Fish Diet Shifts Associated with the Northern Gulf of Mexico Hypoxic Zone
The occurrence of low dissolved oxygen (hypoxia) in coastal waters may alter trophic interactions within the water column. This study identified a threshold at which hypoxia in the northern Gulf of Mexico (NGOMEX) alters composition of fish catch and diet composition (stomach contents) of fishes using fish trawl data from summers 2006–2008. Hypoxia in the NGOMEX impacted fish catch per unit effort (CPUE) and diet below dissolved oxygen thresholds of 1.15 mg L−1 (for fish CPUE) and 1.71 mg L−1 (for diet). CPUE of many fish species was lower at hypoxic sites (≤ 1.15 mg L −1) as compared to normoxic regions (> 1.15 mg L −1), including the key recreational or commercial fish species Atlantic croaker Micropogonias undulatus and red snapper Lutjanus campechanus. Overall, fish diets from hypoxic sites (≤ 1.71 mg L−1) and normoxic sites (> 1.71 mg L−1) differed. Fish caught in normoxic regions consumed a greater mass of benthic prey (ex. gastropods, polychaetes) than fish caught in hypoxic regions. Hypoxia may increase predation risk of small zooplankton, with observations of increased mass of small zooplankton in fish stomachs when bottom hypoxia was present. Changes in contributions of small zooplankton and benthic prey to fish diet in hypoxic areas may alter energy flow in the NGOMEX pelagic food web and should be considered in fishery management.
KeywordsFish diet Dissolved oxygen Predation Fishery
We thank James Roberts, Craig Stow, Stephen Lozano, Jennifer Metes, Aly Peacy, and Katharine Bush for help with collecting the field data. We also thank the captains and crew of the RV Pelican for their help with field sampling.
This research was supported by NOAA-CSCOR Award NA06NOS4780148 and NA09NOS4780198 and National Academies award NAS-GRP-2000006418. This is NOAA GLERL contribution No. 1931 and UMCES contribution No. 5713.
- Anderson, M.J. 2005. PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. https://doi.org/10.1002/9781118445112.stat07841.
- Anderson, M. J. 2014. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. https://doi.org/10.1002/9781118445112.stat07841, .
- Ara, Koichi. 2001. Length-weight relationships and chemical content of the planktonic copepods in the Cananeia Lagoon estuarine system, Sao Paulo, Brazil. Plankton Biology and Ecology 48: 121–127.Google Scholar
- Arend, Kristin K., Dmitry Beletsky, Joseph DePinto, Stuart A. Ludsin, James J. Roberts, Daniel K. Rucinski, Donald Scavia, David J. Schwab, and Thomas O. Höök. 2011. Seasonal and interannual effects of hypoxia on fish habitat quality in Central Lake Erie. Freshwater Biology 56 (2): 366–383. https://doi.org/10.1111/j.1365-2427.2010.02504.x.CrossRefGoogle Scholar
- Benedetti-Cecchi, Lisandro, and Giacomo Chato Osio. 2007. Replication and mitigation of effects of confounding variables in environmental impact assessment: Effect of marinas on rocky-shore assemblages. Marine Ecology Progress Series 334: 21–35. https://doi.org/10.3354/meps334021.CrossRefGoogle Scholar
- Bethea, Dana M., Loraine Hale, John K. Carlson, Enric Cortés, Charles A. Manire, and James Gelsleichter. 2007. Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Marine Biology 152 (5): 1009–1020. https://doi.org/10.1007/s00227-007-0728-7.CrossRefGoogle Scholar
- Bianchi, Thomas S., Steven F. DiMarco, James H. Cowan, Robert D. Hetland, Piers Chapman, John W. Day, and Mead A. Allison. 2010. The science of hypoxia in the northern Gulf of Mexico: A review. Science of the Total Environment 408 (7): 1471–1484. https://doi.org/10.1016/j.scitotenv.2009.11.047.CrossRefGoogle Scholar
- Brandt, Stephen B., Marco Costantini, Sarah Kolesar, Stuart A. Ludsin, Doran M. Mason, Christopher M. Rae, and Hongyan Zhang. 2011. Does hypoxia reduce habitat quality for Lake Erie walleye (Sander vitreus)? A bioenergetics perspective. Canadian Journal of Fisheries and Aquatic Sciences 68 (5): 857–879. https://doi.org/10.1139/f2011-018.CrossRefGoogle Scholar
- Breitburg, Denise L., Aaron T. Adamack, Kenneth A. Rose, Sarah E. Kolesar, Beth Decker, Jennifer E. Purcell, Julie E. Keister, and James H. Cowan. 2003. The pattern and influence of low dissolved oxygen in the Patuxent River, a seasonally hypoxic estuary. Estuaries 26 (2): 280–297.CrossRefGoogle Scholar
- Breitburg, Denise L., J. Kevin Craig, Richard S. Fulford, Kenneth A. Rose, Walter R. Boynton, Damian C. Brady, Benjamin J. Ciotti, et al. 2009. Nutrient enrichment and fisheries exploitation: Interactive effects on estuarine living resources and their management. Hydrobiologia 629 (1): 31–47. https://doi.org/10.1007/s10750-009-9762-4.CrossRefGoogle Scholar
- Costantini, Marco, Stuart A. Ludsin, Doran M. Mason, Xinsheng Zhang, William C. Boicourt, and Stephen B. Brandt. 2008. Effect of hypoxia on habitat quality of striped bass (Morone saxatilis) in Chesapeake Bay. Canadian Journal of Fisheries and Aquatic Sciences 65 (5): 989–1002. https://doi.org/10.1139/f08-021.CrossRefGoogle Scholar
- de Mutsert, Kim, Jeroen Steenbeek, Kristy Lewis, Joe Buszowski, James H. Cowan, and Villy Christensen. 2016. Exploring effects of hypoxia on fish and fisheries in the northern Gulf of Mexico using a dynamic spatially explicit ecosystem model. Ecological Modelling 331: 142–150. https://doi.org/10.1016/j.ecolmodel.2015.10.013.CrossRefGoogle Scholar
- Glaspie, Cassandra N., Melissa A. Clouse, Stuart A. Ludsin, Doran M. Mason, Michael R. Roman, Craig A. Stow, and Stephen B. Brandt. 2018. Effect of hypoxia on diet of Atlantic Bumpers in the Northern Gulf of Mexico. Transactions of the American Fisheries Society 147 (4): 740–748. https://doi.org/10.1002/tafs.10063.CrossRefGoogle Scholar
- Hartigan, John A., and Melissa A. Wong. 1979. A k-means clustering algorithm. Applied Statistics 28: 100–108.Google Scholar
- Hughes, Brent B., Matthew D. Levey, Monique C. Fountain, Aaron B. Carlisle, Francisco P. Chavez, and Mary G. Gleason. 2015. Climate mediates hypoxic stress on fish diversity and nursery function at the land–sea interface. Proceedings of the National Academy of Sciences 112 (26): 8025–8030. https://doi.org/10.1073/pnas.1505815112.CrossRefGoogle Scholar
- Karnauskas, Mandy, Christopher R. Kelble, Seann Regan, Charline Quenée, Rebecca Allee, Michael Jepson, Amy Freitag, et al. 2017. 2017 Ecosystem Status Report Update for the Gulf of Mexico.Google Scholar
- Kimmel, David G., William C. Boicourt, James J. Pierson, Michael R. Roman, and Xinsheng Zhang. 2009. A comparison of the mesozooplankton response to hypoxia in Chesapeake Bay and the northern Gulf of Mexico using the biomass size spectrum. Journal of Experimental Marine Biology and Ecology 381. Elsevier B.V.: S65–S73. https://doi.org/10.1016/j.jembe.2009.07.012.
- Kimmel, David G., William C. Boicourt, James J. Pierson, Michael R. Roman, and Xinsheng Zhang. 2010. The vertical distribution and diel variability of mesozooplankton biomass, abundance and size in response to hypoxia in the northern Gulf of Mexico USA. Journal of Plankton Research 32 (8): 1185–1202.CrossRefGoogle Scholar
- Langseth, Brian J., Kevin M. Purcell, J. Kevin Craig, Amy M. Schueller, Joseph W. Smith, Kyle W. Shertzer, Sean Creekmore, Kenneth A. Rose, and Katja Fennel. 2014. Effect of changes in dissolved oxygen concentrations on the spatial dynamics of the Gulf menhaden fishery in the Northern Gulf of Mexico. Marine and Coastal Fisheries 6 (1): 223–234. https://doi.org/10.1080/19425120.2014.949017.CrossRefGoogle Scholar
- Ludsin, Stuart A., Xinsheng Zhang, Stephen B. Brandt, Michael R. Roman, William C. Boicourt, Doran M. Mason, and Marco Costantini. 2009. Hypoxia-avoidance by planktivorous fish in Chesapeake Bay: Implications for food web interactions and fish recruitment. Journal of Experimental Marine Biology and Ecology 381: 121–131. https://doi.org/10.1016/j.jembe.2009.07.016.CrossRefGoogle Scholar
- Manooch, C.S., and W.T. Hogarth. 1983. Stomach contents and giant trematodes from wahoo, Acanthocybium solanderi, collected along the South Atlantic and Gulf coasts of the United States. Bulletin of Marine Science 33: 227–238.Google Scholar
- NMFS. 2017a. Fisheries Economics of the United States 2015. NOAA Technical Memorandum: 247. https://doi.org/10.1017/CBO9781107415324.004.
- NMFS. 2018. Fisheries of the United States. https://doi.org/10.2307/j.ctv157bc5.9.
- R Core Team. 2019. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
- Rabalais, Nancy N., and R. Eugene Turner. 2001. Hypoxia in the northern Gulf of Mexico: Description, causes and change. In Coastal Hypoxia: Consequences for Living Resources and Ecosystems, ed. Nancy N. Rabalais and R. Eugene Turner. Washington D. C.: American Geophysical Union.CrossRefGoogle Scholar
- Rabotyagov, Sergey S., Todd D. Campbell, Michael White, Jeffrey G. Arnold, Atwood Jay, M. Lee Norfleet, Catherine L. Kling, et al. 2014. Cost-effective targeting of conservation investments to reduce the northern Gulf of Mexico hypoxic zone. Proceedings of the National Academy of Sciences 111 (52): 18530–18535. https://doi.org/10.1073/pnas.1405837111.CrossRefGoogle Scholar
- Remsen, Andrew, Thomas L. Hopkins, and Scott Samson. 2004. What you see is not what you catch: A comparison of concurrently collected net, Optical Plankton Counter, and Shadowed Image Particle Profiling Evaluation Recorder data from the northeast Gulf of Mexico. Deep Sea Research Part I: Oceanographic Research Papers 51 (1): 129–151.CrossRefGoogle Scholar
- Roberts, James J., Tomas O. Höök, Stuart A. Ludsin, Steven A. Pothoven, Henry A. Vanderploeg, and Stephen B. Brandt. 2009. Effects of hypolimnetic hypoxia on foraging and distributions of Lake Erie yellow perch. Journal of Experimental Marine Biology and Ecology 381: S132–S142. https://doi.org/10.1016/j.jembe.2009.07.017.CrossRefGoogle Scholar
- Rose, Kenneth A., Sean B. Creekmore, Dubravko Justić, Thomas Peter, J. Kevin Craig, Rachel Miller Neilan, Lixia Wang, Md S. Rahman, and David Kidwell. 2018. Modeling the population effects of hypoxia on Atlantic croaker (Micropogonias undulatus) in the Northwestern Gulf of Mexico. Estuaries and Coasts 41 (1): 233–254. https://doi.org/10.1007/s12237-017-0266-6.CrossRefGoogle Scholar
- Sutton, Tracy T., and Thomas L. Hopkins. 1996. Trophic ecology of the stomiid (Pisces: Stomiidae) fish assemblage of the eastern Gulf of Mexico: Strategies, selectivity and impact of a top mesopelagic predator group. Marine Biology 127 (2): 179–192. https://doi.org/10.1007/BF00942102.CrossRefGoogle Scholar
- Thomas, Peter, and Md. Saydur Rahman. 2012. Extensive reproductive disruption, ovarian masculinization and aromatase suppression in Atlantic croaker in the northern Gulf of Mexico hypoxic zone. Proceedings of the Royal Society B: Biological Sciences 279 (1726): 28–38. https://doi.org/10.1098/rspb.2011.0529.CrossRefGoogle Scholar
- Thronson, Amanda, and Antonietta Quigg. 2008. Fifty-five years of fish kills in Coastal Texas. Estuaries and Coasts 31 (4): 802–813. https://doi.org/10.1007/sl2237-008-9056-5.
- Vanderploeg, Henry A., Stuart A. Ludsin, Joann F. Cavaletto, Tomas O. Höök, Steven A. Pothoven, Stephen B. Brandt, James R. Liebig, and Gregory A. Lang. 2009a. Hypoxic zones as habitat for zooplankton in Lake Erie: Refuges from predation or exclusion zones? Journal of Experimental Marine Biology and Ecology 381: S108–S120. https://doi.org/10.1016/j.jembe.2009.07.015.CrossRefGoogle Scholar
- Vanderploeg, Henry A., Stuart A. Ludsin, Steven A. Ruberg, Tomas O. Höök, Steven A. Pothoven, Stephen B. Brandt, Gregory A. Lang, James R. Liebig, and Joann F. Cavaletto. 2009b. Hypoxia affects spatial distributions and overlap of pelagic fish, zooplankton, and phytoplankton in Lake Erie. Journal of Experimental Marine Biology and Ecology 381: S92–S107. https://doi.org/10.1016/j.jembe.2009.07.027.CrossRefGoogle Scholar
- Zhang, Hongyan, Stuart A. Ludsin, Doran M. Mason, Aaron T. Adamack, Stephen B. Brandt, Xinsheng Zhang, David G. Kimmel, Michael R. Roman, and William C. Boicourt. 2009. Hypoxia-driven changes in the behavior and spatial distribution of pelagic fish and mesozooplankton in the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 381: S80–S91. https://doi.org/10.1016/j.jembe.2009.07.014.CrossRefGoogle Scholar
- Zhang, Hongyan, Doran M. Mason, Craig A. Stow, Aaron T. Adamack, Stephen B. Brandt, Xinsheng Zhang, David G. Kimmel, Michael R. Roman, William C. Boicourt, and Stuart A. Ludsin. 2014. Effects of hypoxia on habitat quality of pelagic planktivorous fishes in the northern gulf of Mexico. Marine Ecology Progress Series 505: 209–226. https://doi.org/10.3354/meps10768.CrossRefGoogle Scholar