal stages. A higher percentage of endemic species was found in isolated habitats and environments, with only annelids showing significantly higher number of endemic species in anchialine caves. Our results might be biased by the high number of indeterminate species found in our samples and the lack of knowledge of the meiofauna of the African coast. Our findings, however, provide the first insight of patterns of diversity of soft-bodied meiofauna in Atlantic oceanic islands, suggesting that island endemic species might also exist amongst microscopic animals.
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Introduction
Oceanic islands act as natural evolutionary laboratories for biologists because they are isolated, well delineated areas, comparatively younger and smaller than nearby continental zones, representing unique and independent replicates for evolutionary trajectories (Losos & Ricklefs 2009; Shaw & Gillespie 2016). In contrast to continental islands, oceanic islands have never been in contact with any other landmass, so any organism inhabiting them must have dispersed across oceanic barriers. Studies on macrofaunal biodiversity in oceanic islands usually focus on terrestrial fauna, while the marine fauna has attracted far less attention (Dawson 2016). Whereas terrestrial fauna in oceanic islands typically is characterized by high endemism and differs sharply from its continental counterpart, island marine fauna is less different from the nearby continents, due to the connectivity and dispersal facilitated by ocean currents (Ekman, 1953; Pineda et al. 2007). For example, while the percentage of endemic species in freshwater and terrestrial Hawaiian fauna averages 48%, reaching 95% in some groups, it averages only 11% in the Hawaiian marine fauna (Wagner & Funk 1995; Randall 1998; Paulay & Meyer 2002; Drew & Roderick 2005), though this difference is clouded because the marine fauna (except for fishes) has been less studied. In contrast, the occurrence of marine endemic species in oceanic islands is still significantly higher than what is found in continental marine regions (Meynard et al. 2012; Palacios-Salgado et al. 2012). This suggests that the same processes leading to a higher level of endemic species might affect both terrestrial and oceanic fauna of islands, and that differences between both realms might depend on the ecological and biological traits of different taxa. As a consequence, additional studies comparing a wider range of environmental and biological factors are necessary to understand the ecological and evolutionary processes that favour the origin of endemic species in oceanic islands (Dawson 2016).
The Canary Islands are an oceanic archipelago composed of eight volcanic islands and several islets located on the African Oceanic Plate. The number (ca. 120) and proportion (ca. 2%) of known endemic species in this archipelago’s marine habitats is lower than the number (3407) and proportion (36.8%) of endemic species in terrestrial habitats (Moro et al. 2003, Izquierdo et al. 2004). In addition, the number of marine endemic species is not evenly distributed across animal groups. For example, there are only two endemic species amongst the 299 recorded coastal fish (0.7%), which contrasts with the 96 endemic species amongst the 811 species of marine prosobranchs (11.8%) (Ávila et al., 2018). These differences may be related to biological traits found in specific groups, such as the secondary loss of pelagic larvae in several of the gastropod lineages endemic to the island (Curini-Galletti 1985, Moolenbeek and Hoenseelaar, 1989, 1998, Gofas 2007), versus the high motility of most species of fish. Yet, no study covered more groups of animals to look for differences and commonalities in the patterns of occurrence of endemic species, in order to provide inference on the potential processes driving endemism. The percentage of endemic species also differs amongst marine habitats, with the most striking case represented by the so-called anchialine ecosystems, hosting a high proportion of endemic species, often limited to one or very few populations (Iliffe et al. 1984). Anchialine habitats consist of land-locked water bodies with marine origin, which are partially isolated from the sea (Stock et al. 1986). Such habitats are relatively common in the Canary Islands, although they mostly consist of open, tidally influenced ponds colonized by marine species (Sangil et al. 2008). Extensive subterranean anchialine ecosystems are only found on the island of Lanzarote (Martínez et al. 2016), favoured by the low precipitation and the porous geological substrate of the island, which allows marine infiltration through the coastline of the island. So far, 38 species out of the 50 recorded species in the anchialine ecosystems of Lanzarote are endemic to the island (Martínez and Gonzalez, 2018). This high proportion of endemic species is probably favoured both by the partial isolation of the anchialine system and by the different ecological conditions that this environment offers compared to the surrounding coastal environments (Martínez et al. 2009).
Most faunistic studies in the coastal habitats of Lanzarote focused on macroscopic organisms, leaving microscopic animals neglected (Moro et al. 2003). This lack of studies not only obscures the contribution of these organisms to local diversity but, given that meiofauna represent a major component of biodiversity (Fonseca et al. 2018), such lack of knowledge might as well affect our understanding of general colonization and diversification processes in the island. We here present an inventory of the majority of soft-bodied meiofauna phyla in the oceanic island of Lanzarote, focusing on different types of aquatic habitats, including anchialine systems. The inventory was produced during the I International Workshop on Anchialine and Marine Meiofauna. This study has a twofold focus. First, we present an updated checklist of the soft-bodied meiofaunal species recorded during the workshop, including a description and a discussion of the main findings. Second, taking advantage of this first comprehensive dataset of soft-bodied meiofauna in an oceanic island, we assess the effects of biological and environmental variables on a set of predictors for meiofaunal diversity at two levels. (1) Regional level: we test the effect of biological variables on the number of soft-bodied meiofaunal endemic species found in the entire island. (2) Local level: we investigate the effect of environmental variables within the island, to test for differences in species richness, percentage of endemic species, and species composition across different types of habitats. At the regional level, we expect for example that groups with higher dispersal capabilities and smaller average size will have a lower percentage of endemic species in Lanzarote than other groups, as these traits are known to be associated to a more widespread distribution (Curini-Galletti et al. 2012). At the local level, we expect that the possibility for speciation events in isolated environments such as anchialine habitats and caves will be favoured; thus, a higher proportion of endemic species should be found in anchialine water bodies compared to the surrounding marine coastal environments.
Material and methods
Sampling localities
Between the 4th and 20th of October 2011, we sampled a total of 23 different localities in the island of Lanzarote, covering all types of marine, anchialine, and freshwater water bodies along the island and including habitats such as sandy beaches, pools, wells, caves, and open subtidal habitats (Fig. 1, Supplementary Table 1). Within each locality, which typically represented a single type of habitat (except for subtidal environments with caves, such as Mala, where two habitats were present), we sampled different substrates in order to obtain as many meiofaunal species as possible. Following this procedure, a total of 57 samples were collected, including sediments of different granulometry, mud, algae, and plankton tows from the water column. Sediments, mud, and algae were collected manually using plastic jars. We only collected the upper 5 cm of sediments, as this well-oxygenated layer contains the highest abundance of meiofauna (Higgins and Thiel 1988). Plankton tows were done only in the anchialine environments with a 100-μm mesh net, as 63-μm mesh nets are not efficient collecting fauna when towed by a diver (Iliffe, 2018). Freshwater and intertidal marine habitats were sampled on foot; subtidal habitats and anchialine caves were explored by scuba diving. Cave diving gear and techniques were employed within La Corona lava tube.
Different types of localities sampled during the workshop, including a Charcos de Luis anchialine pools near Órzola; b freshwater reservoir in El Chafarís; c anchialine lake at Los Jameos del Agua; d Túnel de la Atlántida; e reflective beach in El Golfo; f dissipative beach in Famara; g Mala at 48 m; h La Catedral marine cave entrance; and i cuevita de Mala entrance (photo a, Gorka Leqclerq; g, h, i, Juan Valenciano)
Soft-bodied meiofauna extraction and identification
Samples were taken to the laboratory soon after collection and processed within 1–2 days. Plankton tows were processed directly by siphoning off the water through a 63-μm mesh, in order to concentrate the fauna and get rid of the excess of water. Macroalgae samples were collected by hand, rinsed in MgCl2, and squeezed into a 63-μm mesh before sorting out the meiofauna contained. Permeable sediments were processed daily using the MgCl2 decantation technique, or by siphoning off the water just above the sediments (Higgins and Thiel 1988). Individual animals were identified alive by the specialist of each group participating in the workshop, and either fixed for detailed morphological studies or preserved in 100% ethanol for subsequent molecular analyses. We considered soft-bodied meiofauna in a broader sense and also included Priapula and Heterobranchia molluscs in our study, if they were smaller than a few millimetres. Despite ones having a moulting cuticle, and others epidermal spicules, these latter two groups of fragile animals share many traits of the soft-bodied group. We categorized as new species those that undoubtedly represented new species to science, while species with uncertain identity for which neither the status as new species nor an unambiguous identification could be performed we called doubtful. The latter ones typically included members of species complex, potential cryptic species, as well as immature and/or broken individuals showing unique traits. The total number of species recorded in the workshop are included in Table 1. A detailed description of the soft-bodied meiofaunal species obtained is provided in the first part of the manuscript.
Biological correlates of regional meiofaunal diversity
Our first goal was to investigate the effect and the importance of a set of biological variables, namely body size, dispersing capabilities, reproductive mode, and endobenthic preference, as predictors for endemism in island marine soft-bodied meiofauna. For analysing biogeographical patterns, small body size and the ecological consequences of being small are considered relevant as potentially favouring long-distance dispersal (Fontaneto 2019) and enabling widespread distribution according to the ubiquity theorem in microscopic animals (Fenchel and Finlay 2004). In both macrofauna and meiofauna, the presence of dispersal stages is known to affect endemism in many island groups (Ávila et al. 2012; Curini-Galletti et al. 2012), with taxa that are able to disperse through pelagic larval stages or dormant stages having widespread distributions. Considering reproductive mode, we expect parthenogenetic species to be able to establish a population after dispersal, even starting from a single individual, and therefore, we expect to find fewer endemic species amongst exclusively parthenogenetic species (Tilquin and Kokko 2016). We also expect to find a higher proportion of endemic species amongst endobenthic than amongst epibenthic species: endobenthic species are expected to have smaller distribution areas because they typically show adaptations to remain in the sediment (Bush 1968; Martin 1978), such as negative phototropism and adhesive glands, negatively affecting their dispersal capabilities (Curini-Galletti et al. 2012) (Table 2).
All data at the species level were merged in order to have one entry for each meiofaunal group, considering both the species found during the workshop as well as all the soft-bodied meiofaunal species previously found Lanzarote (Table 3). The proportion of endemic species for the Canary Islands for each group was calculated as including those species that are actually known as endemic plus those that are new species to science, which, being unknown anywhere else, are potentially endemic. The few species new to science found in Lanzarote that were subsequently found elsewhere outside the Canary Islands were excluded from the count of endemic species.
Explanatory variables that could affect the proportion of endemic species included body size, dispersal potential, reproductive mode, and substrate specificity. An estimate of body size (median body length) for each species was obtained from the adult individuals collected in the field and/or from literature data. Potential for dispersal was estimated by collecting information on the presence/absence of larval and resting or dispersing stages, including cysts, dormant embryos, resting eggs, and epitokous reproductive stages. For reproductive mode, we categorized organisms as exclusively parthenogenetic or not. For habitat specificity, species were grouped as exclusively endobenthic (either as interstitial or burrower) or not.
We investigated the relative importance of each of these variables using generalized linear models, including the proportion of endemic species for each meiofaunal group as a response variable and all four biological predictors as explanatory variables. A binomial distribution was assumed, as the response variable was proportion data. The significance and importance of each explanatory variable were evaluated using model averaging (Burnham et al. 2002). The relevance of the results will be based on the relative importance values from model averaging and on p values. Model averaging and relative importance of the explanatory variables were calculated with the package MuMIn v. 1.15.6 (Bartoń 2016) of the statistic software R v. 3.5.0 (Team, 2013).
Environmental correlates of local meiofaunal diversity
Our second goal was to investigate the effect of environmental differences on the occurrence of endemic species, focusing at a local level of different habitat. We used species richness (i.e. number of species), percentage of endemic species (i.e. proportion of species only found in the Canary Islands and considered as actually or potentially endemic), and differences in species composition across sampling sites as response variables against a set of environmental parameters. For these analyses, we focused only on saltwater habitats and disregarded freshwater habitat in order to avoid the statistical confounding factors of several groups that are not present or were not searched in freshwater habitats.
In saltwater habitats, we expect differences between anchialine and marine environments, between type of habitat (i.e. sandy beaches, ponds, caves, and subtidal habitats), and between type of substrate (i.e. mud, sand, algae, water column) would affect communities of microscopic animals. Anchialine environments in Lanzarote are known to harbour fewer species, but have a higher percentage of endemic species, with different communities than marine waters, especially in terms of crustaceans (Martínez et al. 2009). Thus, we expect that differences between anchialine and marine environments may have a strong effect also on meiofauna, in terms of species richness, percentage of endemic species, and species composition. Regarding type of habitat and type of substrate, we have no a priori expectations, except that differences in habitat and substrate may differentially affect meiofauna.
Richness and percentage of endemic species were investigated for the total meiofauna, as well as separately for groups with more than ten species (Annelida, Gastrotricha, Proseriata, and Rhabdocoela). As explanatory variables, we considered three factors: environment (two levels: anchialine, marine), habitat (four levels: cave, beach, pond, subtidal), and substrate (four levels: algae, mud, sediment, water). We used analysis of variance (AnoVA), implemented in R, to investigate the differences in species richness and endemism. Richness was measured as number of species, which is count data and therefore was transformed to its logarithm in the models; the proportion of endemic species for each community varied between 0 and 1, and given that this distribution is bound at the two extremes, it was transformed using the arcsine of the square root (Crawley 2012). We checked model fit by visually confirming the normal distribution of the residuals, the absence of deviation in the residual versus fitted plot, Q-Q plot, and plot of Cook’s distances.
Differences in meiofauna community composition were investigated using the Jaccard similarity index (Jaccard 1901; Chao et al. 2012) calculated for the total meiofauna and separately for the groups with more than ten species (Annelida, Gastrotricha, Proseriata, and Rhabdocoela). The explanatory variables were the same for the richness models. We used a permutational multivariate analysis of variance to investigate the differences in species composition, using the R package vegan v. 2.5.2 (Oksanen et al. 2017), since the response variable was a matrix of pairwise distances.
Results
Overview of meiofaunal diversity of Lanzarote
We recorded a total of 239 species, 86 of them undescribed and new to science and 81 with uncertain identity (Fig. 2). Amongst the 86 undescribed species, 11 were already known or subsequently found also outside of the Canary Islands. The total number of endemic species was 88, including 7 known only from the Canary Islands, and therefore considered actually endemic, together with 75 new species for science that have not been found anywhere else so far, and therefore are considered potentially endemic. From these potentially endemic species, 13 are described in this special issue and can be considered actually endemic (Di Domenico et al. 2019; Gobert et al., 2019; Scarpa et al., 2019a, b; Todaro et al., 2019a; Worsaae et al., 2019a, b), while 5 were described elsewhere (Reygel et al. 2014; Schockaert et al. 2014; 2019). Out of the 239 total species, 135 species are new records from the Canary Islands. We here provide an overview on the results for all the recorded, in alphabetical order.
Light micrographs of different animals collected during the worshop. Proseriate platyhelminth aParatoplana sp.; gastrotrichs bMusellifer delamarei, cOregodasys cirratus, and dChaetonotus lacunosus; the heterobranch gastropod eHelminthope sp. 3; the annelid fTrochonerilla sp., and gMegadrilus schneideri; the nemertean hOtotyphlonermes duplex
The 81 doubtful, unidentified species will be used in the following analyses together with the total number of species, assuming that they were not endemic, in order to use only the most consistent estimate of endemic species in the inference.
Annelida
Annelida is an animal phylum with more than 17,000 described species colonizing all types of aquatic and terrestrial environments. More than 400 meiofaunal species are found across 25 families, with 11 of these being exclusively meiofaunal or interstitial. Since the definition of both interstitial and meiofaunal is not very stringent, we here include all the species recorded in the Canary Islands belonging to these groups listed as meiofaunal in the latest published review on meiofaunal annelids (Worsaae et al 2019b). In the Canary Islands, 658 species of non-clitellate annelids (“polychaetes”) are known, out of which meiofaunal annelids accounts for 101 species, including those of the last checklist of annelids published for the islands (Núñez et al. 2005), plus a few new species described subsequently (Núñez et al. 2009; Worsaae et al. 2009).
During the workshop, we recorded 36 species of interstitial annelids, 13 of them representing new records for the archipelago (Table 2). These new records include 7 new species, three of them described in this issue (Worsaae et al 2019a, b; Di Domenico et al. 2019). The most diverse family in our samples was Nerillidae with ten recorded species. Amongst them, Mesonerilla cf. luederitzi was the most common, recorded in five stations, followed by Nerillidium sp. and Mesonerilla armoricana, both recorded in two marine stations as well as from sediments in Montaña de Arena (Túnel de la Atlántida). Nerillidium troglochaetoides, N. gracile, and Trochonerilla sp. were recorded in single marine localities. In addition, five species of Nerillidae were exclusively found in anchialine localities inside La Corona lava tube: Meganerilla cesari and Mesonerilla runae only occurred in the sediments of Montaña de Arena; Mesonerilla xurxoi and Leptonerilla diatomeophaga were found in different cinder patches, being more abundant in Los Jameos del Agua (Worsaae et al. 2009, 2019b); and the stygobitic species Speleonerilla isa was exclusively found drifting in the water column in several parts of the flooded lava tube (Worsaae et al 2019a).
Protodrilidae was the second most abundant family in number of species, with nine recorded taxa. In the open ocean, Claudrilus helgolandicus (in eight stations) and Megadrilus schneideri (three stations) were the most common species, both exhibiting high numbers of individuals. The remaining marine species, i.e. Lindrilus sp., Meiodrilus sp. 1, Meiodrilus sp. 3, and Protodrilus cf. hatscheki, were recorded in one locality each. The stygobitic protodrilid Megadrilus pelagicus was common in the water column of the dark sections of La Corona lava tube, Túnel de la Atlántida and Cueva de los Lagos (Martínez et al. 2017).
Saccocirridae was represented by two species: Pharyngocirrus cf. gabriellae and Saccocirrus parvus, while the remaining interstitial families found in this study had only one species: Polygordiidae, Psammodrilidae, Aeolosomatidae, Diurodrilidae, and Parergodrilidae (Worsaae et al. 2018).
Other interstitial annelids found in our samples were meiobenthic representatives of otherwise macrofaunal families, including two new species of the genus Macrochaeta (Acrocirridae), Raphidrilus nemasoma (Cirratulidae), Fauveliopsis glabra and F. jameoaquensis (Fauveliopsidae), Hesionides arenaria (Hesionidae), Questa cf. riseri (Orbiniidae), Hesionura elongata (Phyllodocidae), and Laubierpholoe sp. and Pisione guanche (Sigalionidae). Most of these species already were recorded from the Canary Islands in previous studies (Núñez et al. 1997, 2005, 2009; Martín et al. 1999; Moro et al. 2003; Martínez et al. 2016; Gonzalez et al., 2017, 2018).
In total, 71 species of meiofaunal annelids are known from Lanzarote, and 115 in the Canary Islands, 27 of them are considered endemic (Tables 1 and 2, Supplementary Table 2).
Cnidaria
Most meiofaunal Cnidaria belong to the order Actinulida, which includes two exclusively interstitial genera, Halammohydra with nine accepted species, and Otohydra with one. Halammohydra was previously recorded in the sediments of Montaña de Arena (Martínez et al. 2009), although the species was absent in the samples taken during the workshop, as well as in subtidal sediments from Los Abades (Tenerife) (Martínez, unpublished). During our workshop, we found representatives of both genera in Mala. Halammohydra was recorded in two stations, from sediments at 11- and 48-m depth; Otohydra was recorded only at 11-m depth (Table 2).
In total, two species of meiofaunal cnidarians seem to be present in Lanzarote and the Canary Islands, none of them endemic (Supplementary Table 2).
Gastrotricha
Gastrotricha includes, as of May 2019, 855 species, 514 of which are marine and 341 are found in fresh water (Todaro et al., 2019b). Marine species live both intertidally and subtidally, being most abundant in fine- to medium-grained sediments in crystalline waters of coastal areas (e.g. Todaro and Rocha 2004). Selected species have been found in caves or in muddy substrates (Todaro et al. 2006; Sergeeva et al. 2019). Like most other meiobenthic organisms, marine gastrotrichs have a short life cycle and lack larval stages useful for dispersal; consequently, they spend their entire existence within the sediments. Despite these life history traits, many species are not restricted to confined areas; on the contrary, they seem to be widely distributed, with some species being amphi-Atlantic or cosmopolitan (Artois, 2011; Chatterjee et al. 2019).
In the course of the current investigation, gastrotrichs were found at 7 locations and 16 stations along the eastern coast of the island of Lanzarote. Samples yielded 61 species for a total of 96 records. Thirty-six species (27 genera and 11 families) belong to Macrodasyida while 25 species (18 genera, 7 families) to Chaetonotida. Thirty-two are known species while 29 appear to be undescribed taxa or putatively so. Of the 32 known species, two were described from Tenerife and so far appear to be endemic to the Canary Islands, while the other 30 species are also present in other nearby geographic areas, e.g. the Mediterranean Sea and/or the North European coasts. More specifically, 28 species found in Lanzarote are in common with the Mediterranean and 22 are shared with the North European coasts (for detail see Supplementary Table 2 and Todaro et al., 2019a).
Gnathostomulida
Gnathostomulida is a group of microscopic, interstitial marine worms with about 100 described species (Sterrer & Sørensen 2015). Previously, five species were known from the Canary Islands (Supplementary Table 2), recorded from the islands of Gran Canaria (Playa de las Canteras) and Tenerife (Los Cristianos Bay) in shallow Cymodocea nodosa meadows (Sterrer 1997, Riera 2012). During the workshop, individuals of Austrognathia were collected in sediments from Montaña de Arena (Túnel de la Atlántida), as well as Mala at the stations at 17 m and 20 m (Table 2). This represents the second record of Gnathostomulida in cave environments, after Labidognathia longicollis was recorded from the sediments of a marine cave in Plemmirio (Sicily) (Gąsiorowski et al. 2017). Both records most likely represent marine species that survive in cave interstitial environments rather than a cave exclusive species.
In total, one gnathostomulid species has been recorded in Lanzarote, whereas in total six are now known from the Canary Islands, two of them endemic (Supplementary Table 2).
Heterobranchia, Mollusca
Mollusca is a very diverse lineage of animals with 85,000 species. Several lineages traditionally represented amongst the permanent interstitial meiofauna, mostly belonging to Gastropoda (Higgins and Thiel 1988). In this study, we focus on the heterobranchian lineages Acochlidacea and Rhodopemorpha, with 55 described species worldwide (Jörger et al. 2014).
The only Acochlidacea previously recorded in the Canary Islands is Hedylopsis spiculifera (recorded as H. suecica), found in coarse sand at Los Cancajos beach (La Palma) (Ortea et al. 2009). During our workshop survey, we found another species of acochlidacean, probably representing Pontohedyle milaschewitchii, although the specific identification needs to be confirmed with molecular barcoding (Jörger et al. 2012). The species was found in coarse poorly sorted sediments inside La Catedral marine cave. Pontohedyle milaschewitchii is widespread in the Mediterranean. In addition to these records, there is an unpublished record for Hedylopsis spiculifera, found in subtidal sandy patches at Los Abades, in Tenerife (Martínez and Jörger, unpublished).
We also provide the first record for Rhodopemorpha for the Canary Islands, which we found represented by three different forms, provisionally considered as different species, belonging to the genus Helminthope. They were collected at Punta Jameos and inside Túnel de la Atlántida, both in the water column and at the sediments of Montaña de Arena. The presence of Helminthope in the water column suggests that the colonization of Montaña de Arena by interstitial meiofauna might happen after individuals get accidentally dragged inside the cave by tidal currents. During the workshop, five additional specimens of Helminthope were collected in littoral coarse sediments at Charca de la Novia (near Orzola) (Norenburg, pers. com.).
In total, four species of heterobranch molluscs are known in Lanzarote, with six species recorded from the Canary Islands, four of them here considered endemic (Supplementary Table 2).
Nemertea
Nemertea is a phylum of animals, mostly marine, with ca. 1400 species. Meiofaunal nemerteans are represent by approximately 80 species belonging to several lineages that have colonized the interstitial realm independently. Our samples yielded six species of interstitial meiofaunal nemerteans in Lanzarote corresponding to three morphospecies of Ototyphlonemertes, two species of Cephalothrix, and one species of Nemertopsis (Table 2).
Interstitial nemerteans include a considerable amount of cryptic diversity, with morphologically distinct species complexes including several cryptic species identifiable only by use of molecular data (Leasi and Norenburg 2014). Molecular analyses allowed the identification of Ototyphlonemertes duplex D04, Ototyphlonemertes duplex D05, and Ototyphlonemertes santacrucensis S04 as putative genetic species (Leasi et al. 2016). All individuals of Cephalothrix and Nemertopsis remain identified to the genus level until molecular analyses are performed.
During the workshop, additional samples collected on the island of La Palma by one of us (JLN) yielded additional individuals of O. duplex D04, O. duplex D05, O. duplex D06, O. macintoshi M02, and O. macintoshi M03, all putative genetic species.
In total, the number of species of meiofaunal nermerteans known from Lanzarote is now six, with nine species in total recorded from the Canary Islands (Supplementary Table 2). Two species of interstitial nemertean are considered endemic to the archipelago at this time, with O. duplex D05 found on both islands, O. macintoshi M02 was found only on La Palma. Ototyphlonemertes santacruzensis S04 (found only on Lanzarote), O. duplex 06 and O. macintoshi M03, both found only on La Palma, had close genetic similarity to one or more populations along the coast of mainland Portugal, whereas O. duplex D04 had connections to Mediterranean France as well as to the UK and Sweden but, despite extensive sampling, no representation along the Portuguese coast (Leasi et al. 2016, JLN unpublished obs.).
Ototyphlonemertes appear to have very strong prey specificity (as is the case for many hoplonemerteans) as well as granulometry preferences; lack of suitably specific prey and/or habitat could limit potential successful survival in caves (JLN unpublished observations).
Priapulida
Priapulid worms (Priapulida) are a small phylum of marine, benthic worms with 22 described species (Schmidt-Rhaesa 2012). Nine species from the genera Priapulus, Priapulopsis, Acanthopriapulus, and Halicryptus are macroscopic, whereas the members the remaining genera Tubiluchus, Meiopriapulus, and Maccabeus are meiobenthic. Amongst those meiobenthic genera, Tubiluchus is the most diverse with 11 described species worldwide. One single species, Tubiluchus lemburgi, was recently described from cave and shallow water sediments in the island of Tenerife (Schmidt-Rhaesa et al. 2013). Additionally, several individuals of that genus were reported from Montaña de Arena, at Túnel de la Atlántida (García-Valdecasas 1985).
During our workshop, Tubiluchus lemburgi was collected in Mala, as well as La Catedral marine cave, Cueva de las Gambas, and Montaña de Arena in Túnel de la Atlantida. The sediments where the animals were collected ranged from fine (Mala and Cueva de las Gambas) to poorly or moderately sorted coarse sand (La Catedral marine cave and Montaña de Arena, respectively) (Table 2). The preference of the species of the genus for cave sediments has been previously highlighted, and several species have been described or recorded in cave environments including Tubiluchus troglodytes (Grotta Piccola del Ciolo, Lecce), T. australensis (unnamed cave in Lizard Island), and T. corallicola (Walsingham cave, Bermuda) (Todaro and Shirley 2003). Unidentified Tubiluchus larvae were recently recovered from small caves near La Restinga, El Hierro (García-Herrero et al. 2017) (see Sánchez and Martínez, 2019 for a complete review).
Tubiluchus lemburgi is so far the only known meiofaunal priapulid in the Canary Islands and it is considered endemic from the archipelago (Supplementary Table 2).
Proseriata, Platyhelminthes
The Proseriata is an order of free-living Platyhelminthes recognizable by their tubiform, plicatus-type pharynx, and usually very elongate, comparatively large body reaching up to 4 mm (Cannon 1986). Proseriates are almost exclusively interstitial and marine, with about 380 species described so far (Tyler 2012). The actual species diversity of the taxon is considered to be largely underestimated (Appeltans et al. 2012), and any sampling campaign reveals previously undescribed species (Curini-Galletti et al. 2012). Only six species were known from the Canary Islands before to this workshop (Supplementary Table 2) (Sopott-Ehlers 1976; Sopott-Ehlers and Ehlers 1980). The high percentage (about 70%) of previously unknown species found in the workshop held at Lanzarote is therefore not entirely unexpected.
West African meiofauna is largely unknown: this is certainly the case for Proseriata of which, apart from few data from Boa Vista (Cabo Verde Islands) (Scarpa et al. 2017, 2019a), nothing is known from the entire nearby continental African coastline. The comparatively low number of species shared with other areas of the Atlantic-Mediterranean province is however remarkable: two species with the southern coast of Portugal, seven with western Mediterranean, and only one species (Otoplana didomenicoi) shared amongst the three areas (Scarpa et al. 2019a).
On the contrary, the number of species found, although high (39, Table 2), does not particularly differ from other sites where similar workshops have been held, in Mediterranean (Curini-Galletti et al. 2012) and in tropical areas (unpubl. data), also in consideration of the high sampling effort and the diversity of habitats available in Lanzarote. Furthermore, the composition of the local proseriate fauna appears rather unbalanced compared to other parts of the world, as most species diversity is due to a few genera only. Two genera in particular (Archimonocelis and Parotoplana), out of a total of 17 genera found in the island, accounted for one-third of the total number of species.
A further peculiarity of the proseriate fauna of Lanzarote was the relative rarity of most species, found in single localities, or in very low numbers, and the stark exception represented by the two species of the genus Archilina, which in contrast were exceptionally abundant and widespread in most stations, in any kind of substrates and depths (Scarpa et al. 2019b).
In total, 39 species of proseriates are known from Lanzarote and 46 from the Canary Islands, 27 of them being endemic to the archipelago (Supplementary Table 2).
Rhabdocoela, Platyhelminthes
Rhabdocoela is a very species-rich taxon of rhabditophoran flatworms, which can be recognized by a true bulbous pharynx and a specific construction of the protonephridial flame cell. Worldwide about 1650 species are described, 60% of which (about 930 species) are from marine or brackish water. Six species of rhabdocoels were previously recorded for the Canary Islands (Supplementary Table 2): Ceratopera canariensis and Diascorhynchu bucina from sandy beaches in Gran Canaria (Sopott-Ehlers and Ehlers 1980), and Polycystis naegeli, Progyrator mamertinus, Graffiellus croceus, and Trigonostomum setigerum from Tenerife (von Graff 1913). These records represent all that was known from the rhabdocoelan fauna of the entire west coast of Africa, highlighting the lack of research in this area. In contrast, about 200 species are known from the Mediterranean (Artois, unpublished data).
During the workshop in Lanzarote, 74 species of rhabdocoels were collected: 28 dalytyphloplanids and 46 kalyptorhynchs. They all belong to the suborder Kalyptorhynchia (Table 2). Amongst them, Carcharodorhynchus flavidus was previously known from the Mediterranean (Gulf of Marseille and Sardinia), and North Carolina (USA), and Gyratrix proavus from the Baltic Sea, the Northwestern Atlantic Ocean, and the Mediterranean, Trigonostomum penicillatum from the Mediterranean and the European and American Atlantic (Willems et al., 2004; Gobert et al., 2019). Gyratrix hermaphroditus is a species complex with a worldwide distribution (Artois and Tessens 2008). Ceratopera sellai and Cystirete graeffei were previously only known from the Mediterranean (Steinböck 1933; Brunet 1965). Three species were described from the material collected during the workshop, but are also known from other areas: Brunetorhynchus microstylis also occurs in Southern France, Corsica, Sardinia, and Sweden; Cheliplana curinii also occurs in Sardinia; Proschizorhynchus martinezi also in Portugal (Gobert et al., 2019); Typhlopolycystis sarda also in Sardinia (Schockaert et al., 2019). Eight species described during the workshop can be considered endemic from Lanzarote: Brunetorhynchus canariensis, Carcharodorhynchus worsaae, Cheliplana canariensis, C. sarniensis, Cheliplanilla cavavulcanica, C. todaroi, Typhlopolycystis pluvialiae, and Pseudoschizorhynchoides timoshkini (Gobert et al. 2019; Schockaert et al., 2019). The five remaining species correspond to four new undescribed species of the genera Rogneda, Paulodora, Parachrorhynchus, Lagenopolycystis (Tessens et al. 2014), an unidentified species of the genus Toia, and a doubtful species provisionally included in the genus Proschozorhynchella (Gobert et al., 2019).
After our workshops, the number of rhabdocoels known in the Canary Islands increased to 80, including 50 kalyptorhynchs and 30 dalytyphloplanids. Fifteen of these species represent so far single island endemic species either from Gran Canaria (2 species) (Sopott-Ehlers 1976) or Lanzarote (13 species) (Tessens et al. 2014; Gobert et al., 2019), while nine are known also from European Atlantic and Mediterranean waters. Carcharodorhynchus flavidus might represent a species with amphi-atlantic distribution, although morphological differences found between European, Canarian, and Eastern Atlantic populations might indicate that different disjunct populations actually represent different species within a species complex.
Regarding the diversity of rhabdocoels in subterranean marine and cave environments, the species Cheliplana sarniensis was found in a marine cavern in Mala, whereas Proschizorhynchus martinezi, Pseuodoschizorhinchus timoshkini, Cheliplanilla cavavulcanica, and Schizochilus lanzarotensis have been collected in the sediments of Montaña de Arena in the anchialine cave of Túnel de la Atlántida. The last two species are exclusive from this locality; the rest are found also in open marine sediments.
In total, for Lanzarote, 74 species of meiofaunal rhabdocoels are known in Lanzarote and 80 in the Canary Islands, 59 of them considered endemic (Supplementary Table 2).
Rotifera
Rotifera represents a lineage of microscopic aquatic animals with around 2000 described species (Segers 2007). Most rotifers live in freshwater and limno-terrestrial habitats, and only about 400 species have been found in saline waters so far (Fontaneto et al., 2006).
The habitats we sampled in Lanzarote provided 15 species of rotifers based on morphological criteria, four bdelloids and 11 monogononts. Amongst the bdelloids, Philodina megalotrocha, P. roseola, and Rotaria rotaria and an undescribed species of Rotaria correspond to new records for Lanzarote. All monogononts were identified to genus level only (Table 2). Amongst them, Testudinella sp. does not correspond morphologically to any known species in the genus, while the remaining ten species are considered doubtful. Rotifers notoriously host a large hidden diversity, with several cryptic species for many morphospecies (Gómez et al. 2002; Fontaneto et al. 2011). DNA taxonomy will be necessary to identify some of them and to look for potential cryptic taxa.
Regarding the habitats, seven species were exclusively found in freshwater environments, including Cueva de las Siete Gotas freshwater mine and the freshwater reservoir of Mala. Philodina roseola and Rotaria sp. were exclusively found in marine environments; Filinia sp. and Lepadella sp. were found both in marine and in hypersaline habitats associated to saltpans associated to two saltworks: Testudinella sp. in Salinas del Janubio and Proales sp. 1 in Salinas del Janubio and Salinas del Río.
In total, 15 species of rotifers are now known in Lanzarote, and one of them can be considered as endemic to the island (Supplementary Table 2).
Biological correlates of regional diversity
The factor significantly explaining which taxonomic groups of the meiofauna had higher proportions of endemic species than others in Lanzarote island was reproductive mode (Multimodel Inference: p = 0.072, RI = 0.77, Table 4). The proportion of parthenogenetic species was negatively related to the number of endemic species: the groups with a higher proportion of parthenogenetic species (e.g. Gastrotricha, Rotifera) had a lower proportion of endemic species. In fact, none of the parthenogenetic species was endemic from the Canary Islands. The other biological traits revealed low relative importance and no significant effect (Table 4).
Environmental correlates of local diversity
Focusing only on the species found during the workshop, for which we had information on the habitat, the overall species richness was not affected by any of the environmental variables (Table 5). Analysing each group separately, significant differences in species richness between marine and anchialine systems were found in Annelida (AnoVA: p = 0.036, Table 5), with a higher number of species in the anchialine environments.
The proportion of endemic species was not affected by environmental differences (Table 6). Analysing each taxonomic group separately, only Annelida were significantly affected by the type of environment (anchialine vs marine) (AnoVA: p = 0.004; Table 6) and by the type of habitat (p = 0.008; Table 6), with a higher proportion of endemic species in anchialine habitats and in caves.
Most of the variability amongst our samples remained unexplained (Adonis: residual R2 = 0.756). Otherwise, differences in species composition were significantly influenced mostly by habitat type (Adonis: R2 = 0.103, p = 0.001) (Table 7), and to a lesser extent by substrate (R22 = 0.080, p = 0.016) and environments (R2 = 0.060, p = 0.042). Species composition for each of the groups separately was more affected by type of habitat rather than by any other variable in Rhabdocoela (R2 = 0.150, p = 0.034) and Proseriata (R2 = 0.128, p = 0.083), and substrate in Gastrotricha (R2 = 0.171, p = 0.185), although the results were only significant for Rhabdocoela. The variability in the species composition of Annelida was significantly explained both by the environments (R2 = 0.125, p = 0.001) and the substrate (R2 = 0.128, p = 0.001) (Table 7). However, as for the total meiofauna, most of the variability in similarity across the samples remained unexplained.
Discussion
Diversity of meiofauna in the Canary Islands
We discovered 239 species during our 2-week inventory. From these, 135 species were new records for the Canary Islands, including 86 new species to science. Our results considerably increase the diversity of most meiofaunal groups known in the Canary Islands (Supplementary Table 2), which were dramatically under-investigated before our workshop. Before this study, only six species of Rhabdocoela and six species of Proseriata were known from the Canary Islands, based on a handful of studies (see references in Gobert et al., 2019). With 74 recognized species of Rhabdocoela and 39 of Proseriata, our study multiplies the diversity of these groups four and seven times respectively. Gastrotricha were slightly better investigated in the Canary Islands, with 10 published records from two studies (Todaro et al. 2003; Rothe and Schmidt-Rhaesa 2010). Yet, out of the 61 species found in our workshop, 35 represent new records and at least 8 new species. Our results increased the diversity even for those groups that have been repeatedly investigated in the Canary Islands, such as annelids (Núñez et al. 2005). From the 36 species of annelids that we found, 13 were new records, accounting for 11 new species.
One might argue that the high proportion of new species is related to the fact that very few studies have been done in the Canary Islands before. However, previous meiofauna surveys performed with a similar sampling intensity in better-studied areas, such as Sweden and Sardinia, also yielded an impressively high number of new records and species (Willems et al. 2009; Curini-Galletti et al. 2012). In Sweden, 154 soft-bodied meiofaunal species were found, including 69 new records for Sweden with 25 new species to science; in Sardinia, 203 species were found, including 76 new species. These findings are relatively similar to those of Lanzarote, despite that comparison between the three surveys is not straightforward. It is difficult to determine whether the observed differences are true or due to different sampling strategies (i.e. investigated taxonomic groups, taxonomic specialist involved, number of stations, diversity of habitats, etc.). The effect of sampling bias and effort is a well-known problem in all biodiversity inventories, even in well-studied groups of organisms (Barbosa et al. 2010; Boakes et al. 2010), and the problem becomes potentially massive for meiofauna (Fontaneto et al. 2012).
While the number of new records and species was similar amongst Sweden, Sardinia, and Lanzarote, the number of indeterminable specimens was higher in Lanzarote. Whereas only 3 species of uncertain identity were found in Sweden, 33 were recorded in Sardinia and 81 in Lanzarote. This high number of doubtful records could be related to the lack of studies in neighbouring areas of Northwest Africa, or to the presence of many morphologically divergent species in the island. In contrast, Sweden and Italy have a long history of taxonomic research on flatworms (Karling 1940; Westblad 1948; Ax 1956a, b; Martens and Curini-Galletti, 1994), meiofaunal annelids (e.g. Pierantoni 1908, Jägersten 1952, Swedmark 1959, Jouin 1970) and rotifers (Ricci and Fontaneto 2003, Fontaneto et al. 2006), so the species found there could more accurately be identified to species level.
The lack of meiofauna studies in Northwest Africa also complicates an evaluation of the biogeographical relationships of the marine meiofauna from the Canary Islands. Mostly based on data on macrofauna, the Canary Islands has been traditionally included within the Atlantic-Mediterranean Marine Province (Bianchi et al. 2012), while more recently, it has been grouped together with Azores, Madeira, and Selvagens as a single marine ecoregion within the Lusitanian province (Spalding et al. 2007). However, due to their geographical position, Canary Islands host a considerable number of West African macrofaunal species (Hernández and Rolán 2011). Future survey in the coast of Northwest Africa might yield several of the meiofaunal species here considered as endemic, thereby changing our picture on the affinities of the Canarian meiofauna. However, with our present knowledge, the peculiarity of the Canarian fauna with respect to the rest of the Atlantic-Mediterranean Province suggests that biogeographical subdivisions based on macrofaunal taxa, mostly with more efficient ways of dispersal, may not apply to meiofaunal taxa.
Effects of biological and environmental variables on diversity
The factor significantly explaining which taxonomic groups had higher proportions of endemic species was the reproductive mode: taxa including more parthenogenetic species had a lower proportion of endemic species. Surprisingly, neither body size nor the presence of dispersal stages, which are known correlates of the possibility for frequent long-distance dispersal (Fenchel and Finlay 2004; Fontaneto 2019), had any significant effect on the number of endemic species. The role of parthenogenesis as a correlate of endemism is difficult to explain. Parthenogenetic species can establish populations starting from a small number of individuals, even only one female, avoiding the energetic costs of sexual reproduction (Tilquin and Kokko 2016). In insular terrestrial fauna, it has been demonstrated that there is a higher proportion of parthenogenetic species than in the nearby continental areas (Cuellar 1977). However, in most of these terrestrial groups, parthenogenesis evolves after the colonization of the insular environments, leading to speciation due to the isolation between insular parthenogenetic and continental sexual populations. In our analyses, we found the opposite effect, with the percentage of parthenogenetic species inversely related to endemism. This is because the parthenogenetic species in our study belong to parthenogenetic lineages (i.e. Rotifera and Gastrotricha) already present outside Lanzarote. Given that, we cannot explain the role of parthenogenesis on endemism with our current data.
Regarding the explanatory effect of environmental variables on differences in richness and percentage of endemic species, we found significant effects of the environment (marine versus anchialine) only on Annelida, which showed more species with a higher percentage of endemic species in anchialine environments. Although the higher richness of annelids in anchialine environments might seem surprising and it might be biased due to the higher effort devoted to the study of annelid diversity in La Corona lava tube, the number of annelids species in La Corona is indeed very high, representing the second group in diversity after crustaceans (Martínez and Gonzalez, 2018). In fact, La Corona lava tube is the cave with the highest number of endemic species of annelids in the world (Gerovasileiou et al. 2016). Part of this high species richness is due to the unusually high diversity of certain families such as Nerillidae, which is represented by six species inside the cave, five of them endemic and often co-occurring in the same samples (Núñez et al. 1997; Worsaae et al. 2009; Worsaae et al 2019a, b). Annelid species richness is high in general in the sediments of Montaña de Arena and Los Jameos del Agua lake (in La Corona lava tube), with a number of marine species present also outside the cave (García-Valdecasas 1985; Núñez et al. 1997; Brito et al. 2009; Martínez et al. 2016). Despite being inside the cave, these sediments resemble marine interstitial environments with comparatively high amounts of trophic resources. While reaching these habitats might be problematic for other meiofaunal groups, the presence of larvae in some species and the ability to glide in the water using the parapodia or the ciliary bands might have favoured the colonization of these environments by the minute annelids from the surrounding non-cave marine sediments possibly travelling underground with the tidal currents. Furthermore, Annelida is also the only soft-bodied meiofaunal group with species that are fully adapted to live in the water column of the cave, with two species exclusively living there (Martínez et al. 2017; Worsaae et al., 2019a). In contrast to annelids, other meiofaunal groups showed no significant differences in richness or endemism between anchialine and marine environments. This might be because many of these meiofaunal groups show lower dispersal abilities than annelids, with many of them lacking a larval dispersal stage, or being interstitial and often provided with adhesive glands and negative phototropism preventing them from emerging outside the sediments. Furthermore, except for annelids, most of the studied species lack appendages or other structures that favour their drifting in the water column, which also might reduce their chances of reaching interstitial environments deep in the cave.
In agreement with our expectations, the largest differences in species composition were found amongst habitats, with type of habitat (i.e. caves, ponds, subtidal environment, and sandy beaches) and of substrates being the most strongly influencing factor on species composition. This result was robust across all groups. The presence of different species assemblages across these different types of habitats is well known across macrofaunal species. Regarding meiofauna, several studies have already shown the presence of specific communities in sandy beaches (Di Domenico et al. 2009) and caves (Todaro et al. 2006; Janssen et al. 2013; Riera et al. 2018), supporting the pattern we could see in Lanzarote.
References
Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Bamber R, Barber A, Bartsch Im Berta A, Błażewicz-Paszkowycz M, Bock P, Boxshall G, Boyko CB, Brandão SN, Bray RA, Bruce NL, Cairns SD, Chan TY, Cheng L, Collins AG, Cribb T, Curini-Galletti M, Dahdouh-Guebas F, Davie PJF, Dawson MN, De Clerck O, Decock W, De Grave S, de Voogd NJ, Domning DP, Emig CC, Erséus C, Eschmeyer W, Fauchald K, Fautin DG, Feist SW, Fransen CMJM, Furuya H, Garcia-Alvarez O, Gerken S, Gibson D, Gittenberger A, Gofas S, Gómez-Daglio L, Gordon DP, Guiry MD, Hernandez F, Hoeksema BW, Hopcroft RR, Jaume D, Kirk P, Koedam N, Koenemann S, Kolb JB, Kristensen RM, Kroh A, Lambert G, Lazarus DB, Lemaitre R, Longshaw M, Lowry J, Macpherson E, Madin LP, Mah C, Mapstone G, McLaughlin PA, Mees J, Meland K, Messing CG, Mills CE, Molodtsova TN, Mooi R, Neuhaus B, Ng PKL, Nielsen C, Norenburg J, Opresko DM, Osawa M, Paulay G, Perrin W, Pilger JF, Poore GCB, Pugh P, Read GB, Reimer JD, Rius M, Rocha RM, Saiz-Salinas JI, Scarabino V, Schierwater B, Schmidt-Rhaesa A, Schnabel KE, Schotte M, Schuchert P, Schwabe E, Segers H, Self-Sullivan C, Shenkar N, Siegel V, Sterrer W, Stöhr S, Swalla B, Tasker ML, Thuesen EV, Timm T, Todaro MA, Turón X, Tyler S, Uetz P, der Land J, Vanhoorne B, van Ofwegen LP, van Soest RVM, Vanaverbeke J, Walker-Smith G, Walter TC, Warren A, Williams GC, Wilson SP, Costello MJ (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202
Artois T, Tessens B (2008) Polycystididae (Rhabditophora: Rhabdocoela: Kalyptorhynchia) from the Indian Ocean, with the description of twelve new species. Zootaxa 1849:1–27
Artois T, Fontaneto D, Hummon WD, McInnes SJ, Todaro MA, Sørensen MV, Zullini A (2011) Ubiquity of microscopic animals? Evidence from the morphological approach in species identification. In: Fontaneto D (ed) Biogeography ofmicroscopic organisms: is everything small everywhere? Cambridge University Press, Cambridge, pp 244–283
Ávila SP, Goud J, de Frias Martins AM (2012) Patterns of diversity of the Rissoidae (Mollusca: Gastropoda) in the Atlantic and the Mediterranean region. Sci World J 2012(164890):30
Ávila SP, Cordeiro R, Madeira P, Silva L, Medeiros A, Rebelo AC, Melo C, Neto AI, Haroun R, Monteiro A, Rijsdijk K, Johnson ME (2018) Global changes impacts on large-scale biogeographic patterns of marine organisms on Atlantic oceanic islands. Mar Pollut Bull 126:101–112
Ax P (1956a) Monographie der Otoplanidae (Turbellaria): Morphologie und Systematik. Abh Math-Naturwiss K 13:3–298
Ax P (1956b). Les turbellariés des etangs côtiers du littoral méditerranéen de la France méridionale. Vie Milieu, Suppl
Barbosa AM, Fontaneto D, Marini L, Pautasso M (2010) Is the human population a large-scale indicator of the species richness of ground beetles? Carabidae, people and sampling effort. Anim Conserv 13:432–441
Bartoń K (2016) MuMIn: multi-model inference. R package (ver. 1.15. 6)
Bianchi CN, Morri C, Chiantore M, Montefalcone M, Parravicini V, Rovere A, Stambler N (2012) Life in the Mediterranean Sea: a look at habitat changes. Nova Publisher, New York, p 739
Boakes EH, McGowan PJK, Fuller RA, Chang-Quing D, Clark NE, O’Connor K, Mace GM (2010) Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biol 8:e1000385
Brito MC, Martínez A, Núñez J (2009) Changes in the stygobiont polychaete community of the Jameos del Agua, Lanzarote, as a result of bioturbation by the echiurid Bonellia viridis. Mar Biodivers 39:183–187
Brunet M (1965) Turbellari’s calyptorhynques de substrats meubles de la région de Marseille. Rec Trav St Mar End 39:127–219
Burnham KP, Anderson DR, Burnham KP (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Bush L (1968) Characteristics of interstitial sand Turbellaria: the significance of body elongation, muscular development, and adhesive organs. Trans Am Microsc Soc 87(2):244-–251
Cannon LRG (1986) Turbellaria of the world: a guide to families & genera. Queensland Museum. 136
Chao A, Chiu C-H, Hsieh TC (2012) Proposing a resolution to debates on diversity partitioning. Ecology 93:2037–2051
Chatterjee T, Priyalakshmi G, Todaro MA (2019) An annotated checklist of the macrodasyidan Gastrotricha from India. Zootaxa 4545(4):495–510
Crawley MJ (2012) The R book. John Wiley & Sons.
Cuellar O (1977) Animal parthenogenesis. Science 197:837–843
Curini-Galletti M (1985) Taxonomic notes on Trochidae (Mollusca, Prosobranchia): two new species of Jujubinus from the Canary Islands. Basteria 49(4):133–144
Curini-Galletti M, Artois T, Delogu V, De Smet WH, Fontaneto D, Jondelius U, Leasi F, Martínez A, Meyer-Wachsmuth I, Nilsson KS, Tongiorgi P, Worsaae K, Todaro MA (2012) Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PLoS One 7(3):e33801
Dawson MN (2016) Island and island-like marine environments: marine island biogeography. Glob Ecol Biogeogr 25:831–846
Di Domenico M, Lana PC, Garraffoni ARS (2009) Distribution patterns of interstitial polychaetes in sandy beaches of southern Brazil. Mar Ecol 30(1):47–62
Di Domenico M, Martínez A, Worsaae K (2019) Saccocirridae (Annelida) from the Canary Islands with descriptions of a new species. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-019-00991-7
Drew AE, Roderick GK (2005) Insect biodiversity on plant hybrids within the Hawaiian silversword alliance (Asteraceae: Heliantheae-Madiinae). Environ Entomol 34:1095–1108
Ekman S (1953) Zoogeography of the sea. Sidgwick and Jackson, London
Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. BioScience 54:777
Fonseca G, Fontaneto D, Di Domenico M (2018) Addressing biodiversity shortfalls in meiofauna. J Exp Mar Biol Ecol 502:26–38
Fontaneto D (2019) Long-distance passive dispersal in microscopic aquatic animals. Mov Ecol 7:10
Fontaneto D, De Smet WH, Ricci C (2006) Rotifers in saltwater environments, re-evaluation of an inconspicuous taxon. J Mar Biol Assoc UK 86:623–656
Fontaneto D, Iakovenko N, Eyres I, Kaya M, Wyman M, Barraclough T (2011) Cryptic diversity in the genus Adineta Hudson & Gosse, 1886 (Rotifera: Bdelloidea: Adinetidae): a DNA taxonomy approach. Hydrobiologia 662:27–33
Fontaneto D, Barbosa AM, Segers H, Pautasso M (2012) The ‘rotiferologist’ effect and other global correlates of species richness in monogonont rotifers. Ecography 35:174–182
García-Herrero Á, Sánchez N, García-Gómez G, Pardos F, Martínez A (2017) Two new stygophilic tanaidomorphs (Peracarida, Tanaidacea) from Canary Islands and southeastern Iberian Peninsula. Mar Biodivers 49(1):107–130
García-Valdecasas A (1985) Estudio faunístico de la cueva submarina “Túnel de la Atlántida”, Jameos del Agua, Lanzarote. Nat Hisp 27:1–56
Gąsiorowski L, Bekkouche N, Worsaae K (2017) Morphology and evolution of the nervous system in Gnathostomulida (Gnathifera, Spiralia). Org Divers Evol 17:447–475
Gerovasileiou V, Martínez A, Álvarez F, Boxshall G, Humphreys WF, Jaume D, Becking LE, Muricy G, van Hengstum PJ, Dekeyzer S, Decock W, Vanhoorne B, Bailly N, Iliffe TM (2016) World Register of marine Cave Species (WoRCS): a new thematic species database for marine and anchialine cave biodiversity. RIO 2:e10451
Gobert S, Reygel P, Artois T (2019) Schizorhynchia (Platyhelminthes Rhabdocoela) of Lanzarote (Canary Islands), with the description of eight new species. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-017-0736-x
Gofas S (2007) Rissoidae (Mollusca: Gastropoda) from Northeast Atlantic seamounts. J Nat Hist 41:779–885
Gómez A, Serra M, Carvalho GR, Lunt DH (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56:1431–1444
Gonzalez BC, Petersen HC, Di Domenico M, Martínez A, Armenteros M, García-Machado E, Møller PR, Worsaae K (2017) Phylogeny and biogeography of the scaleless scale worm (Sigalionidae, Annelida). Ecol Evol 7:2894–2915
Gonzalez BC, Martínez A, Borda E, Iliffe TM, Eibye-Jacobsen D, Worsaae K (2018) Phylogeny and systematics of Aphroditiformia. Cladistics 34:225–259
Hernández J, Rolán E (2011) Moluscos y conchas marinas de Canarias: Solenogastres, Caudofoveata, Polyplacophora, Gastropoda, Bivalvia, Cephalopoda y Scaphopoda. ConchBooks, Hackenheim, p 716
Higgins RP, Thiel H (eds) (1988) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, p 488
Iliffe TM (2018) Collecting and processing crustaceans from anchialine and marine caves. J Crustac Biol 38(3):374–379
Iliffe TM, Wilkens H, Parzefall J, Williams D (1984) Marine lava cave fauna: composition, biogeography and origins. Science 225:309–311
Izquierdo I, Esquivel JLM, Zurita N, Arechavaleta M (2004) Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres. Consejería de Medio Ambiente y Ordenación Territorial. Gobierno de Canarias
Jaccard P (1901) Étude comparative de la distribution florale dans une portion des Alpes et des Jura. Bull Soc Vaudoise Sci Nat 37:547–579
Jägersten G (1952) Studies on the morphology, larval development and biology of Protodrilus. Zool Bidrag Uppsala 29:427–512
Janssen A, Chevaldonné P, Martínez-Arbizu P (2013) Meiobenthic copepod fauna of a marine cave (NW Mediterranean) closely resembles that of deep-sea communities. MEPS 479:99–113
Jörger KM, Norenburg JL, Wilson NG, Schrödl M (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evol Biol 12:245
Jörger KM, Neusser TP, Brenzinger B, Schrödl M (2014) Exploring the diversity of mesopsammic gastropods: how to collect, identify, and delimitate small and elusive sea slugs? Am Malacol Bull 32:290–307
Jouin C (1970) Recherches sur les Protodrilidae (Archiannélides). I. Etude morphologique et systématique du genre Protodrilus. Cah Biol Mar 11:367–434
Karling T (1940) Zur Morphologie und Systematik der Alloeocoela cumulata und Rhabdocoela lecithophora (Turbellaria). Acta Zool Fenn 26:1–260
Leasi F, Norenburg JL (2014) The necessity of DNA taxonomy to reveal cryptic diversity and spatial distribution of meiofauna, with a focus on Nemertea. PLoS One 9(8):e104385
Leasi F, da Andrade SC S, Norenburg JL (2016) At least some meiofaunal species are not everywhere. Indication of geographic, ecological and geological barriers affecting the dispersion of species of Ototyphlonemertes (Nemertea, Hoplonemertea). Mol Ecol 25:1381–1397
Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836
Martens PM, Curini-Galletti MC (1994) Revision of the Archiloa genus complex with description of seven new Archilina species (Platyhelminthes, Proseriata) from the Mediterranean. Bijdr Dierkd 64(3):129–150
Martin GG (1978) The duo-gland adhesive system of the archiannelids Protodrilus and Saccocirrus and the turbellarian Monocelis. Zoomorphologie 91(1):63–75
Martín GS, López E, Núñez J (1999) Two new species of the genus Pisione Grube, 1857 from Cuba and the Canary Islands (Polychaeta: Pisionidae). Ophelia 51:29–38
Martínez A, Gonzalez BC (2018) Volcanic anchialine habitats of Lanzarote. In: Moldovan OT, Kováč Ľ, Halse S (eds) Cave ecology. Springer International Publishing, Cham, pp 399–414
Martínez A, Palmero AM, Brito MC, Núñez J, Worsaae K (2009) Anchialine fauna of the Corona lava tube (Lanzarote, Canary Islands): diversity, endemism and distribution. Mar Biodivers 39:169–187
Martínez A, Gonzalez BC, Núñez J, Wilkens H, Oromí P, Iliffe TM, Worsaae K (2016) Guide to the anchialine ecosystems of Jameos del Agua and Túnel de la Atlántida. Medio Ambiente, Cabildo de Lanzarote
Martínez A, Kvindebjerg K, Iliffe TM, Worsaae K (2017) Evolution of cave suspension feeding in Protodrilidae (Annelida). Zool Scr 46:214–226
Meynard CN, Mouillot D, Mouquet N, Douzery EJ (2012) A phylogenetic perspective on the evolution of mediterranean teleost fishes. PLoS One 7:e36443
Moolenbeek RG, Hoenseelaar HJ (1989) The genus Alvania on the Canary Islands and Madeira (Mollusca: Gastropoda), part 2. Bull Zool Mus Ams 11(27):215–228
Moolenbeek RG, Hoenseelaar HJ (1998) The genus Alvania on the Canary Islands and Madeira (Mollusca: Gastropoda), part 2. Bull Zool Mus Ams 16(8):53–62
Moro LA, Martin JL, Garrido MJ, Izquierdo I (2003) Lista de especies marinas de Canarias (algas, hongos, plantas y animales). Consejería de Política Territorial y Medio Ambiente del Gobierno de Canarias
Núñez J, Ocaña O, Brito M (1997) Two new species (Polychaeta: Fauveliopsidae and Nerillidae) and other polychaetes from the marine lagoon cave of Jameos del Agua, Lanzarote (Canary Islands). Bull Mar Sci 60:252–260
Núñez J, del Brito MC, Docoito JR (2005) Anélidos poliquetos de Canarias: catálogo de especies, distribución y hábitats. Vieraea 33:297–321
Núñez J, Martínez A, Brito MC (2009) A new species of Sphaerosyllis Claparède, 1863 (Polychaeta: Syllidae: Exogoninae) from the Atlantida tunnel, Lanzarote, Canary Islands. Mar Biodivers 39:209–214
Oksanen J, Blanchet F, Friendly M, et al (2017) Vegan: community ecology package 2017. R package version 2.4–4
Ortea J, Moro L, Bacallado JJ, Sanchez JJ, Telle A, Herrero R (2009). Nuevas aportaciones al inventario de las babosas marinas del archipiélago canario (Mollusca: Opisthobranchia y Sacoglossa). Vieraea 37:105–117.
Palacios-Salgado DS, Burnes-Romo LA, Tavera JJ, Ramirez-Valdez A (2012) Endemic fishes of the Cortez biogeographic province (Eastern Pacific Ocean). Acta Ichthyol Piscat 42:153–164
Paulay G, Meyer C (2002) Diversification in the tropical Pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integr Comp Biol 42:922–934
Pierantoni U, 1908. Protodrilus Fauna Flora Golf Neapel 31:1–226
Pineda J, Hare JA, Sponaugle SU (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20(3):22–39
Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268
Reygel P, Schockaert E, Janssen T, Artois T (2014). Two new species of Carcharodorhynchus Meixner, 1938 (Platyhelminthes: Rhabdocoela: Schizorhynchidae) from Brazil and Lanzarote. Marine Biodiversity, 44(3):279–285.
Ricci C, Fontaneto D (2003) Mediterranean rotifers: a very inconspicuous taxon. Biogeographia 24(1):161–167
Riera R (2012) Check-list of the gnathostomulids from the Canary Islands (NE Atlantic Ocean). Rev Acad Can Cienc 24:51–54
Riera R, Monterroso Ó, Núñez J, Martínez A (2018) Distribution of meiofaunal abundances in a marine cave complex with secondary openings and freshwater filtrations. Mar Biodivers 48(1):203–215
Rothe B, Schmidt-Rhaesa A (2010) Oregodasys cirratus, a new species of Gastrotricha (Macrodasyida) from Tenerife (Canary Islands), with a description of the muscular and nervous system. Meiofauna Mar 18:49–66
Sánchez N, Martínez A (2019) Dungeons and dragons: two new species and records of Kinorhyncha from anchialine cenotes and marine lava tubes. Zool Anz 282:161–175
Sangil C, Clemente S, Concepción L, Hernández JC, Toledo K, Martínez A, De León RF (2008) Ambientes litorales marginales en las islas Canarias: estructura y composición de las comunidades bentónicas en las Lagunas de Echentive (La Palma). Vieraea 36:143–162
Scarpa F, Cossu P, Delogu V, Lai T, Sanna D, Leasi F, Norenburg JL, Curini-Galletti M, Casu M (2017) Molecular support for morphology-based family-rank taxa: The contrasting cases of two families of Proseriata (Platyhelminthes). Zool Scr 46:753–766
Scarpa F, Cossu P, Sanna D, Lai T, Casu M, Curini-Galletti M (2019a) New insights on the genus Otoplana Du Plessis, 1889 (Platyhelminthes: Proseriata), with description of two new species from the Canary Islands. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-017-0785-1
Scarpa F, Sanna D, Cossu P, Lai T, Casu M, Curini-Galletti M (2019b) How to achieve internal fertilization without a vagina: the study case of the genus Archilina Ax, 1959 (Platyhelminthes, Proseriata) from Canary Islands. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-018-0890-9
Schmidt-Rhaesa A (2012) Priapulida. In: Handbook of zoology. Gastrotricha, Cycloneuralia and Gnathifera. Volume 1: Nematomorpha, Priapulida, Kinorhyncha and Loricifera. De Gruyter Berlin, pp 147–180
Schmidt-Rhaesa A, Rothe BH, Martínez A (2013) Tubiluchus lemburgi, a new species of meiobenthic Priapulida. Zool Anz 253:158–163
Schockaert E, Moons P., Janssen T, Tessens B., Reygel P, Revis N, Jouk P & Artois T (2019). On the genus Typhlopolycystis Karling, 1956 (Platyhelminthes, Kalyptorhynchia, Polycystididae) with data on the five known species and the description of eleven new species. Zootaxa Zootaxa 4603(1):81-104
Schockaert ER, Martens PM, Revis N, Janssen T, Willems W & Artois TJ (2014). A new genus with six new species of Typhlopolycystidinae Evdonin, 1977 (Platyhelminthes, Kalyptorhynchia, Polycystididae). Zootaxa 3755(3):259–272.
Sergeeva NG, Ürkmez D, Todaro MA (2019) Significant occurrence of Musellifer profundus Vivier, 1974 (Gastrotricha, Chaetonotida) in the Black Sea. Check List 15(1):219–224
Segers H (2007) Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy, and distribution. Zootaxa 1564(1):1–104
Shaw KL, Gillespie RG (2016) Comparative phylogeography of oceanic archipelagos: hotspots for inferences of evolutionary process. PNAS 113:7986–7993
Sopott-Ehlers B (1976) Interstitielle Macrostomida und Proseriata (Turbellaria) von der französischen Atlantikküste und den Kanarischen Inseln. Mikr Meeres 60:1–35
Sopott-Ehlers B, Ehlers U (1980) Zur Systematik und geographischen Verbreitung interstitieller Turbellarien der Kanarischen Inseln. Mikrofauna des Meeresboden 80:1–23
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. AIBS Bull 57:573–583
Steinböck O (1933) Die Turbellarienfauna der Umgebung von Rovigno. Thalassia 1:117–149
Sterrer W (1997) Gnathostomulida from the Canary Islands. Proc Biol Soc Wash 110:186–197
Sterrer W, Sørensen MV (2015) Phylum Gnathostomulida. In: Handbook of zoology: gastrotricha. Walter de Gruyter, Cycloneuralia and Gnathifera, pp 135–196
Stock JH, Iliffe TM, Williams D (1986) The concept of “anchialine” reconsidered. Stygologia 2:90–92
Swedmark B (1959) Archiannélides Nerillidae des côtes du Finistère. Arch Zool Exp Gén 98:26–42
Team RC (2013) R development core team. RA Lang Environ Stat Comput 55:275–286
Tessens B, Janssen T, Artois T (2014) Molecular phylogeny of Kalyptorhynchia (Rhabdocoela, Platyhelminthes) inferred from ribosomal sequence data. Zool Scr 43:519–530
Tilquin A, Kokko H (2016) What does the geography of parthenogenesis teach us about sex? Philos Trans R Soc Lond Ser B Biol Sci 371:20150538
Todaro MA, Rocha CEF (2004) Diversity and distribution of marine Gastrotricha along the northern beaches of the state of São Paulo (Brazil), with a description of Macrodasys fornerisae sp. nov. (Macrodasyida, Macrodasyidae). J Nat Hist 38:1605–1634
Todaro MA, Shirley T (2003) A new meiobenthic priapulid (Priapulida, Tubiluchidae) from a Mediterranean submarine cave. Ital J Zool 70:79–87
Todaro MA, Ancona P, Marzano A, D’Addabbo MG (2003) A new Tetranchyroderma species (Gastrotricha, Macrodasyida, Thaumastodermatidae) from the Canary Islands (Spain). Cah Biol Mar 44:191–197
Todaro MA, Leasi F, Bizzarri N, Tongiorgi P (2006) Meiofauna densities and gastrotrich community composition in a Mediterranean Sea cave. Mar Biol 149(5):1079–1091
Todaro MA, Cesaretti A, Dal Zotto M (2019a) Marine gastrotrichs from Lanzarote, with a description of a phylogenetically relevant species of Urodasys (Gastrotricha, Macrodasyida). Mar Biodivers 49(5). https://doi.org/10.1007/s12526-017-0747-7
Todaro MA, Dal Zotto M, Kanneby T, Hochberg R (2019b) Integrated data analysis allows the establishment of a new, cosmopolitan genus of marine Macrodasyida (Gastrotricha). Sci Rep 9:7989
Tyler S (2012) Turbellarian taxonomic database. http://turbellaria.umaine.edu. Accessed Dec 2018
von Graff L (1913) Das Tierreich, 35. Turbellaria II. Rhabdocoelida. Verlag von Friedklander und Sohn, Berlin, 484
Wagner WL, Funk VA (1995) Hawaiian biogeography. Smithsonian Institution Press, 467
Westblad E (1948) Studien über skandinavische Turbellaria. Acoela V Ark Zool, A 33:1–82
Willems W, Artois T, Vermin W, Schockaert E (2004) Revision of Trigonostomum Schmidt, 1852 (Platyhelminthes, Typhloplanoida, Trigonostomidae) with the description of seven new species. Zool J Linn Soc-Lond 141:271–296
Willems WR, Curini-Galletti M, Ferrero TJ, Fontaneto D, Heiner I, Huys R, Ivanenko VN, Kristensen RM, Kånneby T, MacNaughton MO, Martínez-Arbizu P, Todaro MA, Sterrer W, Jondelius U (2009) Meiofauna of the Koster-area, results from a workshop at the Sven Lovén Centre for Marine Sciences (Tjärnö, Sweden). Meiofauna Mar 17:1–34
Worsaae K, Martínez A, Núñez J (2009) Nerillidae (Annelida) from the Corona lava tube, Lanzarote with description of Meganerilla cesari n. sp. Mar Biodivers 39:195–207
Worsaae K, Giribet G, Martínez A (2018) The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae. Invertebr Syst 32:774–793
Worsaae K, Mikkelsen M, Martínez A (2019a) Description of six new species of Mesonerilla (Nerillidae, Annelida) and an emended description of M. intermedia Wike, 1953, from marine and cave environments. Mar Biodivers 49(5). https://doi.org/10.1007/s12526-019-00984-6
Worsaae K, Gonzalez BC, Kerbl A, Nielsen SH, Jørgensen JT, Armenteros M, Iliffe TM, Martínez A (2019b) Description and evolution of the stygobitic Speleonerilla nom. nov. (Nerillidae, Annelida) with description of three new species from anchialine caves in the Caribbean and Lanzarote. Mar biodivers 49(5). https://doi.org/10.1007/s12526-018-0906-5
Acknowledgements
We are grateful to Elena Mateo and Leopoldo Moro for their assistance obtaining the permissions to sample during the workshop. We are in debt to the divers Luis E. Cañadas, Enrique Domínguez, Carola D. Jorge, and Ralf Schoenemark, who assisted us collecting sediments, especially those from Montaña de Arena. The workshop was funded by Consejería de Medio Ambiente del Cabildo de Lanzarote and Reserva de la Biosfera. We thank Aula de la Naturaleza de Lanzarote for providing housing and space to set up our labs during the workshop. We are in debt to the diving clubs Pastinaca (Arrecife) and Punta Mujeres (Haria), and particularly to Antonio Martín and Juan Valenciano, for lending us diving gear and support. Juan Valenciano kindly sailed us for the collection of samples outside La Corona lava tube and provided some of the pictures used to illustrate this manuscript.
Funding
Collections in Lanzarote and secondary laboratory costs were financially supported by the Danish Research Council (grant no. 272–06–0260 to KW) and the Carlsberg Foundation (2010_01_0802 to KW) as well as Consejería de Medio Ambiente del Gobierno de Lanzarote and authorized by Gobierno de Canarias and Centros Turísticos. AM was supported by Marie Skolodowska-Curie Individual Fellowship (grant number 745530 – “ANCAVE – Anchialine caves to understand evolutionary processes”). Nemertean fieldwork by JLN, subsequent laboratory work, and analyses were supported by the Smithsonian National Museum of Natural History and private funds.
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This article is a contribution to the Topical Collection Interstitial and cave diversity in Atlantic oceanic islands
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Martínez, A., Di Domenico, M., Leasi, F. et al. Patterns of diversity and endemism of soft-bodied meiofauna in an oceanic island, Lanzarote, Canary Islands. Mar Biodiv 49, 2033–2055 (2019). https://doi.org/10.1007/s12526-019-01007-0
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DOI: https://doi.org/10.1007/s12526-019-01007-0