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1) The study tested the hypothesis that the endemic Hawaiian shrimp Halocaridina rubra acts as a keystone grazer in anchialine habitats by modifying benthic algal communities. 2) Laboratory experiments found that aquaria with higher densities of H. rubra resembling fishless habitats had lower chlorophyll a concentrations than aquaria without shrimp, indicating shrimp grazing reduced algal abundance. 3) Preliminary analysis of environmental and gut microbiome samples suggests H. rubra selectively grazes on a genus of bacteria called Massilia that comprises a large portion of its gut community. Determining how grazing impacts microbial communities is a focus of ongoing work.

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The effects of shrimp grazing on the microbial communities of Hawaiian anchialine habitats Justin C. Havird, Alan E. Wilson, & Scott R. Santos Dept. of Biological Sciences Auburn University
Animals can modify their habitat Well-known keystone modifiers Beavers -dams alter hydrology, bio-geochemistry, and productivity on a wide scale Corals -create habitat for other species on a wide scale http://www.extremescience.com/coral-reefs.htm Mills et al. 1993; Naiman et al. 1986; Monaco & Helmuth 2011
Atyid shrimp are modifiers as well Puerto Rican streams ? Used electrified hoops to exclude shrimp or fishes from certain areas ? Excluded shrimp treatments had higher levels of ? inorganic sediments ? organic material ? carbon ? Nitrogen ? Atyid shrimp may be habitat Pringle et al. 1999 modifiers in streams, but atyids are also found in Pringle et al. 1993, Pringle 1996, Pringle et al. 1999
Anchialine habitats Anchialine habitat characteristics: ? Ponds/pools ? Coastal ? Land-locked ? Have a cave component ? Underground seawater and freshwater influences ? Intermediate salinity ? Extreme habitats J. Craft Sket 1996; Iliffe 2004
Anchialine habitats are rare worldwide, but most concentrated in Hawaii ~600 of the ~1000 known anchialine habitats are in Hawaii Iliffe 2004; Brock et al. 1987; Carey et al. 2011
Endemic Hawaiian anchialine biota Diverse, but: ? Mainly shrimp ? Halocaridina rubra: C Most abundant C Most widespread C Small (~10 mm) C Concentrated C An atyid C A keystone grazer? Bailey-Brock and Brock 1993; Maciolek 1983
One hypothesis Anchialine pools containing exotic fish are devoid of shrimp because of predation*, and the subsequent absence of shrimp appears to initiate changes in the benthic biology of pools. Filamentous algae grow over the substrate and cover the diverse bacterial/algal community that previously flourished in the pools. We contend that the shrimp are the keystone species in maintaining the benthic community of the anchialine pools. -Bailey-Brock & Brock 1993 *Invasive fishes dont consume shrimp under most scenarios (Havird et al., in review Hydrobiologia)
Testing the hypothesis 1) Are fish-invaded anchialine ponds devoid of shrimp? ? Recent studies suggest shrimp may be present nocturnally in some fish-invaded ponds ? We quantified shrimp densities during day and night surveys in 14 fish-invaded and fishless ponds using quadrants and timed counts Capps et al. 2009; Carey et al. 2011; Sakihara 2012
These densities were used in a lab Tiles being cultured with algae in study to investigate grazing impacts common culture aquarium ? Tiles with algal communities from AL ponds used as a proxy for anchialine benthic communities ? 24 replicate experimental aquaria w/ 9 tiles each & variable shrimp densities ? Chl a concentration measured over 2 months of grazing Algae coated tiles in experimental aquarium Laboratory studies in ecology Pros Cons ? Replication ? May be less applicable ? Controls to natural systems ? Causation, ? E.g., are AL pond not correlation algal communities a good proxy for HI anchialine pond communities? Eberhardt and Thomas 1991; Edmondson 1993; Kimball and Levin 1985; Schmitdz 2005
Experimental set-up # Shrimp Variable densities based on ecologically relevant densities measured in field (see previous movie) 5 25 0 15 5 15 25 0 15 0 25 5 5 0 15 25 15 0 5 25 0 15 5 25
Results *Error bars show 95% C.I. throughout 180000 P > 0.3 No effect of shrimp densities on [Chl a] No shrimp 160000 before 1 month Low P = 0.09 140000 Med 120000 High Chlorophyll a (?g/L) 100000 80000 A A 60000 A,B A,B 40000 B 20000 B B B 0 -20000 0 10 20 30 40 50 60 Day After one month, aquaria with no shrimp had higher [Chl a] than aquaria with either High or Med levels of shrimp (ANOVA, letters show significant groupings at P < 0.05)
Remember, these densities of shrimp are ecologically relevant: Fishless Habitats High treatment Med treatment Low treatment No treatment Densities measured in the field from four ecological states (day invaded, night invaded, non-invaded, and highest measured) were used in the aquaria experiments ? E.g., for the High treatment: 1300 shrimp m-2 = 25 shrimp per 0.02 m2 (the size of the experimental aquaria used in this study)
Conclusions ? H. rubra can alter algal abundance by grazing ? But, how does community composition change? SKIP Gut SKIP Environmental Samples ? Preliminary microbiome profiling of environmental samples and shrimp guts from the habitat SKIP suggest < 7% of that shrimp are specifically grazing on 79% environmental a small fraction of microbes of gut community is community is Massilia sp. Massilia sp. ? Given this, how does selective shrimp grazing change the microbial community?
Sample processing 2) Environmental DNA extracted from samples 1) Samples preserved in RNALater 3) DNA amplified with two markers: ? V6 region of 16S (prokaryotic specific) ? V9 region of 18S (eukaryotic specific) Gloor et al. 2010
4) Amplified DNA sequenced using 5) Reads annotated Illumina technology with BLAST pipeline Metzker 2010 6) Annotated OTUs used to generate community composition profiles www.washington.edu
This sampling scheme will allow determination of how: ? grazing affects environmental Dissected shrimp gut microbial communities ? grazing affects microbial communities in shrimp guts ? gut communities continue to remain altered after grazing ends (can gut communities recover from grazing?) ? microbial communities in shrimp feces relate to environmental and gut communities
Discussion ? H. rubra grazing can shape benthic microbial communities in the laboratory C Tanks without shrimp had more algae than tanks with higher levels of shrimp ? Ongoing laboratory experiments and field- based experiments (in collaboration with ecologists at Cornell University) will shed light on how grazing shapes microbial communities
Discussion ? Fish-invaded habitats may have altered microbial communities due to reduced grazing C Tanks with shrimp densities representative of invaded habitats had greater algal abundances ? A recent field survey supports this as invaded habitats had: = invaded = fishless ? benthic biomass ? productivity ? nutrients Dalton et al. 2012
Acknowledgments Co-authors Molette Lab (esp. Rebecca Vaught) Scott R. Santos Alan E. Wilson Funding Sources NSF-DEB #0949855 to S.R.S. Others to J.C.H.
Literature Cited 1. Mills, L.S., M.E. Soul, and D.F. Doak. 1993. The keystone-species concept in ecology and conservation. BioScience 43:219-224. 2. Naiman, R. J., J. M. Melillo, andJ. M. Hobbie. 1986. Ecosystem alteration of boreal forest streams by beaver (Castor canadensis). Ecology 67:1254-1269. 3. Monaco, C.J. and B.M. Helmuth. 2011. Tipping points, thresholds, and the keystone role of physiology in marine climate change research. Pp. 123-151 in Advances in Marine Biology, Volume 60, M. Lesser, ed., Elsevier, London, UK. 4. Pringle, C.M., Blake, G.A., Covich, A.P., Buzby, K.M., Finley, A., 1993. Effects of omnivorous shrimp in a montane tropical stream sediment removal, disturbance of sessile invertebrates and enhancement of understory algal biomass. Oecologia 93, 1C11. 5. Pringle, C.M., 1996. Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of algal communities over different scales in tropical montane streams, Puerto Rico. Freshw. Biol. 35, 125C140. 6. Pringle, C.M., Hemphill, N., McDowell, W.H., Bednarek, A., March, J.G., 1999. Linking species and ecosystems: different biotic assemblages cause interstream differences in organic matter. Ecology 80, 1860C1872. 7. Sket, B. 1996. The ecology of anchialine caves. Trends in Ecology and Evolution 11:221-225. 8. Iliffe, T. M. 2004. Anchialine caves, biodiversity in. Pp. 24-30 in Encyclopedia of Caves, D.C. Culver and W.B. White, eds., Elsevier, Burlington, MA. 9. Brock, R. E., J. E. Norris, D. A. Ziemann, and M. T. Lee. 1987. Characteristics of water quality in anchialine ponds of the Kona, Hawaii, coast. Pacific Science 41:200-208. 10. Carey, C.C., M.P. Ching, S.M. Collins, A.M. Early, W.M. Fetzer, D. Chai, and N.G. Hairston, Jr. 2011. Predator-dependent diel migration by Halocaridina rubra shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools. Aquatic Ecology 45: 35-41. 11. Bailey-Brock, J. H. and R. E. Brock. 1993. Feeding, reproduction, and sense organs of the Hawaiian anchialine shrimp Halocaridina rubra (Atyidea). Pacific Science 47:338-355. 12. Maciolek, J. A. 1983. Distribution and biology of Indo-Pacific insular hypogeal shrimps. Bulletin of Marine Science 33:606-618. 13. Havird, J. C., J. R. Weeks, S. Hau, and S. R. Santos. In review. Invasive species alter endemic species distributions via direct predation and behavioral modification in the Hawaiian anchialine ecosystem. Hydrobiologia. 14. Capps, K.A., C.B. Turner, M.T. Booth, D.L. Lombardozzi, S.H. McArt, D. Chai, and M.G. Hariston Jr. 2009. Behavioral responses of the endemic shrimp Halocaridina rubra (Malacostraca: Atyidae) to an introduced fish, Gambusia affinis (Actinopterygii: Poeciliidae) and implications for the trophic structure of Hawaiian anchialine ponds. Pacific Science 63:27C37. 15. Sakihara, T. S., 2012. A diel comparison of the unique faunal assemblage in remote anchialine pools on Hawaii Island. Pacific Science 66: 83C96. 16. Eberhardt, L. L. and J. M. Thomas. 1991. Designing environmental field studies. Ecological Monographs 61: 53-73. 17. Edmondson, W. T. 1993. Experiments and quasi-experiments in limnology. Bulletin of Marine Science 53:65-83. 18. Kimball, K. D. and S. A. Levin. 1985. Limitations of laboratory bioassays - the need for ecosystem-level testing. Bioscience 35:165-171. 19. Schmitz, O. J. 2005. Scaling from plot experiments to landscapes: studying grasshoppers to inform forest ecosystem management. Oecologia 145:225- 234. 20. Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, et al. (2010) Microbiome Profiling by Illumina Sequencing of Combinatorial Sequence-Tagged PCR Products. PLoS ONE 5(10): e15406. doi:10.1371/journal.pone.0015406 21. Metzker, M. L. 2010. Sequencing technologies C the next generation. Nature Reviews Genetics 11:31-46. 22. Dalton, C. M., A. Mokiao-Lee, T. S. Sakihara, M. G. Weber, C. A. Roco, Z. Han, B. Dudley, R. A. MacKenzie & N. G. Hairston Jr., 2012. Density- and trait-mediated topCdown effects modify bottomCup control of a highly endemic tropical aquatic food web. Oikos doi: 10.1111/j.1600-0706.2012.20696.x

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Havird show case

  • 1. The effects of shrimp grazing on the microbial communities of Hawaiian anchialine habitats Justin C. Havird, Alan E. Wilson, & Scott R. Santos Dept. of Biological Sciences Auburn University
  • 2. Animals can modify their habitat Well-known keystone modifiers Beavers -dams alter hydrology, bio-geochemistry, and productivity on a wide scale Corals -create habitat for other species on a wide scale http://www.extremescience.com/coral-reefs.htm Mills et al. 1993; Naiman et al. 1986; Monaco & Helmuth 2011
  • 3. Atyid shrimp are modifiers as well Puerto Rican streams ? Used electrified hoops to exclude shrimp or fishes from certain areas ? Excluded shrimp treatments had higher levels of ? inorganic sediments ? organic material ? carbon ? Nitrogen ? Atyid shrimp may be habitat Pringle et al. 1999 modifiers in streams, but atyids are also found in Pringle et al. 1993, Pringle 1996, Pringle et al. 1999
  • 4. Anchialine habitats Anchialine habitat characteristics: ? Ponds/pools ? Coastal ? Land-locked ? Have a cave component ? Underground seawater and freshwater influences ? Intermediate salinity ? Extreme habitats J. Craft Sket 1996; Iliffe 2004
  • 5. Anchialine habitats are rare worldwide, but most concentrated in Hawaii ~600 of the ~1000 known anchialine habitats are in Hawaii Iliffe 2004; Brock et al. 1987; Carey et al. 2011
  • 6. Endemic Hawaiian anchialine biota Diverse, but: ? Mainly shrimp ? Halocaridina rubra: C Most abundant C Most widespread C Small (~10 mm) C Concentrated C An atyid C A keystone grazer? Bailey-Brock and Brock 1993; Maciolek 1983
  • 7. One hypothesis Anchialine pools containing exotic fish are devoid of shrimp because of predation*, and the subsequent absence of shrimp appears to initiate changes in the benthic biology of pools. Filamentous algae grow over the substrate and cover the diverse bacterial/algal community that previously flourished in the pools. We contend that the shrimp are the keystone species in maintaining the benthic community of the anchialine pools. -Bailey-Brock & Brock 1993 *Invasive fishes dont consume shrimp under most scenarios (Havird et al., in review Hydrobiologia)
  • 8. Testing the hypothesis 1) Are fish-invaded anchialine ponds devoid of shrimp? ? Recent studies suggest shrimp may be present nocturnally in some fish-invaded ponds ? We quantified shrimp densities during day and night surveys in 14 fish-invaded and fishless ponds using quadrants and timed counts Capps et al. 2009; Carey et al. 2011; Sakihara 2012
  • 9. These densities were used in a lab Tiles being cultured with algae in study to investigate grazing impacts common culture aquarium ? Tiles with algal communities from AL ponds used as a proxy for anchialine benthic communities ? 24 replicate experimental aquaria w/ 9 tiles each & variable shrimp densities ? Chl a concentration measured over 2 months of grazing Algae coated tiles in experimental aquarium Laboratory studies in ecology Pros Cons ? Replication ? May be less applicable ? Controls to natural systems ? Causation, ? E.g., are AL pond not correlation algal communities a good proxy for HI anchialine pond communities? Eberhardt and Thomas 1991; Edmondson 1993; Kimball and Levin 1985; Schmitdz 2005
  • 10. Experimental set-up # Shrimp Variable densities based on ecologically relevant densities measured in field (see previous movie) 5 25 0 15 5 15 25 0 15 0 25 5 5 0 15 25 15 0 5 25 0 15 5 25
  • 11. Results *Error bars show 95% C.I. throughout 180000 P > 0.3 No effect of shrimp densities on [Chl a] No shrimp 160000 before 1 month Low P = 0.09 140000 Med 120000 High Chlorophyll a (?g/L) 100000 80000 A A 60000 A,B A,B 40000 B 20000 B B B 0 -20000 0 10 20 30 40 50 60 Day After one month, aquaria with no shrimp had higher [Chl a] than aquaria with either High or Med levels of shrimp (ANOVA, letters show significant groupings at P < 0.05)
  • 12. Remember, these densities of shrimp are ecologically relevant: Fishless Habitats High treatment Med treatment Low treatment No treatment Densities measured in the field from four ecological states (day invaded, night invaded, non-invaded, and highest measured) were used in the aquaria experiments ? E.g., for the High treatment: 1300 shrimp m-2 = 25 shrimp per 0.02 m2 (the size of the experimental aquaria used in this study)
  • 13. Conclusions ? H. rubra can alter algal abundance by grazing ? But, how does community composition change? SKIP Gut SKIP Environmental Samples ? Preliminary microbiome profiling of environmental samples and shrimp guts from the habitat SKIP suggest < 7% of that shrimp are specifically grazing on 79% environmental a small fraction of microbes of gut community is community is Massilia sp. Massilia sp. ? Given this, how does selective shrimp grazing change the microbial community?
  • 14. Sample processing 2) Environmental DNA extracted from samples 1) Samples preserved in RNALater 3) DNA amplified with two markers: ? V6 region of 16S (prokaryotic specific) ? V9 region of 18S (eukaryotic specific) Gloor et al. 2010
  • 15. 4) Amplified DNA sequenced using 5) Reads annotated Illumina technology with BLAST pipeline Metzker 2010 6) Annotated OTUs used to generate community composition profiles www.washington.edu
  • 16. This sampling scheme will allow determination of how: ? grazing affects environmental Dissected shrimp gut microbial communities ? grazing affects microbial communities in shrimp guts ? gut communities continue to remain altered after grazing ends (can gut communities recover from grazing?) ? microbial communities in shrimp feces relate to environmental and gut communities
  • 17. Discussion ? H. rubra grazing can shape benthic microbial communities in the laboratory C Tanks without shrimp had more algae than tanks with higher levels of shrimp ? Ongoing laboratory experiments and field- based experiments (in collaboration with ecologists at Cornell University) will shed light on how grazing shapes microbial communities
  • 18. Discussion ? Fish-invaded habitats may have altered microbial communities due to reduced grazing C Tanks with shrimp densities representative of invaded habitats had greater algal abundances ? A recent field survey supports this as invaded habitats had: = invaded = fishless ? benthic biomass ? productivity ? nutrients Dalton et al. 2012
  • 19. Acknowledgments Co-authors Molette Lab (esp. Rebecca Vaught) Scott R. Santos Alan E. Wilson Funding Sources NSF-DEB #0949855 to S.R.S. Others to J.C.H.
  • 20. Literature Cited 1. Mills, L.S., M.E. Soul, and D.F. Doak. 1993. The keystone-species concept in ecology and conservation. BioScience 43:219-224. 2. Naiman, R. J., J. M. Melillo, andJ. M. Hobbie. 1986. Ecosystem alteration of boreal forest streams by beaver (Castor canadensis). Ecology 67:1254-1269. 3. Monaco, C.J. and B.M. Helmuth. 2011. Tipping points, thresholds, and the keystone role of physiology in marine climate change research. Pp. 123-151 in Advances in Marine Biology, Volume 60, M. Lesser, ed., Elsevier, London, UK. 4. Pringle, C.M., Blake, G.A., Covich, A.P., Buzby, K.M., Finley, A., 1993. Effects of omnivorous shrimp in a montane tropical stream sediment removal, disturbance of sessile invertebrates and enhancement of understory algal biomass. Oecologia 93, 1C11. 5. Pringle, C.M., 1996. Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of algal communities over different scales in tropical montane streams, Puerto Rico. Freshw. Biol. 35, 125C140. 6. Pringle, C.M., Hemphill, N., McDowell, W.H., Bednarek, A., March, J.G., 1999. Linking species and ecosystems: different biotic assemblages cause interstream differences in organic matter. Ecology 80, 1860C1872. 7. Sket, B. 1996. The ecology of anchialine caves. Trends in Ecology and Evolution 11:221-225. 8. Iliffe, T. M. 2004. Anchialine caves, biodiversity in. Pp. 24-30 in Encyclopedia of Caves, D.C. Culver and W.B. White, eds., Elsevier, Burlington, MA. 9. Brock, R. E., J. E. Norris, D. A. Ziemann, and M. T. Lee. 1987. Characteristics of water quality in anchialine ponds of the Kona, Hawaii, coast. Pacific Science 41:200-208. 10. Carey, C.C., M.P. Ching, S.M. Collins, A.M. Early, W.M. Fetzer, D. Chai, and N.G. Hairston, Jr. 2011. Predator-dependent diel migration by Halocaridina rubra shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools. Aquatic Ecology 45: 35-41. 11. Bailey-Brock, J. H. and R. E. Brock. 1993. Feeding, reproduction, and sense organs of the Hawaiian anchialine shrimp Halocaridina rubra (Atyidea). Pacific Science 47:338-355. 12. Maciolek, J. A. 1983. Distribution and biology of Indo-Pacific insular hypogeal shrimps. Bulletin of Marine Science 33:606-618. 13. Havird, J. C., J. R. Weeks, S. Hau, and S. R. Santos. In review. Invasive species alter endemic species distributions via direct predation and behavioral modification in the Hawaiian anchialine ecosystem. Hydrobiologia. 14. Capps, K.A., C.B. Turner, M.T. Booth, D.L. Lombardozzi, S.H. McArt, D. Chai, and M.G. Hariston Jr. 2009. Behavioral responses of the endemic shrimp Halocaridina rubra (Malacostraca: Atyidae) to an introduced fish, Gambusia affinis (Actinopterygii: Poeciliidae) and implications for the trophic structure of Hawaiian anchialine ponds. Pacific Science 63:27C37. 15. Sakihara, T. S., 2012. A diel comparison of the unique faunal assemblage in remote anchialine pools on Hawaii Island. Pacific Science 66: 83C96. 16. Eberhardt, L. L. and J. M. Thomas. 1991. Designing environmental field studies. Ecological Monographs 61: 53-73. 17. Edmondson, W. T. 1993. Experiments and quasi-experiments in limnology. Bulletin of Marine Science 53:65-83. 18. Kimball, K. D. and S. A. Levin. 1985. Limitations of laboratory bioassays - the need for ecosystem-level testing. Bioscience 35:165-171. 19. Schmitz, O. J. 2005. Scaling from plot experiments to landscapes: studying grasshoppers to inform forest ecosystem management. Oecologia 145:225- 234. 20. Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, et al. (2010) Microbiome Profiling by Illumina Sequencing of Combinatorial Sequence-Tagged PCR Products. PLoS ONE 5(10): e15406. doi:10.1371/journal.pone.0015406 21. Metzker, M. L. 2010. Sequencing technologies C the next generation. Nature Reviews Genetics 11:31-46. 22. Dalton, C. M., A. Mokiao-Lee, T. S. Sakihara, M. G. Weber, C. A. Roco, Z. Han, B. Dudley, R. A. MacKenzie & N. G. Hairston Jr., 2012. Density- and trait-mediated topCdown effects modify bottomCup control of a highly endemic tropical aquatic food web. Oikos doi: 10.1111/j.1600-0706.2012.20696.x