Invasive Species

Invasive Species Factsheet. Click image to expand.

There are about 67 non-native species on the GLANSIS watchlist that pose a threat to the Great Lakes. Some of them, like the invasive carps, have been identified as potential invasive species. Invasive carps include four species, bighead carp, silver carp, grass carp, and black carp. Although they all bear the name carp, grass carp feed on aquatic plants, black carp eat mussels and snails, and bighead and silver carp feed on plankton in the water column. Bighead and silver carp are highly abundant in the Illinois River and have been captured 47 miles away from Lake Michigan. They threaten to invade the Great Lakes and disrupt aquatic food webs and fisheries through their voracious consumption of large volumes of plankton. In river and other lake ecosystems throughout North America, Asia, and Europe, invasive carps have caused a decline in many of the native fish species.

CIGLR has helped produce models for Lakes Huron, Erie, Michigan, and Ontario (in development). The model for Lake Erie shows if invasive carps were to invade, they would dominate the fish community and seriously devalue the vital recreational and commercial fisheries present there. Lake Michigan is colder and has less plankton than the environments where they currently exist. But, accounting for diet flexibility and subsurface habitat in the model, the research team demonstrated that nearly all of Lake Michigan contains suitable habitat for bigheaded carp. Habitats with greatest potential to support bigheaded carp were located near river mouths and in Green Bay, which agrees with previous studies. However, their research also demonstrates that Lake Michigan’s offshore areas are suitable for bigheaded carp. Although offshore areas offer a relatively low-quality habitat, making them less appealing for resident populations, they may provide migration corridors through which bigheaded carp could spread to more food-rich areas in the lake. Lake Michigan’s vulnerability to these fishes will likely continue to increase as climate change progresses or if nutrient pollution increases, despite a competitive feeding pressure from dreissenid mussels on the plankton communities.

Invasive carp impacts are likely driven by lake productivity and fish community structure, thus potentially impacting each of the Great Lakes differently. In our most recent study, we developed a Lake Ontario EwE model and initiated a collaboration network with scientists at USGS Great Lakes Center, Cornell University, Department of Fisheries and Oceans Canada, Ministry of Natural Resources and Forestry (Canada), SUNY Buffalo State College, NYSDEC, and Toronto and Region Conservation Authority. The Ecopath with Ecosim (EwE) food web model to quantify the potential impacts of invasive carp to the Lake Ontario and lower Illinois River food web and fisheries. Preliminary results for bigheaded carp impacts on the Lake Ontario food web showed bigheaded biomass could reach 4.6 tonne/km2, or 34% of the total fish biomass at the end of simulation.

We plan to continue developing similar ecosystem models to assess the invasive carp threat in the other Great Lakes and their embayments. Since the Great Lakes each have unique characteristics, the potential growth, survival, and impacts of invasive carps are expected to be different from those predicted for Lake Erie, Lake Michigan, and Lake Ontario. This information is urgently needed to support informed management decisions regarding invasive carp control and to identify the resident species at risk for impacts by a silver and bighead carp invasion. CIGLR is also using these models to predict ecological impacts on the Great Lakes food webs by other invasive species from the watchlist, such as killer shrimp and golden mussels.

Click image to read and watch 13 ABC’s interview with NOAA GLERL and CIGLR about how mussels “spit out’ toxic microcystin and play a part in Lake Erie algae.

Invasive mussels in Lake Erie may be contributing to the lake’s harmful algal bloom (HAB) problem, according to scientists from Central Michigan University, University of Michigan, CIGLR, and the National Oceanic and Atmospheric Administration (NOAA) Great Lakes Environmental Research Laboratory (GLERL). After three decades of water quality improvements in Lake Erie, the recent proliferation of HABs has motivated research teams to better understand the role that zebra and quagga mussels play in the lake. Results from a recent series of laboratory experiments suggest that the plankton in Lake Erie provide invasive mussels with enough food that they can reject the not-so-appetizing and less nutritious HAB species Microcystis. This research team completed 10 trials of two-week laboratory experiments to measure mussel grazing on intact plankton assemblages from Lake Erie. In all 10 experiments, mussels fed heavily on small algae, diatoms, and larger protists, while Microcystis and some colonial green algae were left uneaten. The implication of this selectivity is that conventional approaches to measuring phytoplankton biomass and community composition are inadequate for studying the impacts of mussels on the lower food web. Instead, future studies will need to leverage ‘omics approaches to quantify the impacts of these invaders. This result is critical for the management of HABs in the Great Lakes because it shows that nutrient availability is not the only factor that leads to success of Microcystis.

The Cooperative Institute for Great Lakes Research (CIGLR) in partnership with NOAA-GLERL has been working to develop genomic tools that will advance conservation biology and biodiversity management. For successful management of bio-invasions and monitoring the reintroduction of threatened or endangered species in the Great Lakes or elsewhere, managers and stakeholders need timely and robust scientific advice.

Dr. Nate Marshall sampling eDNA and eRNA from a mesocosm experiment. Click image to learn more. Photo Credit: Aubrey Lashaway.

The Laurentian Great Lakes are one of the most rapidly changing ecosystems in the world in large part due to more than 185 species invasions over the past two centuries. The Lakes are swiftly undergoing changes in temperature, hypoxia, and invasive species representations, whose effects are especially acute in warmer productive areas that are important to fisheries, e.g., western Lake Erie and Saginaw Bay in Lake Huron. Arguably the most radical change has been and continues to be mediated by invasive Dreissenid mussels (Dreissena polymorpha (zebra mussel) and D. bugensis (quagga mussel)). Dreissenids radically change community structure and the flow of energy and matter in most systems they invade. In offshore regions, they starve the pelagic food web by sharply reducing phytoplankton biomass, causing zooplankton and fish population declines and dietary shifts from phytoplankton to littoral benthic algae. In contrast, in nearshore regions invasive Dreissenid mussels promote nuisance benthic algal growth and harmful cyanobacterial blooms by selective removal of non-cyanobacterial phytoplankton. For Microcystis, which often dominates harmful algal blooms in the Great Lakes, observations indicate that a trade-off between adaptation to nutrient levels and grazing resistance may exist. Nutrient levels, in particular nitrogen levels and N:P ratios, also influence toxin levels produced by Microcystis-dominated blooms, adding additional complexity to the regulation of key Microcystis traits that affect its ecosystem-levels impacts. 

Traditionally, scientists have relied on conventional approaches such as visual surveys to try and determine the dynamic responses of entire lake biological communities to ongoing physical and chemical changes in key regions of the Great Lakes. However, low rates of species detection can increase the cost and labor required for this approach. During the last decade, eDNA has become a powerful tool used to collect information from aquatic habitats. eDNA methodology is cost-effective and easier to collect compared to traditional sampling, and has improved the management and assessment of a species’ distribution. eDNA analysis has been incorporated into Great Lakes monitoring programs for detection of a wide-range of organisms, including species that are endangered/threatened, invasive, or economically important.

The team has developed a new methodology that uses environmental DNA and RNA (eDNA and eRNA) to accurately detect and distinguish the presence of living organisms and improve estimators of their relative abundances. eDNA and eRNA refer to genetic material naturally released from an organism into the environment, through feces/urine, mucus, gametes, skin/tissue, carcasses, and so on. It can be collected from the environment (such as lake water), rather than directly from an organism, and analyzed to identify the species present. Because the concentration of eRNA degrades much faster than the eDNA, it provides a predictor for estimating time since genomic material was released from an organism into the environment, thus improving spatiotemporal estimates of community composition. This new method is easily modified and can be applied to monitoring different species within the Great Lakes or elsewhere in the world. The researchers will apply this method to examine how Dreissenid mussels alter the composition of cyanobacterial communities, and more specifically the composition of Microcystis populations. It is a powerful technique that will enhance the confidence of rapid decision-making by environmental managers and stakeholders and expand monitoring of ecosystem health.

GLANSIS Poster. Click image to expand.

The Great Lakes Aquatic Nonindigenous Species Information System (GLANSIS) is a searchable regional database with species-specific fact sheets, threat assessments, and maps designed to improve public education and inform prevention, management, and control of invasive and non-native species. The database is a collaboration between Michigan Sea Grant, NOAA, Michigan DNR Institute for Fisheries Research, USGS, EPA, and CIGLR. CIGLR has helped the partnership by maintaining current data, making updates when needed, as well as improving the database through technologies and products. This has involved programming enhancements for improved functionality, adding reports of non-native species in new locations, adding new species to the watchlist of likely invaders, moving species from the watchlist to the established category, and adding maps habitat suitability for non-native species. The Sea Grant Great Lakes Network works to ensure the most current state of knowledge regarding current and future threats is being delivered to the public and managers. Information served through GLANSIS helps managers make informed decisions when formulating and implementing strategies to prevent, control, and mitigate the introduction and impacts of invasive and non-native species.

• GLANSIS database and information (website): Great Lakes Aquatic Nonindigenous Species Information System (GLANSIS) is a searchable database with fact sheets, threat assessments, and maps designed to improve stakeholder education, and inform prevention, management, and control of aquatic nonindigenous species (ANS).
• Invasive Carp Assessment (website)
• GLANSIS (poster)
• GLANSIS Watchlist (poster)
• How Would and Asian Carp Invasion Affect Fish in Lake Erie? (Infographic)
• Invasive Mussels and the Productivity of Lake Michigan (Infographic)
• Invasive Species Research (bookmark)
• Mussel Research (bookmark)
• Dreissenid Mussel Crossword Puzzle (game)
• Great Lakes Food Web Information (trivia)
• Invasive Carp Information (trivia)

Factsheets

• • Invasive Species
  • Lake Erie Food Web
  • Lake Huron Food Web
  • Lake Michigan Food Web
  • Lake Ontario Food Web
  • Lake St. Clair Food Web
  • Lake Superior Food Web
  • Invasive Carp Studies at GLERL and CIGLR 

• Using Environmental DNA and RNA to Inform Biomonitoring and Bioassessment Management Plans, CIGLR 2019 Fall eNews, 12/2019
• Great Lakes Water Life Database Documents Biodiversity of Great Lakes Native Species, MSU Extension, 8/21/2019
• Large Lakes Worldwide Share Many of the Same Threats, Great Lakes Echo, 8/15/2019
• A Mussel Poop Diet Could Fuel Invasive Carp’s Spread Across Lake Michigan, Science News, 8/13/2019
• GLANSIS: A Database of Aquatic Invaders for Scientists and Citizens Alike, CIGLR 2018 Spring eNews, 06/2018
• GLANSIS: A ‘one-stop shop’ for information on aquatic invaders, Michigan State University Extension, 2/25/2018
• Alien language: Stages of invasion, Michigan State University Extension, 2/24/2019
• Alien language: Understanding terminology about nonindigenous species, Michigan State University Extension, 2/24/2019
• Quagga Mussels and Nutrients Linked to Lake Michigan Productivity Loss, CIGLR 2017 Fall eNews, 12/2017
• Invasive Hitchhikers: Catching a Ride on Lake Currents; CIGLR 2017 Spring eNews, 06/2017
• Modelling the Spread of Aquatic Invasive Species in Great Lakes; Water Canada, 5/29/2017
• Collaborative team identifies 16 high-risk Great Lakes invaders; NOAA Great Lakes Environmental Research Laboratory’s Blog, 12/2/2016

Asian Carp

• Warming Could Lower One Barrier to Invasive Fish Reaching Great Lakes, newsakmi, 7/9/2020
• Climate Change Would Limit Competition For Asian Carp If Introduced In Lake Michigan, Study Finds, Wisconsin Public Radio, 7/8/2020
• Warming Could Lower One Barrier to Invasive Fish Reaching Great Lakes, Scientific American, 7/8/2020
• U of M study: Climate change may aid Asian carp invasion of Great Lakes, Michigan Radio, 7/8/2020
• Climate warming increases Asian carp threat to Lake Michigan by offsetting quagga mussel ‘ecological, phys.org, 7/8/2020
• Climate warming increases Asian carp threat to Lake Michigan by offsetting quagga mussel ‘ecological barrier’, Michigan News, 7/7/2020
• Global warming could help Asian carp invade Lake Michigan, Earth.com, 7/7/2020
• Modeling Lake Michigan’s Suitability for Asian Carp, CIGLR 2020 Summer eNews, 09/2020
• Bigheaded carp pose big threat, new model suggests, Great Lakes Echo, 6/5/2020
• NOAA researchers model risk of Asian carp invasion in Lake Huron, NOAA Research News, 4/30/2020
• Big Fish Story: Asian carp are poised to enter Lake Michigan, but to what extent is a matter of debate. Rackham alumnus Peter Alsip’s research sheds light on the watery invaders’ potential whereabouts, Discover Rackham, 1/22/2020
• Asian Carp Capable of Surviving in Much Larger Areas of Lake Michigan Than Previously Thought, University of Michigan Faculty News, 11/22/2019
• Favorite Food Not on the Menu? No Problem for Asian Carp – They Eat Almost Anything, Great Lakes Echo, 8/21/2019
• Lake Michigan’s ‘Plankton Desert’ No Problem for Bighead Carp, Peninsula Pulse, 8/16/2019
• Study: Asian Carp Could Thrive in Lake Michigan, Despite Earlier Doubts, Bridge, 8/12/2019
• U-M study: Asian Carp Capable of Surviving in Much Larger Areas of Lake Michigan than Previously Thought, Michigan News, 8/12/2019
• Study: Asian Carp Could Expand Across Greater Area of Lake Michigan than Previously Thought, Michigan Radio, 8/12/2019
• Asian Carp have Never Breached a Body of Freshwater the Size of Lake Michigan. Here’s the Bizarre Way They Could Survive and Thrive in the World’s Fifth Largest Lake, Chicago Tribune, 8/12/2019
• U-M: Asian Carp Would have Sufficient Food Supply in Lake Michigan, Holland Sentinel, 8/12/2019
• Asian Carp Could be a lot Worse to the Great Lakes than Previously Thought, UofM Study Shows, Fox 2 Detroit, 8/12/2019
• New Study Finds Asian Carp Could Survive Throughout Lake Michigan, Wisconsin Public Radio, 8/12/2019
• Are the Great Lakes Next? Video Shows Hundreds of Asian Carp Shocked in Kentucky Lake, Fox 2 Detroit, 8/1/2019
• Can Asian Carp Survive in Lake Michigan?, CIGLR 2019 Spring eNews, 06/2019
• Asian carp would damage fish species in Lake Erie; Capital News Service, 2/5/2016
• Ecological casualties: winners and losers in the war on carp; Great Lakes Echo, 1/28/2016
• All-you-can-eat Asian carp are gluten free; The Times Herald, 1/28/2016
• Forecasting Future of Asian Carp In Great Lakes: An Erie Story; Medill News Service, 1/13/2016
• Asian Carp Would Significantly Alter – But Not Destroy – Lake Erie Fisheries; WaterNews, 1/7/2016
•  Impact of Asian carp on Great Lakes could be overestimated; The Michigan Daily, 1/7/2016
• Report: Asian carp could become dominant Lake Erie fish; Sandusky Register, 1/6/2016
• ASIAN CARP COULD CLAIM ONE-THIRD OF LAKE ERIE BIOMASS; Newsweek, 1/6/2016
• Lake Erie Asian carp: How great a threat to Great Lakes?; Christian Science Monitor, 1/5/2016
• Invasive Asian carp could overtake Lake Erie, study finds; Washington Post, 1/5/2016
• Asian Carp Could Dominate Lake Erie, Study Says; The Weather Channel, 1/5/2016
• Researchers Forecast Impact Of Invasive Asian Carp On Lake Erie’s Native Fish Species; Tech Times, 1/5/2016
• Invasive Asian carp could overtake Lake Erie, study finds; Chicago Tribune, 1/5/2016
• LOCAL Report sounds alarm of Asian carp threat; Toledo Blade, 1/5/2016
• Asian carp could cause some Lake Erie fish to decline, others to increase; Michigan News, 1/4/2016
• Study: Asian carp could develop huge presence in Lake Erie; The Seattle Times, 1/4/2016
• Asian carp would dominate Lake Erie biomass, study finds; Milwaukee Journal Sentinel, 1/4/2016
• Study: Walleye, trout will be hardest hit by Asian carp; Detroit News, 1/4/2016
• Asian Carp Invasion Of Lake Erie Would Probably Have Little Impact On Fish Biomass; Headline and Global News, 8/9/2014
• Experts doubt Asian carp invasion would harm Lake Erie fishery; Milwaukee-Wisconsin Journal Sentinel, 8/8/2014
• Study Shows Asian Carp Could Establish in Lake Erie with Little Effect to Fishery; Science Newsline Nature and Earth, 8/7/2014

Alsip, P.J., H. Zhang, M.D. Rowe, D.M. Mason, E.S. Rutherford, C.M. Riseng and Z. Su. 2019. Lake Michigan’s Suitability for Bigheaded Carp: The Importance of Diet Flexibility and Subsurface Habitat. Freshwater Biology. (DOI:10.1111/fwb.13382). [Altmetric Score]

Alsip, P.J., H. Zhang, M.D. Rowe, E. Rutherford, D.M. Mason, C. Riseng and Z. Su. 2020. Modeling the interactive effects of nutrient loads, meteorology, and invasive mussels on suitable habitat for Bighead and Silver Carp in Lake Michigan. Biological Invasions. (DOI:10.1007/s10530-020-02296-4). [Altmetric Score]

Beletsky D. , R. Beletsky, E.S. Rutherford , J.L. Sieracki, J.M. Bossenbroek, W.L. Chadderton, M.E. Wittmann, G. Annis and D. Lodge. 2017. Spread of aquatic invasive species by lake currents. Journal of Great Lakes Research. 43:14-32. (DOI:10.1016/j.jglr.2017.02.001). [Altmetric Score]

Cooke, R.M., M.E. Wittmann, D.M. Lodge, J.D. Rothlisberger, E.S. Rutherfod, H. Zhang and D.M. Mason. 2014. Out-of-sample validation for structured expert judgment of Asian Carp establishment in Lake Erie. Integrated Environmental Assessment and Management. 10(4):522-528. (DOI:10.1002/ieam.1559). 

Davidson, A.D., A.J. Fusaro, R.A. Sturtevant, E.S. Rutherford and D.R. Kashian. 2017. Development of a risk assessment framework to predict invasive species establishment for multiple taxonomic groups and vectors of introduction. Management of Biological Invasions. 8:25-36. (DOI:10.3391/mbi.2017.8.1.03). 

Denef, V.J., H.J. Carrick, J.F. Cavaletto, E. Chiang, T.H. Johengen and H.A. Vanderploeg. 2017. Lake Bacterial Assemblage Composition Is Sensitive to Biological Disturbance Caused by an Invasive Filter Feeder. American Society for Microbiology: mSphere. 2(3). (DOI:10.1128/mSphere.00189-17). [Altmetric Score]

Fusaro, A.J., E. Baker, W. Conrad, A. Davidson, K. Dettloff, J. Li, G. Núñez-Mir, R.A. Sturtevant and E.S. Rutherford. A risk assessment of potential Great Lakes aquatic invaders. NOAA Technical Memorandum GLERL-169. 

Kao, Y-C., S. Adlerstein and E.S. Rutherford. 2016. Assessment of bottom-up and top-down controls on the collapse of alewives Alosa pseudoharengus in Lake Huron. Ecosystems. 19:803-831. (DOI:10.1007/s10021-016-9969-y). [Altmetric Score]

Lodge, D.M., P.W. Simonin, S.W. Burgiel, R.P. Keller, J.M. Bossenbroek, C.L. Jerde, A.M. Kramer, E.S. Rutherford, M.A. Barnes, M.E. Wittmann, W.L. Chadderton, J.L. Apriesnig, D. Beletsky, R.M. Cooke, J.M. Drake, S.P. Egan, D.C. Finnoff, C.A. Gantz, E.K. Grey, M.H. Hoff, J.G. Howeth, R.A. Jensen, E.R. Larson, N.E. Mandrak, D.M. Mason, F.A. Martinez, T.J. Newcomb, J.D. Rothlisberger, A.J. Tucker, T.W. Warziniack and H. Zhang. 2016. Risk analysis and bioeconomics of invasive species to inform policy and management. Annual Review of Environment and Resources. 41:453-88. (DOI:10.1146/annurev-environ-110615-085532). [Altmetric Score]

Marshall, Nathaniel T., Henry A. Vanderploeg & Subba Rao Chaganti. 2021. Environmental (e)RNA advances the reliability of eDNA by predicting its age. Scientific Reports. 11:2769. (DOI: 10.1038/s41598-021-82205-4). [Altmetric Score]

Nalepa, T.F. 2014. Relative comparison and perspective on invasive species in the Laurentian and Swedish Great Lakes. Aquatic Ecosystem Health and Management. 17(4):394-403. (DOI:10.1080/14634988.2014.972494). 

Reisinger, L.S., A.K. Elgin, K.M. Towle, D.J. Chan and D.M. Lodge. 2017. The influence of evolution and plasticity on the behavior of an invasive crayfish. Biological Invasions. 19(3):815-830. (DOI:10.1007/s10530-016-1346-4). [Altmetric Score]

Rowe, M.D., E.J. Anderson, H.A. Vanderploeg, S.A. Pothoven, A.K. Elgin, J. Wang and F. Yousef. 2017. Influence of invasive quagga mussels, phosphorus loads, and climate on spatial and temporal patterns of productivity in Lake Michigan: A biophysical modeling study. Limnology and Oceanography. (DOI:10.1002/lno.10595). [Altmetric Score]

Smith, J.P., E.K. Lower, F.A. Martinez, C.M. Riseng, L.A. Mason, E.S. Rutherford, M. Neilson, P. Fuller, K.E. Wehrly and R.A. Sturtevant. 2019. Interactive mapping of nonindigenous species in the Laurentian Great Lakes. Management of Biological Invasions. 10(1):192-199. (DOI:10.3391/mbi.2019.10.1.12).

Sturtevant, R.A., L. Berent, T. Makled, A.J. Fusaro and E.S. Rutherford. 2016. An overview of the management of established nonindigenous species in the Great Lakes. NOAA Technical Memorandum GLERL-168. 

Sturtevant, R.A., J. Larson, L. Berent, M. McCarthy, A. Bogdanoff, A.J. Fusaro and E.S. Rutherford. 2014. An Impact Assessment of Great Lakes Aquatic Nonindigenous Species. NOAA Technical Memorandum GLERL-161.

Sturtevant, R., D.M. Mason, E.S. Rutherford, A. Elgin, E. Lower and F. Martinez. 2019. Recent history of nonindigenous species in the Laurentian Great Lakes; An update to Mills et al., 1993 (25 years later). Journal of Great Lakes Research.  (DOI:10.1016/j.jglr.2019.09.002). [Altmetric Score]

Tucker, A.J, W.L. Chadderton, C.L. Jerde, M.A. Renshaw, K. Uy, C. Gantz, A.R. Mahon, A. Bowen, T. Strakosh, J.M. Bossenbroek, J.L. Sieracki, D. Beletsky, J. Bergner and D.M. Lodge. 2016. A sensitive environmental DNA (eDNA) assay leads to new insights on Ruffe (Gymnocephalus cernua) spread in North America. Biological Invasions. 18:3205-3222. (DOI:10.1007/s10530-016-1209-z). [Altmetric Score]

Wang, L., C.M. Riseng, L.A. Mason, K.E. Wehrly, E.S. Rutherford, J.E. McKenna, Jr., C. Castiglione, L.B. Johnson, D. Infante, S.E. Sowa, M. Robertson, J. Schaeffer, M. Khoury, J. Gaiot, T. Hollenhorst, C. Brooks and M. Coscarelli. 2015. A spatial classification and database for management, research, and policy making: The Great Lakes aquatic habitat framework. Journal of Great Lakes Research. 41:584-596. (DOI:10.1016/j.jglr.2015.03.017). [Altmetric Score]

Wittman, M.E., G. Annis, A.M. Kramer, L. Mason, C. Riseng, E. S. Rutherford, W. L. Chadderton, D. Beletsky, J.M. Drake and D.M. Lodge. 2016. Refining species distribution model outputs using landscape scale habitat data: Forecasting Grass Carp and Hydrilla verticillata establishment in the Great Lakes Region. Journal of Great Lakes Research. 43:298-307. (DOI:10.1016/j.jglr.2016.09.008). [Altmetric Score]

Wittmann, M., R. Cooke, J. Rothlisberger, E.S. Rutherford, H. Zhang, D.M. Mason and D. Lodge. 2014. Use of structured expert judgment to forecast invasions by Bighead and Silver carp in Lake Erie. Conservation Biology. 29(1):187-197. (DOI:10.1111/cobi.12369). [Altmetric Score]

Zhang, H., E. Rutherford, D.M. Mason, J. Breck, R. Cooke, M. Wittmann, T. Johnson, X. Zhu and D. Lodge. 2016. Forecasting the Impacts of Silver and Bighead Carp on the Lake Erie Food Web. Transactions of the American Fisheries Society. 145(1):136-162. (DOI:10.1080/00028487.2015.1069211). [Altmetric Score]