By Lynette Williams Duman, Elsie Platzer, and John Durand
An invaded estuary
There is widespread concern about the effect of introduced species on native species. The San Francisco Estuary (SFE) is a highly invaded system (Cohen and Carlton 1995), with a mix of native and introduced species that didn’t evolve together. Humans introduced non-native species in a variety of ways, ranging from recreation to ship ballast water to aquarium and pond releases (Hanak et al. 2013). Non-native species within the estuary are often treated as a monolithic problem to be solved through eradication (Grossman 2016). However, not all non-native species disrupt an ecosystem. Many introduced fishes do not have clear negative impacts on populations of native species, and some may provide benefits to humanity in the form of recreation opportunities, ecosystem services, or as indicator species (Moyle et al. 1986, Bork 2018, Grossman 2016). In this blog, we’ll review the complex roles of non-native fishes within our novel estuary and propose a systematic framework evaluating the “invasiveness” of these introduced species.
In the SFE, the primary drivers of ecosystem disruption are almost certainly broad ecosystem-scale changes, including historic sediment dumping from placer mining, alteration of flows by damming, hydrologic manipulations, loss of seasonal wetlands, and water diversions for agriculture (Cloern and Jassby 2012). Such powerful physical drivers in turn facilitated the invasion success of non-native invertebrate and plant species that decreased habitat quality for native fishes and disrupted aquatic food webs. These so-called “ecosystem engineers” are distinct from other introduced species in that they are aggressive invaders that develop a widespread distribution and change fundamental physical ecosystem properties. For example, water weeds overshade and compete for nutrients with phytoplankton. Overbite clams have become highly abundant in the system and caused a dramatic decline in phytoplankton abundances and degradation of pelagic habitats (Jassby 2008, Baumsteiger et al 2017, Sommer et al 2007).
While these plant and invertebrate ecosystem engineers exert clear negative impacts on the SFE, there is still debate surrounding whether other introduced species do the same, in part because we don’t fully understand how natives and non-natives interact within the novel ecology of the estuary. Many new arrivals to the SFE seem to have integrated well, without outsized effects on food web dynamics or habitat structure: for example, the introduced gobies (family Gobiidae) prevalent in Suisun Marsh (Matern et al 2002). Yet some are more controversial. Largemouth bass (Micropterus salmoides) and striped bass (Morone saxitilis) are two examples of fishes non-native to the SFE which have been targeted by eradication campaigns, primarily because they prey on endangered salmon (Onchorhynchus tshawytscha).
While largemouth bass may periodically eat large numbers of salmon, and striped bass are a piscivorous species (Grossman 2016), there is little evidence that these fishes have population-level effects on natives. Predation is an important part of ecological and evolutionary processes in most ecosystems, including the SFE (Moyle and Bennett 2011). Predators regulate boom-bust cycles of prey, create food-web stability by maintaining complex trophic dynamics, prevent over-exploitation of certain resources, and, somewhat counter-intuitively, regulate their own populations through cannibalism of juveniles. Additionally, the estuary’s native low-salinity piscivore, thicktail chub (Gila crassicauda), has been extinct since 1957 (Miller et al. 1989) so it’s possible that introduced bass species are merely filling that empty niche. More research on this subject could help us parse how much of continued salmon declines are simply due to the extreme remaking of the estuary’s flow and habitat regimes, versus how current populations are impacted by bass predation.
One important reason conservationists should strive to understand how introduced species affect the broader ecosystem before assuming negative impacts is that control or eradication attempts are often expensive—and their results unreliable. With sustained effort, eradication can be successful: for example, Northern pike (Esox lucidus), a somewhat aggressive piscivore, was removed from Lake Davis in the Sierra Nevada foothills after two major efforts that involved using a fish toxin on the whole lake over the span of a decade (CDFW 2024). On the other hand, a four-year attempt to eradicate striped bass from the State Water Project intake pond at Clifton Court had limited success on reducing the population there (DWR 2024, Golden State Salmon Association 2023). An attempt to reduce invasive green crabs from Bodega Harbor had the opposite effect from what was intended: the population of crabs increased without the large adults to cannibalize juveniles (Grosholz et al. 2021). If eradication is a costly business with mixed outcomes, managers must be pragmatic about which species to target.
To address the nuances of invasive species management in the SFE, we offer a framework for ranking non-native species based on a set of criteria that would help streamline management decisions and assess how to effectively target and prioritize control measures, rather than approaching all non-natives as a monolith. Researchers have expressed a need to delineate between non-natives which have the potential to irreparably alter a system and those which may integrate into a new community with limited disruption (Williamson & Fitter 1996, Shackelford et al. 2013). To analyze non-natives in the SFE on a stratified, comparable, case-by-case basis, this framework aims to:
- Outline the ecological role that introduced species have in the system;
- Support control methods for the most damaging introduced species only where they pose a real and preventable threat to valued species and ecosystem services;
- Evaluate habitat restoration outcomes in terms of benefits for native species rather than the control or reduction of invasive species; and
- Reconsider the way that some non-natives are viewed within the ecosystem, acknowledging that some may provide beneficial services.
The framework
To explore such an approach, consider a simple ranking of species on a scale from 0-5 on each of the following categories. The numbers can be totaled to produce an overall management index of invasiveness, in which higher ranking species would be considered more potentially harmful, and lower ranking species more benign. All categories would be weighted equally in this assessment.
1. Recreation Opportunities – Is this species valuable for anglers and fisheries? Striped bass, for example, are recreationally important, beloved by local communities, and motivate public investment in the well-being of the estuary (Stompe 2020). (0= highly valued, 5=not valued)
2. Habitat Quality Indicators – Is this species an indicator of habitat quality for native species? Planktivorous and pelagic non-native fish, such as threadfin shad, can indicate habitat quality for native planktivorous, pelagic fish, such as Delta smelt. (0=excellent indicator, 5=poor indicator)
3. Direct Impacts on Native Species – Does this species exert observable harm on native species through predation or competition? For example, bluegill (Lepomis macrochirus) compete directly with Sacramento perch (Archoplites interruptus), a native but extirpated sunfish, in controlled laboratory settings (Marchetti 1999). It is key to consider that negative effects towards natives should not be assumed simply due to a species being non-native to the system. (0=no negative interactions, 5=major predation or competition with natives).
4. Feasibility of Control – Is it possible to eradicate or meaningfully reduce this species from an economic perspective? Many species are so widespread and established that no meaningful control is possible (0=population self regulates or is highly isolated making eradication feasible, 5=population is increasing in density and expanding its range, making eradication nearly impossible).
5. Ecosystem Transformation Capacity – Does this species have the ability to modify, create, or destroy particular habitats? The overbite clam, for instance, has caused an overall alteration of the pelagic food web within the estuary (Baumsteiger et al. 2017). (0=coexists without fundamentally altering habitat, 5=creates major shifts in ecosystem function).
Example:
| Striped Bass | Threadfin Shad | Bluegill Sunfish | Largemouth Bass | Mississippi Silversides | Overbite Clam | |
| Recreation | 0 | 4 | 1 | 0 | 5 | 5 |
| Indicator Species | 2 | 0 | 5 | 5 | 4 | 5 |
| Competition or Predation | 3 | 2 | 2 | 4 | 3 | 5 |
| Control | 2 | 2 | 3 | 4 | 5 | 5 |
| Ecosystem Engineer | 1 | 0 | 2 | 3 | 1 | 5 |
| Totals | 8 | 8 | 13 | 16 | 18 | 25 |
Example breakdown: Mississippi silverside (Menidia audens)
Recreation: Besides their occasional use as baitfish, Mississippi silversides have little recreational value. 5
Indicator species: Native to the southeastern United States, silversides prefer warm and turbid conditions (Mahardja et al. 2016) but are dietary generalists and somewhat resilient to swings in salinity (Howe et al. 2014, Moyle 2023). Their presence in a given habitat may suggest poor suitability for cool-water species, but a strong association has not been identified. 4
Competition or predation: One study has identified silversides as a potential larval predator of Delta smelt (Baerwald et al. 2012), but more research is needed. Still, we can assume silversides exert some negative impact, at least through competition, on small native fishes. 3
Control: Mississippi silversides are currently the most abundantly caught fish in many regions of the upper SFE (O’Rear et al. 2022). They may number in the millions. Attempts at eradication would likely be fruitless. 5
Ecosystem engineering capacity: Very little is known about silverside impacts on surrounding physical habitat. Likely, the fish itself only benefits from an already altered ecosystem state. 1
Total: 18/25
Mississippi Silverside Conclusion: Mississippi silversides, despite being ubiquitous across the estuary, are relatively understudied. Current research and trends suggest that rather than engineering a system to suit their habitat requirements, they simply benefit from an already altered environment. Timely and extensive diet studies to assess impacts on larval fish would be beneficial. They are numerous, expanding, and benefit from continued warming due to climate change. Eradication will likely be impossible for this species, and recreational value is low, but they may be a key indicator of poor ecosystem health. The results suggest a need for more research to better understand their life history strategies within the SFE, followed by specific studies on whether they are directly impacting native species or whether they are using habitat otherwise unsuitable for native species.
Conclusion
The SFE is a novel and highly unique system that now hosts species from all around the world due to human introduction. Time, money, and effort could be conserved by reframing how managers, ecologists, and policymakers view these non-natives. Non-native species are here to stay in the SFE. Targeted habitat enhancement should be adopted to mitigate the effects of the highest impact species that degrade habitat value and food resources, rather than focused on attempts to eliminate economically valuable, ecologically informative, and culturally important fish species. This framework seeks to fill a knowledge gap in vertebrate invasion ecology, and proposes a standardized method to quantify non-native impacts, in order to create more streamlined and scientifically informed management plans.
Lynette Williams Duman and Elsie Platzer are graduate students at the Center for Watershed Sciences. John Durand is a senior researcher specializing in estuarine ecology and restoration at the Center for Watershed Sciences.
Further Reading
Aguilar-Medrano, R., Durand, J. R., Cruz-Escalona, V. H., & Moyle, P. B. (2019). Fish functional groups in the San Francisco Estuary: Understanding new fish assemblages in a highly altered estuarine ecosystem. Estuarine, Coastal and Shelf Science, 227, 106331.
Baerwald, M. R., Schreier, B. M., Schumer, G., & May, B. (2012). Detection of threatened Delta Smelt in the gut contents of the invasive Mississippi Silverside in the San Francisco Estuary using TaqMan assays. Transactions of the American Fisheries Society, 141(6), 1600-1607
Baumsteiger, J., Schroeter, R. E., O’Rear, T., Cook, J. D., & Moyle, P. B. (2017). Long-term surveys show invasive overbite clams (Potamocorbula amurensis) are spatially limited in Suisun Marsh, California. San Francisco Estuary and Watershed Science, 15(2).
Bork, K. (2018). What about the non-native species we like? May 28. https://californiawaterblog.com/2018/05/28/guest-species-what-about-the-nonnative-species-we-like/
California Department of Fish and Wildlife. (2024). California’s Invaders: Northern Pike. https://wildlife.ca.gov/Conservation/Invasives/Species/Northern-Pike#:~:text=An%20unsuccessful%20eradication%20effort%20occurred,eradicated%20from%20California%20in%202007.
California Department of Water Resources. (2024). Clifton Court Forebay Predation Alternatives – Fish Relocation Study. https://water.ca.gov/Programs/Integrated-Science-and-Engineering/Fisheries-Infrastructure-and-Operations-Program/Clifton-Court-Forebay-Predatory-Fish-Relocation-Study
Cloern, J. E., & Jassby, A. D. (2012). Drivers of change in estuarine‐coastal ecosystems: Discoveries from four decades of study in San Francisco Bay. Reviews of Geophysics, 50(4).
Cohen, A. N., & Carlton, J. T. (1995). Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta.
Grosholz, E., Ashton, G., Bradley, M., Brown, C., Ceballos-Osuna, L., Chang, A., … & Tepolt, C. (2021). Stage-specific overcompensation, the hydra effect, and the failure to eradicate an invasive predator. Proceedings of the National Academy of Sciences, 118(12), e2003955118.
Grossman, G. D. (2016). Predation on fishes in the Sacramento–San Joaquin Delta: current knowledge and future directions. San Francisco Estuary and Watershed Science, 14(2).
Golden State Salmon Association. (2023). Reduce Predator Habitat at Clifton Court Forebay. https://goldenstatesalmon.org/reduce-predator-habitat/
Hanak, E., Lund, J., Durand, J., Fleenor, W., Gray, B., Medellín-Azuara, J., Mount, J., Moyle, P. and Phillips, C. (2013). Stress Relief: Prescriptions for a Healthier Delta Ecosystem.
Hobbs, R. J., Higgs, E., & Harris, J. A. (2009). Novel ecosystems: implications for conservation and restoration. Trends in ecology & evolution, 24(11), 599-605.
Howe, E. R., Simenstad, C. A., Toft, J. D., Cordell, J. R., & Bollens, S. M. (2014). Macroinvertebrate prey availability and fish diet selectivity in relation to environmental variables in natural and restoring north San Francisco bay tidal marsh channels. San Francisco Estuary and Watershed Science, 12(1).
Jassby, A. (2008). Phytoplankton in the upper San Francisco Estuary: recent biomass trends, their causes, and their trophic significance. San Francisco Estuary and Watershed Science, 6(1).
Moyle, P. B. (1986). Fish introductions into North America: patterns and ecological impact. In Ecology of biological invasions of North America and Hawaii (pp. 27-43). New York, NY: Springer New York.
Sommer, T., Armor, C., Baxter, R., Breuer, R., Brown, L., Chotkowski, M., … & Souza, K. (2007). The collapse of pelagic fishes in the upper San Francisco Estuary: El colapso de los peces pelagicos en la cabecera del Estuario San Francisco. Fisheries, 32(6), 270-277.
Mahardja, B., Conrad, J. L., Lusher, L., & Schreier, B. (2016). Abundance trends, distribution, and habitat associations of the invasive Mississippi Silverside (Menidia audens) in the Sacramento–San Joaquin Delta, California, USA. San Francisco Estuary and Watershed Science, 14(1).
Marchetti, M. P. (1999). An experimental study of competition between the native Sacramento perch (Archoplites interruptus) and introduced bluegill (Lepomis macrochirus). Biological invasions, 1, 55-65.
Matern, S. A., Moyle, P. B., & Pierce, L. C. (2002). Native and alien fishes in a California estuarine marsh: twenty-one years of changing assemblages. Transactions of the American Fisheries Society, 131(5), 797-816.
Miller, R. R., Williams, J. D., & Williams, J. E. (1989). Extinctions of North American fishes during the past century. Fisheries, 14(6), 22-38.
Moyle, P.B. (2023). The Rapid Invasion of Mississippi Silverside in California. California Waterblog. March 19. https://californiawaterblog.com/2023/03/19/the-rapid-invasion-of-mississippi-silverside-in-california/
Moyle, P.B. and Bennett, W.A. (2011). Striped bass control: cure worse than disease? California WaterBlog, January 31. https://californiawaterblog.com/2011/01/31/striped-bass-control-the-cure-worse-than-the-disease/
O’Rear, T., Durand, J.R., Moyle, P.B. (2018). Killing Native Fishes for Fun and Predator Control. California Waterblog. August 5. https://californiawaterblog.com/2018/08/05/killing-native-fishes-for-fun-and-predator-control/
O’Rear, T. A., Moyle, P.B., Durand, J. R. (2022). Trends in fish and invertebrate populations of Suisun Marsh January 2021-December 2021.
Shackelford, N., Hobbs, R. J., Heller, N. E., Hallett, L. M., & Seastedt, T. R. (2013). Finding a middle-ground: the native/non-native debate. Biological conservation, 158, 55-62.
Stompe, D. (2020). Striped Bass in the Pacific Ocean: When, where and why? California Waterblog. April 12. https://californiawaterblog.com/2020/04/12/striped-bass-in-the-pacific-ocean-when-where-and-why/
Williamson, M., & Fitter, A. (1996). The varying success of invaders. Ecology, 77(6), 1661-1666.
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