Advertisement

Oecologia

pp 1–14 | Cite as

Habitat filters mediate successional trajectories in bacterial communities associated with the striped shore crab

  • Catalina Cuellar-GempelerEmail author
  • Pablo Munguia
Community ecology – original research

Abstract

The relative importance of stochastic- and niche-based processes shifts during successional time and across different types of habitats. Microbial biofilms are known to undergo such successional shifts. However, little is known about the interaction between these successional trajectories and habitat filters. Harsh habitat filters could affect biofilm successional trajectories by strengthening niche-based processes and weakening stochastic processes. We used mesocosms to track successional trajectories in bacterial communities associated with the striped shore crab (Pachygrapsus transversus). We followed replicated microbial communities under strong and weak habitat filters associated with the crab’s gut and carapace. For bacteria, colonization of the crab’s gut is constrained by strong chemical and physical filtering, while the carapace remains relatively open for colonization. Consistent with successional models of bacterial biofilms, carapace microbial communities initially converged in community composition at day 8 and diverged thereafter. We expected gut microbial communities to deviate from the trajectory in the carapace and converge towards a subset of tolerant species. Instead, bacterial communities in the gut exhibited low richness, unchanging similarity in composition and turnover in species identities throughout the duration of our study. These habitat filter effects were linked with weak species interactions and low influence from colonization in the gut. If these findings are representative of differences in filter strength in a continuum of successional trajectories, habitat filters may provide basis for predictions that link successional models and habitat types.

Keywords

Habitat filters Succession Community assembly Community structure Colonization 

Notes

Acknowledgements

We would like to thank Deana Erdner for her guidance and generous sharing of laboratory space. Mathew Leibold and Casey terHorst provided excellent comments to early drafts. Finally, we thank Kathryn Thompson for her participation in crab collection.

Author contribution statement

CCG and PM conceived and designed the experiment. CCG conducted the experiment, and analyzed the data. CCG and PM wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

442_2019_4549_MOESM1_ESM.docx (1.5 mb)
Supplementary material 1 (DOCX 1494 kb)

References

  1. Abele LG, Campanella PJ, Salmon M (1986) Natural history and social organization of the semiterrestrial grapsid crab Pachygrapsus transversus (Gibbes). J Exp Mar Biol Ecol 104:153–170CrossRefGoogle Scholar
  2. Anderson KJ, Allen AP, Gillooly JF, Brown JH (2006a) Temperature-dependence of biomass accumulation rates during secondary succession. Ecol Lett 9:673–682PubMedCrossRefGoogle Scholar
  3. Anderson MJ, Ellingsen KE, McArdle BH (2006b) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693PubMedCrossRefGoogle Scholar
  4. Andrews S (2010) FastQC: a quality control tool for high throughput sequence dataGoogle Scholar
  5. Baasch A, Tischew S, Bruelheide H (2010) Twelve years of succession on sandy substrates in a post-mining landscape: a Markov chain analysis. Ecol Appl 20:1136–1147PubMedCrossRefGoogle Scholar
  6. Barker PL, Gibson R (1977) Observations on the feeding mechanism, structure of the gut, and digestive physiology of the european lobster Homarus gammarus (L.) (Decapoda: Nephropidae). J Exp Mar Biol Ecol 26:297–324CrossRefGoogle Scholar
  7. Baselga A (2013) Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol Evol 4:552–557CrossRefGoogle Scholar
  8. Belote RT, Sanders NJ, Jones RH (2009) Disturbance alters local–regional richness relationships in Appalachian forests. Ecology 90:2940–2947PubMedCrossRefGoogle Scholar
  9. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from illumina amplicon sequencing. Nat Methods 10:57–59PubMedCrossRefGoogle Scholar
  10. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, Lusis AJ, Knight R, Caporaso JG, Svanback R (2014) Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun 5:4500PubMedPubMedCentralCrossRefGoogle Scholar
  11. Branda SS, Vik A, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13:20–26PubMedCrossRefGoogle Scholar
  12. Brorcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:511–525Google Scholar
  13. Brosing A (2010) Recent developments on the morphology of the brachyuran foregut ossicles and gastric teeth. Zootaxa 2510:1–44CrossRefGoogle Scholar
  14. Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography—effect of immigration on extinction. Ecology 58:445–449CrossRefGoogle Scholar
  15. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848PubMedCrossRefGoogle Scholar
  16. Cannicci S, Gomei M, Boddi B, Vannini M (2002) Feeding habits and natural diet of the intertidal crab Pachygrapsus marmoratus: opportunistic browser or selective feeder? Estuar Coast Shelf Sci 54:983–1001CrossRefGoogle Scholar
  17. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pẽa AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing dataGoogle Scholar
  18. Carstensen DW, Lessard JP, Holt BG, Borregaard MK, Rahbek C (2013) Introducing the biogeographic species pool. Ecography 36:1310–1318CrossRefGoogle Scholar
  19. Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890PubMedCrossRefGoogle Scholar
  20. Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci USA 104:17430–17434PubMedCrossRefGoogle Scholar
  21. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  22. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Tran R Soc B Biol Sci 366:2351–2363CrossRefGoogle Scholar
  23. Chave J (2004) Neutral theory and community ecology. Ecol Lett 7:241–253CrossRefGoogle Scholar
  24. Christofoletti RA, Murakami VA, Oliveira DN, Barreto RE, Flores AAV (2010) Foraging by the omnivorous crab Pachygrapsus transversus affects the structure of assemblages on sub-tropical rocky shores. Mar Ecol Prog Ser 420:125–134CrossRefGoogle Scholar
  25. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  26. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126CrossRefGoogle Scholar
  27. Cuellar-Gempeler C, Leibold MA (2018) Multiple colonist pools shape fiddler crab-associated bacterial communities. ISME J 12:825–837PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cuellar-Gempeler C, Leibold MA (2019) Key colonist pools and habitat filters mediate the composition of fiddler crab-associated bacterial communities. Ecol pressGoogle Scholar
  29. Cuellar-Gempeler C, Munguia P (2013) Fiddler crabs (Uca thayeri, Brachyura: Ocypodidae) affect bacterial assemblages in mangrove forest sediments. Commun Ecol 14:59CrossRefGoogle Scholar
  30. Cuesta JA (1998) Morphological and molecular differentiation between three allopatric populations of the littoral crab Pachygrapsus transversus (Gibbes, 1850) (Brachyura: Grapsidae). J Nat Hist 32:1499–1508CrossRefGoogle Scholar
  31. Dang HY, Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66:467–475PubMedPubMedCentralCrossRefGoogle Scholar
  32. de Oliveira DN, Christofoletti RA, Barreto RE (2015) Feeding behavior of a crab according to cheliped number. Plos One 10PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dempsey AC, Kitting CL (1987) Characteristics of bacteria isolated from panaeid shrimp. Crustaceana 52:90–94CrossRefGoogle Scholar
  34. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dilhari A, Sampath A, Gunasekara C, Fernando N, Weerasekara D, Sissons C, McBain A, Weerasekera M (2017) Evaluation of the impact of six different DNA extraction methods for the representation of the microbial community associated with human chronic wound infections using a gel-based DNA profiling method. AMB Express 7:179PubMedPubMedCentralCrossRefGoogle Scholar
  36. Drake JA, Flum TE, Witteman GJ, Voskuil T, Hoylman AM, Creson C, Kenny DA, Huxel GR, Larue CS, Duncan JR (1993) The construction and assembly of an ecological landscape. J Anim Ecol 62:117–130CrossRefGoogle Scholar
  37. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461PubMedPubMedCentralCrossRefGoogle Scholar
  38. Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82PubMedCrossRefGoogle Scholar
  39. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105:17994–17999PubMedCrossRefGoogle Scholar
  40. Franzenburg S, Fraune S, Altrock PM, Künzel S, Baines JF, Traulsen A, Bosch TCG (2013) Bacterial colonization of hydra hatchlings follows a robust temporal pattern. Isme J 7:781PubMedPubMedCentralCrossRefGoogle Scholar
  41. Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. In: Futuyma DJ (ed) Annual review of ecology, evolution, and systematics, Vol 46. pp 1–23CrossRefGoogle Scholar
  42. Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621CrossRefGoogle Scholar
  43. Gotelli NJ, Entsminger GL (2003) Swap algorithms in null model analysis. Ecology 84:532–535CrossRefGoogle Scholar
  44. Gotelli NJ, McCabe DJ (2002) Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology 83:2091–2096CrossRefGoogle Scholar
  45. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910CrossRefGoogle Scholar
  46. Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127CrossRefGoogle Scholar
  47. Handley KM, Wrighton KC, Miller CS, Wilkins MJ, Kantor RS, Thomas BC, Williams KH, Gilbert JA, Long PE, Banfield JF (2015) Disturbed subsurface microbial communities follow equivalent trajectories despite different structural starting points. Environ Microbiol 17:622–636PubMedCrossRefGoogle Scholar
  48. Harris JM (1993) The presence, nature and role of gut microflora in aquatic invertebrates—a synthesis. Microb Ecol 25:195–231PubMedCrossRefGoogle Scholar
  49. Harrison S, Ross SJ, Lawton JH (1992) Beta-diversity on geographic gradients in Britain. J Anim Ecol 61:151–158CrossRefGoogle Scholar
  50. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  51. Horn HS (1974) The ecology of secondary succession. Annu Rev Ecol Syst 5:25–37CrossRefGoogle Scholar
  52. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  53. Jabot F, Etienne RS, Chave J (2008) Reconciling neutral community models and environmental filtering: theory and an empirical test. Oikos 117:1308–1320CrossRefGoogle Scholar
  54. Jackson CR (2003) Changes in community properties during microbial succession. Oikos 101:444–448CrossRefGoogle Scholar
  55. Jackson CR, Churchill PF, Roden EE (2001) Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology 82:555–566CrossRefGoogle Scholar
  56. Karger DN, Tuomisto H, Amoroso VB, Darnaedi D, Hidayat A, Abrahamczyk S, Kluge J, Lehnert M, Kessler M (2015) The importance of species pool size for community composition. Ecography 38:1243–1253CrossRefGoogle Scholar
  57. Kraft NJB, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Vellend M, Boyle B, Anderson MJ, Cornell HV, Davies KF, Freestone AL, Inouye BD, Harrison SP, Myers JA (2011) Disentangling the drivers of beta diversity along latitudinal and elevational gradients. Science 333:1755–1758PubMedCrossRefGoogle Scholar
  58. Lang JM, McEwan RW, Benbow ME (2015) Abiotic autumnal organic matter deposition and grazing disturbance effects on epilithic biofilm succession. FEMS Microbiol Ecol 91:060CrossRefGoogle Scholar
  59. Laurie CC, Doheny KF, Mirel DB, Pugh EW, Bierut LJ, Bhangale T, Boehm F, Caporaso NE, Cornelis MC, Edenberg HJ, Gabriel SB, Harris EL, Hu FB, Jacobs KB, Kraft P, Landi MT, Lumley T, Manolio TA, McHugh C, Painter I, Paschall J, Rice JP, Rice KM, Zheng XW, Weir BS, Investigators G (2010) Quality control and quality assurance in genotypic data for genome-wide association studies. Genet Epidemiol 34:591–602PubMedPubMedCentralCrossRefGoogle Scholar
  60. Legendre P (2014) Interpreting the replacement and richness difference components of beta diversity. Glob Ecol Biogeogr 23:1324–1334CrossRefGoogle Scholar
  61. Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: elements of meta-community structure. Oikos 97:237–250CrossRefGoogle Scholar
  62. Lessard JP, Belmaker J, Myers JA, Chase JM, Rahbek C (2012a) Inferring local ecological processes amid species pool influences. Trends Ecol Evol 27:600–607PubMedCrossRefGoogle Scholar
  63. Lessard JP, Borregaard MK, Fordyce JA, Rahbek C, Weiser MD, Dunn RR, Sanders NJ (2012b) Strong influence of regional species pools on continent-wide structuring of local communities. Proc R Soc B Biol Sci 279:266–274CrossRefGoogle Scholar
  64. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  65. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963PubMedPubMedCentralCrossRefGoogle Scholar
  66. Maire V, Gross N, Borger L, Proulx R, Wirth C, Pontes LD, Soussana JF, Louault F (2012) Habitat filtering and niche differentiation jointly explain species relative abundance within grassland communities along fertility and disturbance gradients. New Phytol 196:497–509PubMedCrossRefGoogle Scholar
  67. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12CrossRefGoogle Scholar
  68. Martiny AC, Jørgensen TM, Albrechtsen HJ, Arvin E, Molin S (2003) Long-term succession of structure and diversity of a biofilm formed in a model drinking water distribution system. Appl Environ Microbiol 69:6899–6907PubMedPubMedCentralCrossRefGoogle Scholar
  69. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS OneGoogle Scholar
  70. Meiners SJ, Cadotte MW, Fridley JD, Pickett STA, Walker LR (2015) Is successional research nearing its climax? New approaches for understanding dynamic communities. Funct Ecol 29:154–164CrossRefGoogle Scholar
  71. Middlemiss KL, Urbina MA, Wilson RW (2015) Microbial proliferation on gill structures of juvenile European lobster (Homarus gammarus) during a moult cycle. Helgol Mar Res 69:401–410CrossRefGoogle Scholar
  72. Miller TE, terHorst CP (2012) Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities. Oecologia 170:243–251PubMedCrossRefGoogle Scholar
  73. Mouquet N, Loreau M (2003) Community patterns in source-sink metacommunities. Am NatGoogle Scholar
  74. Munguia P (2004) Successional Patterns on Pen Shell Communities at Local and Regional Scales. J Anim Ecol 73:64–74CrossRefGoogle Scholar
  75. Munguia P (2014) Life history affects how species experience succession in pen shell metacommunities. Oecologia 174:1335–1344PubMedCrossRefGoogle Scholar
  76. Myers JA, Chase JM, Crandall RM, Jiménez I (2015) Disturbance alters beta-diversity but not the relative importance of community assembly mechanisms. J Ecol 103:1291–1299CrossRefGoogle Scholar
  77. Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin P, O’Hara GL, Simpson GL, Solymos P, Stevens MHH, Wagner H (2017) Vegan: community ecology packageGoogle Scholar
  78. Oksanen AJ, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, Minchin PR, Hara RBO, Simpson GL, Solymos P, Szoecs SE, Wagner H (2018) Vegan: community ecology package. https://github.com/vegandevs/vegan
  79. Ortiz-Álvarez R, Fierer N, de los Ríos A, Casamayor EO, Barberán A (2018) Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J 12:1658–1667PubMedPubMedCentralCrossRefGoogle Scholar
  80. Podani J, Schmera D (2011) A new conceptual and methodological framework for exploring and explaining pattern in presence-absence data. Oikos 120:1625–1638CrossRefGoogle Scholar
  81. Pruzzo C, Vezzulli L, Colwell RR (2008) Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10:1400–1410PubMedCrossRefGoogle Scholar
  82. Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49CrossRefGoogle Scholar
  83. Pulsford SA, Lindenmayer DB, Driscoll DA (2016) A succession of theories: purging redundancy from disturbance theory. Biol Rev 91:148–167PubMedCrossRefGoogle Scholar
  84. Ramachandran P, Reed E, Ottesen A (2018) Exploring the microbiome of callinectes (Maryland Blue Crab). Genome Announc 6:e00466-18PubMedPubMedCentralCrossRefGoogle Scholar
  85. Rao D, Webb JS, Kjelleberg S (2005) Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol 71:1729–1736PubMedPubMedCentralCrossRefGoogle Scholar
  86. Rathbun MJ (1918) The grapsoid crabs of America. Bull US Natl Museum 97:1–461Google Scholar
  87. Revetta RP, Gomez-Alvarez V, Gerke TL, Curioso C, Santo Domingo JW, Ashbolt NJ (2013) Establishment and early succession of bacterial communities in monochloramine-treated drinking water biofilms. FEMS Microbiol Ecol 86:404–414PubMedCrossRefGoogle Scholar
  88. Robinson JV, Edgemon MA (1988) Annual experimental evaluation of the effect of invasion history on community structure. Ecology 69:1410–1417CrossRefGoogle Scholar
  89. Robinson CJ, Bohannan BJM, Young VB (2010) From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 74:453PubMedPubMedCentralCrossRefGoogle Scholar
  90. Rognes T, Flouri T, Nichols B, Quince C, Frédéric M (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJGoogle Scholar
  91. Roxburgh SH, Wilson JB, Mark AF (1988) Succession after disturbance of a New Zealand high-alpine cushionfield. Arct Alp Res 20:230–236CrossRefGoogle Scholar
  92. Schamp BS, Laird RA, Aarssen LW (2002) Fewer species because of uncommon habitat? Testing the species pool hypothesis for low plant species richness in highly productive habitats. Oikos 97:145–152CrossRefGoogle Scholar
  93. Schröder A, Persson L, De Roos AM (2005) Direct experimental evidence for alternative stable states: a review. Oikos 110:3–19CrossRefGoogle Scholar
  94. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611CrossRefGoogle Scholar
  95. Shipley B, Paine CET, Baraloto C (2012) Quantifying the importance of local niche-based and stochastic processes to tropical tree community assembly. Ecology 93:760–769PubMedCrossRefGoogle Scholar
  96. Shmida AVI, Wilson MV (1985) Biological determinants of species diversity. J Biogeogr 12:1–20CrossRefGoogle Scholar
  97. Stevenson BM, Howard FR (1937) Properties of sufficiency and statistical tests. Proc R Soc Lond Series A Math Phys Sci 160:268–282CrossRefGoogle Scholar
  98. Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85:74–79CrossRefGoogle Scholar
  99. Teng F, Darveekaran Nair SS, Zhu P, Li S, Huang S, Li X, Xu J, Yang F (2018) Impact of DNA extraction method and targeted 16S-rRNA hypervariable region on oral microbiota profiling. Sci Reports 8:16321CrossRefGoogle Scholar
  100. Terhorst CP, Miller TE, Levitan DR (2010) Evolution of prey in ecological time reduces the effect size of predators in experimental microcosms. Ecology 91:629–636PubMedCrossRefGoogle Scholar
  101. Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214CrossRefGoogle Scholar
  102. Tilman D, Elhaddi A (1992) Drought and biodiversity in grasslands. Oecologia 89:257–264PubMedCrossRefGoogle Scholar
  103. Trevisan M, Leroy D, Decloux N, Thome JP, Compere P (2014) Moult-related changes in the integument, midgut and digestive gland in the freshwater amphipod Gammarus pulex. J Crustac Biol 34:539–551CrossRefGoogle Scholar
  104. Ulrich W, Zaplata MK, Winter S, Schaaf W, Fischer A, Soliveres S, Gotelli NJ (2016) Species interactions and random dispersal rather than habitat filtering drive community assembly during early plant succession. Oikos 125:698–707CrossRefGoogle Scholar
  105. Vavrek MJ (2011) fossil: palaeoecological and palaeogeographical analysis tools. Palaeontol Electron 14:1–16Google Scholar
  106. Veach AM, Stegen JC, Brown SP, Dodds WK, Jumpponen A (2016) Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem. Mol Ecol 25:4674–4688PubMedCrossRefGoogle Scholar
  107. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206PubMedCrossRefGoogle Scholar
  108. Vogan CL, Powell A, Rowley AF (2008) Shell disease in crustaceans—just chitin recycling gone wrong? Environ Microbiol 10:826–835PubMedCrossRefGoogle Scholar
  109. Vogt G, Stocker W, Storch V, Zwilling R (1989) Biosynthesis of astacus protease, a digestive enzyme from crayfish. Histochemistry 91:373–381PubMedCrossRefGoogle Scholar
  110. Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. Plos One 4:e7401PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund- an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474CrossRefGoogle Scholar
  112. Wang W, Wu XG, Liu ZJ, Zheng HJ, Cheng YX (2014) Insights into hepatopancreatic functions for nutrition metabolism and ovarian development in the crab Portunus trituberculatus: gene discovery in the comparative transcriptome of different hepatopancreas stages. Plos One 9:e84921PubMedPubMedCentralCrossRefGoogle Scholar
  113. Whitfeld TJS, Kress WJ, Erickson DL, Weiblen GD (2012) Change in community phylogenetic structure during tropical forest succession: evidence from New Guinea. Ecography 35:821–830CrossRefGoogle Scholar
  114. Williams PH (1996) Mapping variations in the strength and breadth of biogeographic transition zones using species turnover. Proc R Soc B Biol Sci 263:579–588CrossRefGoogle Scholar
  115. Wilson JB, Lee WG (2000) C-S-R triangle theory: community-level predictions, tests, evaluation of criticisms, and relation to other theories. Oikos 91:77–96CrossRefGoogle Scholar
  116. Woodcock S, Sloan W (2017) Biofilm community succession: a neutral perspective. Microbiology 163:664–668CrossRefGoogle Scholar
  117. Wright JP, Fridley JD (2010) Biogeographic synthesis of secondary succession rates in eastern North America. J Biogeogr 37:1584–1596Google Scholar
  118. Zha H, Jeffs A, Dong Y, Lewis G (2018) Potential virulence factors of bacteria associated with tail fan necrosis in the spiny lobster, Jasus edwardsii. J Fish Dis 41:817–828PubMedCrossRefGoogle Scholar
  119. Zhang M, Sun Y, Chen L, Cai C, Qiao F, Du Z, Li E (2016) Symbiotic bacteria in gills and guts of Chinese mitten crab (Eriocheir sinensis) differ from the free-living bacteria in water. Plos One 11:e0148135PubMedPubMedCentralCrossRefGoogle Scholar
  120. Zobel M (2016) The species pool concept as a framework for studying patterns of plant diversity. J Veg Sci 27:8–18CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department Biological SciencesHumboldt State UniversityArcataUSA
  2. 2.Royal Melbourne Institute of TechnologyMelbourneAustralia

Personalised recommendations