Fish community responses to ecosystem stressors in coastal estuarine wetlands: a functional basis...

ORIGINAL PAPER

Fish community responses to ecosystem stressors in coastalestuarine wetlands: a functional basis for wetlandsmanagement and restoration

Sharook P. Madon

Received: 14 December 2006 / Accepted: 18 November 2007 / Published online: 6 December 2007

� Springer Science+Business Media B.V. 2007

Abstract Functional responses of estuarine fish

species to environmental perturbations such as wet-

land impoundment, changes in water quality, and

sediment accretion are investigated. The study

focuses on the feeding, growth and habitat use by

California killifish (Fundulus parvipinnis), topsmelt

(Antherinops affinis), and juvenile California halibut

(Paralichthys californicus) in impacted coastal wet-

lands to provide an ecological basis for guidance on

the management and restoration of these ecosystems.

The ecology of California killifish, Fundulus parvi-

pinnis, is closely tied with the marsh surface, which

they access at high tide to feed and grow. Field

estimates of food consumption show that killifish can

increase their food intake by two-fold to five-fold by

adding marsh surface foods to their diet. Bioenerget-

ics modeling predicts that killifish can grow over an

order of magnitude faster if they add intertidal marsh

surfaces to their subtidal feeding areas. Tidal inlet

closures and increased marsh surface elevations due

to sediment accretion can restrict killifish access to

the marsh surface, affecting its growth and fitness. An

open tidal inlet and tidal creek networks that allow

killifish to access the marsh at high tide must be

incorporated into the restoration design. Topsmelt

and California halibut are also adversely affected by

tidal inlet closures. Food consumption rates of

topsmelt are 50% lower when the tidal inlet is closed,

compared to when the estuary is tidally-flushed. Tidal

inlet closures inadvertently induce variations in water

temperature and salinity and negatively affect growth

of juvenile California halibut. Tidal creek networks

which consist of channels and creeks of various

orders are also important to halibut. Large halibut

([200 mm TL) inhabit deeper, high order channels

for thermal refuge, while small halibut (\120 mm

TL) are abundant in lower order channels where they

can feed on small-sized prey which are typically less

abundant in high order channels. Maintaining an open

tidal inlet, implementing sediment management pro-

grams and designing coastal wetlands with tidal creek

networks adjacent to intertidal salt marsh habitat (for

fish access) are key elements that need to be

considered during the planning and implementation

of coastal wetland restoration projects.

Keywords Salt marshes � Lagoons �Indicators of anthropogenic stressors �Estuaries � Fish ecology

Introduction

Coastal wetlands in southern California have expe-

rienced substantial anthropogenic alterations in the

S. P. Madon (&)

Water Resources and Environmental Management

Practice, Ecosystem Planning and Restoration, CH2M

HILL, Inc, 402 W. Broadway, Suite 1450, San Diego,

CA 92101, USA

e-mail: [email protected]

123

Wetlands Ecol Manage (2008) 16:219–236

DOI 10.1007/s11273-007-9070-6

past century. Increased human populations along the

coast have led to an accelerated loss of wetland

habitat and resulted in the fragmentation of remnant

coastal wetland habitats (Zedler 2001). Most wet-

lands along the southern California coast are bisected

by railroad tracks and roadways, and compromised

by the development of housing complexes, marinas,

docks, tide gates, culverts and dikes (Zedler 1996a,

2001). As a result, the tidal prism in these wetlands is

greatly reduced, often causing the ocean inlets to

close, with resultant changes in water quality and

water level (PERL 1990; Zedler et al. 1992, Zedler

1996a, 2001) that can negatively affect wetland biota

(Nordby and Zedler 1991). Most of the region’s

coastal wetlands have closed to tidal flushing peri-

odically, and sometimes for several months (Zedler

2001). Episodic sedimentation is also a problem in

these wetlands (Zedler et al. 1992, Zedler 2001), with

sediment accretion rates in excess of 1 cm yr-1 at

certain sites (Onuf 1987; Callaway and Zedler 2004;

Thrush et al. 2004; Wallace et al. 2005). High

sedimentation rates can have profound effects on

estuarine biota. Episodic deposition of sediments, on

one hand, can directly cause mortality of benthic

organisms via smothering. More subtle effects of

sediment accretion include increases in marsh surface

elevations and subsequent changes in marsh inunda-

tion patterns that affect use of the marsh surface by

fish during high tides (West and Zedler 2000; Madon

et al. 2001).

Wetland mitigation, restoration and creation prac-

tices are increasingly being used to compensate for

anthropogenic impacts to coastal ecosystems and for

the loss of wetland habitats (Zedler 1996b). Often, a

major goal of such projects is to provide habitat and

support a variety of ecological functions for fish

populations including feeding, nursery support and

refuge from predators (Zedler et al. 1997; Williams

and Zedler 1999). Coastal wetlands in southern

California support unique fish assemblages valued

for their contribution to the region’s biodiversity and

food web support (Onuf et al. 1979; Swift et al. 1993;

Horn and Allen 1985; Kwak and Zedler 1997; Horn

et al. 1999). Studies have shown that among other

factors, the composition of these fish assemblages is

related to channel habitat characteristics and channel

morphometry (Williams and Zedler 1999; Desmond

et al. 2000). Thus, restoration projects that are

planned and implemented to more closely

approximate the hydrogeomorphic characteristics of

a natural marsh would likely provide greater func-

tional support to fish communities than those that

lack these important habitat features.

Assessment of restoration projects that utilize

better estimates of fish habitat function based on

feeding, growth and individual and community-based

species trends, rather than commonly used measures

such as species diversity and abundance has also been

recommended (Williams and Zedler 1999). Scientists

and restoration practitioners generally agree that

mitigation and restoration should be modeled on

natural systems and functional processes (Brinson

and Rheinhardt 1996). However, some restoration

projects in southern California have simply involved

the excavation of deep sub-tidal basins or channels

for fish habitat, rather than intertidal creek networks

seen in natural systems (Zedler 2001). Due to the lack

of intertidal creek networks, these designs have little

marsh-creek connectivity and a highly reduced

marsh–water interface, and may curtail use of the

marsh surface by fish during high tides (West and

Zedler 2000; Madon et al. 2001).

The need for a set of guiding principles for coastal

wetland restoration and management practices is

acute, especially in the heavily urbanized southern

California region. For restoration to be a success, it is

critical that ecologically meaningful elements are

incorporated into the restoration design and that

management practices are based on supporting eco-

logical function.

This study shows how investigations of functional

responses of estuarine fish species to specific envi-

ronmental perturbations can be effectively used to

guide the restoration and management of coastal

wetlands. The three species, California killifish,

topsmelt and California halibut, represent various

trophic levels in the estuarine food web and together

provide a broad representation of the diversity of

ecological function in the fish community. For

example, the California killifish, Fundulus parvipin-

nis, is a year-round salt marsh resident, and can be

classified as a secondary consumer, primarily feeding

on macroinvertebrates in subtidal channels and the

marsh surface. The topsmelt, Antherinops affinis, is a

pelagic schooling species common in estuaries and

nearshore coastal waters in southern California.

Juvenile topsmelt are primarily secondary consumers

and feed on macroinvertebrates, switching to a diet

220 Wetlands Ecol Manage (2008) 16:219–236

123

consisting of macroalgae (primary consumers) as

adults. The California halibut, Paralichthys califor-

nicus, is a coastal marine species that primarily uses

estuaries and lagoons as nursery areas for refuge from

predation and to support feeding and growth of

juveniles. Newly settled juvenile halibut (\50 mm

total length, TL) are primarily secondary consumers

that feed on macroinvertebrates, but switch to a

piscivorous diet (tertiary consumers) at larger sizes.

Juvenile halibut spend from 1 to 2 years in estuaries

and lagoons, moving back into coastal marine

environments once they reach a size of approximately

200–250 mm TL.

The objectives of this study are, (1) to evaluate

feeding, growth and habitat use by California killi-

fish, topsmelt and California halibut in coastal

wetlands impacted by tidal inlet closures, excessive

sedimentation, sharp variations in water quality, and

disruption of tidal inundation patterns, and (2) to use

what is learnt from these assessments as an ecological

basis for guidance on the restoration and management

of these wetlands.

Materials and methods

Study sites

Fish were sampled at two estuarine locations in San

Diego County, California: the Tijuana River

National Estuarine Research Reserve (henceforth

called Tijuana Estuary) and Los Penasquitos

Lagoon (Fig. 1). Tijuana Estuary is located just

north of the U.S.-Mexico border (32�340 N,

117�70 W) and at 1024 ha is one of the largest

remaining estuarine salt marshes in southern Cali-

fornia. Unlike other estuarine systems in southern

California, where salt marshes areas are criss-

crossed by railroad lines and roadways that affect

the tidal prism and cause frequent closures of the

tidal inlet, Tijuana Estuary’s salt marsh habitat is

one of the least fragmented and has remained

almost continuously open to tidal circulation

(Zedler 2001). Approximately three-fourths of

Tijuana Estuary’s watershed, however, lies in

Mexico, where increasing human populations,

unstable slopes and soils, inadequate sewer systems

and agricultural runoff contribute to water quality

problems and high sediment loads in Tijuana

Estuary (Zedler 2001). Episodic flood events in

the past two decades have deposited high loads of

sediment into the channels and salt marsh areas,

resulting in unnaturally high salt marsh elevations

at certain locations within the estuary and reduced

tidal inundation of the marsh surface (Ward et al.

2003; Zedler 2001).

Los Penasquitos Lagoon (32�560 N, 117�150 W) is

a relatively small salt-marsh (252 ha) with tidal

channels that typifies many fragmented coastal

wetland habitats in southern California. The lagoon

is bisected near the tidal inlet by a roadway, through

its center by a railroad, and through its southeastern

portion by a berm over a sewer line (Zedler 2001).

As a result, tidal flushing in the lagoon is impeded

and the inlet frequently closes to tidal circulation

(Zedler 2001). Extensive development in the

255 km2 watershed in recent decades has increased

freshwater and sediment input to the lagoon (Zedler

2001).

Fish sampling

California killifish, topsmelt and California halibut

were sampled at various sites between October 1998

and November 1999 in Los Penasquitos Lagoon and

Tijuana Estuary (Table 1, Fig. 1) for the purpose of

estimating their food consumption and diet compo-

sition. California halibut were also collected in

routine quarterly surveys (March, June, September,

December) as part of a long-term monitoring program

to evaluate fish community patterns at three estab-

lished monitoring sites in Tijuana Estuary (Table 1,

Fig. 1). In Tijuana Estuary, the ‘‘Mouth’’ site (M) is

located in a shallow side channel (mean depth at low

tide 0.26 + 0.03 m) approximately 0.35 km from the

ocean entrance of Tijuana Estuary and consists of a

substrate composed of organic sediment. The ‘‘Sea-

coast’’ site (SC) is located 1.34 km from the ocean

entrance in a broad, deep channel ([20 m width and

mean depth at low tide of 0.71 + 0.04 m) composed

mainly of sandy sediments. The ‘‘East-West’’ site

(EW) is in a connector channel located about 1.87 km

from the ocean entrance between the northern arm of

the estuary the inland ponds (Fig. 1). The EW site is

11 m wide with a mean depth of 0.56 + 0.04 m at

low tide, and has a clay substrate lined with cobble

and empty bivalve shells.

Wetlands Ecol Manage (2008) 16:219–236 221

123

Fish were collected for diet analysis using a beach

seine. In the long-term monitoring surveys (1999–

2001), California halibut were collected using two

blocking nets and a bag seine (13.3 m long and 2.1 m

deep) with a 3 mm mesh. At each site, blocking nets

were deployed to confine all fish within a known area.

The bag seine was then swept in the area between the

two blocking nets across the channel to the opposite

bank. Passes were repeated (typically 3–4 sweeps)

until the catch neared depletion levels in the area

between the nets. All halibut in the catch were

counted and measured.

Daily food consumption (Daily ration)

On each sampling date (Table 1), California killifish,

topsmelt and California halibut were collected with a

beach seine every 3 h over a 24-h period, preserved

in 95% ethanol in the field, then transferred to 70%

ethanol in the laboratory. California killifish were

sampled on various occasions (Table 1) to include

days when daytime tidal heights were sufficient to

inundate the marsh surface and provide fish with

access to the inundated habitat, and also on days

when tidal heights were insufficient to flood the

marsh surface (no marsh access).

Topsmelt were sampled in Tijuana Estuary

(Table 1) to evaluate their feeding patterns in an

estuarine system that has remained consistently open

to tidal flushing. Topsmelt were also sampled in Los

Penasquitos Lagoon (Table 1), a system that fre-

quently gets impounded due to tidal inlet closures, in

order to quantify the effects of lagoon impoundment

on their food consumption patterns. Daily feeding

patterns of topsmelt in Los Penasquitos Lagoon were

quantified on two separate occasions in March 1999,

(1) when the tidal inlet to the lagoon was completely

blocked with sand and cobble, impounding the

lagoon, and (2) when the tidal inlet to the lagoon

was subsequently scoured open by high surf events.

California halibut were sampled at two locations in

Tijuana Estuary, the mouth site and the seacoast site

(Fig. 1, Table 1), in order to quantify their daily food

consumption in channels with different habitat char-

acteristics. While similar size classes of each fish

species were chosen for food consumption analysis

on each sampling date, two distinct size classes of

Fig. 1 Location of coastal

wetland sampling sites in

southern California


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California halibut (small sized juveniles = 108–

135 mm TL and large sized juveniles = 190–

250 mm TL) were additionally sampled at the

Seacoast site in Tijuana Estuary (Table 1) to assess

size-specific differences in daily food consumption

levels of juvenile halibut.

For each fish species, gut fullness for each 3-h

period was determined by measuring (mm, total

length, TL) and weighing (g, wet weight) from 5 to

15 fish, then dissecting out and weighing the entire

gut. Food weights in the guts were estimated as the

difference between total gut and empty gut weights

(EGW). Empty gut weights were estimated from

previously determined regressions of EGW on fish

body mass. Gut evacuation rates were calculated by

fitting appropriate mathematical curves (Post 1990) to

the decline in gut contents during the night when

feeding had ceased (indicated by empty anterior

digestive tracts). Gut evacuation rates (E, h-1) were

combined with time-specific estimates of gut-fullness

(Ft, g/g) to yield daily food consumption (DFC, g/g/

d), based on the method of Elliott and Persson (1978):

DFC =Eh

1�e� Ehð Þ

X9

t¼1

Ftþ1 � Fte� Ehð Þ

� �

where h represents the time interval (3 h) between

gut fullness estimates, and t represents each of the

nine time periods when gut fullness was determined.

Ninety-five percent confidence intervals (CI) were

estimated for each daily food consumption value by

pooling the standard errors of each of the nine 3-h

point estimates of gut fullness on a sampling date,

using the method described by Madon (1998).

Data on tidal hydroperiods for each of the sampling

dates were obtained from water level records published

by the National Oceanic and Atmospheric Adminis-

tration (NOAA; http://tidesandcurrents.noaa.gov/).

Table 1 Sampling sites, dates, number of fish used in diet analysis and size ranges for fish collected in Tijuana Estuary (TJE) and

Los Penasquitos Lagoon (LPL)

Fish species Estuary Sampling site Sampling dates No. of fish (N) Fish size range (mm)

California killifish LPL Mouth October 1–2, 1998 59 41–93

TJE Mouth October 29–30, 1998 85 48–76



TJE Mouth November 16–17, 1999 112 31–79

Topsmelt LPL Mouth* March 11–12, 1999 90 140–192

LPL Mouth� March 29–30, 1999 113 133–197


TJE Mouth March 13–14, 1999 121 118–184

TJE Seacoast August 5–6, 1999 87 120–175


California halibut TJE Seacoast August 5–6, 1999 51 108–135

TJE Seacoast August 5–6, 1999 45 190–250


TJE Mouth November 16–17, 1999 54 98–118

TJE Mouth Every May, June, September

and December between 1995–1999

76! 5–120!

TJE Seacoast Every May, June, September


392! 8–498!

TJE East-West Every May, June, September


19! 9–125!

Symbols indicate that the collection of topsmelt occurred during a natural experiment on days when the tidal inlet to LPL was closed

(*) and open (�) to tidal flushing. California halibut were sampled for diet analysis and were also collected as part of a long-term

biological monitoring effort in Tijuana Estuary to be used for site-specific size distribution analysis in this study (!)


123

http://tidesandcurrents.noaa.gov/

Diet composition—topsmelt

A weighted index of relative importance (IRI, Pinkas

et al. 1971) was used to characterize the importance

of common prey categories in topsmelt diets. Ran-

domly chosen subsamples of 30–60 gastrointestinal

tracts of topsmelt collected in each of the six diel

samples (Table 1) were dissected and contents were

counted and identified to the lowest taxonomic level

possible. Prey items were grouped to form general

taxonomic categories (e.g., algae, copepods, amphi-

pods) for the IRI analyses. The volume of small prey

items was determined by flattening the gut contents to

a uniform thickness of 1 mm on a clear Petri dish

placed over graph paper, estimating the area (mm2),

then volume (mm3) of each prey group (Hyslop 1980;

Rozas and LaSalle 1990; West et al. 2003). The

volume of larger prey items was measured as the

volume of water displaced by the prey items in a

graduated 10-ml (+0.1 ml) cylinder. The IRI was

calculated for each sampling date (Table 1) as:

IRI ¼ % N + % Vð Þ �% FO

where N is the prey number, V is the prey volume and

FO is the frequency of occurrence of each prey

category. A %IRI value was then calculated for each

prey category by dividing the summed IRI value of

the prey item by the total IRI value of all prey items

(West et al. 2003).

Bioenergetics modeling of fish growth potential

A bioenergetics approach was used to estimate the

growth potential of California killifish and California

halibut under a range of environmental conditions.

Growth of California killifish on each of the sampling

dates was predicted with a killifish bioenergetics

model developed and independently validated by

Madon et al. (2001). The bioenergetics model is

based on an energy budget where specific growth rate

(dB/Bdt) is modeled as:

dB

Bdt¼ C � ðRþ F þ UÞ

where B is the weight of the fish, t is time, C is

consumption, R is respiration, F is egestion, and U is

excretion. The model predicts killifish growth on a

daily basis using food consumption and water

temperature as model inputs (Madon et al. 2001)

and was used to predict the growth of a 55 mm

killifish (2 g wet weight) based on inputs of field

estimates of killifish food consumption and water

temperature measured in this study.

Energy budgets developed for California halibut

acclimated to a range of salinities and water temper-

atures (Madon 2002) were used to predict its growth

under a range of salinities (5–35) and water temper-

atures (10–30�C). Growth contours were generated

for small (26 g wet mass, 120 mm TL) and large

juvenile halibut (200 g wet mass, 270 mm TL) over a

range of salinities and water temperatures at low and

high levels of prey availability. Low prey availability

reflected prey levels where halibut of a specific size

consumed only 25% of its maximum daily ration;

high prey availability reflected food consumption

levels of 75% of the maximum daily ration (Madon

2002). Growth contours were used to evaluate the

potential effects of episodic salinity and water

temperature changes caused by tidal inlet closures

on the growth of small and large juvenile halibut.

Energy budgets (Madon 2002) were also used to

predict the specific growth rates of juvenile Califor-

nia halibut at the Mouth and Seacoast sites in Tijuana

Estuary. Specific growth rates of juvenile California

halibut were predicted at ambient water temperatures

and at 20�C using field estimates of daily food

consumption measured for halibut sampled at the

Mouth and Seacoast sites in August, October and

November of 1999.

Results

Daily food consumption (Daily ration)

California killifish in Tijuana Estuary displayed

crepuscular feeding patterns with gut fullness peaking

during twilight hours on the two sampling periods

(October 12–13, 1999 and October 27–28, 1999)

when daytime tides were sufficiently high to provide

fish with access to the marsh surface (Fig. 2). The

feeding peaks followed peak high tides on both these

sampling occasions. In contrast, feeding activity of

killifish remained at relatively low levels throughout

each of the three 24-h sampling periods (October 1–2,

1998, in Los Penasquitos Lagoon, and October 29–

30,1998 and November 16–17, 1999, in Tijuana

Estuary) when tidal heights were insufficient to


123

provide fish with marsh access (Fig. 2). Gut fullness

during each of the sampling periods without marsh

access never exceeded 0.024 g/g, in contrast to gut

fullness of fish with marsh access which peaked at

0.04 -0.05 g/g (Fig. 2).

Daily food consumption by killifish with access to

the marsh surface was two to five times higher than in

killifish that were restricted to feeding in subtidal

channels (Fig. 3). Field estimates of daily ration in

fish with marsh access ranged from 0.274 + 0.025 g/g

(27.4 + 2.5% body weight) to 0.329 + 0.024 g/g, and

were significantly higher compared to daily rations of

0.064 + 0.045 g/g to 0.132 + 0.021 g/g in fish with-

out marsh access (Fig. 3).

Crepuscular feeding patterns were also observed in

topsmelt sampled in Tijuana Estuary, and peaks in

gut fullness followed peak daytime high tides,

regardless of sampling location and date (Fig. 4).

Daily food consumption by topsmelt in Tijuana

Estuary varied significantly between sampling dates

and ranged from 0.216 + 0.035 g/g/d (21.6 + 3.5%

body weight; + 95% CI) to 0.589 + 0.032 g/g/d

(Fig. 5).

Topsmelt were also sampled in Los Penasquitos

Lagoon over a 24-h period when the lagoon was

impounded due to closure of the tidal inlet, and again

when the lagoon was open to tidal flushing due to

scouring of the tidal inlet by high surf. During March

11–12, 1999 when the lagoon was impounded and

closed to tidal circulation, topsmelt feeding occurred

at low levels and did not show distinct peaks in

feeding activity, as indicated by gut fullness. Gut

fullness during this period never exceeded 0.045 g/g

(Fig. 6). In contrast, when the lagoon was open to

Fig. 2 Daily food consumption cycles (bold dark lines) of

California killifish (31–93 mm, total length, TL range) at

Tijuana Estuary and Los Penasquitos Lagoon in relation to daily

tidal cycles (dotted lines). For each time period, food consump-

tion is given in terms of the average food mass (+1 standard

error, SE) observed in the guts of a sample of killifish. The

horizontal dotted black line indicates the tidal height relative to

mean low low water (MLLW) required for marsh access. Bold

dark bars below the x-axis signify post-dusk and nighttime hours.

N is the number of fish sampled on each date

Fig. 3 Field estimates of daily amounts of food consumed

(+95% confidence limits, CI) by California killifish at Tijuana

Estuary (TJE) and Los Penasquitos Lagoon (LPL) on days with

and without marsh access. N is the number of fish sampled on

each date


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tidal circulation as indicated by the distinct tidal

patterns observed on March 29–30, 1999, topsmelt

resume normal feeding patterns with a distinct peak

in gut fullness (0.103 g/g) following the daytime

peak in high tide (Fig. 6).

Daily food consumption by topsmelt was approx-

imately twice as high when the lagoon was open to

tidal circulation, compared to when the lagoon was

impounded and lacked tidal influence (Fig. 7). Daily

ration of topsmelt under impounded conditions

(0.124 + 0.030 g/g/d) was the lowest among all

food consumption levels observed in topsmelt under

normal tidal patterns (0.216 + 0.035 to 0.589 +

0.032 g/g/d) in Tijuana Estuary and Los Penasquitos

Lagoon (Figs. 5, 7).

Small juvenile California halibut (95–135 mm,

TL) at the Seacoast and Mouth sites in Tijuana

Estuary showed distinct peaks in gut fullness that

coincided with daytime peaks in high tide (Fig. 8).

Fig. 4 Daily food

consumption cycles (bold

dark lines) of topsmelt

(118–190 mm, total length,

TL range) at Tijuana

Estuary in relation to daily

tidal cycles (dotted lines;

tides are in relation to mean

low low water, MLLW).

For each time period, food

consumption is given in

terms of the average food

mass (+1 standard error,

SE) observed in the guts of

a sample of topsmelt. Bold

dark bars below the x-axis

signify post-dusk and

nighttime hours. N is the

number of fish sampled on

each date


(+95% confidence limits, CI) by topsmelt at Tijuana Estuary

(TJE), 1998–1999. N is the number of fish sampled on each

date


topsmelt in Los Penasquitos Lagoon on two days in March

1999, when the tidal inlet was closed and then subsequently

open to tidal flushing. For each time period, food consump-

tion is given in terms of the average food mass (+1 standard

error, SE) observed in the guts of a sample of topsmelt. Daily

tidal cycles are indicated by dotted lines, relative to mean low

low water (MLLW) and reveal the lack of a tidal cycle within

the lagoon when the inlet was closed. The bold dark bars

signify post-dusk and nighttime hours. N is the number of fish

sampled on each date and TL is total length range of fish

sampled


123

Daily rations of small juvenile halibut at these sites

ranged from 0.104 + 0.011 to 0.136 + 0.018 g/g/d,

but did not differ significantly between sampling

dates (Fig. 9). Conversely, feeding level of large

juvenile halibut (190–250 mm, TL) at the Seacoast

site was significantly low throughout the 24-h period,

compared to feeding activity of small juveniles

(Fig. 8). Daily ration of large juvenile halibut at the

Seacoast site was at least an order of magnitude lower

than that of small juveniles collected on the same

sampling date (August 5–6, 1999) (Fig. 9).

Diet composition

Algae was the most important food item in topsmelt

diets in Tijuana Estuary with an IRI of 68.4%,

significantly higher than all other prey categories

(Fig. 10, One-way ANOVA; F6,21 = 13.2, P \0.001). Tukey’s HSD test revealed that there were

no significant differences in % IRIs of copepods,

amphipods, insects, digested matter, sand and ‘‘other’’

prey categories (P [ 0.05) which ranged from 0.2%

to 14.4% (Fig. 10). The ‘‘other’’ prey category mostly

consisted of bivalve, cyprid and gastropod veligers,

small gastropods, ostracods, oligochaetes, crabs lar-

vae, and isopods, of which none exceeded an IRI of

1% in topsmelt diet.


(+95% confidence limits, CI) by topsmelt in Los Penasquitos

Lagoon on days when tidal inlet was closed, and then

subsequently open to tidal flow between the ocean and the

lagoon. N is the number of fish sampled on each date


small (95–135 mm, TL) and large (190–250 mm, TL) juvenile

California halibut at study sites within Tijuana Estuary in

relation to daily tidal cycles (dotted lines, tides are in relation

to mean low low water, MLLW). For each time period, food

consumption is given in terms of the average food mass

(+1 standard error, SE) observed in the guts of a sample of

halibut. The bold dark bars signify post-dusk and nighttime

hours. N is the number of fish sampled on each date and TL is

total length range of fish sampled


123

Under normal tidal patterns when the inlet of Los

Penasquitos Lagoon was open to the tidal flushing,

diet composition of topsmelt was similar to that of

topsmelt in Tijuana Estuary. That is, algae dominated

topsmelt diet at 83.8% IRI and copepods, amphipods,

insects, digested matter, sand and ‘‘other’’ prey

categories ranged from an IRI of 0.7% to 3.6%

(Fig. 11). Topsmelt diet composition, however,

changed dramatically under conditions when the

lagoon was impounded due to closure of the tidal

inlet. Under impounded conditions, topsmelt diets

consisted mainly of copepods, sand, and digested

unidentifiable matter (IRIs ranging from 14.7% to

44.2%), with algae contributing to only a small

fraction of the diet (IRI = 0.8%, Fig. 11).

Bioenergetics modelling of fish growth potential

Bioenergetic model predictions of specific growth

rates of California killifish with marsh access ranged

from 0.132 + 0.016 g/g/d (13.2 + 1.6% body weight/d)

to 0.174 + 0.015 g/g/d, and were significantly higher

compared to growth rates of 0.002 + 0.028 g/g to

0.049 + 0.013 g/g in fish without marsh access

(Fig. 12). The model predicted positive specific

growth rates for killifish in Tijuana Estuary at all

levels of food consumption tested; however, killifish

would lose weight (specific growth rate = -0.026 g/g/d)

at its lower range of estimated food consumption in

Los Penasquitos Lagoon (Fig. 12).

Contours of specific growth rates of small

(Fig. 13) and large juvenile halibut (Fig. 14) show

areas of growth and weight loss across a range of

water temperatures and salinities. When prey


(+95% confidence limits, CI) by large (dark bar) and small

(light bars) juvenile California halibut at the Seacoast and

Mouth sites in Tijuana Estuary, 1999. N is the number of fish

sampled on each date

Fig. 10 Mean (+1 SE)% dietary index of relative importance

(IRI) of food items observed in guts of topsmelt (128–190 mm,

total length) from Tijuana Estuary

Fig. 11 Percent dietary index of relative importance (IRI) of

food items observed in guts of topsmelt (133–197 mm, total

length) in Los Penasquitos Lagoon during March 1999 on days

when the tidal inlet was closed, and then subsequently opened

to tidal circulation between the ocean and the lagoon

Fig. 12 Growth rates of California killifish with and without

marsh access in Los Penasquitos Lagoon (LPL) and Tijuana

Estuary (TJE), predicted with a killifish bioenergetics model

developed by Madon et al. (2001)


123

availability is high (food consumption level = 75%

of maximum consumption), small halibut can grow

across almost the entire ranges of water temperature

and salinity tested, except at water temperatures of

29�C and above and at very low water temperature

and salinity conditions where weight loss occurs

(Fig. 13a). Under low prey availability (food con-

sumption level = 25% of maximum consumption),

the upper water temperature limit at which weight

loss occurs drops to approximately 28�C; below 17�C,

weight loss also occurs across the entire range of

salinities tested (Fig. 13b).

Large juvenile halibut grow between water tem-

peratures of approximately 16�C and 22�C across the

entire range of salinities tested when prey availability

is high; weight loss occurs in large juvenile halibut

below and above this water temperature range across

all salinities (Fig. 14a). Under low prey availability,

large juvenile halibut can grow only in a very narrow

range of water temperatures (19–21�C) and salinities

(27–35 ppt), and generally experience weight loss

under a broad range of environmental conditions

(Fig. 14b).

The effect of tidal inlet closure on the water

temperature and salinity of Los Penasquitos Lagoon

is illustrated for the time period between March 15

and 29, 1998 (Fig. 15). During periods when the tidal

inlet was open (March 15–March 18), water temper-

atures and salinities in LPL averaged approximately

19�C and 31 ppt, respectively (Fig. 15). The tidal

inlet partially closed on March 18 and was com-

pletely obstructed by March 19. In the period

following closure of the tidal inlet, water temperature

and salinity dropped sharply and then stabilized at

approximately 14�C and 6 ppt, respectively (Fig. 15).

Growth contours indicate that under water tem-

peratures and salinities typical of pre-closure

environmental conditions in Los Penasquitos Lagoon,

specific growth rates of small juvenile halibut would

range between 0.005 and 0.01 g/g/d when food

Fig. 13 Growth rates of small juvenile halibut (26 g wet

mass) in Los Penasquitos Lagoon under (a) high prey

availibility conditions and (b) low prey availability conditions,

predicted using energy budgets developed for halibut by

Madon (2002). Red dots indicate growth potential of halibut

under open and closed tidal inlet conditions within the lagoon

Fig. 14 Growth rates of large juvenile halibut (200 g wet

mass) in Los Penasquitos Lagoon under (a) high prey

availability conditions and (b) low prey availability conditions,

predicted using energy budgets developed for halibut by

Madon (2002). Red dots indicate growth potential of halibut

under open and closed tidal inlet conditions within the lagoon


123

availability was high, and between 0 to 0.002 g/g/d

under low prey availability conditions (Fig. 13a, b).

However, under post-closure conditions, small hali-

but would experience weight loss regardless of prey

availability (Fig. 13a, b). Similarly, at high prey

availability, large juvenile halibut would grow at a

rate of approximately 0.006 g/g/d under pre-closure

conditions but begin to lose weight under post-

closure conditions (Fig. 14a). Under low prey avail-

ability, large juvenile halibut experience would

experience slight weight loss under pre-closure

conditions, but would rapidly begin to lose weight

under post-closure conditions (Fig. 14b).

Based on field estimates of daily food consumption

in Tijuana Estuary, specific growth rates of small and

large juvenile California halibut at the Seacoast site

(August 5–6, 1999) differed significantly at the ambi-

ent water temperature (24�C) and at 20�C (Fig. 16).

Energy budgets predicted that small juvenile halibut

would have specific growth rates of approximately

0.055 + 0.008 g/g/d at the Seacoast site in contrast to

large juveniles which would lose weight on average

(Fig. 16). At the Mouth site, energy budgets for small

juvenile halibut predicted specific growth rates ranging

from 0.040 + 0.005 to 0.047 + 0.005 g/g/d, depending

on water temperature, sampling date and field esti-

mates of food consumption (Fig. 16).

California halibut size distributions and channel

characteristics

Quarterly sampling for juvenile halibut was conducted

at three sites with different channel characteristics

every year between 1995 and 2001 as part of a long-

term biological monitoring effort at Tijuana Estuary.

Juvenile halibut were present at all three sites. At the

shallow ‘‘Mouth’’ site and the ‘‘East-West Channel’’

site, the sizes of juvenile halibut ranged between

5 mm and 125 mm, TL. No halibut exceeding

125 mm TL was found at the Mouth and East-West

Channel sites in the 28 sampling events that occurred

between 1995 and 2001 (Fig. 17). Summer water

temperatures at the Mouth and East-West Channel

sites often exceed the lethal limit (28�C) for large

juvenile halibut ([200 mm TL, Madon 2002), but

water temperatures and salinities at these sites

(Fig. 18) were within the ranges tolerated by smaller

juveniles (Madon 2002). Conversely, the large, deep,

Seacoast site was the only one where large juvenile

halibut exceeding 200 mm TL were collected fre-

quently (Fig. 17). Water temperatures at the Seacoast

site never exceeded, and were substantially lower

than the lethal limit for large juvenile halibut

(Fig. 18).

Discussion

California killifish

The marsh surface clearly plays an important ecolog-

ical role in the life history of the California killifish,

Fundulus parvipinnis, which depend on marsh access

Fig. 15 The effects of tidal inlet closure and rainfall on water

temperature (solid line, circles) and salinity (broken line,

triangles) in Los Penasquitos Lagoon, March 15–29, 1998

Fig. 16 Specific growth rates (+95% confidence limits, CI) of

small and large juvenile halibut at 20�C and ambient water

temperatures (shown in figure) on specific dates and sites in

Tijuana Estuary. Growth rates were predicted using field

estimates of food consumption and energy budgets developed

for juvenile halibut (Madon 2002)


123

during high tides to support their feeding and growth.

The marsh surface also plays a similar ecological role

for the mummichog, F. heteroclitus, in Atlantic Coast

estuaries by providing trophic connectivity between

subtidal and intertidal habitats (Weisberg and Lotrich

1982; Kneib 1986). In contrast to subtidal channels,

the marsh surface floods only intermittently, thereby

limiting access to invertebrate predators and allowing

invertebrate food resources to build up between

periods of inundation (Kneib 1997). The marsh

surface also supports high densities of surface-dwell-

ing invetebrate prey that are otherwise not available or

abundant in subtidal channels (Kneib 1997; West and

Zedler 2000).

Using baited minnow traps in a southern Califor-

nia estuary, West and Zedler (2000) have shown that

California killifish will access the marsh surface

during spring high tides and that the coastal marsh

provides a rich foraging area for this species.

Analysis of killifish guts revealed that killifish with

marsh access had gut fullness indices that were as

much as six times higher than in fish restricted to

creek habitats (West and Zedler 2000). Madon et al.

(2001) subsequently used the killifish gut fullness

data collected by West and Zedler (2000) in a

bioenergetics model to show that killifish could

potentially grow from 20–100% faster if they add

intertidal marsh surfaces to their subtidal feeding

areas. These two studies (West and Zedler 2000;

Madon et al. 2001) were based on single point

estimates of gut fullness, and neither directly mea-

sured the food consumption of California killifish

over 24-h periods when fish were restricted to

Fig. 17 Size distributions of juvenile halibut at the three

sampling sites in Tijuana Estuary, 1995–2001. N is the total

number of fish sampled at each site and TL is total length range

of fish sampled

Fig. 18 Seasonal average

water temperatures and

salinities measured at the

three sampling sites in

Tijuana Estuary during

March (M), June (J),

September (S) and

December (D), 1995–2001.

The dotted line in each

panel indicates the lower

limit of lethal water

temperature (28�C) for

large juvenile halibut,

which is often reached or

exceeded in the shallow and

mid-sized channels during

summer months


123

subtidal channels and compared those to daily food

consumption estimated during periods when high

tides provided killifish access to the marsh surface.

This study is the first to provide direct field evidence

that killifish can increase their daily food intake by

two- to five-fold by feeding on the marsh surface.

Furthermore, this study also shows that increased

levels of feeding on the marsh surface translate into

growth rates that are up to two orders of magnitude

higher than growth rates of fish restricted to feeding

in subtidal channels. This study offers strong and

direct field evidence that supports two previous

studies (West and Zedler 2000; Madon 2001) on

the functional benefits of marsh surface access to

California killifish, as well as studies on its Atlantic

coast congener, F. heteroclitus (Weisberg et al. 1981;

Weisberg and Lotrich 1982; Kneib 1986).

Tidal inlet closures and increased marsh surface

elevations due to sedimentation are common prob-

lems in the coastal wetlands of southern California

(Zedler 2001; Callaway and Zedler 2004; Wallace

et al. 2005) and have direct implications for killifish

feeding and growth. High tides are essential for

inundation of the marsh surface and for facilitating

the movement of California killifish from subtidal

channels to the marsh plain. During high tides, field

observations have shown that killifish use the

extensive marsh-creek connectivity offered by natu-

ral ‘‘tidal creek networks’’ to access the marsh

surface from subtidal areas; that is, they move from

deeper subtidal channels into connecting smaller

channels and tidal creeks to gain access to the

interior marsh surface (Desmond et al. 2000). If the

tidal inlet were to close, fish access to the marsh

surface would be restricted as the coastal wetland

would no longer be under tidal influence and would

lack the tidal elevations necessary to inundate the

marsh surface. Sediment accretion on the marsh plain

would also have the effect of restricting fish access to

the marsh surface. High sedimentation rates would

lead to an increase in marsh surface elevations,

which over time, could reduce marsh inundation

periods or even completely restrict the flooding of

the marsh surface under extreme cases of sedimen-

tation. In either case (tidal inlet closure or

sedimentation), marsh access for killifish could be

restricted, confining killifish to subtidal channels

which appear to be sub-optimal in terms of support-

ing killifish feeding and growth.

In light of the implications of tidal inlet closures

on killifish feeding and growth, coastal restoration

projects must ensure that their restoration designs

incorporate hydrologic and structural elements that

are conducive to maintaining an open tidal inlet.

Coastal wetland management plans must also incor-

porate specific actions that include the prompt

removal of sand, sediment and cobble blocking tidal

inlets. For example, Los Penasquitos Lagoon has a

management plan that specifically involves the

clearing of debris, sand, cobble and sediment from

the blocked inlet with a bulldozer. A sediment

management plan that is aimed at controlling the

input of excessive sediment into coastal wetland

areas is also necessary. The Tijuana River National

Estuarine Research Reserve, as part of its phased

program to restore salt marshes in degraded upland

areas that were historically wetlands, has recently

built basins to capture and retain large volumes of

sediment that may otherwise be deposited into

adjacent salt marsh areas. However, these basins are

sometimes overwhelmed by the sheer volume of

sediment that gets deposited during winter storm

events, resulting in sediment bypassing the basins and

subsequently depositing in the salt marsh areas.

Finally, restoration plans must incorporate tidal

creek networks into the design of coastal wetlands

(Madon et al. 2002; Wallace et al. 2005). Tidal creek

networks will provide sufficient marsh surface-creek

connectivity required by fish for marsh surface access

during high tide events. In southern California,

excavation of deep basins or deep channels within

areas of filled wetlands is allowed by resource

agencies as compensatory mitigation for damages to

fish habitat (Zedler et al. 1997; Zedler 2001). The

marsh-water interface in these constructed wetlands

is greatly reduced and these wetlands bear little

structural or functional resemblance to the tidal creek

networks characteristic in natural coastal wetlands

(Zedler 1996a; West and Zedler 2000). Tidal creek

networks can be excavated in restoration sites or

measures can be taken to at least jump-start their

development (Wallace et al. 2005). For example,

tidal creek networks designed after a natural tidal

drainage network were excavated into an 8-ha

experimental salt marsh in Tijuana Estuary and

played an important role in aiding the further

development of a drainage network comparable to

reference systems in 4–5 years (Wallace et al. 2005).


123

Excavating these drainage networks is, however,

costly and other methods to jump-start the process of

tidal network formation have been suggested. These

include the manipulation of elevation gradients and

location of vegetation plantings so that erosion can be

promoted along unplanted corridors to eventually

form tidal creeks (Wallace et al. 2005), using kelp

amendments in wetland soils to reduce soil bulk

density and counteract soil compaction to promote

the erosive formation of creeks (Wallace et al. 2005),

building internal peninsulas in graded restoration

sites to guide hydrologic inundation and drainage

patterns which eventually lead to channel and creek

formation, and making shallow excavations to jump-

start creek formation (Williams 2001; Williams et al.

2002).

Topsmelt

Daily food consumption and diet composition of

topsmelt, Antherinops affinis, both appear to be

influenced by tidal patterns and tidal inlet closures.

Under normal 24-h tidal patterns in an estuary with

an unobstructed tidal inlet (Tijuana Estuary), top-

smelt exhibit diel feeding patterns with peak feeding

following daytime high tides. Daily rations of

topsmelt in Tijuana Estuary ranged from approxi-

mately 22% to 59% of body weight, and macroalgae

(primarily Enteromorpha sp.) dominated topsmelt

diets. The high degree of herbivory exhibited by

topsmelt in Tijuana Estuary appears to be common in

this species; large topsmelt ([100 mm, comparable

to topsmelt sizes in this study) in other California

bays and estuaries are also known to forage almost

exclusively on macroalgae (Horn and Allen 1985;

Barry et al. 1996). Topsmelt have pharyngeal jaws

which they likely use to lyse algal cells; high amylase

activity in their guts allows them to extract and

assimilate nutrients and energy from algae with high

efficiency (Logothetis et al. 2001). High levels of

food consumption by topsmelt (up to 59% of body

weight) also point to an algae-rich diet. Macroalgae

have low protein content and are relatively hard to

break down and assimilate, requiring herbivorous fish

to compensate by maintaining high levels of food

intake (Horn et al. 1999).

Los Penasquitos Lagoon, like most coastal wet-

lands in southern California, experiences frequent

tidal inlet closures. This study shows that such

closures have a negative impact on feeding by

topsmelt. One such tidal inlet closure event and the

subsequent opening of the inlet in March 1999

allowed quantification of topsmelt feeding in the

impounded lagoon. Food consumption rate of top-

smelt was 50% lower when the tidal inlet was

closed, compared to when the lagoon was under tidal

influence. Under impounded conditions and lack of a

tidal pattern in the lagoon, topsmelt did not show any

distinct peaks in feeding activity and maintained low

levels of feeding throughout the 24-h period. Algae

was not the dominant food item in topsmelt diet,

which instead exhibited a higher proportion of sand,

digested matter and copepods under impounded

conditions. When the lagoon subsequently opened

to tidal flushing, topsmelt resumed their normal

feeding patterns with a characteristic peak in

daytime feeding activity following high tide and

macroalgae dominating the diet, much like the

populations of topsmelt in Tijuana Estuary. Mainte-

nance of an open tidal inlet and promoting

unrestricted tidal flow between the ocean and lagoon

are important management actions that are necessary

to support the health of topsmelt populations in

coastal wetlands.

California Halibut

Paralichthys californicus are also adversely affected

by tidal inlet closures. In southern California, tidal

inlet closures are particularly common during the

winter (November–March) when offshore storms

accumulate sand, cobble and debris near the inlet

and restrict or prevent tidal flow between the ocean

and the lagoon or estuary. Water temperature and

salinity changes rapidly in these impounded wetlands,

particularly during precipitation events and could

adversely affect growth of juvenile California halibut.

Small juvenile halibut appear to be well adapted to

variable estuarine conditions (Madon 2002), but may

still be impacted by sudden and dramatic fluctuations

in water temperature and salinity in these impounded

systems during the winter. For example, the tidal inlet

closure that occurred in Los Penasquitos Lagoon

during March 1998 resulted in sharp declines in water

temperature and salinity within the impounded

lagoon. Growth contours of halibut indicate that


123

small juveniles would lose body mass under these

impounded conditions, regardless of prey availability.

Large juvenile halibut are relatively intolerant of

variable water temperatures and salinities, and their

growth would likely be more adversely impacted by

tidal inlet closures. Growth contours reveal that even

when the tidal inlet is open, large juvenile halibut

appear to lose some body mass when prey availability

is low. Tidal inlet closures occur more frequently

during winter months, often coinciding with periods

when prey densities (e.g., arrow gobies, Clevelandia

ios), are typically at their lowest levels compared to

other times of the year (West et al. 2003). Reduced

levels of prey availability, combined with sharp

variations in water temperature and salinity induced

by tidal inlet closures would prove to be particularly

stressful for large juvenile halibut and lead to rapid

weight loss.

Tidal creek networks consisting of channels and

creeks of various orders are also important to halibut

and should be incorporated into restoration designs

for coastal wetlands. Large juvenile halibut occupy

only deeper, higher order channels while small

halibut are abundant in both low and high order

channels. High order channels may primarily func-

tion as thermal refugia for large juvenile halibut, but

likely offer little food support. In Tijuana Estuary,

large juvenile halibut were only present at the

Seacoast site, which is located in a broad, deep

channel (a high order channel) where water temper-

atures typically remain below the lethal temperature

for large juvenile halibut. However, daily food

consumption of large juvenile halibut at the Seacoast

site was very low and below levels required to

support significant growth. Quarterly monitoring of

fish conducted between 1997–2001 in low and high

order channels in Tijuana Estuary reveal that densi-

ties of C. ios, the primary prey of juvenile halibut

(West et al. 2003), were frequently lower in higher

order channels compared to low order channels

(M. Cordrey and J. West 2003, Pacific Estuarine

Research Laboratory, San Diego State University,

CA, personal communication). Densities of gobies in

high order channels could conceivably fall below

prey thresholds necessary for supporting growth of

large juvenile halibut (Madon 2002). Alternately, the

arrow goby is a small-sized fish and may no longer

be energetically efficient as a food source for large

juvenile halibut.

Conclusions: guidelines for managing and

restoring impacted coastal wetlands

This study provides an in-depth analysis of the effects

of common environmental stressors such as tidal inlet

closures, sedimentation events and water quality

variations on ecological function of key components

of the fish community in the coastal wetlands of

southern California. By focusing on species exhibit-

ing a range of life histories and occupying different

trophic positions within the fish community, mean-

ingful insights are gained into, (1) how environmental

stressors affect ecological function in coastal wet-

lands and, (2) how these results can be used to

provide guidance on the appropriate management and

restoration of these valuable ecosystems.

In conclusion, this study underscores the impor-

tance of implementing the specific management and

restoration activities in coastal wetlands, based on an

evaluation of the effects of anthropogenic stressors on

the fish community:

• Maintenance of an open tidal inlet, either through

physical clearance of materials blocking the inlet

and/or through the careful design and engineering

of the tidal inlet in restoration plans.

• Incorporating tidal creeks into the restoration

design, either through excavation or through

implementation of various measures that can

jump-start their natural development.

• Restoration designs should include specific ele-

ments to ensure that tidal creeks are adjacent to

intertidal salt marsh habitats to facilitate fish

access to the marsh surface.

• Restoration designs should incorporate tidal creek

networks consisting of creeks of various orders to

support diversity in ecological function. For

example, large, deep higher order creeks may

provide thermal refuge for juvenile fish but will

also contain higher densities of fish predators and

lower food resources, compared to shallower low

order creeks. Even with a specific fish species

(e.g., California halibut), individuals may parti-

tion the use of these tidal creek networks based on

size. For example, small juvenile halibut primar-

ily use shallow, small creeks (low order) for

refuge from predation and feeding, whereas larger

juveniles use deeper, high order creeks and

channels for thermal refuge.


123

• Management plans need to be developed and

implemented to curtail excessive input of sedi-

ment into coastal wetlands, which can have

negative effects on the fish community ranging

from acute (mortality of biota) to subtle (rise in

marsh surface elevations which reduces march

access to fish).

Acknowledgements This study was supported by funding

provided by the Earth Island Institute and the National Science

Foundation (NSF Award DEB 0212005) while the author was

at the Pacific Estuarine Research Laboratory, San Diego State

University. CH2M HILL, Inc. also provided support in time

and materials to the author through an initiative grant for data

analysis and writing. John Callaway, Janelle West, Michelle

Cordrey, Michael Kiener, Brian Weller, Michelle Bowman,

Kecia Kerr and Gregory Williams assisted with field sampling

and data collection efforts. Thanks are due to Joy B. Zedler for

her guidance and support throughout this study. Thanks are

also due to the staff at the Tijuana River National Estuarine

Research Reserve and the Los Penasquitos Lagoon Foundation

for supporting this research. This paper is dedicated to the

memory of Khorshed Shyam Verma.

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