期刊论文详细信息
BMC Evolutionary Biology
Temporal genetic structure in a poecilogonous polychaete: the interplay of developmental mode and environmental stochasticity
K Emily Knott3  Benni W Hansen1  Christoffer Boström2  Marina Mustonen3  Jenni E Kesäniemi3 
[1] Department of Environmental, Social and Spatial Change, Roskilde University, Universitetsvej 1, Roskilde DK-4000, Denmark;Environmental and Marine Biology, Åbo Akademi University, Artillerigatan 6, Turku FI-20520, Finland;Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, Jyväskylä FI-40014, Finland
关键词: Full-sibs;    Sweepstakes reproductive success;    Temporal;    Genetic drift;    Developmental mode;    Population genetics;    Poecilogony;    Pygospio elegans;   
Others  :  858085
DOI  :  10.1186/1471-2148-14-12
 received in 2013-09-22, accepted in 2013-12-30,  发布年份 2014
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【 摘 要 】

Background

Temporal variation in the genetic structure of populations can be caused by multiple factors, including natural selection, stochastic environmental variation, migration, or genetic drift. In benthic marine species, the developmental mode of larvae may indicate a possibility for temporal genetic variation: species with dispersive planktonic larvae are expected to be more likely to show temporal genetic variation than species with benthic or brooded non-dispersive larvae, due to differences in larval mortality and dispersal ability. We examined temporal genetic structure in populations of Pygospio elegans, a poecilogonous polychaete with within-species variation in developmental mode. P. elegans produces either planktonic, benthic, or intermediate larvae, varying both among and within populations, providing a within-species test of the generality of a relationship between temporal genetic variation and larval developmental mode.

Results

In contrast to our expectations, our microsatellite analyses of P. elegans revealed temporal genetic stability in the UK population with planktonic larvae, whereas there was variation indicative of drift in temporal samples of the populations from the Baltic Sea, which have predominantly benthic and intermediate larvae. We also detected temporal variation in relatedness within these populations. A large temporal shift in genetic structure was detected in a population from the Netherlands, having multiple developmental modes. This shift could have been caused by local extiction due to extreme environmental conditions and (re)colonization by planktonic larvae from neighboring populations.

Conclusions

In our study of P. elegans, temporal genetic variation appears to be due to not only larval developmental mode, but also the stochastic environment of adults. Large temporal genetic shifts may be more likely in marine intertidal habitats (e.g. North Sea and Wadden Sea) which are more prone to environmental stochasticity than the sub-tidal Baltic habitats. Sub-tidal and/or brackish (less saline) habitats may support smaller P. elegans populations and these may be more susceptible to the effects of random genetic drift. Moreover, higher frequencies of asexual reproduction and the benthic larval developmental mode in these populations leads to higher relatedness and contributes to drift. Our results indicate that a general relationship between larval developmental mode and temporal genetic variation may not exist.

【 授权许可】

   
2014 Kesäniemi et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Shama LNS, Kubow KB, Jokela J, Robinson CT: Bottlenecks drive temporal and spatial genetic changes in alpine caddisfly metapopulations. BMC Evol Biol 2011, 11:278. BioMed Central Full Text
  • [2]Lamy T, Pointier JP, Jarne P, David P: Testing metapopulation dynamics using genetic, demographic and ecological data. Mol Ecol 2012, 21(6):1394-1410.
  • [3]Sotka E, Wares J, Barth J, Grosberg R, Palumbi S: Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 2004, 13(8):2143-2156.
  • [4]Selkoe KA, Gaines SD, Caselle JE, Warner RR: Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology 2006, 87(12):3082-3094.
  • [5]Pringle JM, Wares JP: Going against the flow: maintenance of alongshore variation in allele frequency in a coastal ocean. Mar Ecol Prog Ser 2007, 335:69-84.
  • [6]Johnson M, Black R: Pattern beneath the chaos - the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 1984, 38(6):1371-1383.
  • [7]Kordos L, Burton R: Genetic differentiation of Texas gulf-coast populations of the blue-crab Callinectes Sapidus. Mar Biol 1993, 117(2):227-233.
  • [8]Moberg P, Burton R: Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 2000, 136(5):773-784.
  • [9]Barber PH, Moosa M, Palumbi S: Rapid recovery of genetic diversity of stomatopod populations on Krakatau: temporal and spatial scales of marine larval dispersal. Proc R Soc Lond B: Biological Sciences 2002, 269(1500):1591-1597.
  • [10]Robainas-Barcia A, Blanco G, Sanchez JA, Monnerot M, Solignac M, García-Machado E: Spatiotemporal genetic differentiation of Cuban natural populations of the pink shrimp Farfantepenaeus notialis. Genetica 2008, 133(3):283-294.
  • [11]Planes S, Lenfant P: Temporal change in the genetic structure between and within cohorts of a marine fish, Diplodus sargus, induced by a large variance in individual reproductive success. Mol Ecol 2002, 11(8):1515-1524.
  • [12]Florin A, Höglund J: Absence of population structure of turbot (Psetta maxima) in the Baltic Sea. Mol Ecol 2007, 16(1):115-126.
  • [13]Lee HJE, Boulding EG: Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol Ecol 2009, 18(10):2165-2184.
  • [14]Christie MR, Johnson DW, Stallings CD, Hixon MA: Self‒recruitment and sweepstakes reproduction amid extensive gene flow in a coral‒reef fish. Mol Ecol 2010, 19(5):1042-1057.
  • [15]Tessier N, Bernatchez L: Stability of population structure and genetic diversity across generations assessed by microsatellites among sympatric populations of landlocked Atlantic salmon (Salmo salar L.). Mol Ecol 1999, 8((2):169-179.
  • [16]Virgilio M, Abbiati M: Temporal changes in the genetic structure of intertidal populations of Hediste diversicolor (Polychaeta: Nereididae). J Sea Res 2006, 56(1):53-58.
  • [17]Guardiola M, Frotscher J, Uriz MJ: Genetic structure and differentiation at a short-time scale of the introduced calcarean sponge Paraleucilla magna to the western Mediterranean. Hydrobiologia 2012, 687(1):71-84.
  • [18]Bohonak AJ: Dispersal, gene flow, and population structure. Q Rev Biol 1999, 74(1):21-45.
  • [19]Hedgecock D, Pudovkin AI: Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull Mar Sci 2011, 87(4):971-1002.
  • [20]Morgan S: Life and death in the plankton: larval mortality and adaptation. In Ecology of marine invertebrate larvae. Edited by McEdward L. Boca Raton Florida: CRC Press; 1995:279-322.
  • [21]Pechenik J: On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 1999, 177:269-297.
  • [22]Pedersen TM, Hansen JLS, Josefson AB, Hansen BW: Mortality through ontogeny of soft-bottom marine invertebrates with planktonic larvae. J Mar Syst 2008, 73(1–2):185-207.
  • [23]Pechenik J: Role of encapsulation in invertebrate life histories. Am Nat 1979, 114(6):859-870.
  • [24]Strathmann R: Feeding and nonfeeding larval development and life-history evolution in marine-invertebrates. Annu Rev Ecol Syst 1985, 16:339-361.
  • [25]Chia F, Gibson G, Qian P: Poecilogony as a reproductive strategy of marine invertebrates. Oceanol Acta 1996, 19(3–4):203-208.
  • [26]Knott KE, McHugh D: Introduction to symposium: poecilogony-a window on larval evolutionary transitions in marine invertebrates. Integ Comp Biol 2012, 52(1):120-127.
  • [27]Levin L: Multiple patterns of development in Streblospio Benedicti Webster (Spionidae) from 3 coasts of North America. Biol Bull 1984, 166(3):494-508.
  • [28]Gibson GD: Variable development in the spionid Boccardia proboscidea (Polychaeta) is linked to nurse egg production and larval trophic mode. Invertebr Biol 1997, 116(3):213-226.
  • [29]Krug PJ: Poecilogony and larval ecology in the gastropod genus Alderia. Am Malacol Bull 2007, 23(1–2):99-111.
  • [30]Collin R: Nontraditional life-history choices: what can “intermediates” tell us about evolutionary transitions between modes of invertebrate development? Integr Comp Biol 2012, 52(1):128-137.
  • [31]Simons AM: Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proc R Soc B, Biological Sciences 2011, 278(1712):1601-1609.
  • [32]Wennersten L, Forsman A: Population-level consequences of polymorphism, plasticity and randomized phenotype switching: a review of predictions. Biol Rev 2012, 87(3):756-767.
  • [33]Levin L: Life-history and dispersal patterns in a dense infaunal polychaete assemblage - community structure and response to disturbance. Ecology 1984, 65(4):1185-1200.
  • [34]Morgan T, Rogers A, Paterson G, Hawkins L, Sheader M: Evidence for poecilogony in Pygospio elegans (Polychaeta: Spionidae). Mar Ecol Prog Ser 1999, 178:121-132.
  • [35]Kesäniemi JE, Rawson PD, Lindsay SM, Knott KE: Phylogenetic analysis of cryptic speciation in the polychaete Pygospio elegans. Ecol Evol 2012, 2(5):994-1007.
  • [36]Rasmussen E: Systematics and ecology of the Isefjord marine fauna (Denmark). Ophelia 1973, 11:1-495.
  • [37]Boström C, Bonsdorff E: Community structure and spatial variation of benthic invertebrates associated with Zostera marina (L.) beds in the northern Baltic Sea. J Sea Res 1997, 37((1):153-166.
  • [38]Anger K, Anger V, Hagmeier E: Laboratory studies on larval growth of Polydora ligni, Polydora ciliata, and Pygospio elegans (Polychaeta, Spionidae). Helgoländer Meeresunters 1986, 40(4):377-395.
  • [39]Desprez M, Rybarczyk H, Wilson J, Ducrotoy J, Sueur F, Olivesi R, Elkaim B: Biological impact of eutrophication in the Bay of Somme and the induction and impact of anoxia. Neth J Sea Res 1992, 30:149-159.
  • [40]Bolam SG: Population structure and reproductive biology of Pygospio elegans (Polychaeta: Spionidae) on an intertidal sandflat, Firth of Forth, Scotland. Invertebr Biol 2004, 123(3):260-268.
  • [41]Bolam SG, Fernandes TF: Dense aggregations of Pygospio elegans (Claparède): effect on macrofaunal community structure and sediments. J Sea Res 2003, 49(3):171-185.
  • [42]Kesäniemi JE, Geuverink E, Knott KE: Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete. Pygospio elegans. Integr Comp Biol 2012, 52(1):181-196.
  • [43]Boström C, Bonsdorff E: Zoobenthic community establishment and habitat complexity-the importance of seagrass shoot-density, morphology and physical disturbance for faunal recruitment. Mar Ecol Prog Ser 2000, 205:123-138.
  • [44]Gudmundsson H: Life history patterns of polychaete species of the family Spionidae. J Mar Biol Assoc U K 1985, 65(01):93-111.
  • [45]Rasmussen E: Asexual reproduction in Pygospio elegans Claparede (Polychaeta, Sedentaria). Nature 1953, 171(4365):1161-1162.
  • [46]Anger V: Reproduction in Pygospio elegans (Spionidae) in relation to its geographical origin and to environmental conditions: a preliminary report. Fortschr Zool 1984, 29:45-51.
  • [47]Constable AJ: Ecology of benthic macro‒invertebrates in soft‒sediment environments: a review of progress towards quantitative models and predictions. Aust J Ecol 1999, 24(4):452-476.
  • [48]Lee S, Fong C, Wu R: The effects of seagrass (Zostera japonica) canopy structure on associated fauna: a study using artificial seagrass units and sampling of natural beds. J Exp Mar Biol Ecol 2001, 259(1):23-50.
  • [49]Fredriksen S, De Backer A, Boström C, Christie H: Infauna from Zostera marina L. meadows in Norway. Differences in vegetated and unvegetated areas. Mar Biol Res 2010, 6(2)):189-200.
  • [50]Moran A, Emlet R: Offspring size and performance in variable environments: field studies on a marine snail. Ecology 2001, 82(6):1597-1612.
  • [51]Zajac R: Macrofaunal responses to pit-mound patch dynamics in an intertidal mudflat: local versus patch-type effects. J Exp Mar Biol Ecol 2004, 313(2):297-315.
  • [52]Calderón I, Ortega N, Duran S, Becerro M, Pascual M, Turon X: Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 2007, 16(9):1799-1810.
  • [53]Barbosa SS, Klanten SO, Puritz JB, Toonen RJ, Byrne M: Very fine-scale population genetic structure of sympatric asterinid sea stars with benthic and pelagic larvae: influence of mating system and dispersal potential. Biol J Linn Soc 2013, 108(4):821-833.
  • [54]Kesäniemi JE, Boström C, Knott KE: New genetic markers reveal population genetic structure at different spatial scales in the opportunistic polychaete Pygospio elegans. Hydrobiologia 2012, 691(1):213-223.
  • [55]Excoffier L, Lischer HE: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under linux and windows. Mol Ecol Resour 2010, 10(3):564-567.
  • [56]Kalinowski S: HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness . Mol Ecol Notes 2005, 5(1):187-189.
  • [57]Goudet J: FSTAT (Version 1.2): a computer program to calculate F-statistics . J Hered 1995, 86(6):485-486.
  • [58]Chapuis M, Estoup A: Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 2007, 24(3):621-631.
  • [59]Jost L: GST and its relatives do not measure differentiation. Mol Ecol 2008, 17:4015-4026.
  • [60]Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P: Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 2010, 19(18):3845-3852.
  • [61]Peakall R, Smouse PE: GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update . Bioinformatics 2012, 28(19):2537-2539.
  • [62]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 115:945-959.
  • [63]Rosenberg N: DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 2004, 4(1):137-138.
  • [64]Jones OR, Wang J: COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 2010, 10(3):551-555.
  • [65]Wang J: Computationally efficient sibship and parentage assignment from multilocus marker data. Genetics 2012, 191(1):183-194.
  • [66]Kalinowski ST, Wagner AP, Taper ML: ml-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molr Ecol Notes 2006, 6((2):576-579.
  • [67]Waples R: A generalized-approach for estimating effective population-size from temporal changes in allele frequency. Genetics 1989, 121(2):379-391.
  • [68]Waples RS: Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 2010, 10(5):785-796.
  • [69]Wang J, Whitlock M: Estimating effective population size and migration rates from genetic samples over space and time. Genetics 2003, 163(1):429-446.
  • [70]Ovenden JR, Peel D, Street R, Courtney AJ, Hoyle SD, Peel SL, Podlich H: The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol 2007, 16(1):127-138.
  • [71]Jorde PE, Ryman N: Unbiased estimator for genetic drift and effective population size. Genetics 2007, 177(2):927-935.
  • [72]Ostergaard S, Hansen M, Loeschcke V, Nielsen E: Long-term temporal changes of genetic composition in brown trout (Salmo trutta L.) populations inhabiting an unstable environment. Mol Ecol 2003, 12(11):3123-3135.
  • [73]Ng W, Leung FCC, Chak STC, Slingsby G, Williams GA: Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores. Mar Biol 2010, 157(2):325-337.
  • [74]Robainas-Barcia A, Lopez G, Hernandez D, García-Machado E: Temporal variation of the population structure and genetic diversity of Farfantepenaeus notialis assessed by allozyme loci. Mol Ecol 2005, 14(10):2933-2942.
  • [75]Barshis D, Sotka E, Kelly R, Sivasundar A, Menge B, Barth J, Palumbi S: Coastal upwelling is linked to temporal genetic variability in the acorn barnacle Balanus glandula. Mar Ecol Prog Ser 2011, 439:139-150.
  • [76]Strathmann R: Hypotheses on the origins of marine larvae. Annu Rev Ecol Syst 1993, 24:89-117.
  • [77]Levin L, Huggett D: Implications of alternative reproductive modes for seasonality and demography in an estuarine polychaete. Ecology 1990, 71(6):2191-2208.
  • [78]Beukema JJ, Flach EC, Dekker R, Starink M: A long-term study of the recovery of the macrozoobenthos on large defaunated plots on a tidal flat in the Wadden Sea. J Sea Res 1999, 42(3):235-254.
  • [79]Bolam SG, Fernandes TF: Dense aggregations of tube-building polychaetes: response to small-scale disturbances. J Exp Mar Biol Ecol 2002, 269(2):197-222.
  • [80]Pannell J, Charlesworth B: Effects of metapopulation processes on measures of genetic diversity. Phil Trans R Soc B-Biological Sciences 2000, 355(1404):1851-1864.
  • [81]Reiss H, Meybohm K, Kroencke I: Cold winter effects on benthic macrofauna communities in near- and offshore regions of the North Sea. Helgol Mar Res 2006, 60(3):224-238.
  • [82]Neumann H, Ehrich S, Kroencke I: Effects of cold winters and climate on the temporal variability of an epibenthic community in the German Bight. Climate Res 2008, 37(2–3):241-251.
  • [83]Naumov AD: Long-term fluctuations of soft-bottom intertidal community structure affected by ice cover at two small sea bights in the Chupa Inlet (Kandalaksha Bay) of the White Sea. Hydrobiologia 2013, 706(1):159-173.
  • [84]Hanski IA, Gaggiotti OE: Ecology, Genetics and Evolution of Metapopulations. USA: Elsevier Academic Press; 2004.
  • [85]Swearer S, Shima J, Hellberg M, Thorrold S, Jones G, Robertson D, Morgan S, Selkoe K, Ruiz G, Warner R: Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 2002, 70(1):251-271.
  • [86]Warner RR, Cowen RK: Free Local retention of production in marine populations: evidence, mechanisms, and consequences. Bull Mar Sci 2002, 70((1) Suppl):245-249.
  • [87]Als T, Hansen M, Maes G, Castonguay M, Riemann L, Aarestrup K, Munk P, Sparholt H, Hanle R, Bernatchez L: All roads lead to home: panmixia of European eel in the Sargasso Sea. Mol Ecol 2011, 20(7):1333-1346.
  • [88]Iacchei M, Ben-Horin T, Selkoe KA, Bird CE, García-Rodríguez FJ, Toonen RJ: Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations. Mol Ecol 2013, 22(13):3476-3494.
  • [89]Sponaugle S, Cowen R, Shanks A, Morgan S, Leis J, Pineda J, Boehlert G, Kingsford M, Lindeman K, Grimes C, Munro J: Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 2002, 70(1):341-375.
  • [90]Morgan SG, Fisher JL, Miller SH, McAfee ST, Largier JL: Nearshore larval retention in a region of strong upwelling and recruitment limitation. Ecology 2009, 90(12):3489-3502.
  • [91]Hedgecock D, Launey S, Pudovkin AI, Naciri Y, Lapègue S, Bonhomme F: Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Mar Biol 2007, 150(6):1173-1182.
  • [92]Veliz D, Duchesne P, Bourget E, Bernatchez L: Genetic evidence for kin aggregation in the intertidal acorn barnacle (Semibalanus balanoides). Mol Ecol 2006, 15(13):4193-4202.
  • [93]Bernardi G, Beldade R, Holbrook SJ, Schmitt RJ: Full-sibs in cohorts of newly settled coral reef fishes. PloS one 2012, 7(9):e44953.
  • [94]Broquet T, Viard F, Yearsley JM: Genetic drift and collective dispersal can result in chaotic genetic patchiness. Evolution 2013, 67(6):1660-1675.
  • [95]Yearsley JM, Viard F, Broquet T: The effect of collective dispersal on the genetic structure of a subdivided population. Evolution 2013, 63(6):1649-1659.
  • [96]Kanno Y, Vokoun JC, Letcher BH: Sibship reconstruction for inferring mating systems, dispersal and effective population size in headwater brook trout (Salvelinus fontinalis) populations. Conserv Genet 2011, 12(3):619-628.
  • [97]Wang J: Sibship reconstruction from genetic data with typing errors. Genetics 2004, 166(4):1963-1979.
  • [98]Karaket T, Poompuang S: CERVUS vs. COLONY for successful parentage and sibship determinations in freshwater prawn Macrobrachium rosenbergii de Man. Aquaculture 2012, 324:307-311.
  • [99]Waples RS: Evaluating the effect of stage-specific survivorship on the Ne/N ratio. Mol Ecol 2002, 11:1029-1037.
  • [100]Hedgecock D: Does variance in reproductive success limit effective population sizes of marine organisms? In Genetic and Evolution of Aquatic Organisms. Edited by Beaumont AR. London, UK: Chapman & Hall; 1994:122-134.
  • [101]Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, Carvalho GR: Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci 2002, 99(18):11742-11747.
  • [102]Turner T, Wares J, Gold J: Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 2002, 162(3):1329-1339.
  • [103]Waples RS, Yokota M: Temporal estimates of effective population size in species with overlapping generations. Genetics 2007, 175(1):219-233.
  • [104]Palstra FP, Ruzzante DE: Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 2008, 17(15):3428-3447.
  • [105]West-Eberhard M: Developmental Plasticity and Evolution. Oxford: Oxford University Press; 2003.
  • [106]Marshall DJ, Bonduriansky R, Bussiere LF: Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 2008, 89(9):2506-2517.
  • [107]Jørgensen AT, Hansen BW, Vismann B, Jacobsen L, Skov C, Berg S, Bekkevold D: High salinity tolerance in eggs and fry of a brackish Esox lucius population. Fish Manage Ecol 2010, 17(6):554-560.
  • [108]Larsen PF, Nielsen EE, Meier K, Olsvik PA, Hansen MM, Loeschcke V: Differences in salinity tolerance and gene expression between two populations of atlantic Cod (Gadus morhua) in response to salinity stress. Biochem Genet 2012, 50(5–6):454-466.
  • [109]Rossi F: Short-term response of deposit-feeders to an increase of the nutritive value of the sediment through seasons in an intertidal mudflat (Western Mediterranean, Italy). J Exp Mar Biol Ecol 2003, 290(1):1-17.
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