The Clever Strategies That Fishes Use to Survive in San Francisco’s Dynamic Estuary

Estuaries are places where fresh water from rivers mixes with salty water from the ocean. Why does this matter? This mixing creates dynamic, ever-changing conditions that fishes must navigate in order to survive. Environmental conditions can change yearly, seasonally, daily, and even hourly. Fishes use many different strategies to adjust to this wild variation. Some are picky and only use certain habitats. Others use many different kinds of habitats and move between them at different times of the year. Adults and juveniles might even live away from each other in different parts of the estuary. In this article, we describe some of the clever strategies that fishes use to survive in estuaries. We also consider how scientists uncover these clever strategies and what each of us can do to help protect the fishes of the San Francisco Estuary and elsewhere.

The San Francisco Estuary. (A) Fresh water from rain and snowmelt flows as rivers into a network of channels known as the Delta (riverine environment). This fresh water then mixes with the salty water of the ocean (marine environment) and creates the San Francisco Estuary (estuarine environment). (B) Salinity and temperature (in • Celsius) change in the San Francisco Estuary with the seasons (left) and daily with the tides (right). Salinity in estuaries is usually between that of marine and riverine habitats, and temperatures are often between those of rivers and the ocean.

WHY IS IT SO HARD TO LIVE IN AN ESTUARY?
An estuary is where fresh water from rivers mixes with salty water from the ocean ( Figure A). The furthest upstream region of an estuary is influenced most by the riverine (river-like) environment, making the RIVERINE Related to, found in, or produced by rivers or riverbanks.
water typically fresh or slightly salty. The furthest downstream region is influenced most by the marine (ocean-like) environment, so the water MARINE Related to, found in, or produced by seas or oceans.
is often very salty. Changes in both river and ocean conditions greatly a ect habitats inside estuaries, making them dynamic, ever-changing environments ( Figure B) [ ].
Salinity (saltiness) is one of the changing conditions in estuaries that SALINITY The amount of salt dissolved in a body of water. fishes must deal with. The salinity of estuaries is linked to how much fresh water from rain and snowmelt flows in from rivers. In the San Francisco Estuary, winter and spring are the rainiest seasons. During these wet seasons, more fresh water flows in from rivers, making the estuary less salty. During the hotter, drier months of summer and fall, less freshwater flow results in saltier conditions. The amount of rain and snow can also change from year to year. In a dry year there is less fresh water, making estuaries saltier. Salinity can also change daily and hourly due to the tides. High tides push saltier water further up into the estuary, whereas low tides allow rivers to push fresh water further downstream toward the ocean.
Temperature is another changeable condition within estuaries. The temperatures of estuaries vary with the seasons, getting warmer in the summer and cooler in the winter. Temperatures of inflowing rivers are often the most variable. In contrast, temperatures in the ocean are more stable. Since estuaries lie between riverine and marine habitats, their temperatures are often somewhere between the two. However, some parts of estuaries are shallow and can be rapidly heated by the hot sun during the day, while cooling o at night [ ].
These constantly changing conditions make estuaries a tough place for fishes to live. Imagine if it were rainy day, hot and sunny the Did you ever wonder when to use the word "fish" vs. "fishes"? "Fish" refers to one or multiple individuals of the same species. "Fishes" refers to multiple individuals of multiple species. next, and a blizzard the day after that. You would need to be prepared to adjust your clothing and plans at a moment's notice! Similarly, estuarine fishes have figured out many di erent strategies to help ESTUARINE Related to, found in, or produced by estuaries.
them deal with all this wild environmental variation.

CLEVER STRATEGIES USED BY ESTUARINE FISHES
The way a fish uses and moves between di erent habitats throughout its life is called its life history. Di erent species of fish, and even di erent individuals within a species, have developed unique life history strategies [ ]. These di ering life history strategies can be quite clever and are classified into several groups.
Freshwater stragglers, such as Sacramento suckers ( Figure A), live and reproduce in freshwater riverine habitats. They become strong swimmers to navigate river and tidal flows. They tolerate variable temperatures, but strongly prefer lower salinities. These fishes sometimes travel into the estuary to feed when salinity is low (spring), but otherwise avoid saltier habitats.
Marine stragglers, such as leopard sharks ( Figure B), live and reproduce in marine habitats, including coastal areas and bays. They tolerate variable temperatures, but strongly prefer waters with higher salinity. Leopard sharks venture into the estuary to feed and to give live birth during periods of high salinity (summer) but they avoid certain

LIVE BIRTH
When o spring are fully developed inside the mother and "born alive." Most fishes lay eggs in nests that are externally fertilized, but some fishes give live birth. regions of the estuary during periods of low salinity (winter).
Estuarine residents, such as tule perch (Figure C), live and reproduce entirely within the estuary. Like leopard sharks, tule perch also give live birth, but they can tolerate greater variations in salinity. This allows them to remain in the estuary year-round. Anadromous migrants, such as Chinook salmon ( Figure D), live most of their adult lives in the open ocean, migrating quickly through the estuary to lay eggs far upstream in rivers. The fish larvae and juveniles grow up in these rivers and eventually move through the estuary on their way out to the ocean, where they grow into adulthood.
For this group, the estuary is like a bridge between juvenile and adult habitats.
Freshwater-linked migrants, such as delta smelt ( Figure E), can live and reproduce in both freshwater and low-salinity estuarine environments. As juveniles, most live in the somewhat-salty (brackish)

BRACKISH
Slightly salty water that is less salty than seawater but saltier than fresh water. Often used to describe water found in estuaries. the following winter, as adults, to lay their eggs. Delta smelt can tolerate some variation in both temperature and salinity, but often move seasonally to find the best habitats with the most food [ ].
Although di erent species tend to use di erent life history strategies, some fish within a species may not follow those strategies! For example, delta smelt are often considered a migratory species, but we found that not all individuals migrate. While most delta smelt do migrate between fresh and estuarine habitats, some spend their entire lives in either riverine or estuarine habitats. This variation is believed to help delta smelt survive unpredictable environmental stress, by making sure that some members of the species are always in di erent parts of the estuary [ ].

HOW DO SCIENTISTS STUDY THE CLEVER LIFE HISTORY STRATEGIES OF FISHES?
Scientists use many methods to discover how fishes survive in estuaries ( Figure ). Each technique provides a di erent perspective on fish life history strategies.
A classic method for studying fishes in the wild is simply fishing for them ( Figure A). These studies are called field surveys. Another way to study life history is to track individual fish with artificial, human-made tags. Artificial tags allow scientists to discover how individual fish move and use di erent habitats. However, artificial tags require that tracking equipment be attached to each fish being studied. Some tags consist of small pieces of metal placed under a fish's skin, each with a code inscribed, so when a fish is caught, researchers can identify where it was tagged and how far it moved [ ]. For larger fishes, like sharks or salmon, researchers can use archival tags that record a fish's location and environment over time ( Figure B). Archival tags are attached to a fish's back by performing a minor surgery, similar to a large ear piercing. Once the fish has recovered, it is released back into its habitat to resume a normal life.
Instead of using artificial tags, scientists can also use the chemistry of hard, calcified body parts as natural tags to retrace the movements of fishes. Di erent natural tags hold di erent information about a fish's life. Some parts, like scales and fin spines, can be removed and the fish released, with minimal harm to the fish. But, for internal parts like otoliths, fishes must be euthanized (killed without pain or su ering)

OTOLITH
The ear stone of some fishes. Scientists can analyze chemicals in the otolith to reconstruct the movement of a fish and the salinity the fish lived in.
before removal. Otoliths are tiny structures that help with hearing and balance, located in the inner ear of many fishes ( Figure C). Otoliths grow during the entire life of a fish. As they grow, chemical elements from the surrounding water are deposited into the otoliths. Scientists can then infer where a fish previously lived based on its otolith chemistry, because the chemical elements in the water of rivers, estuaries, and oceans can be very di erent [ ]. Otoliths also grow rings, like inside a tree trunk, that reflect the age and growth of the fish. By combining otolith chemistry with otolith growth, we can even detect the timing of fish movements. This allows scientists to uncover the complex details of a species' life history [ ].

WHAT CAN WE DO TO HELP FISHES IN THE SAN FRANCISCO ESTUARY?
As we have learned, fishes have developed many di erent strategies to thrive in an estuary. But fishes are not the only users of estuaries. Did you know that, just around the San Francisco Estuary, there are . million people? That is a lot of humans! Human activities, such as farming, city water use, and pollution, have changed estuaries across the world. This has led to the decline of many fish and wildlife populations whose clever strategies might not fit their environment anymore. Some species, like delta smelt, may even go extinct. Delta smelt are highly impacted by human activities, but we have not yet figured out how to fully protect them. Life history research helps We thank Andrew Seitz and Michael Courtney of the University of Alaska Fairbanks for consent to use their photo in Figure B. Comments from Pedro Morais and two reviewers greatly improved the manuscript.
. Comparing and integrating fish surveys in the San Francisco estuary: why diverse long-term monitoring programs are important. San Francisco Estuary Watershed Sci.

CONFLICT OF INTEREST:
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
COPYRIGHT © Fichman, Khen, Willmes, Kuntz, Scott, Hobbs and Lewis. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

YOUNG REVIEWERS
HANNAH, AGE: I am in th grade of a middle school in Austria. I am interested in dogs. My hobbies are gymnastics, other sports, and acting. I have got an old cat and we are getting a dog soon. I also like meeting my friends and listening to some music.

VALERIE, AGE:
I am in th grade of a middle school in Austria. My hobbies are horseback riding, skating, and dancing. I have got a very old cat and we are getting a dog soon. I also like meeting my friends and listening to some music.

AUTHORS RACHEL A. FICHMAN
Rachel is a graduate student at University of California, Davis, studying conservation ecology. Through collaboration between the Otolith, Geochemistry and Fish Ecology Lab and the Freshwater Ecology Lab, Rachel studies how di erent environmental conditions a ect body and otolith (ear stone) growth in delta smelt, a critically endangered fish endemic to the San Francisco Estuary. After graduation, Rachel looks forward to a career as a wildlife and fisheries researcher, focusing on projects that directly impact conservation policy throughout the state of California (USA). *rafichman@ucdavis.edu kids.frontiersin.org September | Volume | Article |

ADI KHEN
Adi is a Ph.D. candidate at the Scripps Institution of Oceanography, U.C. San Diego. She is interested in how corals and algae are responding to global climate change. She uses image analysis to measure coral bleaching, recovery, growth, and/or death over time in the context of heat stress. In addition to research, Adi is passionate about communicating science through art and she makes digital drawings of marine life in her spare time. She also loves taking care of animals and mentoring young students. You can find some of her drawings at adlysia.wordpress.com.

MALTE WILLMES
Dr. Willmes is a postdoc at U.C. Santa Cruz in the Institute of Marine Sciences and NOAA Fisheries Collaborative Program. In his research, he applies geochemical tracers to investigate habitat changes and movement patterns of di erent fish species, including Chinook salmon, delta and longfin smelt, and white sturgeon, to provide scientific input into their management and conservation. In his most recent project, Malte gets to combine modern fish ecology, geochemistry, and archaeology to study how ancient salmon thrived in California over the last , years.

JONATHON KUNTZ
Jonathon Kuntz is a marine ecologist interested in life history research of sharks. In , he received a B.Sc. in environmental and organismal biology from the University of Utah, where he used stable isotopes to study smooth hammerhead sharks. He has since worked with longfin smelt and leopard sharks, using stable isotopes to better understand their use of the San Francisco Estuary.
ALEXANDER R. SCOTT Alec Scott, a Bay Area native, received a B.A. in biology from Carleton College, after which he spent some time doing fieldwork and becoming a divemaster in southeast Asia. He then spent a year working on coral reef ecology at the Scripps Institution of Oceanography. Most recently, he completed an M.S. in marine biology at the University of North Carolina Wilmington, where he studied distributional patterns of Caribbean mesophotic sponges. He is broadly interested in the factors that contribute to the decline of endangered species, and the policy solutions that prevent that decline.

JAMES A. HOBBS
Dr. Hobbs is a researcher in the Department of Wildlife, Fish and Conservation Biology, University of California, Davis. His research program integrates long-term monitoring studies with otolith growth and geochemistry to answer important fisheries resource-management questions in the San Francisco Bay-Delta Estuary. James links population monitoring with innovative technologies to reconstruct the migration history and growth of threatened and endangered fishes. He collaborates with scientists that study genetics, fish health, and population modeling, to understand how climate change, habitat restoration, and resource-management actions a ect fishes.