Climate change and invasive species can both have negative impacts on native species diversity. Additionally, climate change has the potential to favor invasive species over natives, dealing a double blow to native biodiversity. It is, therefore, vital to determine how changing climate conditions are directly linked to demographic rates and population growth of non-native species so we can quantitatively evaluate how invasive populations may be affected by changing conditions and, in turn, impact native species. Cordylophora caspia, a hydrozoan from the Ponto-Caspian region, has become established in the brackish water habitats of the San Francisco Estuary (SFE). We conducted laboratory experiments to study how temperature and salinity affect C. caspia population growth rates, in order to predict possible responses to climate change. C. Caspia population growth increased nonlinearly with temperature and leveled off at a maximum growth rate near the annual maximum temperature predicted under a conservative climate change scenario. Increasing salinity, however, did not influence growth rates. Our results indicate that C. caspia populations in the SFE will benefit from predicted regional warming trends and be little affected by changes in salinity. The population of C. caspia in the SFE has the potential to thrive under future climate conditions and may subsequently increase its negative impact on the food web.
Citation: Meek MH, Wintzer AP, Wetzel WC, May B (2012) Climate Change Likely to Facilitate the Invasion of the Non-Native Hydroid, Cordylophora caspia, in the San Francisco Estuary. PLoS ONE 7(10): e46373. https://doi.org/10.1371/journal.pone.0046373
Editor: Kimberly Patraw Van Niel, University of Western Australia, Australia
Received: February 20, 2012; Accepted: September 2, 2012; Published: October 11, 2012
Copyright: © Meek et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was supported by funding from CALFED Science Program Grant 1036 (P.I.s: B May and PB Moyle), NOAA Dr. Nancy Foster Scholarship (to MHM), UC Davis Biological Invasions IGERT NSF-DGE#0114432 (to APW), UC Davis Jastro-Shields Research Scholarship (to MHM and APW), UC Davis Block Grant (to APW), and the Giles W. and Elise G. Mead Foundation (to BPM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Climate change and biological invasions have both reduced native species diversity , . Additionally, climate change has the potential to favor invasive species over natives, dealing a double blow to native species . It is important to understand interactions between invasive species and climate change to better predict how the two forces work together to disrupt native communities. It is, thus, vital to determine how changing climate is directly linked to demographic rates and population growth of non-native species so we can quantitatively evaluate how a species may be affected , . Climate factors can play an important role in invasions if they work to increase reproductive output. For example, increases in temperature can increase rates of dispersal and development, leading to faster spread and higher abundances . Additionally, climate change can create opportunities for non-natives to move into areas that were previously uninhabitable , .
One major obstacle to predicting the future abundance of invasive species under climate change is determining the relationship between growth rates and the environmental variables predicted to change , . Schwenk et al.  noted the need for work on the basic understanding of the link between organisms, environmental conditions, and their population growth parameters as one of the top five challenges in organismal biology. The influence of climate change on a species' population size will depend on the shape of the relationship between population growth rate and climate variables over the range of present and future values for those variables. Over the full theoretical range of any important environmental variable, such as temperature, population growth rates will reach a maximum at optimal environmental values and drop to zero at extreme low and high values. In order to predict the effects of climate change on populations, it is necessary to determine where on the growth curve the population currently is and how its position may shift with change in variables such as temperature. What the shape of the relationship is, where a population currently is on the curve, and how this position will shift under climate change, will play a large role in determining if the population will persist in the future, increase in abundance, or decrease and go locally extinct. Researchers can use these relationships to predict how species' abundances and distributions may change with climate change .
In this study, we experimentally determined the shape of the relationship between population growth rate and climate variables predicted to change for Cordylophora caspia (Pallas 1771), an important, yet understudied non-native hydroid found worldwide , . C. caspia is presumed native to the Ponto-Caspia region (Pallas 1771), but has invaded freshwater and brackish habitats globally, including the Baltic Sea , throughout Europe –,the east coast of the United States , the Great Lakes , and the west coast of the United States, including the Puget Sound and the San Francisco Bay , , , . This distribution is particularly expanding within the United States . In systems it invades, C. caspia can have serious negative economic impacts ,  including biofouling of power plant pipes ,  and drinking water treatment plants . Additionally, it is a voracious predator, feeding largely on zooplankton, and has the potential to negatively impact the food webs it invades , , .
Hydroids may drastically alter food web processes if they become abundant in areas where they are not native members of the trophic community. They can play strong roles as predators, with some estimates placing their ingestion rates among the highest of suspension feeding organisms . The importance of hydroids in the transfer of energy from pelagic to benthic systems is often overlooked due to their relatively small size and low abundance; however hydroid species composing less than 0.5% of the benthic community biomass have been estimated to capture approximately 10% of the annual algal production . Colonies of Eudendrium racemosum, another colonial hydroid, must consume prey equivalent to 7.2% of their own biomass daily to meet their metabolic requirements .
C. caspia is an abundant non-native species in the SFE and is found in brackish water habitats, such as Suisun Marsh. It has density estimates in some areas of Suisun Marsh up to 626,000 hydranths/m2 (Wintzer, AP, unpublished data). Suisun Marsh provides valuable rearing and spawning habitat for many important planktivorous fishes , . Populations of some of these fishes have been experiencing drastic declines in recent years . It is thought that competition with non-natives may be one of the causes for the observed declines –.
Despite its potential importance, relatively little is known about the ecology of C. caspia. Even less is known about how the abundance and distribution of C. caspia will change under future climate change. Climate change scenarios predict an increase of 2–6 C in mean annual air temperature across California , , an increase in variability in salinity regimes in the SFE , and more frequent extreme climatic events . The scenarios for the region predict varied outcomes, with some native species likely to decline due to raising temperatures and others to benefit from increased variability in hydrologic regimes . It is unknown how the changes will impact non-natives in the SFE, though studies elsewhere show climate change is likely to benefit many invasives .
We investigated the relationship between temperature and salinity and C. caspia growth rates through a controlled laboratory experiment using field-collected individuals to better predict how the invasive population of C. caspia in the SFE may respond to changes in climate conditions. This approach is simple, yields conclusive results, and can be applied to any invasive species that is amenable to lab or greenhouse culture, such as plants and invertebrates with short generation times. Over a large range of temperatures, biologically we know the shape of the curve describing the relationship between growth rate and temperature/salinity should peak at the optimum and decrease at extreme conditions. We, however, were interested in investigating the relationship over the range of naturally occurring conditions and those predicted under a conservative climate change scenario (+2 C). The following hypotheses represent different possible relationships between growth rate and temperature/salinity over the current and predicted range:
Hypothesis 1: Growth rate is constant across the current and predicted range of temperature and salinity.
Hypothesis 2: Growth rate increases linearly with increasing temperature and/or salinity.
Hypothesis 3: Growth rate increases initially with increasing temperature and/or salinity and levels off at high temperatures, salinities, or both.
Hypothesis 4: Growth rate is unimodal, with maximal growth at intermediate temperature/salinity, and decreasing growth at the two extremes.
Through this work, we gain an understanding of the link between climate factors and the population growth rate of an important non-native species.
All necessary permits were obtained for the described field collections (California Department of Fish and Game Scientific Collecting permit # SC-008862).
Cordylophora caspia was likely introduced into the SFE system by ballast water exchange or ship hulls as early as the 1920s , . It established populations in the brackish water habitats of the SFE, with the highest densities in Suisun Marsh. Suisun Marsh is a brackish water system covering approximately 34,000 ha in the upper San Francisco Estuary. One-third of the area is a system of tidally influenced sloughs, with margins of tules (Schoenoplectus spp.) and other brackish-water marsh plants, while the rest is a combination of diked seasonal pools and upland grasslands .
On June 12, 2008, we collected C. caspia polyps from Suisun Marsh via settling plate arrays (100 cm2 sheet PVC plates, roughed with an orbital sander on both sides and hung below the water surface to allow C. caspia settlement), maintained them in 6.5 ppt salinity water in an aerated tank, and fed them with an overabundance of 48 hour old Self-Emulsifying Lipid Concentrate (SELCO) enriched Artemia nauplii. On July 27, 2008, we put 3 polyps each into 57 new petri dishes, containing 6.5 ppt water held at 20 C, by gently plucking them off the settling plates with forceps and placing them in the petri dish. We allowed polyps 3 days to settle in the petri dish, providing them with Artemia nauplii every other day. After settlement, we recorded the number of successfully settled polyps per petri dish. In six of the petri dishes, no polyps successfully settled, so these were not used. In four dishes, there were no feeding hydranths remaining, but there was live, intact stolon settled in the dish. We used these in the experiment and counted this as one settled polyp. The resulting sample size per temperature treatment was 18, 16, and 17 for 15, 20 and 25 C respectively, and 17, 18, 16 samples for 2, 6.5, and 11 ppt salinity treatments. We then randomly placed each of the 51 petri dishes containing polyps at the bottom of one of 36 5-gallon tanks holding 6.5 ppt water at 20 C, 1–2 petri dishes per 5-gallon tank. All 5-gallon tanks were randomly placed inside 1 of 6 large water baths to maintain the desired experimental temperature, each water bath holding 6 5-gallon tanks. There were two water baths per temperature treatment. Salinity treatments were achieved by adding Liquid Ocean to fresh water to obtain salinities of 2, 6.5 and 11 ppt. Each of the six 5-gallon tanks were randomly assigned to one of the salinity treatments, with two tanks per salinity treatment per water bath. Each tank was aerated with an aquarium aeration system. These treatment conditions were chosen to represent the range of conditions found in Suisun Marsh during the summer C. caspia growing season, with the upper bracket representing the temperature increase expected under a conservative climate change scenario .
On July 31, 2008 we began to adjust the salinities to reach the desired level. To avoid salinity shock, we altered the salinities by only 1 ppt every 4–12 hours. Once the polyps had a chance to acclimate to their new salinities, we began the temperature adjustment. We achieved the desired temperatures by slowly dropping or rising by 1 C every 1–3 hours over 24 hours. We fed the polyps to satiation every day on 48 hour old Selco enriched Artemia nauplii and executed 1/3 water changes of the tanks every other day to decrease fouling. We ran the experiment for 14 days and then, on August 13, 2008, we removed all the dishes from their experimental tanks and recorded the number of live hydranths (a feeding individual) in each dish using a dissecting microscope. All new hydranths observed in the experiment occurred through asexual propagation.
Data were log-transformed and analyzed using a mixed model ANOVA to determine the effects of temperature and salinity on polyp colony growth. Due to the variation around the number of polyps that settled for the growth experiment (between 1–2 polyps successfully settled per petri dish) we used the proportional increase in polyps (final number of polyps/initial number of polyps) per dish as the dependent variable in the ANOVA analysis.
We used a model comparison approach to test our hypotheses about the affect of temperature and salinity on intrinsic growth rate, which describes the population's potential for instantaneous increase with unlimited resources. The shape of the relationship between the environmental condition of interest and growth rate is very important for predicting how an invasive species' population will persist or grow in the future. If the relationship is non-linear over the range of temperatures expected, then normal fluctuations in temperature may lead to non-intuitive effects on growth rates. The general phenomenon that the mean of a non-linear function of a variable is not the same as the function of the variable's mean, , where x is a random variable and f is a non-linear function, is known as Jensen's inequality. This rule is important for evaluating the relationship between abiotic factors and biotic processes , . In particular, an increase in an environmental condition, such as temperature, can lead to a larger than expected increase in growth rate if researchers fail to take Jensen's inequality into account.
To investigate the relationship between temperature/salinity and growth rate, we built a deterministic model corresponding to each hypothesis mentioned in the introduction. All the models used an exponential growth equation, , where Nd is the number of hydranths at time d, N0 is the initial number of hydranths, and d is the time in days. We represent the different hypotheses for the relationship between temperature and salinity and intrinsic growth rate in r(p). For hypothesis 1 (constant growth rate), r was a constant. For hypothesis 2 (linear increase), we modeled linear relationships between temperature and growth rate, between growth rate and salinity, between temperature, salinity, and growth rate, and the interaction between temperature and salinity. For hypothesis 3 (increasing growth rate but decreasing slope), we used the Michaelis-Menten function: . In this parameterization, p is the condition tested (temperature or salinity) and a and b are estimated parameters. Since it is unlikely that growth rate goes to zero at exactly 0 C or 0 ppt, we also incorporated an additional parameter, c, to allow the growth rate to go to 0 at larger than 0 C or ppt. To represent hypothesis 4 (decrease in growth rate at the upper and lower end of temperature/salinity), we used a quadratic exponential (hump shaped) curve: , again p is the condition tested and a and b are estimated parameters. This is a Gaussian curve without the normalizing term. Table 1 outlines the model parameterizations. We chose the Michaelis-Menten and the quadratic exponential curves as phenomenological representations for the pattern of interest. These models allowed us to distinguish between the different relationships that would arise from the different hypotheses. We used the estimated intrinsic growth rates (r) to estimate population doubling time at different temperatures and salinities:.
We fit these models to the data using maximum likelihood estimation assuming a negative binomial distribution of offspring because we started with small population sizes (1–2 polyps per dish) and thus expected demographic stochasticity to be important. Additionally, the negative binomial distribution allows for individual heterogeneity and the variance in the number of polyps produced at the end of the experiment was more than ten times its mean, indicating our data were over-dispersed. We compared the predictive ability of the fitted models using Akaike's Information Criterion (AIC).
We found a significant effect of temperature on growth of the polyp colonies (p = 0.0007), but no effect of salinity (p = 0.51) with the ANOVA analysis. The average growth rates at the increasing temperature levels were 0.26, 2.42, and 4.15 hydranths per polyp per day (standard error ±0.74, 0.47, 0.83 respectively). The maximum number of hydranths grown per polyp per day was 12.21 in the 25 C treatment.
We found the Michaelis-Menten model (Hypothesis 3) with temperature best explained the variation in colony growth rates (4.7 AIC units better than the next best model). The resulting maximum likelihood estimates for the parameters in this model are: a = 0.30 (95% confidence interval: 0.22, 0.70), b = 1.21 (0.37, 18.77), c = 14.38 (11.48, 14.71). The model with a positive linear relationship between growth and temperature was the next best in modeling the growth rate. The parameter estimates with this model are a = −0.13 (95% confidence interval: −0.26, 0.02) and b = 0.02 (0.01, 0.02). Table 2 provides the intrinsic growth rates and doubling times for each temperature using the Michaelis-Menten and linear models. Figure 1 shows the top two models fitted to the data and Table 1 provides the AIC scores for all the models tested. Salinity had very poor predictive power so we present the non-linear results only incorporating temperature.
Solid line represents the predicted Michaelis-Menten relationship between temperature and growth rate. Dashed line shows the predicted linear relationship between temperature and growth rate. Shaded areas demonstrate the 5th and 95th percent confidence interval for the predicted relationships. Circles show the observed data points. Increased darkness of circle shading corresponds with the number of data points at that location. Circles falling below 0.00 on the y-axis represent polyps that died (i.e., negative growth).
Our results show that climate change may favor C. caspia in the SFE because it has the potential to rapidly propagate if temperatures increase. The current mean water temperature in the San Francisco Delta is 16 C and it is predicted to rise to 18–20 C by 2090 . Climate change scenarios also predict increases in temperature variability . The non-linearity we found in the relationship between growth rate and temperature signals that a relatively small increase in temperature experienced by C. caspia during its growing season could lead to a large increase in population growth during the growing season and in the length of the growing season. This could result in increased negative effects on the SFE system. The increase in growing season recently experienced by C. caspia in United Kingdom is thought to have lead to increased biofouling .
C. caspia is currently present in the brackish water habitats of the SFE system year round , . The sharp downward drop in C. caspia growth rate near 16 C (Fig. 1) has the effect of strongly reducing the length of growing season and growth rate during the growing season under current temperature ranges. Our model shows C. caspia experiences positive growth rates at temperatures above 14 C and the peak growth occurs at temperatures above 19 C. Presently, the average water temperature in Suisun Marsh is above 14 C for 9 months of the year and under the modest climate change scenario (+2 C), it will be above 14 C for 10 months , resulting in an additional month when C. caspia has positive growth rates. Water temperatures in Suisun Marsh are also predicted to be above 20 C for many more days than currently occurs . In Suisun Marsh, the average temperature is at the peak C. caspia growth temperature (above 19 C) from June through October . Under the modest climate warming model (an increase of 2 C), this peak growth period would increase to May through November. The overall effect of climate change, therefore, will be to allow C. caspia to have a longer growing season, higher growth rates for a greater portion of the year, and its mean growth rate will increase disproportionately relative to the increase in temperature.
The growth rate during the growing season likely dominates the annual growth rate as C. caspia has the ability to form a diapause stage, called menonts, which allows tissue to remain dormant inside stems and stolons when conditions are unfavorable . After favorable conditions resume, the menonts are able to regenerate more polyps and resume growth and reproduction. We know of no work that has investigated the survival rate of these menonts through the winter, though studies of methods for controlling C. caspia populations show the ability to form menonts makes eradication of C. caspia difficult , , .
We found, within the ranges tested, salinity did not affect colony growth rate. Suisun Marsh is predicted to experience increased variability in salinity with climate change . While this is likely to have a negative impact on some invasives, such as non-native clams, and may favor important fish species , our study shows that this is unlikely to have a negative impact on C. caspia populations. Other studies have also found C. caspia has a wide range of salinity and temperature tolerance limits, but the actual limits vary with the populations studied , , , , . It has also been shown that C. caspia has the ability to structurally remodel itself, from the cellular level up to colony formation, in response to changes in salinity in order to maintain metabolic function (reviewed in ). Our results add to this body of work by showing that while C. caspia is likely to benefit from a warmer climate, it is unlikely to be harmed by the predicted changes in salinity, making it quite likely that it will thrive under the new conditions.
There are other factors, both abiotic and biotic, that we have not investigated that may limit C. caspia abundance. This includes the availability of settling habitat. However, studies have shown that C. caspia is very adept at taking advantage of available settling habitat, including settling on live cyprinid fish , , . During the height of the C. caspia summer growing season, Wintzer et al.  estimated maximum recruitment to newly available settling habitat at 22,998 hydranths per day per m2 in some areas of Suisun Marsh. However, while C. caspia are very successful colonizers, they may be easily outcompeted for space after initial settlement , . In the SFE, C. caspia has to compete with other non-native fouling species, such as the Australian tubeworm (Ficopomatus enigmaticus), the common sea grape (Molgula manhattensis), the bay barnacle (Balanus improvises), and an unidentified bryozoan .
Food resources and predators may also limit population growth. C. caspia may be limited by zooplankton availability, as there has been a decreasing trend in biomass of some native zooplankton species, but this may be offset by an increasing trend in non-native zooplankton biomass . The non-native shimofuri (Tridentiger bifasciatus) and shokihaze (T. barbatus) gobies are known to be C. caspia predators in the SFE , , . Additionally, the aeolid nudibranch, Tenellia adspersa, which is also native to the Ponto-Caspian region, preys upon C. caspia and was found in large quantities on our settling plates in Suisun Marsh , . Our study shows warmer temperatures will likely result in increased growth rates of C. caspia, which may in turn promote growth rates of their non-native predators through increased prey availability. It will be important to investigate how these interactions may be altered by climate change and evaluate which non-natives may be favored or limited under future conditions.
Our method of experimentally studying the relationship between environmental factors and population growth rate provided valuable insights into the ecology of C. caspia and how it might be affected by climate change. Through our study, it is clear that the environmental factors predicted to change under climate change are likely to promote C. caspia population growth. The understanding that can be gained from experimental studies of demography such as this should not be overlooked.
The experimental approach we employ has the benefit of quantifying a piece of the puzzle that will determine non-native species' abundances and distributions under climate change: the relationship between population growth rate and climate variables , . Laboratory experiments such as this one should be employed more often to investigate the direct relationship between population growth rates and climate variables predicted to change under climate change. The results can then be incorporated in hybrid niche models, which combine a mechanistic understanding with phenomenological models, in order to gain a more complete picture of how non-native species' populations will be altered by climate change , , . An informative extension of this study will be to incorporate the mechanistic understanding gained with an environmental niche model to further predict how the invasive population of C. caspia may change in both extent and abundance.
Our experiments found that C. caspia growth rates increased non-linearly with temperature and were not influenced by salinity. This non-linear relationship predicts that a small increase in temperature can result in a large increase in growth rate by reducing the proportion of time C. caspia growth is limited by temperature. If C. caspia populations in the SFE increase in abundance with climate change, as suggested by our results, they may negatively influence the zooplankton community or become a biofouling nuisance, as they have in other systems. This impact may be detrimental to native planktivorous fish populations, which also depend on zooplankton as a food source. This study highlights the valuable insights that can be gained through direct experimental investigations of environmental conditions and population growth rates.
We would like to thank Dr. Peter Moyle, Dr. Mike Dawson, Dr. Nadine Folino-Rorem, Nicole Shepherd, Suisun City Marina, and the Suisun Resource Conservation District for their assistance during this project.
Conceived and designed the experiments: MHM APW BPM. Performed the experiments: MHM APW. Analyzed the data: MHM WCW. Contributed reagents/materials/analysis tools: BPM WCW. Wrote the paper: MHM WCW APW BPM.
- 1. Vitousek PM (1994) Beyond global warming: ecology and global change. Ecology 75: 1861–1876.
- 2. Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84: 468–478.
- 3. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14: 135–139.
- 4. Boyce MS, Haridas CV, Lee CT, the NSDWG (2006) Demography in an increasingly variable world. Trends Ecol Evol 21: 141–148.
- 5. Walther G, Roques A, Hulme P, Sykes M, Pysek P, et al. (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24: 686–693.
- 6. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. P Natl Acad Sci 99: 15497–15500.
- 7. Gallien L, Münkemüller T, Albert CH, Boulangeat I, Thuiller W (2010) Predicting potential distributions of invasive species: where to go from here? Divers Distrib 16: 331–342.
- 8. Morin X, Lechowicz MJ (2008) Contemporary perspectives on the niche that can improve models of species range shifts under climate change. Biol Lett 4: 573–576.
- 9. Schwenk K, Padilla DK, Bakken GS, Full RJ (2009) Grand challenges in organismal biology. Integr Comp Biol 49: 7–14.
- 10. Kearney M, Porter W (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges. Ecol Lett 12: 334–350.
- 11. Folino-Rorem NC, Darling JA, D'Ausilio CA (2009) Genetic analysis reveals multiple cryptic invasive species of the hydrozoan genus Cordylophora. Biol Invasions 11: 1869–1882.
- 12. Folino-Rorem NC (2000) The freshwater expansion and classification of the colonial hydroid Cordylophora (Phylum Cnidaria, Class Hydrozoa). In: Pederson J, editor. Marine bioinvasions: proceedings of the first national conference. Cambridge, MA: Massachusetts Institute of Technology Sea Grant College Program. pp. 139–144.
- 13. Leppäkoski E (2005) The first twenty years of invasion biology in the Baltic Sea area. Oceanol Hydrobiol Stud 34: 5–17.
- 14. Jensen KR, Knudsen J (2005) A summary of alien marine benthic invertebrates in Danish waters. Oceanol Hydrobiol Stud 34: 137–162.
- 15. Goulletquier P, Bachelet G, Sauriau PG, Noel P(2002) Open Atlantic coast of Europe—a century of introduced species into French waters. In: Leppäkoski E, Gollasch S, Olenin S, editors. Invasive aquatic species of Europe Distribution, impacts and management. Kluwer, The Netherlands. pp. 276–290.
- 16. Nehring S (2006) Four arguments why so many alien species settle into estuaries, with special reference to the German river Elbe. Helgoland Mar Res 60: 127–134.
- 17. Musko IB, Bence M, Balogh C (2008) Occurrence of a new Ponto-Caspian invasive species, Cordylophora caspia (Pallas, 1771) (Hydrozoa : Clavidae) in Lake Balaton (Hungary). Acta Zool Academ Sci Hung 54: 169–179.
- 18. Smith DG, Werle SF, Klekowski E (2002) The rapid colonization and emerging biology of Cordylophora caspia (Pallas, 1771) (Cnidaria : Clavidae) in the Connecticut River. J Freshw Ecol 17: 423–430.
- 19. Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: A history of biotic crises and anthropogenic introductions. J Great Lakes Res 19: 1–54.
- 20. Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Evol Syst 31: 481–531.
- 21. Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7: 369–392.
- 22. Mant RC, Moggridge G, Aldridge DC (2011) Biofouling by bryozoans, Cordylophora and sponges in UK water treatment works. Water Sci Technol 63: 1815–1822.
- 23. Gutierre S (2012) pH tolerance of the biofouling invasive hydrozoan, Cordylophora caspia. Hydrobiologia 679: 91–95.
- 24. Folino-Rorem NC, Indelicato J (2005) Controlling biofouling caused by the colonial hydroid Cordylophora caspia. Water Res 39: 2731–2737.
- 25. Berg MB, Folino-Rorem NC (2009) Alterations of Lake Michigan benthic communities by the invasive colonial hydroid, Cordylophora caspia: effects on fish prey. Final report to Illinois-Indian Sea Grant: 21 p.
- 26. Gili JM, Alva V, Coma R, Orejas C, Pagès F, et al. (1998) The impact of small benthic passive suspension-feeders in shallow marine ecosystems: the hydroids as an example. Zoologische verhandelingen 323: 99–105.
- 27. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13: 316–321.
- 28. Gili JM, Hughes RG (1995) The ecology of marine benthic hydroids. Oceanogr Mar Biol Annu Rev 33: 351–426.
- 29. Matern SA, Moyle PB, Pierce LC (2002) Native and alien fishes in a California estuarine marsh: twenty-one years of changing assemblages. T Am Fish Soc 131: 797–816.
- 30. Meng L, Matern SA (2001) Native and introduced larval fishes of Suisun Marsh, California: The effects of freshwater flow. T Am Fish Soc 130: 750–765.
- 31. Sommer T, Armor C, Baxter R, Breuer R, Brown L, et al. (2007) The collapse of pelagic fishes in the Upper San Francisco Estuary. Fisheries 32: 270–277.
- 32. IEP (2008) Interagency Ecological Program 2008 workplan to evaluate the decline of pelagic species in the Upper San Francisco Estuary. 125 p.
- 33. Schroeter RE (2008) Biology and long-term trends of alien hydromedusae and striped bass in a brackish tidal marsh in the San Francisco Estuary. Dissertation. University of California, Davis, CA. 223 p.
- 34. Loarie SR, Carter BE, Hayhoe K, McMahon S, Moe R, et al. (2008) Climate change and the future of California's endemic flora. PLoS ONE 3: 1–10 doi:10.1371/ journal.pone.0002502.
- 35. Brown RL (2004) Making science work for Suisun Marsh. Prepared for the San Francisco Bay-Delta Science Consortium: 125 p. Available: http://www.science.calwater.ca.gov/pdf/suisunmarsh_report_093004.pdf. Accessed 2012 Sept 26.
- 36. Moyle PB, Lund JR, Bennett WA, Fleenor WE (2010) Habitat variability and complexity in the upper San Francisco Estuary. San Francisco Estuary and Watershed Science 8: 1–23.
- 37. Cloern JE, Knowles N, Brown LR, Cayan D, Dettinger MD, et al. (2011) Projected Evolution of California's San Francisco Bay-Delta-River System in a Century of Climate Change. PLoS ONE 6: e24465.
- 38. Moyle PB, Quiñones RM, Kiernan JD (2012) Effects of climate change on the inland fishes of California, with emphasis on the San Francisco Estuary region. California Energy Commission California Climate Change Center CEC-500-2012-029: Available: http://uc-ciee.org/downloads/Effects of Climate Change on the Inland Fishes of California.pdf. Accessed 2012 Sept 26.
- 39. Wagner RW, Stacey M, Brown L, Dettinger M (2011) Statistical models of temperature in the Sacramento–San Joaquin Delta under climate-change scenarios and ecological implications. Estuaries and Coast doi:10.1007/s12237-12010-19369-z.
- 40. Ruel JJ, Ayres MP (1999) Jensen's inequality predicts effects of environmental variation. Trends Ecol Evol 14: 361–366.
- 41. Drake JM (2005) Population effects of increased climate variation. P Biol Sci 272: 1823–1827.
- 42. van Rheenen NT, Wood AW, Palmer RN, Lettenmaier DP (2004) Potential implications of PCM climate change scenarios for Sacramento-San Joaquin River basin hydrology and water resources. Climate Change 62: 257–281.
- 43. Wintzer AP, Meek MH, Moyle PB, May BP (2011) Ecological insights into the polyp stage of non-native hydrozoans in the San Francisco Estuary. Aquat Ecol 45: 151–161.
- 44. Matern SA, Brown LR (2005) Invaders eating invaders: exploitation of novel alien prey by the alien shimofuri goby in the San Francisco Estuary, California. Biol Invasions 7: 497–507.
- 45. O'Rear TA, Moyle PB (2009) Trends in fish populations of Suisun Marsh, January 2008–December 2008. Davis, CA: University of California. 54 p.
- 46. Roos PJ (1979) Two stage life-cycle of a Cordylophora population in the Netherlands. Hydrobiologia 62: 231–239.
- 47. Mant RC, Moggridge GD, Aldridge DC (2012) Control of biofouling by Cordylophora caspia in freshwater using one-off, pulsed and intermittent dosing of chlorine: laboratory evaluation. Biofouling 28: 433–440.
- 48. Kinne O (1958) Über die Reaktion erbgleichen Coelenteratengewebes auf verschiedene Salzgehalts-und Temperaturbedingungen. II Zoologische Jahrbucher (Physiologic) 67: 407–486.
- 49. Fulton C (1962) Environmental factors influencing growth of Cordylophora. J Expl Zool 151: 61–78.
- 50. Kinne O (1964) Non-genetic adaptation to temperature and salinity. Helgoland Mar Res 9: 433–457.
- 51. Boero F (1984) The ecology of marine hydroids and effects of environmental factors: a review. Mar Ecol 5: 93–118.
- 52. Winder M, Jassby A (2011) Shifts in zooplankton community structure: implications for food web processes in the Upper San Francisco Estuary. Estuaries and Coast 34: 675–690.
- 53. Moyle PB (2002) Inland fishes of California: University of California Press, Berkeley.
- 54. Slater SB (2005) Life history and diet of the shokihaze goby (Tridentiger barbatus) in the San Francisco Estuary. Thesis. California State University, Sacramento, CA.
- 55. Mills CE, Sommer F (1995) Invertebrate introductions in marine habitats: two species of hydromedusae (Cnidaria) native to the Black Sea, Maeotias inexspectata and Blackfordia virginica, invade San Francisco Bay. Mar Biol 122: 279–288.
- 56. Chester CM (1996) The effect of adult nutrition on the reproduction and development of the estuarine nudibranch, Tenellia adspersa (Nordmann, 1845). J Exp Mar Biol Ecol 198: 113–130.
- 57. Huntley B, Barnard P, Altwegg R, Chambers L, Coetzee BWT, et al. (2010) Beyond bioclimatic envelopes: dynamic species' range and abundance modelling in the context of climatic change. Ecography 33: 621–626.
- 58. Buckley LB, Urban MC, Angilletta MJ, Crozier LG, Rissler LJ, et al. (2010) Can mechanism inform species' distribution models? Ecol Lett 13: 1041–1054.