However, in order for policies to be effective, conservation management must have an accurate record of the native biota and must be able to trace and manage potential introduction pathways and vectors [7, 8]. In El Arbeyal, low recruitment may have led to the strongly female-biased sex ratio in April 2012. In all specimens, the external edge of the outer marginal was smooth. With a few exceptions [38–40], slipper limpets tend to be gregarious to variable degrees [15, 17, 18, 20, 21, 39]. This change in sex ratio was probably due to higher male mortality. Four linear shell dimensions, SL, shell width (SW), width of the shell septum (SS), and maximum height of the septum curvature (SC) were measured on scaled images (Fig 1). Shell shape polymorphism was unevenly distributed among sites and among sexes. 11 metric tons) of mussels once, in 2002 (S2 Table). No, Is the Subject Area "Sex ratio" applicable to this article? Conceptualization, Citation: Richter A, Gándara AM, Silva F, Brante A (2018) The alien slipper limpet Crepipatella dilatata (Lamarck, 1819) in northern Spain: A multidisciplinary approach to its taxonomic identification and invasive biology. During the period from 1999 to 2014, the Principality of Asturias, the autonomic community to which Gijon pertains, did not import fresh mussels from Chile. Among stack-forming species, shell morphs that are highly convex and narrow form larger chains than shell morphs that are broader and shallower [81]. Data points from a multidimensional vector space defined by seven linear and non-dimensional morphological shell variables and 59 individuals were plotted on the bi-dimensional space spanning the first two PCs of the PCA. The remaining three individuals were intersex stages. Males of C. dilatata have a more flexible and less adhesive foot [100] and may be more easily detached from the substratum than females and thus more vulnerable to wave action and predators. Since SW/SL, SC/SS and SC/SL explained the highest variance for PC 3, PC 2 and PC 1 respectively, these explanatory variables (untransformed) were used to test for significant differences among the four morphotypes. A relationship between aggregate composition and timing or size at sex change has been reported in other protandric marine gastropods with socially controlled sex change; this includes calyptraeids [17–21, 64]. Simultaneous hermaphrodites may double the number of mating partners [11]. lecithotrophy, adelphophagy, or nurse egg feeding) and the intracapsular larval stages were recorded. Recruits larger than 2 mm and outside the mother shell were absent. An a posteriori Tukey test for unequal sample sizes (unequal N HSD) was run to detect significant differences among pairs. Grigore Antipa National Museum of Natural History, Bucharest, Romania, The intercontinental import of fresh mussels cultivated in Chilean farms is a likely source of this mussel in Spain. Gregariousness may occur throughout most of the benthic life phase or be restricted to the breeding season, as in the invasive Japanese oyster drills Ocinebrellus inornatus and Rapana venosa [92]. https://doi.org/10.1371/journal.pone.0205739.g009. par no tener blen fljadaa IaA Ln- Este org-JAM0 Ldopt4 to. Phone: +56 9 9219 2787 Call. Click through the PLOS taxonomy to find articles in your field. Significance was also tested. urmis lilt df- asentarse ell Ia ou'r,,wd I batido problenia del desarme de lost 'a fotografia de las doe; chaps que wRaa DroDone. Less apparent and finer details of the soft body such as the morphology of the male penis and female genital papilla, the arrangement of the pallial reproductive system, extension of the mantle, the dorsal arrangement of the visceral organs (Fig 2A and 2B) and the internal anatomy of the feeding system also largely match Collin’s observations [72]. In contrast to El Arbeyal, the O Grove population was intensively recruiting juveniles in autumn 2012. In O Grove, the total number of eggs per egg-capsule varied between 46 and 977 (mean = 549.00, SD = ± 75.71, n = 15) and estimated female fecundity ranged from 962.5 to 14247 (mean = 6487.14, SD = ± 1904.44, n = 7) in September 2012. Comparison with available data of native populations of C. dilatata strongly indicate that ecophenotypic plasticity, socially controlled sex change, high gregariousness, increased nurse egg supply to viable larvae during the encapsulated developmental period, later maturation and larger female sizes altogether enhance establishment success of this non-indigenous species. For purporses of simplifying the present and eventual future descriptive and comparative studies of C. dilatata’s shell morphology, a General Linear Model (GLM) analysis of variance was in addition conducted to establish differences among the four morphotypes only in those explanatory variables contributing most to the variance of each extracted PC; this was done in STATISTICA 8.0 [60]. In El Arbeyal, individuals were found both clinging to clumps of M. galloprovincialis mussels of marketable size scattered on the sea bottom and to wild native mussels overgrowing artificial substrata; individuals were not, however, found on the cup oyster Crassostrea sp. Mean female SL, size at female maturity or sex change (L50), and maximum SL (Lmax) vary greatly across the current distribution ranges (both native and introduced) of this species with values for Spanish populations falling within the range of variation observed in native populations (Table 7). Considering that the Ebro Delta is an important shellfish production centre and the second largest M. galloprovincialis mussel culture region in Spain [108], and assuming the presence of C. dilatata in this locality as certain, we propose that any of the following activities may contribute to a hypothetical secondary dispersal of C. dilatata from Galicia to the Ebro Delta: a) transplantation of mussel seeds produced on floating Galician nursery rafts to mussel farms in the Ebro Delta for growth to commercial size, b) transplantation of ripe mussels from Galician rafts to rafts in the Ebro Delta to restock mussel farms, and c) transplantation of marketable size mussels to the Ebro Delta to satisfy consumer demands. It may be used as reference for future comparative studies. https://doi.org/10.1371/journal.pone.0205739.t002. … NO trate de cambiar ninguna pieza del lente laser. In Spanish specimens of C. dilatata, a maximum of five to six members per stack was observed in O Grove, while in El Arbeyal, where the cluster 2 shell morph was absent, stacks were formed by a maximum of three individuals. External gross anatomy of the head-foot and soft body pigmentation (Fig 2A and 2B) coincided with the descriptions and figures of Crepipatella dilatata (as Crepidula dilatata) provided by Gallardo [71], Collin [72] and Strebel [73]. In two focal individuals with dislodged hitchhikers from the September 2012 O Grove sample, home scars with maximum diameters between 8.0 and 20.25 mm were assigned to males, those between 20.25 and 29.75 mm were assigned to intersex stages, and those larger than 29.75 mm were assigned to females. The radulae of all the specimens from Spain here examined (Fig 2C) were typically taenioglossate, bilateral-symmetrical with a trapezoidal rachidian tooth in the centre of the radular ribbon flanked on either side by a broad lateral tooth and two slender marginal teeth, a sickle-shaped inner marginal and a thinner, hooked outer marginal. The COI gene was amplified using the universal primers HCO2198 and LCO1490 [67] in 30 μL reactions containing 3 μL of PCR buffer (10X), 3.6 μL MgCl2 (25 mM), 1.5 μL dNTPs (2.5 mM), 0.3 μL BSA (100X), 0.3 μL of each primer (10 μM), 0.25 μL Taq polymerase TopTaq (Quiagen, 5 U μL-1) and 3 μL of genomic DNA diluted 1/25. In the period between 1998 and 2006, Galicia imported annually between 10 and 532.02 metric tons of fresh mussels (M. galloprovincialis) from Chile for its canning industry. Crassostrea sp. Taking into account that C. dilatata is a protandric species and that females incubate their offspring in the free space between the free edge of the septum and the mantle edge [31], an increase in the SC/SL ratio during ontogeny allows for an expansion of the brood area per unit of shell aperture area in individuals changing sex from male to female. The sex ratio of the declining population was female biased while in the established population the sex ratio changed during the study period from being balanced to being female biased. Methodology, This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. In 2010, a reproductive population of C. dilatata was reported close to the commercial port of Gijon on the central Cantabrian coast (North Spain) [49, 50], and more recently, in 2014, several individuals were found in the Ebro Delta on the Mediterranean coast of Spain [51]. An estimate of the fecundity could not be done for specimens from El Arbeyal, because the eggs in each capsule had fixation problems. Secondly, in the introduced region, living C. dilatata may be found attached to stones and empty bivalve shells (present study). Small individuals (SL < 4 mm) were measured under a dissecting microscope using an ocular micrometer. The size-gender distribution of each population was studied, and size differences among genders within each population and within genders among populations were tested for significance using a one-way Analysis of Variance (ANOVA) when the assumptions for the parametric analysis were met. Additionally, others have shown that the proportion of individuals in native populations that form aggregations is also generally low (0%–29%) [32, 33, 39]. Larger SC/SL ratios, as found in females here, imply a deeper notch in the left side of the septum and a left sided extension of the mantle edge along the free edge of the septum. sus orienw.- Le. RDC: incursion d’une milice dans la grande ville minière de Lubumbashi, RDC : Moïse Katumbi récupère son entreprise, MCK, par une décision judiciaire, Serge Ibaka lance “How talented are you”, son télé-crochet sur Instagram Live. Therefore, to determine unambiguosly the taxonomic identity of C. dilatata, a quantitative morphological analysis of the shell of non-native specimens is helpful. The osphradium in non-native specimens was bipectinate and asymmetric or monopectinate, and the salivary glands reached the nervous ring or were shorter and extended only halfway along the neck region. Its role in the invasion success becomes evident in invasive species with flexible reproductive modes that switch from a predominantly sexually reproductive mode in the native range of distribution to a widespread asexual reproduction following introduction [9, 11, 16]. Shell morphotypes were unevenly distributed among sexes (Gadj = 36.828; P < 10−5; df = 6) and among sites (Gadj = 8.433; P < 0.05; df = 3). Theoretical models predict male-biased sex ratios for protandric species [99], however protandric species can also have balanced sex ratios or female biased sex ratios [15, 17, 20, 99]. GLM Pteroglanis manni Pearson 1924 RLC Rhamdella eriarcha HPN Hypophthalmus edentatus Highwaterman catfish Bagre paysan Bagre paisano HBU Hypophthalmus spp Loweye catfishes nei RIM Rhamdiopsis moreirai SIH Sorubimichthys planiceps Firewood catfish SAY Steindachneridion amblyurua TBK Typhlobagrus kronei Miranda-Ribeiro 1907 ZUM Zungaropsis multimaculatus HWE Conorhynchos … Is the Subject Area "Mussels" applicable to this article? Department of Molecular Biology, University of Bucharest, Bucharest, Romania, Affiliations Females from O Grove produced in autumn 2012 significantly fewer viable embryos per egg-capsule and per brood than females from the same site and from Gijon in spring 2016 and 2010 respectively (Fig 7B and 7C). When eliminating the non-dimensional shape variables from the original dataset, the PCA combined with the k-means clustering analysis failed to recover the shell polymorphism recognized previously. In addition, it may allow tracking temporal and/or spatial changes in the variability of phenotypic traits in postintroduction stages of the invasion process. In intertidal gastropods, these factors have been reported as determinants of shell shape [78, 82–84], and in Calyptreaidae, it has been suggested that shell convexity influences the vulnerability to predation by shore crabs. The number of viable embryos per egg-capsule (range across all broods: 2–30) and the number of viable embryos per brood (range across all broods: 18–715.5) (S5 Dataset) were also variable. In O Grove, approximately 63% of the slipper limpets aggregated into stacks in autumn 2012 and around 60% did so in spring 2016 (Fig 9). For more information about PLOS Subject Areas, click Digital detector of ferrous & non-ferrous metals (106 pages) Measuring Instruments Bosch GLM 15 Operating/Safety Instructions Manual (49 pages) … No, Is the Subject Area "Eggs" applicable to this article? The William’s correction factor was applied to compute an adjusted G statistic (Gadj) for the global analysis and all pair-wise comparisons [61]. Close to one quarter of the population were juveniles (23.1%), while 34.1% were females, 10% intersex stages, and 31.8% males (S3 Dataset). The osphradia of the dissected Spanish individuals were either bipectinate and asymmetric, with the external leaflets oriented towards the mantle edge being shorter than those oriented internally, or monopectinate. Yes In the established population, gregariousness was significantly greater; the size when sex changes was found to be plastic and socially controlled. In contrast, there are no records of fresh mussel imports from Argentina for the same period (S2 Table). However, a few females from O Grove collected in April 2016 endowed some of their eggs with a very thick and milky-white capsular fluid of gelatinous consistency. The average SL of the intersex stages was smaller than the L50 estimated (24.665 mm) (Table 6). To understand invasions and to develop methods of invasion control it is also necessary to identify the factors, and their interactions, that promote establishment success and the spread of NIS [9].
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