PACIFIC HERRING (Clupea Pallasii) EGG ACCUMULATION on EELGRASS

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PACIFIC HERRING (Clupea pallasii) EGG ACCUMULATION ON EELGRASS

(Zostera marina) AND OTHER SUBSTRATES

IN TOMALES BAY, CALIFORNIA

A Thesis

Presented to the faculty of the Department of Biological Sciences

California State University, Sacramento

Submitted in partial satisfaction of the requirements for the degree of

MASTER OF SCIENCE

Biological Science

(Ecology, Evolution, and Conservation)

Hali Rederer

SPRING 2020

Hali Rederer

PACIFIC HERRING (Clupea pallasii) EGG ACCUMULATION ON EELGRASS

(Zostera marina) AND OTHER SUBSTRATES

IN TOMALES BAY, CALIFORNIA

A Thesis

Hali Rederer

Approved by:

______, Committee Chair Ronald M. Coleman, Ph.D.

______, Second Reader Timothy Davidson, Ph.D.

______, Third Reader Benjamin Becker, Ph.D.

______Date iii

Student: Hali Rederer

I certify that this student has met the requirements for format contained in the University format manual, and that this thesis is suitable for electronic submission to the Library and credit is to be awarded for the thesis.

______, Graduate Coordinator ______James Baxter, Ph.D. Date

Department of Biological Sciences

Abstract

PACIFIC HERRING (Clupea pallasii) EGG ACCUMULATION ON EELGRASS

(Zostera marina) AND OTHER SUBSTRATES

IN TOMALES BAY, CALIFORNIA

Hali Rederer

Pacific Herring (Clupea pallasii) as a species is a microcosm of the biodiversity conservation and restoration challenges facing our time. Overfishing is a global concern to the point of being considered an extinction crisis for particular fisheries. Understanding how, where, and when a particular species reproduces may be critical to understanding how a species responds to fishing pressure. The Pacific Herring is a small pelagic fish of the family Clupeidae. It is found throughout the Northern Pacific Ocean and has a North America range from Alaska to Baja

Mexico.

The Pacific Herring fishery in Tomales Bay has been closed to commercial fishing since

2007 because of overfishing, market price decline, and low fishing effort. This closure provided an opportunity to gain insight into the spawning habits and ecological context of spawning

Tomales Bay Pacific Herring living under low fishing pressure. It has been long noted that herring tend to spawn in eelgrass (Zostera marina) meadows, but the extent of this dependency has not been thoroughly examined. So, it becomes essential to clarify and quantify the role of eelgrass as a spawning substrate for herring.

Reported here are the results of a two-year field study of Pacific Herring spawning activity

(2016 -2018) in Tomales Bay investigating the following question: Do Pacific Herring prefer

natural eelgrass for spawning compared to other natural or artificial substrates? Eelgrass is the dominant vegetation in Tomales Bay. It is a submerged seagrass found nearshore, ranging from

Alaska through Baja California and is found around the globe.

Two nearshore westerly sites in Tomales Bay were selected for this project: Sacramento

Landing and Chicken Ranch Beach. Experimental intertidal and subtidal spawning sites were built using three different types of artificial substrate and installed at each site. The experimental substrates were Artificial Eelgrass, Concrete, and the existing Bottom (bare, sand, silt, or rock).

The spawning data from the experimental substrate meadows were compared to natural eelgrass meadows near the study sites. Herring roe abundance and density (layering of roe) were measured on each substrate. Potential predators on or near the sites were counted during herring roe data collection and environmental conditions were recorded (tide, turbidity, and temperature). Results from data analysis with Repeated Measures One-Way ANOVA and with multiple comparisons using Sidak’s multiple comparisons test strongly support the hypothesis that spawning Pacific

Herring roe is mostly found on natural eelgrass compared to alternative substrate measured by the accumulation of eggs after spawning events. This finding indicates that herring will spawn in natural eelgrass beds even in the presence of predators. Findings from this study support local eelgrass conservation and restoration efforts as an important component of Pacific Herring fisheries preservation and sustainability .

______, Committee Chair Ronald M. Coleman, Ph.D.

______Date

ACKNOWLEDGEMENTS

I began this science adventure as a citizen scientist volunteer at Point Reyes

National Seashore in 2008 over ten years ago. I was a furloughed State of California field surveyor for Caltrans. Like most state employees during the recession, I had extra time on my hands. I take great pride in completing this research project. Many people have generously contributed their time and energy to this thesis and my success. Heartfelt thanks to National Park Service Scientist Dr. Sarah Allen. She was the first person to talk to me about carrying out a research project on Pacific Herring in Tomales Bay. She also allowed me access to her residence to conduct eelgrass herring spawning surveys from her dock. Dr. Allen connected me to the Inverness Yacht Club who also allowed herring surveys from their facilities. Dr. Benjamin Becker gave his time and advice generously on design, methods, and statistical analysis. As a Point Reyes National Seashore Scientist and Science Coordinator, Dr. Becker was instrumental in providing support for the duration of my Tomales Bay field research, including the use of the Sacramento Landing

Marine Research Station. Dr. Timothy Davidson was new to Sacramento State when I approached him to be on my committee. He accepted and I couldn’t be more grateful. Dr.

Davidson has provided advice on the design and the scope of this research. I am grateful for the assistance of Ryan Bartling, Environmental Scientist and Pacific Herring biologist for the California Department of Fish and Wildlife. David Bui and Laura A. Givens assisted me in the field as undergraduate students, even in cold rainy weather. David is an awesome field technician and scuba diving buddy and Laura is an excellent researcher.

My advisor and the chair of my committee Dr. Ronald Coleman is an extraordinary vii

teacher, fisheries biologist, and mentor. At every step of this thesis project he has provided insight, expertise, and encouragement. Heartfelt thanks to my Caltrans supervisors and coworkers. They allowed me to take time off from work for graduate school. Thanks to the remarkable Biological Sciences faculty at CSUS whose classes I took and learned so much from. Most of all I thank Dawn Whitney whose encouragement and support continues to make this endeavor possible.

Grants funded this research. Thank you:

Point Reyes National Seashore Association Fund for Marine Science Research

Professional Engineers in California Government

CSU Council on Ocean Affairs, Science and Technology Travel Grant

Sigma XI

This thesis is dedicated to scientists who study common “unremarkable” species, leaving the charismatic animals and plants to others. It takes willing researchers digging deep to explain to people why they need to care about species that are considered an unlimited resource, so abundant they need little attention or concern (e.g., the Passenger

Pigeon, Pacific Herring,...). Carry-on.

viii

TABLE OF CONTENTS Page Acknowledgements ...... vii

List of Tables ...... x

List of Figures ...... xi

Chapter

1. INTRODUCTION ...... 1

The Pacific Herring Fishery ...... 3

Tomales Bay Spawning Pacific Herring Biomass Fluctuations ...... 7

Reproductive Biology of Pacific Herring ...... 12

Key Importance of Eelgrass for Spawning Herring ...... 14

Spawning Site Selection: Where Do Pacific Herring Lay Their Eggs? ...... 15

Hypothesis and Objectives ...... 18

2. MATERIALS AND METHODS ...... 19

Tomales Bay ...... 19

Sites ...... 21

Approach to Field Work ...... 22

Data Analysis ...... 36

3. RESULTS ...... 38

4. DISCUSSION ...... 42

Appendix A Common Species List and Counts (2016 -2018) ...... 52

Appendix B. Field Work Schedule and Environmental Conditions ...... 55

Appendix C. Chronology of Tomales Bay Fishery ...... 56

References ...... 61

LIST OF TABLES

Tables Page

1. Tomales Bay Commercial Pacific Herring Fisheries Seasons (1988 -2007) ...... 8

A1. Summary of Species Counts ...... 54

B1. Field Work Schedule 2016-2018 and Conditions ...... 55

LIST OF FIGURES

Figures Page

1. Fluctuations in Biomass of Pacific Herring in Tomales Bay (1977-2007) ...... 9

2. Biomass of Pacific Herring versus Eelgrass Coverage (1986 -2006) ...... 11

3. Maps: Tomales Bay Overview and Eelgrass Beds with Research Sites ...... 20

4. Experimental Layout ...... 24

5. Field Work Flow Chart ...... 25

6. Design and Build (photographs) ...... 27

7. Deploy Substrates (photographs) ...... 30

8. Counting Pacific Herring Eggs (photographs) ...... 32

9. Grab Sample: Eggs on Natural Eelgrass (photograph) ...... 33

10. Sacramento Landing Site Results ...... 40

11. Chicken Ranch Beach Site Results ...... 41

12. Eelgrass Structure (photographs) ...... 47

xi 1

INTRODUCTION

Pacific Herring (Clupea pallasii) is emerging as a lightning rod species in conflicts over what constitutes sustainable fisheries, coastal habitat restoration, and nearshore conservation. Herring are characterized by their abundance, though long term industrial commercial fishing is challenging this idea of it being a fish of inexhaustible plenitude (Blaxter et al. 1982, Horn et al. 2006). To make informed decisions about how to manage this species and its fisheries, it is critical that we understand the biology, including the basic reproductive biology, of the species.

Fisheries managers typically organize commercial catches by setting quotas for each season based on models which predict expected abundance such as maximum sustainable yield (MSY) models and yield per recruit models, among others. These models include, to a greater or lesser extent, key biological parameters of the fish population being targeted. Such parameters include recruitment or survival, mortality, age structure, and sex (Jennings et al. 2001). From the beginnings of industrial scale herring fishing, a management goal has been to explain and predict herring population fluctuations relative to production, recruitment, spawning habitat, and ocean conditions

(Reum et al. 2011, Spratt 1992). Collecting field data that ground truth these parameters is often difficult (Hubbard 2018, Lam et al. 2019).

The underreporting of catches, overfishing, and the tendency to blame depleted catches on the environment is sometimes referred to as the toxic triad of fisheries (Pauly et al. 2005). Another dimension of this is blaming depleted catches on nonhuman

2 predators. In the case of Pacific Herring, this would be marine mammals (e.g., Harbor

Seals Phoca vitulina, Humpback Whales Megaptera novaeangliae) and seabirds, along with their protections under the Endangered Species Act (Boldt et al. 2019, Froese et al.

2019, Pauly et al. 2005). Fisheries managers sometimes attribute non-human forage of

Pacific Herring for population collapses. How herring are selected by predators is unclear

(Koehn et al. 2017). Some studies indicate marine mammals like Harbor Seals seek juvenile and unripe adult herring for consumption rather than the ripe females sought by commercial fishing. Moran et al. (2018) found that Humpback Whales were abundant in

Sitka Sound Alaska, as is Pacific Herring, but the whales foraged predominately on euphausiids there and not herring (Surma et al. 2018, Stacey et al. 1982, Moran et al.

2018).

As a low trophic level keystone species, Pacific Herring play a critical role in marine nearshore ecosystems (Fox et al. 2018, Gauvreau et al. 2017). Once consumed by predators, herring provide energy that converts lower trophic species (e.g., phytoplankton and zooplankton) into higher trophic species that prey on them (Surma et al. 2018).

Herring are forage to seabirds, larger fish, and marine mammals (Konar et al. 2019).

Absent forage fish, the populations of birds, fish, and marine mammals’ numbers are diminished and negatively impacted, some to the point of trophic collapse (Xu et al.

2019, Shelton et al. 2014).

Spawning habitat availability, quality, and structure are critical components for

Pacific Herring reproduction (Unsworth et al. 2018, Eldridge et al. 1973). Pacific Herring spawn nearshore in areas which are also desirable coastal habitats for human occupation,

3 commercial activity, and recreation. Nearshore spawning areas are critical to the self- renewal of herring.

The Pacific Herring Fishery

The Pacific Herring fishery has been an important fishery for millennia and is thought to have played a central role in developing coastal ecological-human social systems (Laakkonen et al. 2013, McKechnie et al. 2014). Along with its deep human social-economic and ecological connections, Pacific Herring remains an important food staple. Human fish consumption translates to an average worldwide wild fish catch of

93,000,000 tons (FAO 2018). Worldwide, the Pacific Herring commercial catch has lately been around 500,000 tons (FAO 2018). Canada catches about two-thirds of the worldwide catch, 250-300,000 tons per annum, worth around 2.5 billion US Dollars

(FAO 2018). Female Pacific Herring are the focus of much of the commercial herring fishing because herring eggs command a high market price. It follows that catching the fish while they are ripe with eggs, but before they spawn, is the target of commercial

Pacific Herring fishing. Whole fish, which are typically males and “unripe” females, are sold at a lower price for fish meal, oil, and fertilizer products (Suer 1987, Spratt 1992,

California Department of Fish and Wildlife 2019).

Pacific Herring biomass has been in decline since the late 1970s, coinciding with increasing market demand and industrial scale fishing (Essington et al. 2015, Thompson et al. 2017). Pacific Herring, like all species of forage fish, are considered Species of

Least Concern (IUCN 2018, Seafood Watch 2019). A widely reported problem for

Pacific Herring is findings of truncated age structure throughout their biogeographic ranges (Siple et al. 2018, Xu et al. 2019). Older larger herring are extricated from their ecosystem leaving smaller younger reproductive age fish removed by fishing before they reproduce and replenish the stock (Pauly et al. 2005). Attempts to list Pacific Herring, or any species of forage fish, under the Endangered Species Act have thus far been denied

(73 FR 19824 04/11/2008).

The species, in some respects, is proving itself to be resilient. It is still found throughout most of its range, although it is completely extirpated from a few spawning grounds such as San Diego, California (McKechnie et al. 2014). Pacific Herring live in a wide range of latitudes with variations in oceanographic conditions including temperatures, salinity, and depth. This adaptive plasticity seems to explain the persistence of Pacific Herring, given that it is a heavily fished and predated upon species. Further evidence of this plasticity includes the ability to strategically use the water column to vertically evade predation within the nearshore habitats. Herring seemingly can shift survival strategies in response to environmental and predation pressure, including small scale fishing (Hardwick 1973, Szoboszlai et al. 2015).

Instability in herring fisheries and concerns about their future have precipitated research by academics, fish and wildlife management agencies, commercial fishing stakeholders, and environmental groups (Levin et al. 2018). Recent Pacific Herring research includes 1) The causes of boom or bust cycles characteristic of industrial commercial herring fisheries (McKechnie et al. 2014); 2) Predicting biomass abundance and setting fishing quotas (Sadovy 2005); 3) Encouraging basic life history research

5 regarding the oceanographic and habitat needs of Pacific Herring, particularly for spawning (Shelton et al. 2014); 4) Negative impacts from overfishing compared to nonhuman predation (Fox et al. 2018, Kelly et al. 2018); and 5) Environmental threats such as oil spills and climate change (Incardona et al. 2012). A goal of research efforts is improving fisheries management by integrating and quantifying herring’s role as a keystone species (Dickey-Collas et al. 2010).

Herring populations and their overall abundance can fluctuate from year-to-year even when fishing activity is low and there are eelgrass beds present (Levin et al. 2016,

Heck et al. 2003). Some results have suggested that the condition of the eelgrass is directly related to successful herring spawns (Lassuy et al. 1989). However, other results have indicated that beds of eelgrass do not necessarily attract spawning herring (Erisman et al. 2011). At times oceanographic and environmental factors have explained the absence or depletion of herring and their failure to spawn. These factors include El Niño conditions, water pollution, and overfishing (Levin et al. 2018).

The California Pacific Herring Fishery

The range of Pacific Herring in North America spans from Alaska to Baja

California. At times, California exports of Pacific Herring have exceeded all other North

American herring fisheries (PacFIN 2019). Commercial herring fisheries have largely taken place in Crescent City Harbor, Humboldt Bay, Tomales Bay and San Francisco

Bay. California Department of Fish and Wildlife unpublished data (1972 - 2018) illustrate that California herring fisheries exhibit boom and bust cycles characterized by

6 unexpected drops in biomass followed by peaks (Hazen et al. 2018). In the Department’s annual reports, overfishing is rarely called out as the problem in the bust part of the cycle.

The California Department of Fish and Wildlife is responsible for regulating and monitoring Pacific Herring resources in a manner that avoids overfishing. However, the department also has a mission to support the fishing industry’s commercial success.

These are conflicting responsibilities at times.

California commercial herring fishing quotas have, in recent years, been set at a seemingly conservative 5% of predicted biomass (California Department of Fish and

Wildlife 2018). Yet Pacific Herring biomass continues to decline in California,

Washington, Alaska, and Canada (PacFIN 2019, Okamoto et al. 2018). Annual roe surveys count eggs on vegetation, abiotic substrates such as riprap rock, in herring samples, and reported commercial catches. These comprise the largest portion of data used to estimate Pacific Herring biomass annually (Hazen et al. 2018). It is possible that fisheries managers at times overestimate Pacific Herring abundance (McKechnie et al.

2014, Earthjustice 2013). This past herring season (2018-2019), San Francisco Bay, the only commercial herring fishery currently operating in California, closed early due to low biomass and lack of fishing effort.

The California Department of Fish and Wildlife is recognizing more must be done to ensure that Pacific Herring are sustainably fished. However, addressing the linchpin to sustainable herring fisheries; namely, conserving nearshore spawning habitats is challenging (Essington et al. 2015,Thompson et al. 2017, Pauly et al. 2005, Hazen et al.

2018, Audubon 2018).

Tomales Bay Spawning Pacific Herring Biomass Fluctuations

Tomales Bay, Marin County, California contains an historically important commercial herring fishery (Sanchez et al. 2018, Avery 2009, Suer 1987). It is a microcosm of coastal areas rich in natural resources experiencing increasing anthropomorphic pressure from nearby urban centers. From a wildlife conservation perspective, demands for multiple uses create management challenges. Some of these conflicting demands include water quality issues from terrestrial and upland cattle ranching versus mariculture businesses, heavy recreational traffic versus wildlife habitat needs across all taxa (e.g., beach space needed by pupping Harbor Seals is also desired by people harvesting clams or picnicking).

Tomales Bay has a long history of overfishing issues. This includes overfishing shellfish, salmon, and abalone, dating back to the early 1900s (Avery 2009). As a case study, the Tomales Bay Pacific Herring fishery illustrates the challenges posed by biomass fluctuations reported for most commercially fished small pelagic fish (Table 1,

Figure 1). Determining biomass and sustainable catch quotas for an eelgrass rich spawning habitat is particularly difficult (Sanchez et al. 2018, Scofield 1952, Suer 1987).

Eelgrass meadows tend to be low visibility, high turbidity environments notoriously difficult to monitor (Fort et al. 2013).

Pacific Herring spawn in Tomales Bay annually from November through March

(Spratt 1992, Watanabe et al. 2003). However, herring historically spawned in the Bay twice annually, eight months out of the year (Marin Journal 1917). In the 1990s Tomales

Table 1. Tomales Bay Commercial Pacific Herring Fisheries Seasons (1988 -2007)). In 1986 the biomass estimate was over 5000 tons (5550). Prior to 1986, Tomales Bay biomass estimates was as high as 22,000 tons. The 1988 -1989 seasonal landings data likely were from combining landings from Tomales Bay and Bodega Bay. The Tomales Bay commercial herring fishery closed after the 2007 season. 15 permit holders still actively renew yearly as of 2018. 69 permits were once allowed for the Tomales-Bodega Bay areas until the late 1990’s when 35 permits were allowed for Tomales Bay alone and Bodega Bay was closed. Data Sources: Pacific Fisheries Information Network (PacFIN) 2019 retrieval and California Department of Fish and Wildlife annual reports 1988 - 2007.

Ex-Vessel Biomass Tomales $ per Estimate Bay Quota Landings % Catch Season pound (tons) (tons) (tons) Exploitation 1988-1989 $0.22 2000 350 213 10.65 1989-1990 $0.43 345 Closed Closed Closed 1990-1991 $0.51 779 Closed Closed Closed 1991-1992 $0.61 1214 250 Closed Closed 1992-1993 $0.26 1900 200 222.31 11.70 1993-1994 $0.47 2464 250 219 8.89 1994-1995 $0.93 3980 450 275 6.91 1995-1996 $1.21 2000 300 355 17.75 1996-1997 $0.64 1510 226 222 14.70 1997-1998 $0.13 586 Closed Closed Closed 1998-1999 $0.38 4071 390 54 1.33 1999-2000 $0.30 2010 400 42 2.09 2000-2001 $0.45 4,000 400 298.5 7.46 2001-2002 $0.25 7242 500 354.2 4.89 2002-2003 $0.24 4382 400 78 1.78 2003-2004 $0.25 12,124 500 279.7 2.31 2004-2005 $0.11 9080 400 30 0.33 2005-2006 $0.27 3000 350 19 0.63 2006-2007 $0.11 2200 350 1.2 0.05

Herring Biomass

Seasons

Figure 1. Fluctuations in Biomass of Pacific Herring in Tomales Bay (1977-2007) Biomass by Season 1977 -2007. The California Department of Fish and Wildlife generated estimates of Pacific Herring biomass every season before the fishery Shuttered in 2007. Low fishing effort was typical of the Pacific Herring fishery prior to the 1970’s (Spratt 1992, California Department of Fish and Wildlife annual reports 1976 -2007).

Bay, Bodega Bay, and San Francisco Bay combined to form the largest herring fishery on the United States West Coast (Suer 1987).

Once commercial herring fishing ceased in Tomales Bay (2007), the California

Department of Fish and Wildlife stopped monitoring herring entirely after 60 straight years of doing so (Watanabe et al. 2003, Watters et al. 2004). The latest 2019 Pacific

Herring Fisheries Management Plan does not mention any future monitoring plans for

Tomales Bay (Hazen et al. 2018). As of 2020 there is a 13-year data gap for monitoring the Tomales Bay Pacific Herring population.

Eelgrass, a 5-7 mm wide roughly 1 m long submerged flowering seagrass

( Hyndes et al. 2018) is prolific in Tomales Bay. Eelgrass might or might not provide more structure for spawning Pacific Herring in comparison to other available substrates.

This study sought to examine this in Tomales Bay (Table 1, Figure 2).

Eelgrass Coverage Hectares

Figure 2. Biomass of Pacific Herring versus Eelgrass Coverage (1986 -2006). As eelgrass coverage increases the biomass of Pacific Herring fluctuates, e.g., the largest eelgrass coverage, 394 ha, was a season (1985-86) with a small herring biomass (560 short tons). from a Spearman correlation analysis. Eelgrass coverage is not a predictor of the biomass of Pacific Herring (R2 = 0.22, df = 1,19, P = 0.07). Data source: California Department of Fish and Wildlife annual reports (1986 -2006).

Reproductive Biology of Pacific Herring

Understanding Pacific Herring biogeography and reproductive biology is the basis for effective fisheries management (Hay et al. 2009). There are very few studies on

Pacific Herring migration and their life in the open ocean (Flostrand et al. 2009). Pacific

Herring are believed to migrate distances between 2 to 5 miles from a spawning ground

(Hay et al. 2009). They also migrate vertically through the water column reportedly down to maximum depths of 1200 feet. At night they rise towards the surface to feed on phytoplankton, copepods, small fish, and crustaceans (Blaxter et al. 1982, Bell et al.

1987).

Though Pacific Herring move towards shore to spawn and offshore to feed, some research suggests that they might not have fidelity to a school and schools might not have spawning ground fidelity (Hay et al. 2009). Other studies, with limited use of tags, have suggested herring might have fidelity to particular stock and spawning grounds

(Flostrand et al. 2009). Pacific Herring do not necessarily remain in the same schools throughout their lives (Hay et al. 2009, Hart et al.1934, Cury et al. 2000, Flostrand et al.

2009). Genetic studies have not produced evidence that Pacific Herring relatedness and characteristics vary by geographic stocks though there are research efforts underway testing related hypothesis (Speller et al. 2012).

A conventional assumption that Pacific Herring has fidelity to a particular school and spawning ground is a paradigm that might not be grounded in herring biology

(Sinclair et al. 2002, Sadovy et al. 2005). The assumption that fish species organize themselves in stocks might be only a convenient human construct for commercial

13 exploitation (Flostrand et al. 2009, Sinclair et al. 2002). Pacific Herring’s movements into nearshore coastal habitats to spawn make them easily catchable in bays, estuaries, and urbanized coastlines, especially when they enter the shallows as defensive bait balls

(Lassuy et al.1989).

Spawning in Pacific Herring has been studied more than any other aspect of its biology because that is when Pacific Herring are commercially fished and easy to access

(Blaxter et al. 1985). Commercially fishing a schooling species in the reproductive phase of its life cycle is suspected to lead to the abundance variance observed throughout their range in boom or bust cycles (McKechnie et al. 2014, Laakkonen et al. 2013, Funk et al.

2001, Schweigert et al. 1985).

Herring do not form male and female pairs. However, male and females school together in large numbers to spawn at various times of the year, typically late Winter or early Spring to Fall (Carolsfeld et al. 1997). The timing of herring spawn seems to depend on the spawning ground’s geographical latitude (Blaxter et al. 1982). Pacific

Herring sperm release may be triggered by female pheromones signaling that a female is about to lay eggs (Carolsfeld et al. 1997). Female herring physically ventrally contact the substrate they lay their eggs on (Palsson 1984, Spratt 1987). Specific environmental triggers of herring spawning events have been suggested but are not known, though hypotheses abound (Hardwick 1973). One hypothesis is the changes in barometric pressure, including storms and intrusion of fresh water into spawning grounds, dilute the salinity, potentially triggering spawning (Moll et al. 2018).

Spawning commonly takes place in waves. Spawning episodes last over several days to weeks in nearshore environments, close to vegetation or along protected rocky shores (Hyndes et al. 2018, Hoshikawa et al. 2001). The fertilized eggs are sticky and attach to vegetation, eelgrass, algae, grass, rocks, and marine over-structure such as docks or piers in intertidal and subtidal zones. Each adult female, 2 to 7-years, can produce

10,000-50,000 eggs (Froese et al. 2019). The male releases milt with sperm into the water to fertilize eggs that females lay (Hay et al. 1985). Pacific Herring eggs hatch in 4 to 10 days. Herring usually reach maturity in 2 to 4 years and can live up 19 years, though they usually live up to 7 years in San Francisco Bay and Tomales Bay (Froese et al. 2019,

Lassuy et al. 1989, Spratt et al. 1992).

Key Importance of Eelgrass for Spawning Herring

The “nursery role of eelgrass” hypothesis (Heck et al. 2003) is that eelgrass meadows, in coastal marine environments, function as a nursery to herring and a variety of fish species (Unsworth et al. 2018). Pacific Herring research has often focused on the early stages of herring development, including spawning biology (Hay et al. 1985) but has not focused on spawning habitat conservation for sustainable herring fisheries. It is noted that spawning herring tend to use eelgrass as substrate (Shelton et al. 2014).

However, herring have also been known to be highly variable and sometimes indiscriminate regarding spawning substrate (Hay et. al. 2009). In California it has been noted that herring use rocks as substrate as well as a variety of vegetation in San

Francisco (Hazen et al. 2019).

Much is not known about the relationship between eelgrass and herring and how they impact one another, such as how acreage of eelgrass impacts biomass of herring

(Levin et al. 2018, Hazen et al. 2019, Gardali et al. 2011).

As demonstrated by Project ZEN (Zostera Marina Network), a globally accepted general understanding among eelgrass community ecology researchers is that there is a relationship between eelgrass meadows and ichthyofaunal abundance (Heck et al. 2003).

Yet there are few U.S. West Coast studies that specifically examine the habitat structure requirements of spawning fish, including Pacific Herring (Muphy et al. 2000). Questions regarding how Pacific Herring use eelgrass habitat in comparison to other habitat types have been raised as a need for more research in California (Hazen et al. 2018, Sherman et al. 2018, Ha et al. 2018, Heck 2019). Hardwick (1973) in a California Fish and Game paper, linked biomass estimates of spawning herring, herring eggs, and associated vegetation, namely eelgrass, in Tomales Bay.

Spawning Site Selection: Where Do Pacific Herring Lay Their Eggs?

Spawning site selection may vary by location and may depend on the substrate available (Bell et al. 1987). Eelgrass is a dominant nearshore species from Alaska to Baja

(Heck 2019). It is a submerged marine aquatic vegetation that forms intertidal and subtidal meadows or beds typically down to 4m depth in California (Sherman et al.

2018). Eelgrass is credited with providing numerous ecological services by supporting biodiversity (Murphy et al. 2000) . Some research suggests that decreased eelgrass

16 populations may contribute to the declining herring numbers (Plummer et al. 2013).

Some findings support the hypothesis that the condition of eelgrass is directly related to successful herring spawns (Lassuy et al. 1989). Others contradict this hypothesis and contend that eelgrass may be vital to protecting herring roe from predation, but not as spawning habitat and fish nursery in every way (Heck et al. 2003). Other results suggest herring indiscriminately spawn on impulse using a variety of substrates, not just eelgrass

(Haegele et al. 1985, Shelton et al. 2014, Kelly et al. 2018). Some findings suggest eelgrass, as far as herring is concerned, is neutral in providing ecological services for spawning (Anderson et al. 2009).

The California Department of Fish and Wildlife Herring Fisheries Management

Plan scientific review panel members (Hazen et al. 2019) noted these same contradictions. The panel members pointed out the difficulty of planning for herring conservation when there are so many outstanding questions about herring’s use of its spawning habitat. For example, Hardwick (1973) observed that once the herring have moved into coastal waters nearshore, they spawn on any available substrate. Haegele et al. (1985) disagreed and strongly suggested that herring eggs are laid almost exclusively on marine vegetation. He found that there was no preference for one type of marine vegetation over another.

Others have implied that Pacific Herring have a hierarchy of substrate preferences

(Hoshikawa et al. 2001, Bell et al. 1987). In San Francisco Bay, herring have been thought to choose eelgrass first, red algae next, then abiotic surfaces such as rocks if necessary (Eldridge et al.1973). In Tomales Bay and Humboldt Bay, eelgrass was noted

17 as the most used substrate by spawning herring and Spratt (1992) described eelgrass as preferred for spawning (Wattanabe et al. 2003). However, others noted that herring season annual reports, seasons 2000-2003, indicate that red algae (Gracilaria sp.) and brown algae (Sargassum sp.) were used as spawning substrate in spots and as much as eelgrass in the inner Tomales Bay.

A review of Tomales Bay Pacific Herring and eelgrass California Department of

Fish and Wildlife data for over 20 years (1983-2004) shows that the eelgrass meadows are relatively stable in quantity and fluctuate year to year in contrast to Pacific Herring biomass. Herring and eelgrass do not fluctuate in abundance at the same time annually.

Eelgrass is dormant in winter when herring actively spawn. From 1996-2006, Tomales

Bay eelgrass had mean quantities of around 360 hectares (Standard Error of 8 hectares) and was table year to year. Whereas herring biomass, for the same period, fluctuated year to year, ranging from 500 short tons to 11,000 short tons. In Tomales Bay in the 1970s through the early 2000s, eelgrass beds were mapped and numbered for associating, at a fine scale, annual herring biomass surveys with specific eelgrass beds in the Bay. By

2006, the California Department of Fish and Wildlife abandoned their established eelgrass bed maps and field procedures, making it difficult to compare the eelgrass and herring data collected after 2005 with the previous thirty-years of herring monitoring data, geographically referenced (Spratt 1992, Bartling 2006). Contradictions such as these (Figure 2) surrounding the importance of eelgrass for spawning herring provided the impetus for this research.

Hypothesis and Objectives

Based on the existing literature and observations, I hypothesize that Pacific

Herring eggs will accumulate on natural eelgrass spawning substrate over other plants or human built structures, such as piers, concrete, artificial eelgrass, and the nearshore existing bottom of the bay, which is typically sand, rock, gravel, or silt. In Tomales Bay, egg accumulation could plausibly suggest a preference for eelgrass as spawning substrate.

Objectives:

1. To determine by observation if Pacific Herring eggs are largely found on natural eelgrass after spawning events over other substrates, Alternative spawning substrates were provided in spawning sites.

2. To measure egg accumulation by counting eggs adhering to the different spawning habitat substrates.

3. Review and analyze the available Tomales Bay Pacific Herring fishery historical data to gain an understanding of this collapsed herring fishery. Doing this will support efforts to recover the Tomales Bay Pacific Herring stock by Point Reyes National Seashore, and the California Department of Fish and Wildlife (CDFW), among other stakeholders (e.g.,

The Audubon Society).

MATERIALS AND METHODS

Tomales Bay

Tomales Bay is located 73 km North of San Francisco. It is influenced by upwelling within the highly productive and biodiverse central California Current ecosystem. Out of eleven potential California Pacific Herring spawning areas (Hazen et al. 2018), 4 of the 11 sites have had commercial herring fisheries. San Francisco and

Tomales Bay were the largest. Geologically, Tomales Bay is a shallow rift valley basin between the Pacific and Continental shelves with the San Andreas Fault running through its center (Avery 2009). Tomales Bay is characterized by its brackish waters, relative calmness, and extensive eelgrass meadows lining the shoreline (Merkel and Associates

2017). The bay divides into an outer and inner bay. The inner bay includes marshy sloughs and mudflats. The outer bay has multiple coves, sandy and rocky beaches, and ultimately opens to the ocean. The middle area of the bay contains 20m deep holes where

Pacific Herring hold up before moving close to shore for spawning (Figure 3a).

Tomales Bay State Park and conservation land trusts are part of the mosaic of land uses that comprise the coastal and upland areas that adjoin Tomales Bay. Inverness is a small beach town featuring marinas and commercial businesses. Above Inverness are patches of private ranches. The eastern side of Tomales Bay includes well established oyster mariculture businesses, county parks, private residences, hotels, and upland

20 ranches. All share the bay with diverse resident and migratory marine and terrestrial wildlife (Avery 2009). The west shore of Tomales Bay forms the eastern boundary of

3a 3b

Figure 3. Maps: Tomales Bay Overview and Eelgrass Beds with Research Sites 3a. Tomales Bay depth at Mean Low Low Water (MLLW) is -0 to -20m maximum depth (NOAA and United States Geologic Survey Map Viewer 2019). 3b. Overlay of the research sites on a historic California Department of Fish and Wildlife map of numbered Tomales Bay eelgrass beds (Hardwick 1973 and Spratt 1989).

Point Reyes National Seashore. It is within the west shore intertidal and subtidal zones of

Tomales Bay that the two research sites for this study were located (Figure 3b.)

Sites

Two sites in Tomales Bay, Sacramento Landing and Chicken Ranch Beach, were selected for this study based on a California Department of Fish and Wildlife map of eelgrass beds (Figure 3b, Spratt 1989), reports of herring spawning activity, and direct observations of herring spawning:

1. Sacramento Landing Site is between Sacramento Landing and Duck Cove. Typically, this mid-bay area has an average maximum subtidal water depth of 6m at mean high tide.

This is a rural site accessible by a dirt road, and dotted with a few houses, within an undeveloped wilderness. The site was in close proximity to the Sacramento Landing

Marine Research Station, National Park Service Facility.

2. Chicken Ranch Beach Site is a relatively urbanized site is on the south edge of the town of Inverness close to the Inverness Yacht Club and nearby Shell Beach. It has an average maximum subtidal water depth of 5m at mean high tide. This Chicken Ranch

Beach is a Marin County Park and a popular location for people (e.g., swimmers, kayakers, dog walkers, picnickers). Under low tide conditions, experimental plots would sometimes be partly unsubmerged and visible.

The California Department of Fish and Wildlife had annually reported on the location of eelgrass beds with robust herring spawning during the years they monitored herring. Also indicated was that herring spawning activity was occurring in the inner

23 more urbanized sections of Tomales Bay as well as in the outer less developed areas

(Watanabe et al. 2003). Preliminary data were collected at these two sites during the

2015-2016 spawning season. This was done to ensure that these sites had herring spawning activity and contained intertidal and subtidal eelgrass as well as large areas with little to no eelgrass. The sites were assessed for safety and accessibility for SCUBA and snorkeling, moving equipment in and out, and access to facilities such as restrooms and water. Both sites experienced herring spawning activity during the preliminary field season, 2015-2016, and over the 2016-2018 field seasons. Eelgrass was the dominant vegetation in most nearshore areas along the west side of Tomales Bay, though uneven in density and patchy rather than forming contiguous meadows. Eelgrass beds were sometimes found to have other vegetation growing within their beds such as Gracilaria sp. and Zostera japonica.

Approach to Field Work

This study had two components: 1) Experimental component: artificial spawning substrates were designed and installed to compare herring egg accumulation on built artificial substrates versus nearby Natural Eelgrass and existing Bottom substrate to quantify structural versus biological effects of eelgrass on herring eggs; 2) Additional observations and surveys were carried out to look for herring eggs on other potential substrates around the research sites (Pamela Reynolds, personal communication). During surveys, potential herring predators within the sites were counted (Appendix A Table

A1).

Experimental Component

Design of the experimental sites of alternative herring spawning habitat was conceived from a synthesis of methods devised from other herring field studies, the roe- on-kelp herring fisheries, and intertidal and subtidal seagrass studies (Eldridge et al.

1973, Reynolds 2015). The experiment was composed of four substrate treatments types with ten ¼ m2 replicate substrates of each treatment at each independent site. These treatments were Artificial Eelgrass substrate, Concrete substrate, existing Bottom substrate (bare sand, gravel, rock), and nearby Natural Eelgrass beds (Figure 4 and Figure

5).

Design and Construction of Artificial Spawning Substrate

Three types of ¼ m2 spawning alternative substrates to Natural Eelgrass were constructed. These were prototyped and tested in 2015 as follows : 1) Artificial Eelgrass substrates were based on the designs of the Zostera Experimental Network (Project ZEN

2015) and the commercial herring roe- on-kelp fisheries (Bartling 2007); 2) Concrete substrates were based on a San Francisco Bay steppingstone experiment by Eldridge et al.

(1973); and 3) Bottom substrates were composed of sand or rock, or a mix of both materials with whatever was submerged on the bottom. The latter were ¼ m2 quadrats with locations and positions marked with half concrete blocks.

Figure 4. Experimental Layout of the Pacific Herring substrate egg accumulation experiment, Tomales Bay (2016-2018 seasons). For this experiment, two independent sites were selected, namely Sacramento Landing and Chicken Ranch Beach. At each site, artificial substrate treatments were randomly deployed within a 61m2 area. Nearby Natural Eelgrass meadows were also sampled; they were a minimum of 30m away from the artificial substrates.

Figure 5. Field Work Flow Chart of Tomales Bay Experimental Process (2016- 2018).Typically one site was surveyed almost every week though both sites were initially checked for spawning (Table B1). First determined was if herring had spawned. Pacific Herring spawning events precipitate visible wildlife feeding frenzies from seabirds and seals. Environmental parameters were noted (Appendix B, Table B1), spawning limits, search for eggs on other potential spawning substrates, and counted potential herring predators within the research site. Using a 1/4m2 quadrat, egg counting commenced on the Artificial Eelgrass substrates (10), Concrete substrates (10), Bottom substrates (10), and nearby Natural Eelgrass beds (10 samples). SCUBA and snorkeling were used when counting eggs.

Artificial Eelgrass substrates were made of green PVC (polyvinyl chloride) flagging tape tied in strips onto a heavy mesh metal lattice. The PVC flagging, rated at 0

℃, was cut into 0.9m lengths. These PVC strips were then tied onto metal lattice frames at a density of 500 PVC strips per ¼ m2. Each PVC strip was between 5-8 mm wide, comparable to naturally occurring Tomales Bay eelgrass patches. However, Artificial

Eelgrass substrate was designed to be different enough from Natural Eelgrass to provide a vegetation-like alternative spawning substrate. It was important that the material used did not break off easily because of the overwintering and resident seabirds which can consume vegetation, especially Brant’s Cormorant (Phalacrocorax penicillatus). In 2016, before using the materials selected for the Artificial Eelgrass plots, I built and tested a prototype Artificial Eelgrass plot by submerging it in saltwater and leaving it that way in full sun for a year. It was important to determine if the flagging tape would hold up under ocean-like conditions (Figure 6).

The Concrete substrates were ¼ m2 x 2 cm thick squares internally supported with stiff metal mesh wire. The Concrete ¼ m2 substrates were constructed in wooden forms using extra strength Quikrete concrete, hand mixed in buckets, and allowed 10 days to cure in place (Figure 6).

The Bottom substrate quadrats were constructed of 1/2-inch PVC pipe with PVC connectors filled with Tomales Bay rock and sand to achieve negative buoyancy.

Quadrats were subdivided into 25 equal squares for ease of counting herring eggs.

28 a b

c d

Figure 6. Design and Build: ¼ m2 substrates based on a synthesis of Project ZEN designs, the herring roe-on-kelp fishery designs, and Fish and Wildlife departments herring survey manuals. Negative buoyancy was important in design. 6a and 6b Concrete substrate, 6c and 6d Building quadrats, 6e Artificial Eelgrass substrate with plastic bottle buoy.

Deployment

Sacramento Landing and Chicken Ranch Beach had 10 of each type of substrate for a total of 30 substrates within a randomized block experimental spawning site. The experimental spawning meadow dimensions were 61m2 , 61 m along the shoreline and

61m from the shoreline from -0.5m to -3.6m deep during high tide (Fort et al. 2009).

Natural Eelgrass beds were available for counting roe nearby the experimental spawning sites.

In September and October 2016, the two experimental spawning sites were constructed by installing the treatment substrates in Chicken Ranch Beach and

Sacramento Landing nearshore areas. The experimental spawning sites were accessible by trail and vehicle. Most importantly, Pacific Herring spawning was observed at these sites during the previous 2015-2016 season. The 61 m2 experiment was set up in nearshore intertidal and subtidal areas within each of the two sites where there was little to no eelgrass, and Natural Eelgrass nearby within walking distance. Each experimental spawning site was dimensioned using a100m steel chain parallel to the shoreline at the lowest tide (0 tide or less) and a random number generator to determine the experiment limits. During low tide the numbered artificial substrates were randomly installed within each of the established 61 m2 experiment al spawning sites. Small adjustments were made in the placement of the substrates to insure at least 1m2 of space surrounded each as a buffer. Substrates were at minimum 1m apart from each other so that they did not touch

Natural eelgrass nor each other. Half concrete blocks marked the locations of the 10

Bottom substrates. All substrate were completely submerged in water when installed.

The artificial substrates were attached with zip ties to filled sandbags to overcome buoyancy and to avoid currents displacing them. This resulted in the substrate being situated on top of sandbags 0.2-0.3m up from the bottom. Once in place, the artificial substrates were strung together by bright pink rope to assist in locating them relative to one another under anticipated poor visibility conditions.

The Bottom substrates were visually surveyed using 1/4 m2 quadrat frames subdivided into 25 squares equally. The quadrats were placed at the set half concrete blocks marking the Bottom substrate position during herring egg visual surveys

(Figure 7).

Evaluating Spawning

Due to poor visibility, the spawning of Pacific Herring is very difficult to observe directly. Instead, spawning Pacific Herring were located first by observations of movement of their predators on and above the water surface. Observing the movement of feeding flocks of birds and seals suggested that smaller groups of herring appeared to split from the main school, often heading in different directions towards nearshore locations crisscrossing Tomales Bay. They may have been trying to avoid predation.

Visual surveys of eggs on Artificial eelgrass, Concrete, and Bottom experimental substrates were followed by Natural Eelgrass surveys. Herring eggs were counted during a 4-hour time frame around lower tidal conditions whenever possible.

a b

c d

e Figure 7. Deploy Substrates: 30 substrates were installed per each of the two research areas within a 61m2 experimental spawning site during Mean Low Low Water. All substrates were numbered and deployed randomly, submerged with at least 1m of space, a buffer zone, around each substrate to avoid the substrates touching, and spillover or edge effects. Half concrete blocks marked Bottom substrate positions. Rock and sand filled sandbags were attached to each substrate to hold them in position. 7a. Concrete substrate being deployed 7b.Sacramento Landing deployment 7c. and 7d. Artificial Eelgrass deployment 7e. Chicken Ranch Beach deployment.

Field work typically took place at each site over a two-day period. The first day in the field was spent searching for evidence of spawning unless an observed spawning event occurred. Visual surveys consisted of counting eggs on the 30 experimental substrate replicates in the experiment site and then counting eggs in ten quadrat replicates of nearby Natural Eelgrass. Nine sets of data were collected over two herring spawning seasons at each of the experimental sites within Sacramental Landing and Chicken Ranch

Beach. Four sets of data were collected during the 2016-2017 season, and five sets of data were collected during the 2017-2018 season. SCUBA diving and snorkeling were used in the data collection process as per Freiwald et al. (2015).

Herring egg counts were accomplished by overlaying a quadrat on each of the substrates, measuring egg layers on grab samples of eelgrass blades (Spratt 1992), and counting individual eggs. Percent roe covering the quadrat (Fort et al. 2009 was estimated along with individual egg counts during the 2016-2017 spawning season). Individual counts proved preferable and counting individual eggs achievable because small amounts of eggs with less than 3 layers were typically found adhered to the experimental substrates in the research sites. In the natural eelgrass meadows sampled, spawning activity and egg counts were significantly higher than those found in the experimental substrate sites yet still considered slight. Small clusters of eggs on natural eelgrass blades, in 1-4 layers, were typical of what was found during this study (Figure 8 and Figure 9).

a b

c d

e f

g h Figure 8. Counting Pacific Herring Eggs: 8a.Observed herring spawning event 8b.,e.,f.,h. Roe on eelgrass 8c. Natural Eelgrass meadow 8g. Surveying Concrete substrate for herring eggs at low tide

Figure 9. Grab Sample: Eggs on Natural Eelgrass This grab sample of eggs on Natural Eelgrass is evaluation of layering. The photograph shows a sample with one layer of eggs. One to three egg layers were typically found. The herring eggs were individually counted throughout this project. This was possible because of relatively light spawning actvity and low density of eggs.

Herring Egg Surveys: Timing and Process

Tomales Bay field work was carried out within a day of a spawning event from

November through February (Appendix B, Table B1) during the herring spawning seasons of 2016-2017 and 2017-2018. Surveys for herring roe on vegetation were used to confirm a spawning event at the research sites before entering the water to collect data.

When I was away from Tomales Bay and could not directly observe spawning events due to work, contacts who lived on the Bay alerted me that spawning was in process. Egg counts were always done within 24 hours of spawning

When spawning was not observed, herring roe vegetation survey techniques, adapted from California Department of Fish and Wildlife Environmental Scientist Ryan

Bartling, were applied to locate freshly spawned herring roe on eelgrass. This entailed randomly tossing a metal rake head through eelgrass beds to check for the presence of herring roe. Then using the same rake technique to locate the extent of the spawning activity. Often, kayaking was used for these surveys. After checking the sites with vegetation surveys, herring roe data collection was carried out using a combination of

SCUBA, snorkeling, and beach combing as close to lower tides as possible. When directly observing herring spawning events or when informed of spawning events, searching for the presence of roe was bypassed to collect data at the research sites.

Checking for the presence or absence of roe on built structures such as pilings and other abiotic surfaces was included in the experimental design.

Overall, during the two seasons of field work, spawning events were patchy and sporadic. At times spawning occurred when water conditions were rough with poor

36 visibility disallowing data collection. Surveys were attempted or carried-out most weeks during the spawning seasons in 2016-2018 (Appendix B). Most spawning events took place between December-February. However January and February were the most productive for egg surveys and data collection when more herring spawning events occurred.

Eelgrass is notoriously difficult to work in largely because it is in typically brackish water with poor visibility. High quality dive lights were always necessary during data collection. About a third of the experimental substrates were located in the low intertidal zone and sometimes exposed during strong low tides. When this was the case, roe counts were collected on foot from those exposed substrates thus staying dry.

Additional Observations

Watanabe (2002) reported finding herring roe on abiotic structures occasionally in

Tomales Bay. So, additional visual surveys were carried out within the experimental sites, searching different habitat types in the area (e.g., non-eelgrass vegetation, sandy flats, rocks, shells, dock pilings and debris) for herring egg accumulation and distribution on other available potential substrates. This data was collected on a “present or absent” basis.

Before each herring roe survey, surface and above water marine and terrestrial mammals such as: Harbor Seals (Phoca vitulina), River Otters (Lontra canadensis), various birds among other potential herring predators were, when possible, identified and counted within an area of roughly 100 m of the experimental sites. Biodiversity below the

37 water, within and nearby the experimental sites was also identified and counted when possible (Appendix A, Table A1). Seals were counted when they appeared on the water surface only to avoid double counting.

Environmental and oceanographic conditions were tracked for planning field work and for noting conditions while collecting herring roe counts. Data sources included a Tomales Bay buoy operated by Bodega Bay Marine Laboratory, tide tables, weather reports, and a dive computer (Appendix B, Table B1). Visibility/turbidity was recorded in meters (Freiwald et al. 2015). The visibility ranged from 0 to 7m during the two seasons.

Upland water runoff into Tomales Bay during and after rains caused turbidity making field work difficult at times due to low visibility. Salinity dropped slightly after rains according to the Tomales Bay buoy data. Wind driven currents and waves created underwater surges in the afternoon at the Sacramento Landing site. This also sometimes interfered with underwater visibility. When visibility was less than 1m, the survey was abandoned and tried again later.

Depth was measured by dive computer and/or Philadelphia fiberglass 5m rod.

Field work done during low tide rarely exceeded -3.5m depth. Water temperature was between 10-13 oC and varied little as measured by dive watch.

Data Analysis

The hypothesis that Pacific Herring eggs accumulate more on natural eelgrass was tested using a Repeated Measures One-Way ANOVA (Sokal and Rohlf 2001) for 4 treatments with 10 substrates per treatment type (Artificial eelgrass, Concrete, Bottom,

38 and Natural eelgrass) at two independent sites. Nine surveys were completed at each site for a total of 18 during the 2016 -2018 herring spawning seasons. The Geisser-

Greenhouse’s epsilon correction was applied with 3 degrees of freedom (DF) because the treatment group means were found not to be normal, meaning there was no assumption of sphericity. Prism version 8.3.0 software was used to analyze data and graph the results.

A Repeated Measures One-Way ANOVA was used for this experiment because it reduces the error in the mean squares results (MS) by partitioning and reducing the impact of the background variability in field conditions on different days. The F test indicates if there is a significant difference between the treatments. The data were further analyzed using Sidak's multiple comparisons test, specifically between a) artificial eelgrass substrate and concrete substrate, and b) between artificial substrate and bottom substrate.

Additional visual surveys were carried out for the presence or absence of Pacific

Herring roe on built over-water structures such as docks with submerged piers, marine debris, rocks, shells, and driftwood. Other non-eelgrass biotic potential substrates including other vegetation were visually surveyed.

Potential herring and roe predators were counted and are summarized in

Appendix A, Table A1. Potential predators included birds, marine mammals, and invertebrates were counted by volunteers.

RESULTS

The Repeated Measures One-Way ANOVA found a highly statistically significant effect of habitat treatment at both Sacramento Landing and Chicken Ranch Beach ( F =

63.95, df = 1, 8, p< 0.0001 and F= 168.8, df=1,8, p<0.0001 respectively) strongly suggesting spawning herring lay eggs on natural eelgrass.

For each of the two experimental sites, Sacramento Landing and Chicken Ranch

Beach, herring roe count data on the artificial substrates were compared to the counts from Natural Eelgrass. In general, only slight amounts of herring roe appeared on the

Artificial Eelgrass substrate compared to nearby Natural Eelgrass.. Both Concrete substrate and Bottom substrate had miniscule traces of herring eggs. The Repeated

Measures One-Way ANOVA found a highly statistically significant effect of habitat treatment at both Sacramento Landing and Chicken Ranch Beach ( F = 63.95, df = 1, 8, p< 0.0001 and F= 168.8, df=1,8, p<0.0001 respectively). In both cases, far more eggs accumulated on Natural Eelgrass than on any of the other substrate treatments. At

Sacramento Landing (Figure 10), there was no significant difference between the number of eggs on Artificial Eelgrass versus Concrete (p = 0.13) while there was a significant difference between the number of eggs on Artificial Eelgrass and Bottom substrate (p <

0.01). At Chicken Ranch Beach (Figure 11), there was no significant difference between

Artificial Eelgrass and Concrete (p = 0.87) nor between Artificial Eelgrass and Bottom substrate (p = 0.07).

Additional visual surveys for the presence or absence of herring eggs on built structures (e.g., piers, docks, buoys) and abiotic surfaces (marine debris, rocks, discarded oyster shells, driftwood) found virtually no herring roe on either non-eelgrass natural substrate or abiotic substrate alternatives. Trace amounts of herring eggs when found outside of eelgrass beds were attached to displaced blades of eelgrass. My search for herring eggs around the experimental sites included combing beaches, caves, rocks, tree branches, shells, non-eelgrass vegetation, marine debris and built structures. An area within 300m around the experimental sites was visually surveyed for the presence or absence of herring eggs after carrying out egg counts on the experimental spawning substrates and on Natural Eelgrass.

4000

3000

2000

1000

150 140 Mean 130 120 110 100 90 Individual Egg Counts 80 70 60 50 40 30 20 10 0

Bottom Concrete

Natural Eelgrass Artificial Eelgrass

Habitat Structure Treatments

Figure 10. Sacramento Landing Site Results: Pacific Herring Mean Egg Counts vs. Habitat Structure. At a confidence level of 95%, Pacific Herring egg accumulation on Natural Eelgrass was significantly higher than the other substrates (p < 0.0001). Artificial Eelgrass substrate had higher egg accumulation than Bottom substrate (p < 0.01). No difference was found between Concrete and Artificial Eelgrass (p = 0.13).

4000

3000

2000

1000

70 Mean 60 50

Individual Egg Counts 40 30 20 10 0

Bottom Concrete

Natural Eelgrass Artificial EelgrassHabitat Structure Treatments

Figure 11. Chicken Ranch Beach Site Results: Pacific Herring Mean Egg Counts vs. Habitat Structure. At a confidence level of 95%, Pacific Herring egg accumulation on Natural Eelgrass was significantly highly than the other substrates (p < 0.0001). No difference was found between Artificial Eelgrass substrate compared to Bottom substrate p = 0.08. No difference was found between Concrete substrate compared to Artificial Eelgrass, p = 0.87.

DISCUSSION

This study shows that at two sites, Sacramento Landing and Chicken Ranch

Beach, during the 2016-2018 herring spawning seasons in Tomales Bay, California, over

9 spawning events at each site, herring eggs were found almost exclusively on natural eelgrass. This is despite the presence of alternative possible substrates, namely Artificial eelgrass, Concrete and natural Bottom substrate. Natural eelgrass had two orders of magnitude more eggs than any of the other substrates. There was 75 times as many eggs on natural eelgrass versus eggs on the Artificial eelgrass substrate. This ratio was hundreds to one for concrete and bottom substrate. Artificial eelgrass substrate was found to have magnitudes more eggs compared to the Bottom existing substrate, best described as having no structure, in the Sacramento Landing site. At Chicken Ranch Beach there was no significant difference between artificial eelgrass and bottom substrate for herring egg accumulation. I conducted additional visual surveys of abiotic and biotic potential herring egg substrate at both sites and found eggs “not present”.

The results of this study clearly support the hypothesis that herring eggs accumulate on natural eelgrass at a higher rate than other substrates. Thus the results are consistent with hypotheses that Pacific Herring and eelgrass meadows are closely linked during spawning in Tomales Bay (Hughes et al. 2014, Haegele et al. 1985). Study results support observations in Tomales Bay that Pacific Herring lay their eggs on eelgrass, consistent with decades of observations suggesting that Pacific herring might prefer eelgrass as spawning substrate (Suer 1987, Eldridge et al. 1973). Also suggested is that

44 the habitat structure eelgrass provides could be a factor in Pacific Herring spawning choices.

Accumulation of herring eggs on natural eelgrass suggest that herring prefer to spawn on natural eelgrass versus a variety of other substrates; however, this might not be the case. Previous studies have inferred that herring prefer to spawn on eelgrass based on observations of robust egg accumulation on eelgrass (Hughes et al. 2014). It could be that herring broadcast their eggs, but the eggs adhere selectively to natural eelgrass, perhaps due to the surface properties of natural eelgrass, physical and/or chemical. The few observations of Pacific herring spawning suggest that this is not the case. Haegele and

Schweigert (1985) describe observations of Pacific herring spawning in San Francisco

Bay and found the female made contact with the substrate to lay eggs by pressing her abdomen against it. Alternatively, it is possible that accumulation of eggs initially was robust on Artificial eelgrass substrate and Concrete substrate. It is also possible that

Pacific herring spawn on a variety of substrates (Hay et al. 2009). However, the eggs did not adhere very well to the Artificial eelgrass, the Concrete substrate, or the various materials found on the Bottom substrate (gravel, wood, rocks, sand, marine debris, etc.).

Or, Predation might have greatly diminished eggs on these alternative substrates before the counting eggs commenced. Also possible is that eggs washed off substrates other than natural eelgrass during heavy storm events, strong tides, and other hydrodynamic incidents. Disturbances from human activities nearshore, such as kayaking through eelgrass beds and breaking off blades with eggs could have rendered eggs more susceptible to predation in the water column or desiccation on shore. Natural eelgrass

45 accumulated eggs and the herring eggs persevered on natural eelgrass, compared to other substrates, thus giving them a chance to mature to fish.

There are few studies that examine habitat structure and herring spawning preferences. Consequently, this subject is often raised as an area that currently lacks information and needs more research (Hazen et al. 2018, Levin et al. 2016). Pacific

Herring fisheries managers have long focused on eelgrass meadows as critical nursery habitat for this reason (Penttila 2007). Emphasized throughout the Pacific Herring literature is that herring is selective in its spawning habitat yet adaptive as the same time

(Spratt 1992). For example, in San Francisco Bay, where urbanization has diminished eelgrass meadows, herring spawn on rip rap and piers of docks along Fisherman’s Wharf as well as shallow areas with eelgrass. However, over 85% of the San Francisco Bay spawning activity takes place in areas with eelgrass which is why even there the

California Department of Fish and Wildlife refers to eelgrass as substrate preference for herring and focuses monitoring on counting roe on eelgrass to estimate herring biomass annually (Eldridge et al. 1973, Suer 1987, Hazen et al. 2018, among others).

Herring spawning substrate preference possibly varies with latitude. In California, close to a dozen coastal bays and estuaries have been identified as potential spawning grounds largely because they contain eelgrass (Pacific Herring Fisheries Management

Plan 2019). Coos Bay in Oregon and a few other areas along the Tillamook coast are considered herring spawning grounds. Nearshore submerged eelgrass, other vegetation, rocks, and piers are considered preferred substrate for spawning herring by the Oregon

Department of Fish and Game. Washington State has four herring bait fisheries open

46 largely centered in the Puget Sound area. Eelgrass is diminished or has altogether disappeared due to the impacts of urbanization. Shelton et al. (2014) researched spawning herring substrate preferences using SCUBA to collect vegetation with eggs adhered in

Puget Sound. They reported no differences in spawning herring preference between eelgrass, kelp, and red algae. They also concluded that Puget Sound herring is not limited by the availability of a particular vegetation. However, they raised concerns that disappearing eelgrass could be related to collapsing herring populations in Washington

State spawning grounds. In British Columbia and Alaska, Hay et al. (2009) researched the spatial distribution of herring spawn. They considered vegetation including kelp, eelgrass, hemlock, and red algae as preferred suitable spawning substrate as well as rocks. Hay et al. communicated the need for research into the spawning substrate preferences of Pacific Herring. British Columbia and Alaska fisheries managers emphasize vegetation as preferred spawning substrate for herring (Hughes et al. 2014). At least 33 coastal bays and estuaries along the North American West Coast consider Pacific

Herring a focal species (Hughes et al. 2014). Each of these herring habitats contain some degree of eelgrass (Sherman et al. 2018).

Pacific Herring spawning on eelgrass seemingly provides an advantage to eggs compared to spawning on alternative available biotic and abiotic substrate. The herring eggs seen in this experiment were overwhelmingly present on eelgrass. Observations and unpublished data by the California Department of Fish and Wildlife (1972 – 2016) concur with these results. In Tomales Bay and San Francisco Bay, herring seek eelgrass beds for spawning even in the presence of predators. The reason for this advantage might

47 be the structure and topography of eelgrass itself. Eelgrass has longitudinal folds throughout its blades rather than a smooth surface. Plausibly, eelgrass has the ability to form a stronger bond with the adhesive herring egg such that it might better withstand separation due to turbulence from strong currents or storms and predators compared to other substrates ((Figure 12).

Observing the intensity of feeding activity by predators from above the water is the primary method used indicating where and when spawning was going on in the Bay.

Observing the fish by the movement of birds and seals, herring groups appeared to split off from the main school, heading in different directions crisscrossing the bay. They moved fast possibly to avoid predators concentrated along the main school while coming into the eelgrass beds to spawn. Predator behavior influencing Pacific Herring spawning bed selection is an area where research is needed (Fox et al. 2018, Levin et al. 2016).

Herring roe found on natural eelgrass meadows at Chicken Ranch Beach and at

Sacramento Landing area was sparse compared to historic roe counts in these spawning areas. In the early 2000s when California Department of Fish and Wildlife staff sampled eelgrass beds using ¼ m2 quadrats, 10,000 eggs with 7-9 egg layers on eelgrass blades were considered a very small trace spawn (Watanabe et al. 2003). In this study, sampling found an average of 3-4 layers of eggs distributed evenly throughout the study area’s natural eelgrass beds. Eggs largely adhered to the middle of eelgrass blades rather than near the bottom substrate or tip of the blade closer to the water’s surface. Eggs were found on unattached drifting eelgrass blades after spawning events and also eggs were

a b

Figure 12. Eelgrass Structure a. The left photograph shows an eelgrass blade with 3 day old clumps of herring eggs adhered b. The right photograph is a close up of eelgrass showing its topography to be rough and deeply grooved vertically in corduroy fashion (photograph by Ronald Coleman). The bond between herring eggs and eelgrass is strong. Detaching roe from eelgrass blades is difficult. The California Department of Fish and Wildlife rules allows for harvesting herring roe attached to eelgrass, up to 25 pounds in Tomales Bay.

49 also found on eelgrass blades washed up onto the rocky and sandy shores of the high intertidal splash zone. Roe on other types of vegetation was not seen unless on a displaced broken off blade of eelgrass. Eggs were not observed on abiotic substrate such as docks, piers, rocks, marine debris, and discarded oyster shells.

What does this mean for a future herring fishery at Tomales Bay? Loss of coastal habitat for spawning is a threat to Pacific Herring (Kennish 2002). These results support local efforts to conserve eelgrass habitat for the restoration and conservation of sustainable Pacific Herring fisheries. Restoration of wetlands in Tomales Bay might be having positive impacts on eelgrass (Kelly et al. 2017). Also suggested is that eelgrass habitat conservation could boost Pacific Herring fisheries production should commercial fishing begin again. Habitat conservation with an emphasis on maintaining eelgrass meadows for Pacific Herring would support nearshore biodiversity because of its role as a keystone species in its food web including humans. Throughout herring’s range eelgrass meadows are diminishing and how this affects Pacific Herring biomass is a concern. Data gaps with regard to this have been pointed out (Hazen et al. 2018,

Unsworth et al. 2018). Small studies such as this might shed light on contradictory results in the literature regarding the role of eelgrass habitat as a fish nursery (Sherman et al.

2018, Shelton et al. 2014).

This reinforces the recognized need for government and commercial fisheries management to incorporate a precautionary management approach to Pacific Herring which takes into account factors other than Pacific Herring as forage, market forces, and

50 economic gain. New approaches to conserving Pacific Herring might be tried. Landscape level restoration of Tomales Bay, especially mid-bay, might improve eelgrass as spawning substrate habitat thereby improving the future for Tomales Bay Pacific Herring.

Maximum sustainable yield models modified to account for biodiversity and oceanographic conditions support tepid ecological management approaches for establishing fishing quotas and will not change the decline in Pacific Herring (Thompson et al. 2017, Hazen et al. 2018, Pauly et al. 2005). Female herring are commercially fished before spawning, interrupting reproduction. Claiming that commodification of ripe fish has negligible impact on Pacific Herring abundance and recruitment makes little sense in terms of sustainability (Schweigert et al. 2010). Field sampling of herring roe and fish in eelgrass nearshore is difficult, labor intensive work. Poor visibility, common in brackish eelgrass spawning habitat, combined with winter conditions adds to the problematic nature of accurate field sampling of herring roe for biomass estimations.

The new California Department of Fish and Wildlife 2019 Fisheries Management

Plan for Pacific Herring is moving away from counting roe on eelgrass. The plan calls for undertaking different strategies for monitoring Pacific Herring that is reliant on measuring eelgrass habitat, and using rapid assessments of spawning events with visual surveys. Spawning events will be identified by the presence of herring predators and classified as small, medium, or large in intensity. The Department states that they will set herring fishing quotas at 5-10% of estimated biomass annually using Harvest Control

Rule (HCR) based maximum sustainable yield models. San Francisco Bay, the only operating commercial herring fishery in California, is the focus of the new plan with little

51 mention of Tomales Bay or other herring spawning grounds, none of which are currently commercially viable. Environmental groups in Marin County have requested that all herring fishing in Tomales Bay be discontinued. This is because of the lack of plans to resume annual monitoring of herring by the California Department of Fish and Wildlife.

The 2019 Fisheries Management Plan for Pacific Herring states that conserving enough Pacific Herring as forage is a key goal of this new plan. This goal requires research into the ecological context and the habitat complexity of eelgrass communities.

Given the current patchy nature of spawning herring in their spawning grounds, it is difficult to know if even 5% is conservative enough to protect Pacific Herring from collapses without reestablishing baseline herring biomass surveys. The plan does not mention the possibility of trying promising “no kill” roe fisheries which are gaining some traction in British Columbia where herring populations have collapsed.

Building on the specific findings of this project, next steps could involve continuing research on habitat and substrate preferences of spawning because eelgrass habitats are endangered. More research is needed on adaptive plasticity of Pacific Herring substrate choices i.e., in the absence of eelgrass does herring roe accumulate better on one or another type of vegetation?

Virtually no herring roe was observed on vegetation other than eelgrass in this study. However, herring roe had been periodically found on red algae by California

Department of Fish and Wildlife staff. Pairing substrate structure studies with predator exclusion studies could provide insight into whether predation on herring roe is more

52 intense above or below the water. This could further insight into the fish nursery role of eelgrass hypothesis.

California Department of Fish and Wildlife staff had annually conducted field surveys in Tomales Bay between 1972 – 2007 when the fishery closed due to depleted herring and falling market prices. From these surveys, the department estimated Pacific

Herring abundance along with reported landings by commercial fishing vessels.

Throughout the Bay, eelgrass meadows were represented on a map as potential spawning sites. This geographic organization of herring biomass by eelgrass spawning bed provided a detailed picture (Hardwick 1973, Spratt 1992, Watanabe et al. 2003). Given the current low fishing pressure on herring in Tomales Bay, it would be very useful to revive a geo-referenced eelgrass bed method for monitoring herring biomass.

Appendix A. Common Species List and Counts (2016 -2018)

Notes: 2016-17: The most common species observed in research Sites submerged in eelgrass beds was invasive tunicates. Tunicate (Didemnum vexillum) colonies typically blanketed exposed eelgrass blades just above the bottom substrate. 2017-18 Leopard shark were observed at all surveys. Few pelicans were seen. Less invasive tunicates were found this season but were still dominant. Moon jellies where omnipresent in water and on the shore. Periodic explosion of flatworms were observed at both research sites. Listed here are the most observed species in or near the research sites: Invertebrates Birds

Tunicate (Didemnum vexillum) Brants Cormorant (Phalacrocorax penicillatus) Tunicate (Didemnum albidum) Osprey (Pandion haliaetus) Tunicate (Botryllus schlosseri) Herring Gull (Larus smithsonianus) Barnacles (Balanus glandula) California Gull (Larus californicus) Chitin (Mopalia muscosa) Volcano Barnacles (Tetraclita serrata) Bufflehead (Bucephala albeola) Green Shore Crab (Hemigrapsus oregonnensis) Dungeness Crab (Metacarcinus magister) Brown Pelican (Pelecanus occidentalis) Pie Eyed Grebes (Podilymbus podiceps) Isopods (Caecidotea tomalensis ) Egrets (Ardea alba) Purple Shore Crab (Hemigrapsus nudus) California Mussel (Mytilus californianus) Great Blue herons (Ardea herodias) Purple Mussel (Geukensia demissa) Marine Mammals Clams (Thesus nutelli). California Sea Lion (Zalophus californianus) Limpets various Harbor Seal (Phoca vitulina) Moon Jellyfish (Aurelia labiate) River Otter (Lontra canadensis) Oysters (Crassostrea gigas) Vegetation Ochre Sea Star (Pisaster ochraceus). Red Algae (Gracilaria sp.) Rockweed (Fucus distichus) Sunburst Anemone (Anthopleura sola) Brown Algae (Sargassum muticum) Aggregating Anemone Sea Lettuce (Ulva sp.) (Anthopleura elegantissima Japanese Eelgrass (Zostera japonica)

Appendix A continued

Invertebrates Continued

Giant Green Anemone (Anthopleura xanthogrammica)

Fish

Pacific Herring (Clupea palasii) Bay Pipefish (Syngnathus leptorhynchus) Shiner Perch (Cymatogaster aggregate) Tidepool Sculpin (Oligocottus maculosus) Leopard Shark (Triakis semifasciata)

Pacific sanddab (Citharichthys sordidus)

Appendix A continued

Table A1: Summary of Species Counts Sacramento Sea Birds Other Birds Marine Mammals Fish (not Pacific Invertebrates Landing (ducks, egrets) Herring) 27 November 2016 45 7 3 20 75 28 December 2016 22 4 2 5 125 13 January 2017 65 3 5 15 86 24 January 2017 31 2 7 9 112 08 December 2017 18 8 1 4 98 03 January 2018 85 9 4 1 160 13 January 2018 55 12 2 0 63 10 February 2018 35 5 5 6 57 23 February 2018 17 8 1 4 107 Chicken Ranch Beach 12 December 2016 31 7 2 0 45 07 January 2017 22 0 3 3 68 23 January 2017 10 5 1 2 59 04 February 2017 16 0 1 10 36 06 January 2018 58 3 3 6 102 23 January 2018 35 5 2 2 31 04 February 2018 28 2 1 1 17 17 February 2018 43 3 1 0 72 28 February 2018 38 3 0 4 38

Appendix B. Field Work Schedule and Environmental Conditions: From NOAA tide tables, dive watch Used temperatures, salinity data provided by the University of California, Davis, Bodega Marine Laboratory for Tomales Bay Boon Buoy; Visibility/Turbidity was estimated using Reef Check dive procedures.

Table B1: Field Work Schedule 2016-2018 and Conditions Survey Dates Tide Level Visibility/Turbidity Temperature Temperature Salinity* Sacramento (meters) (meters) Air (oC) Water(oC) (PSU) Landing 27 November 2016 0.1 4 12.9 12.2 31.8 28 December 2016 0.1 5 11.0 10.5 28.4 13 January 2017 -0.1 3 10.9 10.5 3.4 24 January 2017 -0.0 4.5 10.7 10.4 5.3 08 December 2017 0.1 2 11.5 11.0 32.8 03 January 2018 0.2 3 11.5 11.0 33.0 13 January 2018 -0.1 6 12.2 11.5 10.9 10 February 2018 0.06 3 12.0 11.5 NA 23 February 2018 0.2 3 10.5 10.0 32.6 Survey Dates Chicken Ranch Beach 12 December 2016 0.3 2 11.5 11.0 28.4 07 January 2017 0.1 3 13.0 11.0 21.1 23 January 2017 -0.0 3 13.7 11.8 8.2 04 February 2017 0.02 3 12.0 11.8 25.4 06 January 2018 0.6 4 12.0 11.5 32.6 23 January 2018 0.5 3 11.7 11.3 30.7 04 February 2018 0.4 4 12.6 11.8 30.9 17 February 2018 0.5 4 12.3 11.5 NA 28 February 2018 0.3 3 11.0 10.8 32.8

Appendix C. Chronology of Tomales Bay Fishery

Source: California Department of Fish and Wildlife Tomales Bay Fishery (1990 – 2007 seasons) gleaned from annual Pacific Herring fishery reports.

Background Miwok tribes fished for herring around 7,000 years ago (Avery 2009, Lightfoot et al. 2009). The commercial herring fishery began operating in the 1910s and has its roots in the gold rush era (Eldridge 1973, Suer 1987). The fishery grew and industrialized throughout the last century (Eldridge et al.1973). In the 1960s, the fishing industry changed course and focused on harvesting herring (Suer 1987). CDFW staff recommended yearly commercial fishing quotas based on their field surveys, commercial fishing reported landings, and biomass predictions. The California Fish and Game Commission (FGC) ultimately made the decisions regarding herring fishing quotas for Tomales Bay. The commission heavily weighted economic factors when setting the quotas (Earthjustice 2013, Eldridge 1973). Pressure from the commercial fishing stakeholders to raise quotas when the market price of herring was high was constant (Table 1). The quota for Pacific Herring set by CDFW was usually landed in 3 – 7 days. As the fishery became depleted of larger older herring, the commission agreed to decreasing the mesh size of fishing nets from 2 ¾ inches to 2 inches over a three-year test period (1999 -2003) that extended until the fishery closed. In 2006 when the herring population was recognized as collapsed and the fishery closed, CDFW staff reported that herring was so small and few they were swimming through the commercial fishing nets (CDFW 1984-2007). The market price of herring fell to less than $300 per short ton. In perspective, herring was the equivalent of $6,000 - $7,000 per short ton in the mid-1990’s (PacFIN 2019). Abundance of herring was such that the fishing quota of about 400 tons was captured in 3 days to a week for the entire season. The herring roe fishery was a lucrative market, but this changed and market prices for herring products have been steadily declining for over a decade (PacFIN 2019, Table 1, Figure 1). The Tomales Bay herring fishery lost its status as a market resource because of low fishing effort between 2004-2006 (CDFW 2010) and the truncated age of the fish. In recent years, from their northern most spawning grounds in Alaska on down to California, fish and wildlife departments have reported Pacific Herring populations trending downward (FAO 2019). Heavily Fished seasons from 1981- 1989. 13% (1981- 1982) of CDFW projected spawning biomass landed to 36% (1987 -1988) and up to 56% biomass landed (1988-1989). After these heavily fished seasons:

Seasons Closed: 1989-1990, 1990-1991, 1991-1992 , 2007 – closed continuously Reason: Spawning Biomass fell to trace amounts on monitored eelgrass beds.

Appendix C. continued

1993-1994. CDFG estimated T. Bay spawning biomass escapement to be 42% below the 20-year average. Even so, the set the fishing quota was 10.2% (allowed a 250-ton catch) of their projection of 2,463 tons biomass. They further added that they would raise the quota to 14% if their monitoring increases the spawning biomass to 2,500 tons.

Note: They switched the seasons net regulations to 2 1/8 inches from 2.5 inches and allowed two gill nets per vessel (meaning 2 permits per vessel).

1995-1996. Spawning escarpment was projected less than the 20-year average of 4,500 tons. Yet catch allowed was 17% of the projected spawning escapement.

Another issue was the obvious shift to allow for the landings of younger herring in their ton spawning years. 2-4 (due to the 2 1/8 inch net switch). At the same time the market ex-vessel price of herring was soaring ($2500 per short ton – over $4,500 in todays’ dollars).

1996-1997. Season Closed. Spawning biomass estimated to be 586 tons, 61% lower than the 1995-1996 season and 21% below the previous 5-year average of 2,820 tons. The 20-year average spawning biomass from 1975 -1996 was 4,500. Now the department begins calling the “long term average” a 5-year average that is a spawning biomass 37% below their 20 year average they had been using to compare the abundance of the herring resource.

Appendix C. continued

1997-1998 CDFW propose a quota of 15% of the collapsing herring fishery to make up for closing it the previous year. Furthermore, they imply the rain – freshwater intrusion – is the reason for the depressed spawning. This is the opposite reaction herring has to a cut in salinity according to the literature. The price of herring was still soaring.

1998-1999 Improved biomass was reported by CDFW - reported an increase to near the 25-year average. However, they also reported that catch per unit effort was down by 50% from the 10-year average because the fish available to catch were younger and smaller and not catchable with 2 1/8” nets. Truncated age structure hinted at in prior years in the departments own data is affecting the catch. The catch was only 1.3% of the estimated herring spawning biomass. The average length of the fish caught was 10mm below the 5-year average at that time (186 mm). Good detailed T Bay eelgrass/spawn map is in this report.

1999 -2000 Spawning biomass estimate drops down to 2,011 tons which is down 68% from the 25-year average spawning biomass of 4,777 tons. CADFW report points out that eelgrass beds in Tomales Bay look very healthy having above average density and coverage. They point out that the biomass is down by 25% compared to the 7-year average of 2,678 tons. No mention of the long-term downward trend in spawning biomass. The departments quota was set at 400 tons which was 19% of the biomass estimate. 42 tons were caught leading to a townhall meeting where the commercial fishing community pushed for decreasing next seasons mesh size of the nets from 2 1/8 inches to 2 inches. Fish were too small to catch in the current regulation size nets. The department pointed out truncated age of herring in T Bay. Reported fewer fish over 4 years. The bulk of the seasons catch was between 3 – 4 ½ year old herring (the age that is the heart of the spawning years).

2000-2001. Smaller net used 2” Higher estimated spawning biomass. Quota set at 400 tons with a 7.1% exploitation proportion of 4,200 tons. Interesting that CADFW elected to go with the 2 inches, a smaller mesh, given the truncated age issue seen and the high spawning biomass projection. It was noted that over 40% of spawning took place on Gracilaria sp. The catch was 298.5 tons.

Appendix C. continued

2001-2002 CDFW set 2 inches for the mesh size of the gill nets – second year of this downsizing of the net mesh test. CADFW reports Gracilaria spp. dominated as the preferred spawning substrate; it accounted for 70% of the spawning escapement. Nothing was noted about the condition of T Bay eelgrass. However, the previous season noted that the eelgrass condition was poor. Interesting though most of the spawn was on non- eelgrass vegetation the spawning biomass was estimated to be 7.243 tons which is the highest in 20 years - since the 1982-1983 season. A hypothesis is that when the abundance of spawning herring is high, herring could be less selective about spawning substrate but will select available vegetation over built or hard surfaces. The catch was 5.1 % of the estimated spawning biomass. The price of herring was falling. The length – age of the fish was over 10 mm less, 187.7 mm, than the 197.9 mm average of 10 seasons prior.

2002 -2003 Table differentiating and comparing eelgrass and Gracilaria substrate for spawning. Table: Spawning by spawning substrate. Noted that sardine school were in the bay at the same time and place as herring schools – mixing. CADFW season analysis showed the 78 tons landed had almost 68% female with 15% roe by weight. That the herring was again characterized as smaller, younger, and female– the net size remained 2 inches. The spawning biomass estimate was 4,382 tons for this season with 1.8% caught which was a very low exploitation proportion. This represents a drop in biomass from the previous year of 39.5%. Still it was the second largest biomass since the 1992-1993 season when the fishery re-opened after being closed for three seasons. Market price was falling.

2003-2004. The net mesh size was set for 2 inches. In early February of 2004 the CDFW field monitors noted in the season write-up, “Most of the fishing activity was along the western shoreline from Duck Cove to Marshall Beach. According to fishermen, there were a lot of small fish going through the nets.” (Watanabe et al. 2004). Also noted was an increase abundance of Sea Lions. The catch was 279.9 tons with a spawn biomass estimation of 12,124. Larger fish were found at one point in the season. The department noted that the catch at time consisted of unripe females & females that had spawned and lots of males. It is curious that no statement is made about the high spawning biomass. Possible due to the low fishing effort.

Appendix C. continued 2005-2006. The net size was still 2 inches. Harbor seals were partially blamed or attributed to low fishing effort because they were crowding fishing nets. Vegetation transects were carried out. “The goal of using the ROV was to observe the red algae Gracilaria sp. distribution and density in areas of Tomales Bay due to the growing importance of Gracilaria sp. as a spawning substrate for herring in Tomales Bay. Distribution and abundance of Gracilaria sp. can fluctuate from season to season. Based on observations from recent seasons, Gracilaria sp. seems to have become more intermixed with the eelgrass beds in Tomales Bay. The catch was 30 tons of the spawning escapement of 3,686 tons, 0.8% exploited. The ex-vessel price of herring this season was about $220 per short ton (2,000 lbs.).

2006-2007. This was the last season CDFW reported with detailed on Pacific Herring. No spawning survey was actually carried out in Tomales Bay. This report changed abruptly in character and in detail. It lacked the careful specifics on spawning by specific location using the numbered beds key and maps. It only briefly calls out spawning locations but does not present a table of this activity as was done in prior years. It fails to update the 2” gill net mesh size study data and it fails to break down the catch by the multi-panel research net in Tomales Bay. No herring samples were collected and processed so the age structure of the herring resource for this season suddenly disappears from this report. Watanabe is not involved in this report. Ryan Bartling took over the job. He holds a B.S. in Biology and started working for CDFW in the 2000-2001 season. Changes in staffing levels along with low market prices and a low fishing effort of only two vessels participating are reasons given for the abbreviated report and Tomales Bay monitoring. It was noted that the herring this season were small and swimming through nets. Most of the fishing activity was reported along the western shoreline from Duck Cove to Marshall Beach. According to fishermen, there were lots of small fish going through the nets. Spawning biomass was down from the previous season, estimated to be 2,436 tons with 1.2 % caught. Several net sets were made using a multi-panel research net. But only two herring were caught. The two active permittees, and the herring buyer believed the fish were uncatchable due to their small size. Numerous anecdotal reports were given of herring “swimming through nets.” Based on previous records, the buyer reported that fish were of average length but underweight. Tim Furlong, of Garofalo Fish Company, reported that female herring landed in December weighed on average 3.2-3.3 ounces (90-94grams), down from the historical average of 3.6-3.7 ounces (102-105 grams). This report marked the closure of the Tomales Bay fishery

REFERENCES

Anderson, E.M., Lovvorn, J.R., Esler, D., Boyd, W.S., Stick, K.C. 2009. Using predator

distributions, diet, and condition to evaluate seasonal foraging sites: sea ducks

and herring spawn. Marine Ecology Progress Series 386: 287-302.

Audubon California. 2018. Eelgrass, herring, and waterbirds in San Francisco Bay: a

threats and opportunities assessment. Report to the Gordon and Betty Moore

Foundation. Richardson Bay Audubon Center & Sanctuary. Tiburon, California.

Avery, C. 2009. Tomales Bay Environmental History and Historic Resource Study: Point

Reyes National Seashore. Pacific West Region, National Park Service, U.S.

Department of the Interior.

Bartling, R. 2007. Summary of the 2006-2007 Pacific Herring Spawning Season and

Commercial Catch in Tomales Bay. California Department of Fish and Game

Pacific Herring Research Project.

https://www.wildlife.ca.gov/Fishing/Commercial/Herring/Season-Summaries

Bell, J.D., Westoby, D., Steffe, A.S. 1987. Fish larvae settling in seagrass: do they

discriminate between beds of different leaf density? Journal of Experimental

Marine Biology and Ecology 111:133-144.

Beverton, R.J. 1990. Small marine pelagic fish and the threat of fishing; are they

endangered? Journal of Fish Biology 37: 5-16.

Blaxter, J.H.S. and Hunter J.R. 1982. The biology of clupeid fishes. Advances in

Marine Biology 20:1- 223.

Boldt, J.L., Thompson, M., Rooper, C.N., Hay, D.E., Schweigert, J.F., Quinn II, T.J.,

Cleary, J.S., Neville, C.M. 2019. Bottom-up and top-down control of small

pelagic forage fish: factors affecting age-0 herring in the Strait of Georgia, British

Columbia. Marine Ecology Progress Series 617: 53-66.

Californa Department of Fish and Wildlife (CDFW). 1984-2007. Tomales Bay Annual

Pacific Herring Status Reports.

https://www.wildlife.ca.gov/Fishing/Commercial/Herring/Season-Summaries

Californa Department of Fish and Game. 2001. California's Living Marine Resources: A

Status Reports. https://www.wildlife.ca.gov/Fishing/Commercial/Herring/Season-

Summaries

Carolsfeld, J., Tester, M., Kreiberg, H., Sherwood, N.M. 1997. Pheromone-induced

spawning of Pacific herring. Hormones and behavior 31:256-268.

Cury, P., Bakun, A., Crawford, R.J.M., Jarre, A., Quin ̃ones, R.A., Shannon, L.J.,

Verheye, H.M. 2000. Small pelagics in upwelling systems: patterns of interaction

and structural changes in ‘‘wasp-waist’’ ecosystems. ICES Journal of Marine

Science 57: 603–618.

Dickey-Collas, M., Nash, R.D.M., Brunel,T., Damme, C.J., Van, G., Marshall, C.T.,

Payne, M.R., Corten, A., Geffen, A.J., Peck, M.A., Hatfield, E.M.C., Hintzen,

N.T., Enberg, K., Kell, L.T., Simmonds E.J. 2010. Lessons learned from stock

collapse and recovery of North Sea herring: a review. ICES Journal of Marine

Science 67: 1875–1886.

EarthJustice, Audubon California, Oceana, Golden Gate Audubon, and Santa Clara

Valley Audubon, 2012. Attorney Letter to California Department of Fish and

Wildlife Re: Pacific herring collapses. Comments on the supplemental

environmental document for the commercial herring fishery 2012-2013.

California Fish and Game Commission,California Department of Fish and

Wildlife. 2013. Final Supplemental Environmental Document (FSED), Pacific

Herring Commercial Fishing Regulations (Sections 163, 163.5, and 164, Title 14,

California Code of Regulations). Edited by State of California. The Natural

Resources Agency. https://www.wildlife.ca.gov/Fishing/Commercial/Herring

Emmett, R.L.1991. Distribution and Abundance of Fishes and Invertebrates in West

Coast Estuaries: Species life history summaries. US Department of Commerce,

National Oceanic and Atmospheric Administration, National Ocean Service. Vol.

55.

Eldridge, M.B. and Kaill, W.M. 1973. San Francisco Bay area’s herring resource: A

colorful past and a controversial future. Marine Fisheries Review 35:25-31.

Erisman, B.E., Allen, L,G., Claisse, J.T., Pondella, D.J., Miller, E.F., Murray, J.H. 2011.

The illusion of plenty: hyperstability masks collapses in two recreational fisheries

that target fish spawning aggregations. Canadian Journal of Fisheries and Aquatic

Sciences 68:1705-1716.

Essington, T.E., Moriarty, P.E., Froehlich, H.E., Hodgson, E.E., Koehn, L.E., Oken,

K.L., Siple, M.C., Stawitz, C.C. 2015. Fishing amplifies forage fish population

collapses. Proceedings of the National Academy of Sciences of the United States

of America 112:6648-6652.

Federal Register 73 FR 19824 04/11/2008. E8-7797:19824-19825

https://www.federalregister.gov/documents/2008/04/11/E8-7797/endangered-and-

threatened-species-notice-of-finding-on-a-petition-to-list-the-lynn-canal-

population

Flostrand, L.A., Schweigert, J.F., Daniel, K.S., Cleary, J.S. 2009. Measuring and

modelling Pacific herring spawning-site fidelity and dispersal using tag-recovery

dispersal curves. ICES Journal of Marine Science 66:1754-1761.

Food Agricultural Organization of The United Nations (FAO). 2018. The State of World

Fisheries and Aquaculture 2018 - Meeting the sustainable development goals.

Rome ISBN: 978-92-5-130562-1

Food Agricultural Organization of The United Nations (FAO)., 2018 . GlobeFish. 2019

Statistics Retrieval. www. UNFAO GlobeFish.org Retrieval 2019.

Fort, C., Daniel, K., Thompson, M. 2009. Herring Spawn Survey Manual. Unpublished

Report. Department of Fisheries and Oceans Vancouver Canada.

http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.214.5948&rep=rep1&t

ype=pdf

Fox, C.H., Paquet, P.C., Reimchen,T.E. 2018. Pacific herring spawn events influence

nearshore subtidal and intertidal species. Marine Ecology Progress Series 595:

157-169.

Freiwald, J., Wisniewski, C., Wehrenberg, M., Shuman, C., Dawson C. 2015. Reef Check

California Instruction Manual: A Guide to Rocky Reef Monitoring, 8th Edition.

Reef Check Foundation, Pacific Palisades, CA, USA.

https://reefcheck.org/PDFs/REEF%20CHECK%20CALIFORNIA_Manual%208t

h%20Edition%202015-web.pdf

Froese R. and Pauly D. (eds). (2019). FishBase (version Feb 2018). In: Species 2000 &

ITIS Catalogue of Life, 2019 Annual Checklist (Roskov Y., Ower G., Orrell T.,

Nicolson D., Bailly N., Kirk P.M., Bourgoin T., DeWalt R.E., Decock W.,

Nieukerken E. van, Zarucchi J., Penev L., eds.). Digital resource at

www.catalogueoflife.org/annual-checklist/2019. Species 2000: Naturalis, Leiden,

the Netherlands Retrieval 2019.

Funk, F.J., Blackburn, D., Hay, A.P., Stephenson, R., Toreson, R., Witherell D. 2001.

Herring: expectations for a new millennium. University of Alaska Sea Grant

College Program. AK-SG-01-04, Fairbanks.

Gardali, T., Kelly, J.P., Evens, J. 2011. Tomales Bay Watershed Species of Local

Interest: native and non-native species of conservation or management concern. A

Report of the Tomales Bay Watershed Council, Box 447, Point Reyes Station, CA

94956. https://www.egret.org/sites/default/files/gardali_etal_2011_tbwc_soli.pdf

Gauvreau, A., Lepofsky, D., Rutherford, M., Reid, M. 2017. Everything revolves around

the herring: the Heiltsuk–herring relationship through time. Ecology and Society

22:10.

Ha, G. and Williams, S.L. 2018. Eelgrass community dominated by native omnivores in

Bodega Bay, California, USA. Bulletin of Marine Science 94:1333-1353.

Haegele, C. and Schweigert, J. 1985a. Estimation of egg numbers in Pacific herring

spawns on giant kelp. North American Journal of Fisheries Management 5:65-71.

Haegele, C. and Schweigert, J. 1985b Distribution and characteristics of herring

spawning grounds and description of spawning behavior. Canadian Journal of

Fisheries and Aquatic Sciences 42:39-55.

Hardwick, J.E. 1973. Biomass estimates of spawning herring, Clupea harengus pallasii,

herring eggs, and associated vegetation in Tomales Bay. California Fish and

Game 59:36–61.

Hart, J.L. and Tester, A.L. 1934. Quantitative studies on herring spawning. Transactions

of the American Fisheries Society 64:307-312.

Hay, D.E. 1985. Reproductive biology of Pacific Herring (Clupea harengus pallasii).

Canadian Journal of Fisheries and Aquatic Sciences 42:111-126.

Hay, D.E., McCarter, P.B., Daniel, K.S., Schweigert, J.F. 2009. Spatial diversity of

Pacific herring (Clupea pallasii) spawning areas. ICES Journal of Marine Science

66:1662-1666.

Hazen, E., Okamoto, D., Selden, R., Szuwalski ,C. 2018. Final report of the scientific and

technical review panel: Scientific review of the draft Fishery Management Plan

for Pacific herring (Clupea pallasii). California Ocean Science Trust, Oakland,

CA. October.

Heck Jr, K.L. 2019. Seagrass Ecosystems: A career-long quest to understand their inner

workings. Gulf and Caribbean Research 30:ii-xv.

Heck Jr, K.L., Hays, G., Orth, R.J. 2003. Critical evaluation of the nursery role

hypothesis for seagrass meadows. Marine Ecology Progress Series 253:123-136.

Horn, M.H. and Ferry-Graham, L.A. 2006. Feeding mechanisms and trophic interactions.

Chapter 14, pp. 387-410. In: The Ecology of marine fishes: California and

adjacent waters. Allen, L.G., Pondella II, D.J., Horn, M.H. eds. University of

California Press, Berkeley.

Hoshikawa, H.K.,Tajima, I., Kawai, T., Ohtsuki T. 2001. Spawning bed selection by

Pacific herring (Clupea pallasii) at Atsuta, Hokkaido, Japan. Herring:

Expectations for a New Millennium. University of Alaska Sea Grant,

Fairbanks:199-226.

Hubbard, J. 2018. Fisheries biology and the dismal science: economists and the

rational exploitation of fisheries for social progress, pp. 31-61. In: Fisheries,

Quota Management and Quota Transfer . Springer, Cham. Switzerland

Hughes, B.B., Levey, M.D., Brown, J.A., Fountain, M.C., Carlisle, A.B., Litvin, S.Y.,

Greene, C.M., Heady,W.N., Gleason, M.G. 2014. Nursery Functions of U.S. West

Coast Estuaries: The State of Knowledge for Juveniles of Focal Invertebrate and

Fish Species. The Nature Conservancy, Arlington, VA.

Hyndes, G.A., Francour, P., Guidetti, P., Heck, K.L., Jenkins, G. 2018. The roles of

seagrasses in structuring associated fish assemblages and fisheries, pp. 589-

627. In: Seagrasses of Australia Structure, Ecology and Conservation,

Springer, Cham., Switzerland

Incardona, J.P., Vines, C.A., Anulacion, B.F., Baldwin, D.H., Day, H.L., French, B.L.,

Labenia, J.S., Linbo, T.L., Myers, M.S., Olson, O.P., Sloan, C.A., Sol, S., Griffin,

F.J., Menard, K., Morgan, S.G., West, J.E., Collier, T.K.,Ylitalo, G.M., Cherr,

G.N., Scholz, N.L. 2012. Unexpectedly High Mortality in Pacific Herring

Embryos Exposed to the 2007 Cosco Busan Oil Spill in San Francisco Bay.

Proceedings of the National Academy of Sciences of the United States of America

109:51-58.

Jennings, S., Kaiser, M.J., Reynolds, J.D. 2001. Marine Fisheries Ecology. Blackwell,

Oxford.

IUCN 2018. The IUCN Red List of Threatened Species. Version 2019-2.

http://www.iucnredlist.org. Retrieval 2018.

Kelly, J.P., Rothenbach, C.A., Weathers, W.W. 2018. Echoes of numerical dependence:

responses of wintering waterbirds to Pacific herring spawns. Marine Ecology

Progress Series 597: 243-257.

Kennish, M.J. 2002. Environmental threats and environmental future of estuaries.

Environmental Conservation 29:78–107.

Koehn, L.E., Essington, T.E., Marshall, K.N., Sydeman, W.J., Szoboszlai, A.I., Thayer,

J.A. 2017. Trade-offs between forage fish fisheries and their predators in the

California Current. ICES Journal of Marine Science 74:2448-2458.

Konar, M., Qiu, S., Tougher, B., Vause, J., Tlusty, M., Fitzsimmons, K., Barrows, R.,

Cao, L. 2019. Illustrating the hidden economic, social and ecological values of

global forage fish resources. Resources, Conservation and Recycling 151:104456.

Laakkonen, H.M., Lajus, D.L.,Strelkov, P.,Väinölä, R. 2013. Phylogeography of amphi-

boreal fish: tracing the history of the Pacific herring Clupea pallasii in North-East

European seas. BMC Evolutionary Biology 13:67.

Lam, M.E., Pitcher, T.J., Surma, S., Scott, J., Kaiser, M., White, A.S., Pakhomov, E.A.,

Ward, L.M. 2019. Value-and ecosystem-based management approach: The

Pacific Herring Fishery Conflict. Marine Ecology Progress Series 617:341-364.

Lassuy, D.R. 1989. Species profiles: life histories and environmental requirements of

coastal fishes and invertebrates (Pacific Northwest)--Pacific herring. U.S. Fish

Wildlife Service Bioliological Report 82 (11.126). U.S. Army Corps of Engineers

TR-EL-82-4.

Levin, P.S., Essington, T.E., Marshall, K.N., Koehn, L.E., Anderson, L.G., Bundy, A.,

Carothers, C., Coleman, F., Gerber, L.R., Grabowski, J.H., Houde, E., Jensen,

O.P., Möllmann, C., Rose, K., Sanchirico, J.N., Smith, A.D.M. 2018. Building

effective fishery ecosystem plans. Marine Policy 92:48–57

Levin, P.S., Francis, T.B., Taylor, N.G., 2016. Thirty-two essential questions for

understanding the social–ecological system of forage fish: the case of Pacific

Herring. Ecosystem Health and Sustainability 2:e01213.

Lightfoot, K.G. and Parrish, O. 2009. California Indians and their environment: an

introduction (No. 96). Univ of California Press.

Liu, J.X., Tatarenkov, A., Beacham, T.D., Gorbachev, V., Wildes, S., Avise, J.C. 2011.

Effects of Pleistocene climatic fluctuations on the phylogeographic and

demographic histories of Pacific herring (Clupea pallasii). Molecular ecology

20:3879-3893.

Marin Journal, 11 January 1917. Tomales Herring Source of Wealth 55:1

https://cdnc.ucr.edu/?a=d&d=MJ19170111.2.14&e=------en--20--1--txt-txIN-----

---1

McKechnie, I., Lepofsky, D., Moss, M.L., Butler, V.L., Orchard, T.J., Coupland, G.,

Foster, F., Caldwell, M., Lertzman, K. 2014. Archaeological data provide

alternative hypotheses on Pacific herring (Clupea pallasii) distribution,

abundance, and variability. Proceedings of the National Academy of Sciences

111:E807-E816.

Merkel and Associates. 2017. Tomales Bay Eelgrass Inventory. Report #05-024-38.

www.merkelinc.com

Moll, D., Kotterba, P., Von Nordheim, L., Polte, P. 2018. Storm-induced Atlantic

herring (Clupea harengus) egg mortality in Baltic Sea inshore spawning

areas Estuaries and Coasts 41:1-12.

Moran, J.R., Heintz, R.A., Straley, J.M., Vollenweider, J.J. 2018. Regional variation in

the intensity of humpback whale predation on Pacific herring in the Gulf of

Alaska. Deep Sea Research Part II: Topical Studies in Oceanography 147:187-

195.

Murphy, M.L., Johnson, S.W., Csepp, D.J. 2000. A Comparison of Fish Assemblages in

Eelgrass and Adjacent Subtidal Habitats near Craig, Alaska. Alaska Fishery

Research Bulletin 7:11–21.

Okamoto, D.K., Hessing-Lewis, M., Samhouri, J.F., Shelton, A.O., Stier, A., Levin, P.

Salomon, A.K. 2018. Spatial variation in exploited metapopulations obscures risk

of collapse. BioRxiv 2018:315481.

Olyarnik, S., 2006. Seagrass beds in Tomales Bay: The Unsung Heroes of Habitat.

Bodega Marine Laboratory UC Davis Evenning Lecture.

https://nmsfarallones.blob.core.windows.net/farallones-

prod/media/archive/eco/tomales/pdf/tomalesbay_seagrass_lecture.pdf

Pacific Fisheries Information Network (PacFIN) Pacific States Marine

Fisheries Commission, Portland, Oregon 2019 retrieval www.psmfc.org

Palsson, W.A. 1984. Egg Mortality Upon Natural and Artificial Substrate Within

Washington State Spawning Grounds of Pacific Herring (Clupea harengus

Pallasii). MSc Thesis, University Washington. DOI: 10.1002/aqc.2757

Pauly, D. and Zeller D. (Editors). 2015. Sea Around Us Concepts, Design and Data

www.seaaroundus.org Retrieval 2019.

Pauly, D. and Palomares, M.L. 2005. Fishing down marine food web: it is far more

pervasive than we thought. Bulletin of Marine Science 76:197-212.

Penttila, D. 2007. Marine forage fishes in Puget Sound. Puget Sound Nearshore

Partnership Report No. 2007- 03. Published by Seattle District, U.S. Army Corps

of Engineers, Seattle, Washington.

Plummer, M.L., Harvey, C.J., Anderson, L.E., Guerry, A.D., Ruckelshaus, M.H. 2013.

The role of eelgrass in marine community interactions and ecosystem services:

results from ecosystem-scale food web models. Ecosystems 16:237-251.

Reum, J.C.P., Essington, T.E., Greene, C.M., Rice, C.A., Fresh, K.L. 2011. Multiscale

influence of climate on estuarine populations of forage fish: the role of coastal

upwelling, freshwater flow and temperature. Marine Ecology Progress Series

425:203–215.

Sadovy, Y. 2005. The threat of fishing to highly fecund fishes. Journal of Fish Biology

59: 90-108.

Sanchez, G.M., Gobalet, KW., Jewett, R., Cuthrell, R.Q., Grone, M., Engel, P.M.,

Lightfoot, K.G. 2018. The historical ecology of central California coast fishing:

Perspectives from Point Reyes National Seashore. Journal of Archaeological

Science 100:1-15.

Schweigert, J., Haegele, C., Stocker, M. 1985. Optimizing sampling design for herring

spawn surveys in the Strait of Georgia, BC. Canadian Journal of Fisheries and

Aquatic Sciences 42:1806-1814.

Schweigert, J.F., Boldt, J.L., Flostrand, L., Cleary, J.S. 2010. A review of factors limiting

recovery of Pacific herring stocks in Canada. ICES Journal Marine Science 67:

1903–1913.

Scofield, W.L. 1952. The Tomales Bay Herring Fishery. California Fish and Game

38:499–504.

Seafood Watch 2019. www.SeafoodWatch.org

Shelton, A.O., Francis, T.B., Williams, G.D., Feist, B., Stick, K., Levin, P.S. 2014.

Habitat limitation and spatial variation in Pacific herring egg survival. Marine

Ecology Progress Series 514:231-245.

Sherman, K. and DeBruyckere, L.A. 2018. Eelgrass habitats on the U.S. West Coast.

State of the Knowledge of Eelgrass Ecosystem Services and Eelgrass Extent. A

publication prepared by the Pacific Marine and Estuarine Fish Habitat Partnership

for The Nature Conservancy. http://www.pacificfishhabitat.org/wp-

content/uploads/2017/09/EelGrass_Report_Final_ForPrint_web.pdf

Sinclair, M.M. and Smith, T.D. 2002. The notion that fish species form stocks. In ICES

Marine Science Symposia 215: 297-304.

Siple, M., Shelton, A.O., Francis, T.B., Lowry, D., Lindquist, A.P., Essington, T.E. 2018.

Age truncation and portfolio effects in Puget Sound Pacific herring. 2018. Salish

Sea Ecosystem Conference 551

https://cedar.wwu.edu/ssec/2018ssec/allsessions/551

Sokal, R.R. and Rohlf, F.J. 2001. Biometry: The Principles and Practice of Statistics in

Biological Research 3rd Edition WH Freeman and Co. New York, USA.

Speller, C.F., Hauser, L., Lepofsky, D., Moore, J., Rodrigues, A.T., Moss, M.L.,

McKechnie, I.,Yang, D.Y. 2012. High potential for using DNA from ancient

herring bones to inform modern fisheries management and conservation. PLOS

One 7:e51122.

Spratt, J.D. 1987. Biological characteristics of the catch from the 1986-87 Pacific herring,

Clupea harengus pallasi, roe fishery in California. California Fish and Game

73:132-138.

Spratt, J.D. 1989. The distribution and density of eelgrass, Zostera marina, in Tomales

Bay, California. California Department of Fish and Game.

Spratt, J.D. 1992. The evolution of California's Herring roe fishery: Catch allocation,

limited entry, and conflict resolution. California Fish and Game 78:20-44.

Stacey, N.E., Hourston, A.S. 1982. Spawning and Feeding Behavior of Captive Pacific

Herring, Clupea harengus pallasii. Canadian Journal of Fisheries and Aquatic

Sciences 39:489- 498.

Suer, A.L. 1987. The Herring of San Francisco and Tomales Bays. The Ocean Research

Institute San Francisco, California 3-64.

Surma, S., Pitcher, T.J., Kumar, R., Varkey, D., Pakhomov, E.A., Lam, M.E. 2018.

Herring supports Northeast Pacific predators and fisheries: Insights from

ecosystem modelling and management strategy evaluation. PLOS One

1: e0196307.

Szoboszlai, A.I., Thayer, J.A., Wood, S.A., Sydeman, W.J., Koehn, L.E. 2015. Forage

species in predator diets: synthesis of data from the California Current. Ecological

Informatics 29:45–56.

Thompson, S.A., Sydeman, W.J., Thayer, J.A., Weinstein, A., Krieger, K.L. 2017. Trends

in the Pacific herring (Clupea pallasii) metapopulation in the California Current

Ecosystem. California Cooperative Oceanic Fisheries Investgations Reports

58:77–94.

Unsworth, R.K.F., Nordlund, L.M., Cullen-Unsworth, L.C. 2019. Seagrass Meadows

Support Global Fisheries Production. Conservation Letters 12:e12566.

Watanabe, R.T. and Spilseth, S. A. 2003. Summary of the 2002-2003 Pacific Herring

Spawning Season and Commercial Catch in Tomales Bay. California Department

of Fish and Game Pacific Herring Research Project.

https://www.wildlife.ca.gov/Fishing/Commercial/Herring/Season-Summaries

Watters, D.L., Brown, H.M., Griffin, F.J., Larson, E.J., Cherr, G.N. 2004. Pacific Herring

spawning grounds in San Francisco Bay: 1973–2000. American Fisheries Society

Symposium 39:3–14.

Xu, Y., Fu, C., Peña, A., Hourston, R., Thomson, R., Robinson, C., Cleary, J., Daniel, K.

Thompson, M. 2019. Variability of Pacific herring (Clupea pallasii) spawn

abundance under climate change off the West Coast of Canada over the past six

decades. Journal of Marine Systems 200:103229.

Zostera Experimental Network (Project ZEN) www.zenscience.org 2019 retrieval.