Abstract
Fragmentation and loss of natural habitat have important consequences for wild populations and can negatively affect long-term viability and resilience to environmental change. Salt marsh obligate species, such as those that occupy the San Francisco Bay Estuary in western North America, occupy already impaired habitats as result of human development and modifications and are highly susceptible to increased habitat loss and fragmentation due to global climate change. We examined the genetic variation of the California Ridgway’s rail (Rallus obsoletus obsoletus), a state and federally endangered species that occurs within the fragmented salt marsh of the San Francisco Bay Estuary. We genotyped 107 rails across 11 microsatellite loci and a single mitochondrial gene to estimate genetic diversity and population structure among seven salt marsh fragments and assessed demographic connectivity by inferring patterns of gene flow and migration rates. We found pronounced genetic structuring among four geographically separate genetic clusters across the San Francisco Bay. Gene flow analyses supported a stepping stone model of gene flow from south-to-north. However, contemporary gene flow among the regional embayments was low. Genetic diversity among occupied salt marshes and genetic clusters were not significantly different. We detected low effective population sizes and significantly high relatedness among individuals within salt marshes. Preserving genetic diversity and connectivity throughout the San Francisco Bay may require attention to salt marsh restoration in the Central Bay where habitat is both most limited and most fragmented. Incorporating periodic genetic sampling into the management regime may help evaluate population trends and guide long-term management priorities.
Similar content being viewed by others
References
Albertson JD (1995) Ecology of the California clapper rail in South San Francisco Bay. MS Thesis, San Francisco State University, San Francisco
Albertson JD, Evens JG (2000) California clapper rail. In: Olofson PR (ed) Baylands ecosystem species and community profiles: life histories and environmental requirements of key plants, fish and wildlife. San Francisco Bay Area Wetland Ecosystem Goals project. San Francisco Bay Regional Water Quality Control Board, Oakland, pp 332–341
Atwater BF, Conrad SG, Dowden JN, Hedel CW, MacDonald RL, Savage W (1979) History, landforms, and vegetation of the estuary's tidal marshes San Francisco Bay : the urbanized estuary : investigations into the Natural History of San Francisco Bay and Delta with reference to the influence of man : fifty-eighth annual meeting of the Pacific division/American Association for the Advancement of Science held at San Francisco State University, San Francisco, California, 12-16 June 1977, pp 347–386
Barr KR, Kus BE, Preston KL, Howell S, Perkins E, Vandergast AG (2015) Habitat fragmentation in coastal southern California disrupts genetic connectivity in the cactus wren (Campylorhynchus brunneicapillus). Mol Ecol 24:2349–2363
Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345
Beerli P (2009) How to use Migrate or why are Markov chain Monte Carlo programs difficult to use? Population genetics for animal conservation, vol 17. Cambridge University Press, Cambridge, pp 42–79
Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326
Bouzat JL, Cheng HH, Lewin HA, Westemeier RL, Brawn JD, Paige KN (1998) Genetic evaluation of a demographic bottleneck in the greater prairie chicken. Conserv Biol 12:836–843
Brackett C, Maley J, Brumfield R, McRae S (2013) Characterization of microsatellite loci for a threatened species, the King Rail, Rallus elegans, using a next-generation sequencing protocol. Conserv Genet Resour 5:1189–1191
Brooks A (1940) The clapper rail of Morro Bay. Condor 42:126–127
Bui T-VD, Takekawa JY, Overton CT, Schultz ER, Hull JM, Casazza ML (2015) Movements of radio-marked California Ridgway’s rails during monitoring surveys: implications for population monitoring. J Fish Wildl Manag 6:227–237
California Department of Fish and Game (2010) California clapper rail and California black rail Suisun Marsh Survey 2009. Monitoring report for the Suisun Marsh by California department of Fish and Game Bay-Delta Region to California Department of Water Resources. Contract #4600008033.
Casazza ML, Overton CT, Takekawa JY, Rohmer T, Navarre K (2008) Breeding behavior and dispersal of radio-marked California clapper rails. West Birds 39:101–106
Chan YL, Arcese P (2002) Subspecific differentiation and conservation of song sparrows (Melospiza melodia) in the San Francisco Bay region inferred by microsatellite analysis. Auk 119:641–657
Chan YL, Hill CE, Maldonado JE, Fleischer RC (2006) Evolution and conservation of tidal-marsh vertebrates: molecular approaches. Stud Avian Biol 32:54–75
Cohen DA (1895) The California clapper rail. Oologist 12:171–173
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Daehler CC, Strong DR (1997) Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. Am J Bot 84:607–611
Dyer RJ, Nason JD, Garrick RC (2010) Landscape modelling of gene flow: improved power using conditional genetic distance derived from the topology of population networks. Mol Ecol 19:3746–3759
Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Eddleman W, Conway C (1998) Clapper rail (Rallus longirostris). The birds of North America, no. 240. The Birds of North America, Inc., Philadelphia
Evanno G, Castella E, Antoine C, Paillat G, Goudet J (2009) Parallel changes in genetic diversity and species diversity following a natural disturbance. Mol Ecol 18:1137–1144
Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16(6):1149–1166
Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280
Fleischer RC, Fuller G, Ledig DB (1995) Genetic structure of endangered clapper rail (Rallus longirostris) populations in Southern California. Conserv Biol 9:1234–1243
Fotheringham AS, O’Kelly ME (1989) Spatial interaction models: formulation and applications. Kluwer Academic, Dordrecht
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biol Conserv 170:56–63
Garcia EJ (1995) Conservation of the California clapper rail: an analysis of survey methods and habitat use in Marin County. University of California-Davis, California
Gill R (1979) Status and distribution of the California clapper rail (Rallus longirostris obsoletus). Calif Fish Game 65:36–49
Girard P, Takekawa J, Beissinger S (2010) Uncloaking a cryptic, threatened rail with molecular markers: origins, connectivity and demography of a recently-discovered population. Conserv Genet 11:2409–2418
Goals Project (1999) Baylands ecosystem habitat goals. A report of habitat recommendations prepared by the San Francisco Bay Area Wetlands Ecosystem Goals Project. Joint Publication of the U.S. Environmental Protection Agency, San Francisco, California, and San Francisco Bay Regional Water Quality Control Board, Oakland
Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727
Grinnell JH, Miller AH (1994) The distribution of the birds of California. Pac Coast Avifauna 27:1–608
Grosholz ED, Levin LA, Tyler AC, Neira C (2009) Changes in community structure and ecosystem function following Spartina alterniflora invasion of Pacific estuaries. In: Silliman BR, Bertness MD, Grosholz ED (eds) Human impacts on saltmarshes-a global perspective. Univsersity of California, Berkeley, pp 23–40
Haddad NM et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052
Harding EK, Doak DF, Albertson J, Takekawa JE (1998) Predator management in San Francisco Bay wetlands: past trends and future strategies. Final Report prepared for U.S. Fish and Wildlife Service, Sacramento
Hedrick PW, Lacy RC, Allendorf FW, Soulé ME (1996) Directions in conservation biology: comments on Caughley. Conserv Biol 10:1312–1320
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Hunter EA, Nibbelink NP, Alexander CR, Barrett K, Mengak LF, Guy RK, Moore CT, Cooper RJ (2015) Coastal vertebrate exposure to predicted habitat changes dues to sea level rise. Environ Manag 56:1528–1537
Intergovernmental Panel on Climate Change (IPCC) (2007) Summary for policymakers. In: Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13
Johnson D (2001) Habitat fragmentation effects on birds in grasslands and wetlands: a critique of our knowledge. Great Plains Res 11:211–231
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Keyghobadi N, Roland J, Matter SF, Strobeck C (2005) Among- and within-patch components of genetic diversity respond at different rates to habitat fragmentation: an empirical demonstration. Proc R Soc Lond B 272(1562):553–560
Kozicky EL, Schmidt FW (1949) Nesting habits of the clapper rail in New Jersey. Auk 66:355–364
Lacy RC (2000) Considering threats to the viability of small populations using individual-based models. Ecol Bull 48:39–51
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu L, Wood J, Nur N, Stralberg D, Herzog M (2009) California clapper rail (Rallus longirostris obsoletus) population monitoring: 2005–2009. Report to California Department of Fish and Game, Stockton
Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Monographs in population biology. Princeton University Press, Princeton
Malamud-Roam FP, Lynn Ingram B, Hughes M, Florsheim JL (2006) Holocene paleoclimate records from a large California estuarine system and its watershed region: linking watershed climate and bay conditions. Quat Sci Rev 25(13–14):1570–1598
Maley JM, Brumfield RT (2013) Mitochondrial and next-generation sequence data used to infer phylogenetic relationships and species limits in the clapper/king rail complex. Condor 115:316–329
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Markert JA et al (2010) Population genetic diversity and fitness in multiple environments. BMC Evol Biol 10:205
Matthysen E (2005) Density-dependent dispersal in birds and mammals. Ecography 28:403–416
McGranahan DA, Balk D, Anderson B (2007) The rising tide: assessing the risks of climate change and human settlements in low elevation coastal zones. Environ Urban 19:17–39
McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724
Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour 14:726–733
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov 2010, New Orleans, pp 1–8
Miller MP, Haig SM, Mullins TD, Popper KJ, Green M (2012) Evidence for population bottlenecks and subtle genetic structure in the yellow rail. Condor 114:100–112
Narum S (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787
Nichols FH, Cloern JE, Luoma SN, Peterson DH (1986) The modification of an estuary. Science 231:567–573
Nusser JA, Goto RM, Ledig DB, Fleischer RC, Miller MM (1996) RAPD analysis reveals low genetic variability in the endangered light-footed clapper rail. Mol Ecol 5:463–472
Overton C, Casazza M, Takekawa J, Strong D, Holyoak M (2014) Tidal and seasonal effects on survival rates of the endangered California clapper rail: does invasive Spartina facilitate greater survival in a dynamic environment? Biol Invasions 16:1897–1914
Peakall R, Lindenmayer DB (2006) Genetic insights into population recovery following experimental perturbation in a fragmented landscape. Biol Conserv 132:520–532
Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539
Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195
Peery MZ et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418
Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503
Pritchard JK, Wen W (2004) Documentation for structure software: version 2. University of Chicago, Department of Human Genetics, Chicago, p 33
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pruett CL, Arcese P, Chan YL, Wilson AG, Patten MA, Keller LF, Winker K (2008) The effects of contemporary processes in maintaining the genetic structure of western song sparrows (Melospiza melodia). Heredity 101:67–74
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Rambaut A, Suchard MA, Drummond AJ (2013) Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/
Rohmer TC (2010) Tracking the California clapper rail: a home range study in anticipation of imminent habitat change. M.Sc. thesis, University of California, Davis
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Rush SA, Gaines KF, Eddleman W, Conaway CJ (2012) Clapper rail (Rallus longirostris). The Birds of North America Online, Issue No. 340
Ryman N, Allendorf FW, Jorde PE, Laikre L, Hössjer O (2014) Samples from subdivided populations yield biased estimates of effective size that overestimate the rate of loss of genetic variation. Mol Ecol Resour 14:87–99
Saether B-E et al (2005) Generation time and temporal scaling of bird population dynamics. Nature 436:99–102
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33
Schwarzbach SE, Albertson JD, Thomas CM (2006) Effects of predation, flooding, and contamination on reproductive success of California clapper rails (Rallus longirostris obsoletus) in San Francisco Bay. Auk 123:45–60
Silliman OP (1915) Range of the California clapper rail. Condor 17:201
Statham MJ, Aamoth S, Barthman-Thompson L, Estralla S, Fresquez S, Hernandez LD, Tertes R, Sacks BN (2016) Conservation genetics of the endangered San Francisco Bay endemic salt marsh harvest mouse (Reithodontomys raviventris). Conserv Genet. doi:10.1007/s10592-016-0843-4
Takekawa JY et al (2006) Environmental threats to tidal marsh vertebrates in the San Francisco Bay Estuary. In: Greenberg R, Maldonado JE, Droege S, McDonald MV (eds) Studies in avian biology, 32nd edn. Cooper Ornithological Society, Camarillo, pp 176–197
Takekawa JY et al (2013) Final report for sea-level rise response modeling for San Francisco bay estuary tidal marshes. USGS Open File Report 2013-1081. USGS, Vallejo
Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) COMPUTER PROGRAMS: onesamp: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301
Thorne KM, Buffington KJ, Swanson K, Takekawa J (2013) Storm surges and climate change implications for tidal marshes: insight from the San Francisco Bay Estuary, California, USA. Int J Clim Change 4:1–25
Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34
Unfried T, Hauser L, Marzluff J (2013) Effects of urbanization on Song Sparrow (Melospiza melodia) population connectivity. Conserv Genet 14:41–53
U.S. Fish and Wildlife Service (2013) Recovery plan for tidal marsh ecosystems of Northern and Central California. Sacramento, pp xviii+605
Van Houtan KS, Pimm SL, Halley JM, Bierregaard RO, Lovejoy TE (2007) Dispersal of Amazonian birds in continuous and fragmented forest. Ecol Lett 10:219–229
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vandergast AG, Wood DA, Thompson AR, Fisher M, Barrows CW, Grant TJ (2015) Drifting to oblivion? Rapid genetic differentiation in an endangered lizard following habitat fragmentation and drought. Divers Distrib. doi:10.1111/ddi.12398
Waples RS, Do C, Chopelet J (2011) Calculating Ne and Ne/N in age-structured populations: a hybrid Felsenstein-Hill approach. Ecology 92:1513–1522
Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780
Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38 (6):1358
Westemeier RL et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
Acknowledgments
We are grateful for the valuable comments from the associate editor and three anonymous reviewers and that helped improve a previous version of the manuscript. The microsatellite data and associated metadata used for this study can be obtained from ScienceBase (http://dx.doi.org/10.5066/F7HD7SQ0) and ND2 mtDNA sequences were deposited in GENBANK (KU505148-KU505209). We thank our field crews including A. Merritt, E. Schultz, K. Barry, L. Koenig, K. Sawyer, and J. Burton for collecting samples and locality information. We thank S. Bobzien, M. Taylor, and R. Trujillo for assistance and access to East Bay Regional Park District properties; and the U.S. Geological Survey San Francisco Bay Field Station staff for assistance with field work. We also thank the California Department of Fish and Wildlife, Don Edwards National Wildlife Refuge, Marin County Parks, and Las Gallinas Valley Sanitary District for granting us access to their properties. This project was funded by the U. S. Geological Survey Western Ecological Research Center and grants from the U.S. Fish and Wildlife Service, Region 8, Coastal Programs and Recovery Branches and by the California State Coastal Conservatory and Department of Fish and Wildlife. The blood and tissue samples were collected under U.S. Fish and Wildlife Service endangered species permit TE-020548, California Department of Fish and Wildlife Memorandum of Understanding and scientific collecting permits, U.S. Geological Survey Bird Banding Laboratory permit 21142, and the U.S. Geological Survey Western Ecological Research Center Animal Care and Use Committee. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wood, D.A., Bui, TV.D., Overton, C.T. et al. A century of landscape disturbance and urbanization of the San Francisco Bay region affects the present-day genetic diversity of the California Ridgway’s rail (Rallus obsoletus obsoletus). Conserv Genet 18, 131–146 (2017). https://doi.org/10.1007/s10592-016-0888-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-016-0888-4