Article | Published:

Multiple colonist pools shape fiddler crab-associated bacterial communities

The ISME Journalvolume 12pages825837 (2018) | Download Citation

Abstract

Colonization is a key component of community assembly because it continuously contributes new species that can potentially establish and adds individuals to established populations in local communities. Colonization is determined by the regional species pool, which is typically viewed as stable at ecological time scales. Yet, many natural communities including plants, birds and microbes, are exposed to several distinct and dynamic sources of colonists and how multiple colonist pools interact to shape local communities remains unclear. Using a 16S rRNA amplicon survey, we profiled bacteria within surface, subsurface and burrow sediments and assessed their role as colonist pools for fiddler crab-associated bacteria. We found significant differences in composition among sediment types, driven by halophilic taxa in the surface, and different Desulfobacteraceae taxa in the subsurface and burrow. Bacteria from burrow sediment colonized the crab carapace whereas gut bacterial communities were colonized by burrow and surface sediment bacteria. Despite distinct colonist pools influencing gut bacteria, variation in composition across gut samples did not lead to significant clusters. In contrast, carapace bacterial communities clustered in six distinct groups loosely associated with crab species. Our findings suggest that multiple colonist pools can influence local communities but factors explaining variation in community composition depend on local habitats. Recognizing multiple colonist pools expands our understanding of the interaction between regional and local processes driving community structure and diversity.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

References

  1. 1.

    Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, et al. The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett. 2004;7:601–13.

  2. 2.

    Ricklefs RE. Community diversity - relative roles of local and regional processes. Science. 1987;235:167–71.

  3. 3.

    Urban MC, Leibold MA, Amarasekare P, De Meester L, Gomulkiewicz R, Hochberg ME, et al. The evolutionary ecology of metacommunities. Trends in Ecology & Evolution. 2008;23:311–7.

  4. 4.

    Freestone AL, Osman RW. Latitudinal variation in local interactions and regional enrichment shape patterns of marine community diversity. Ecology. 2011;92:208–17.

  5. 5.

    Fukami T. Assembly history interacts with ecosystem size to influence species diversity. Ecology. 2004;85:3234–42.

  6. 6.

    Shipley B, Paine CET, Baraloto C. Quantifying the importance of local niche-based and stochastic processes to tropical tree community assembly. Ecology. 2012;93:760–9.

  7. 7.

    Karger DN, Tuomisto H, Amoroso VB, Darnaedi D, Hidayat A, Abrahamczyk S, et al. The importance of species pool size for community composition. Ecography. 2015;38:1243–53.

  8. 8.

    Myers JA, Harms KE. Seed arrival, ecological filters, and plant species richness: a meta-analysis. Ecol Lett. 2009;12:1250–60.

  9. 9.

    Lessard JP, Belmaker J, Myers JA, Chase JM, Rahbek C. Inferring local ecological processes amid species pool influences. Trends in Ecology & Evolution. 2012;27:600–7.

  10. 10.

    Belmaker J, Jetz W. Spatial Scaling of Functional Structure in Bird and Mammal Assemblages. American Naturalist. 2013;181:464–78.

  11. 11.

    Zobel M. The species pool concept as a framework for studying patterns of plant diversity. Journal of Vegetation Science. 2016;27:8–18.

  12. 12.

    Cornell HV, Harrison SP (2014). What Are Species Pools and When Are They Important? In: Futuyma DJ (ed). Annual Review of Ecology, Evolution, and Systematics, Vol 45. pp 45-67.

  13. 13.

    Zobel M. Plant species coexistence- the role of historical, evolutionary and ecological factors. Oikos. 1992;65:314–20.

  14. 14.

    Godfray HCJ, Lawton JH. Scale and species numbers. Trends in Ecology & Evolution. 2001;16:400–4.

  15. 15.

    Rajaniemi TK, Goldberg DE, Turkington R, Dyer AR. Quantitative partitioning of regional and local processes shaping regional diversity patterns. Ecol Lett. 2006;9:121–8.

  16. 16.

    Diamond JM. The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biol Conserv. 1975;7:129–46.

  17. 17.

    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press.

  18. 18.

    da Fonseca-Genevois V, Somerfield PJ, Neves MHB, Coutinho R, Moens T. Colonization and early succession on artificial hard substrata by meiofauna. Marine Biology. 2006;148:1039–50.

  19. 19.

    Langenheder S, Ragnarsson H. The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology. 2007;88:2154–61.

  20. 20.

    Loudon AH, Woodhams DC, Parfrey LW, Archer H, Knight R, McKenzie V, et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). Isme Journal. 2014;8:830–40.

  21. 21.

    Rime T, Hartmann M, Frey B. Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. Isme Journal. 2016;10:1625–1641.

  22. 22.

    Graves GR, Gotelli NJ. Neotropical land-bridge avifaunas - new approaches to null hypothesis in biogeography. Oikos. 1983;41:322–33.

  23. 23.

    Holzapfel C, Schmidt W, Shmida A. The role of seed bank and seed rain in the recolonization of disturbed sites along an aridity gradient. Phytocoenologia. 1993;23:561–80.

  24. 24.

    Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–52.

  25. 25.

    Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R, et al. Microbial Biogeography of Public Restroom Surfaces. Plos One. 2011;6:e28132.

  26. 26.

    Willems JH, Bik LPM. Restoration of high species density in calcareous grassland: the role of seed rain and soil seed bank. Applied Vegetation Science. 1998;1:91–100.

  27. 27.

    Wolters M, Bakker JP. Soil seed bank and driftline composition along a successional gradient on a temperate salt marsh. Applied Vegetation Science. 2002;5:55–62.

  28. 28.

    Kalamees R, Zobel M. The role of the seed bank in gap regeneration in a calcareous grassland community. Ecology. 2002;83:1017–25.

  29. 29.

    Kraft NJB, Adler PB, Godoy O, James EC, Fuller S, Levine JM. Community assembly, coexistence and the environmental filtering metaphor. Functional Ecology. 2015;29:592–9.

  30. 30.

    Chase JM, Myers JA. Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical Transactions of the Royal Society B-Biological Sciences. 2011;366:2351–63.

  31. 31.

    Duneau D, Ebert D. The role of moulting in parasite defence. Proceedings of the Royal Society B-Biological Sciences. 2012;279:3049–54.

  32. 32.

    Gaiser EE, Bachmann RW. The ecology and taxonomy of epizoic diatoms on cladocera. Limnol Oceanogr. 1993;38:628–37.

  33. 33.

    Dye AH, Lasiak TA. Assimilation efficiencies of fiddler crabs and deposit feeding gastropods from tropical mangrove sediments. Comparative Biochemistry and Physiology a-Physiology. 1987;87:341–4.

  34. 34.

    Kristensen E. Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. Journal of Sea Research. 2008;59:30–43.

  35. 35.

    Ferreira TO, Otero XL, Vidal-Torrado P, Macias F. Effects of bioturbation by root and crab activity on iron and sulfur biogeochemistry in mangrove substrate. Geoderma. 2007a;142:36–46.

  36. 36.

    Kopke B, Wilms R, Engelen B, Cypionka H, Sass H. Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol. 2005;71:7819–30.

  37. 37.

    Papaspyrou S, Gregersen T, Cox RP, Thessalou-Legaki M, Kristensen E. Sediment properties and bacterial community in burrows of the ghost shrimp Pestarella tyrrhena (Decapoda: Thalassinidea). Aquatic Microbial Ecology. 2005;38:181–90.

  38. 38.

    Moon YJ, Kim SI, Chung YH. Sensing and Responding to UV-A in Cyanobacteria. International Journal of Molecular Sciences. 2012;13:16303–32.

  39. 39.

    Holguin G, Vazquez P, Bashan Y. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biology and Fertility of Soils. 2001;33:265–78.

  40. 40.

    Rejmankova E, Komarkova J. Response of cyanobacterial mats to nutrient and salinity changes. Aquatic Botany. 2005;83:87–107.

  41. 41.

    Romero IC, Jacobson M, Fuhrman JA, Fogel M, Capone DG. Long-term nitrogen and phosphorus fertilization effects on N-2 fixation rates and nifH gene community patterns in mangrove sediments. Marine Ecology-an Evolutionary Perspective. 2012;33:117–27.

  42. 42.

    Segarra KEA, Comerford C, Slaughter J, Joye SB. Impact of electron acceptor availability on the anaerobic oxidation of methane in coastal freshwater and brackish wetland sediments. Geochim Cosmochim Acta. 2013;115:15–30.

  43. 43.

    Fanjul E, Grela MA, Iribarne O. Effects of the dominant SW Atlantic intertidal burrowing crab Chasmagnathus granulatus on sediment chemistry and nutrient distribution. Mar Ecol Prog Ser. 2007;341:177–90.

  44. 44.

    Fanjul E, Escapa M, Montemayor D, Addino M, Alvarez MF, Grela MA, et al. Effect of crab bioturbation on organic matter processing in South West Atlantic intertidal sediments. Journal of Sea Research. 2015;95:206–16.

  45. 45.

    Hunting ER, Whatley MH, van der Geest HG, Mulder C, Kraak MHS, Breure AM, et al. Invertebrate footprints on detritus processing, bacterial community structure, and spatiotemporal redox profiles. Freshwater Science. 2012;31:724–32.

  46. 46.

    Marinelli RL, Lovell CR, Wakeham SG, Ringelberg DB, White DC. Experimental investigation of the control of bacterial community composition in macrofaunal burrows. Mar Ecol Prog Ser. 2002;235:1–13.

  47. 47.

    Wang JQ, Zhang XD, Jiang LF, Bertness MD, Fang CM, Chen JK, et al. Bioturbation of Burrowing Crabs Promotes Sediment Turnover and Carbon and Nitrogen Movements in an Estuarine Salt Marsh. Ecosystems. 2010;13:586–99.

  48. 48.

    Harris JM. The presence, nature and role of gut microflora in aquatic invertebrates - a synthesis. Microb Ecol. 1993;25:195–231.

  49. 49.

    Robinson CJ, Bohannan BJM, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiology and Molecular Biology Reviews. 2010;74:453–76.

  50. 50.

    Brosing A. Recent developments on the morphology of the brachyuran foregut ossicles and gastric teeth. Zootaxa. 2010;44:33–41.

  51. 51.

    Vogt G, Stocker W, Storch V, Zwilling R. Biosynthesis of Astacus protease, a digestive enzyme from crayfish. Histochemistry. 1989;91:373–81.

  52. 52.

    Wang W, Wu XG, Liu ZJ, Zheng HJ, Cheng YX. 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. 2014;9:e84921.

  53. 53.

    Benson AK, Kelly SA, Legge R, Ma FR, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:18933–8.

  54. 54.

    Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 2006;127:423–33.

  55. 55.

    Smith CCR, Snowberg LK, Caporaso JG, Knight R, Bolnick DI. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. Isme Journal. 2015;9:2515–26.

  56. 56.

    Dillon RJ, Dillon VM. The gut bacteria of insects: Nonpathogenic interactions. Annu Rev Entomol. 2004;49:71–92.

  57. 57.

    Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans. Science. 2011;332:970–4.

  58. 58.

    Brucker RM, Bordenstein SR. The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia. Science. 2013;341:667–9.

  59. 59.

    Fraune S, Bosch TCG. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:13146–51.

  60. 60.

    Martinson VG, Douglas AE, Jaenike J. Community structure of the gut microbiota in sympatric species of wild Drosophila. Ecol Lett. 2017;20:629–39.

  61. 61.

    Munguia P, Levinton JS, Silbiger NJ. Latitudinal differences in thermoregulatory color change in Uca pugilator. J Exp Mar Bio Ecol. 2013;440:8–14.

  62. 62.

    Levinton J, Lord S, Higeshide Y. Are crabs stressed for water on a hot sand flat? Water loss and field water state of two species of intertidal fiddler crabs. J Exp Mar Bio Ecol. 2015;469:57–62.

  63. 63.

    Cuellar-Gempeler C, Munguia P. Fiddler crabs (Uca thayeri, Brachyura: Ocypodidae) affect bacterial assemblages in mangrove forest sediments. Community Ecology. 2013;14:59–66.

  64. 64.

    Darnell MZ, Fowler KK, Munguia P. Sex-specific thermal constraints on fiddler crab behavior. Behavioral Ecology. 2013;24:997–1003.

  65. 65.

    Hartnoll RG. Reproductive investment in Brachyura. Hydrobiologia. 2006;557:31–40.

  66. 66.

    Pennoyer KE, Himes AR, Frederich M (2016). Effects of sex and color phase on ion regulation in the invasive European green crab, Carcinus maenas. Marine Biology 163.

  67. 67.

    Caravello HE, Cameron GN. Foraging time allocation in relation to sex by the Gulf Coast fiddler crab (Uca panacea). Oecologia. 1987;72:123–6.

  68. 68.

    Caravello HE, Cameron GN. Time activity budgets of the Gulf-coast fiddler-crab (Uca panacea). American Midland Naturalist. 1991;126:403–7.

  69. 69.

    Bittler K. Salinity gradients in the Mission-Aransas National Estuarine Research REserve. Port Aransas TX: The Marine Science Institute from the University of Texas at Austin; 2011.

  70. 70.

    Thurman CL. Fiddler-crabs (Genus Uca) of Eastern Mexico (Decapoda, Brachyura, Ocypodidae). Crustaceana. 1987;53:94–105.

  71. 71.

    Bertics VJ, Ziebis W. Biodiversity of benthic microbial communities in bioturbated coastal sediments is controlled by geochemical microniches. Isme Journal. 2009;3:1269–85.

  72. 72.

    Ong SH, Kukkillaya VU, Wilm A, Lay C, Ho EXP, Low L et al. (2013). Species Identification and Profiling of Complex Microbial Communities Using Shotgun Illumina Sequencing of 16S rRNA Amplicon Sequences. Plos One 8

  73. 73.

    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.

  74. 74.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010b;7:335–6.

  75. 75.

    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology. 2006;72:5069–72.

  76. 76.

    Team Rdc (2008). R: A language and environment for statistical computing. R Foundation for Statistical Computing: Vienna, Austria.

  77. 77.

    Pielou EC. The measurement of diversity in different types of biological collections. J Theor Biol. 1966;13:131–44.

  78. 78.

    Bartlett MS. Properties of sufficiency and statistical tests. Proceedings of the Royal Society of London Series a-Mathematical and Physical Sciences. 1937;160:0268–82.

  79. 79.

    Shapiro SS, Wilk MB. An analysis of variance test for normality (complete series). Biometrika. 1965;52:591–&.

  80. 80.

    Anderson MJ. Distance-based tests for homogeneity of multivariate dispersions. Biometrics. 2006;62:245–53.

  81. 81.

    Anderson MJ, Walsh DCI. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr. 2013;83:557–74.

  82. 82.

    Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin P, O’Hara GL et al (2015). vegan: Community ecology package, 2.2-1 edn. p R package.

  83. 83.

    Petraitis PS, Methratta ET, Rhile EC, Vidargas NA, Dudgeon SR. Experimental confirmation of multiple community states in a marine ecosystem. Oecologia. 2009;161:139–48.

  84. 84.

    Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG, et al. Bayesian community-wide culture-independent microbial source tracking. Nat Meth. 2011;8:761–3.

  85. 85.

    Ward JH. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 1963;58:236–44.

  86. 86.

    Tibshirani R, Walther G, Hastie T. Estimating the number of clusters in a data set via the gap statistic. Journal of the Royal Statistical Society Series B-Statistical Methodology. 2001;63:411–23.

  87. 87.

    Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A et al (2016). gplots: Various R programming tools for plotting data, 3.0.1. edn.

  88. 88.

    Clarke KR. Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology. 1993;18:117–43.

  89. 89.

    Warton DI, Wright ST, Wang Y. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution. 2012;3:89–101.

  90. 90.

    Dunn OJ. Multiple comparison among means. J Am Stat Assoc. 1961;56:52–64.

  91. 91.

    Wright JJ, Mewis K, Hanson NW, Konwar KM, Maas KR, Hallam SJ. Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle. ISME J. 2014;8:455–68.

  92. 92.

    Plante CJ, Wilde SB. Biotic disturbance, recolonization, and early succession of bacterial assemblages in intertidal sediments. Microb Ecol. 2004;48:154–66.

  93. 93.

    Abdeljabbar H, Cayol JL, Ben Hania W, Boudabous A, Sadfi N, Fardeau ML. Halanaerobium sehlinense sp nov., an extremely halophilic, fermentative, strictly anaerobic bacterium from sediments of the hypersaline lake Sehline Sebkha. Int J Syst Evol Microbiol. 2013;63:2069–74.

  94. 94.

    Bardavid RE, Oren A. The amino acid composition of proteins from anaerobic halophilic bacteria of the order Halanaerobiales. Extremophiles. 2012;16:567–72.

  95. 95.

    Oren A. Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Frontiers in Microbiology. 2013;4:315.

  96. 96.

    Ferreira TO, Otero XL, Vidal-Torrado P, Macias F. Redox processes in mangrove soils under Rhizophora mangle in relation to different environmental conditions. Soil Science Society of America Journal. 2007b;71:484–91.

  97. 97.

    Oakley BB, Carbonero F, van der Gast C, Hawkins RJ, Purdy KJ. Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations. ISME J. 2010;4:488–97.

  98. 98.

    Dang HY, Lovell CR. Numerical dominance and phylotype diversity of marine Rhodobacter species during early colonization of submerged surfaces in coastal marine waters as determined by 16S ribosomal DNA sequence analysis and fluorescence in situ hybridization. Appl Environ Microbiol. 2002;66:467–75.

  99. 99.

    Kirchman DL. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100.

  100. 100.

    Wang W. Bacterial diseases of crabs: a review. J Invertebr Pathol. 2011;106:18–26.

  101. 101.

    Miletto M, Williams KH, N’Guessan AL, Lovley DR. Molecular analysis of the metabolic rates of discrete subsurface populations of sulfate reducers. Appl Environ Microbiol. 2011;77:6502–9.

  102. 102.

    Shmida A, Wilson MV (1985). Biological determinants of species diversity. Journal of biogeography : 1-20.

  103. 103.

    Gamble MD, Lovell CR. Infaunal Burrows Are Enrichment Zones for Vibrio parahaemolyticus. Appl Environ Microbiol. 2011;77:3703–14.

  104. 104.

    Pruzzo C, Vezzulli L, Colwell RR. Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol. 2008;10:1400–10.

  105. 105.

    Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA. Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. Isme Journal. 2010;4:1531–44.

  106. 106.

    Thompson WE, Molinaro PJ, Greco TM, Tedeschi JB, Holliday CW. Regulation of hemolymph volume by uptake of sand capilary water in desiccated fiddler crabs, Uca pugialtor and Uca pugnax. Comparative Biochemistry and Physiology a-Physiology. 1989;94:531–8.

  107. 107.

    Thurman CL. Osmoregulation in six sympatric fiddler crabs (genus Uca) from the northwestern Gulf of Mexico. Marine Ecology-Pubblicazioni Della Stazione Zoologica Di Napoli I. 2002;23:269–84.

  108. 108.

    Lasher C, Dyszynski G, Everett K, Edmonds J, Ye WY, Sheldon W, et al. The Diverse Bacterial Community in Intertidal, Anaerobic Sediments at Sapelo Island, Georgia. Microb Ecol. 2009;58:244–61.

  109. 109.

    Weissburg M. Functional analysis of fiddler crab foraging sex-specific mechanics and constraints in Uca pugnax (Smith). J Exp Mar Bio Ecol. 1992;156:105–24.

Download references

Acknowledgements

For financial support, we thank the Graduate Doctoral Dissertation Improvement Grant from the Ecology Evolution and Behavior program at the University of Texas at Austin for funding. We would like to thank Deana Erdner for useful comments guiding our molecular work and for her generous sharing of laboratory space. Three anonymous reviewers provided remarkable advice that improved the manuscript considerably. Lastly, we thank undergraduate and graduate students as well as postdocs and friends that contributed to field sampling.

Author information

Affiliations

  1. Department of Biological Sciences, Florida State University, 319 Stadium Drive, Tallahassee, FL, 32304, USA

    • Catalina Cuellar-Gempeler
  2. Section of Integrative Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX, 78712, USA

    • Mathew A. Leibold

Authors

  1. Search for Catalina Cuellar-Gempeler in:

  2. Search for Mathew A. Leibold in:

Conflict of interest

:The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Catalina Cuellar-Gempeler.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

DOI

https://doi.org/10.1038/s41396-017-0014-8