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ACADEMY OF SCIENCES

Number 2

Southern California Academy of Sciences

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Date of this issue 5 October 20 1 5

® This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

Bull. Southern California Acad. Sci.

114(2), 2015, pp. 63-75

Effects of Ocean Recreational Users on Coastal Bottlenose
Dolphins ( Tursiops truncatus) in the Santa Monica
Bay, California

Amber D. Fandel, Maddalena Bearzi and Taylor C. Cook
Ocean Conservation Society, P. O. Box 12860, Marina del Rey, California 90295, USA

Abstract. — Coastal bottlenose dolphins ( Tursiops truncatus) have been observed in
proximity to swimmers, kayakers, stand-up paddle boarders and surfers along near-
shore corridors in the Santa Monica Bay, California. From 1997 to 2012, a total of
220 coastal boat-based focal follows of dolphin schools were conducted in this area
to determine a) the type and proximity of encounters between ocean recreational
users and coastal dolphins, and b) the effects of these encounters on bottlenose
dolphins’ behavior. The majority of encounters involved dolphins and surfers
(77.93%, n— 145 encounters), and overall, neutral reactions were observed in
response to encounters (61.93%, «=176 behavioral responses). Interactions between
bottlenose dolphins and recreational users were recorded only once, and changes in
dolphin behavior were observed more frequently when recreational users were at
distances of less than three meters from a school. Although the current impact of
human activities on coastal bottlenose dolphin behavior does not appear to be
significant in the Santa Monica Bay, there is a need to: 1) adopt a precautionary
approach in view of the increasing presence of ocean recreational users along this
coastline, and 2) regularly monitor these encounters to determine potential changes
in the type and proximity of encounters, as well as changes in dolphin behavioral
responses.

Bottlenose dolphins ( Tursiops truncatus , hereafter bottlenose dolphins) are known to
inhabit both pelagic waters and coastal regions, including bays and tidal creeks
(Leatherwood et al. 1983). In the Pacific Ocean, a coastal and an offshore population of
this species are currently recognized, showing morphological, osteological, and molecular
differentiations (LeDuc and Curry 1998; Rossbach and Herzing 1999). Studies have
suggested that coastal bottlenose dolphins are highly mobile within the inshore waters of
the Santa Monica Bay, but also spend a large amount of time foraging and feeding in the
bay (Bearzi 2005). Further, this species utilizes the region as a regular transit corridor
between foraging hotspots along the California coast (Defran and Weller 1999; Bearzi
2005). An estimated 50 million tourists visit the Santa Monica Bay beaches each year* 1,
many to partake in recreational activities including swimming, surfing, kayaking, and
stand up paddle boarding. Swimmers, surfers, kayakers, and stand up paddle boarders
are collectively defined as Ocean Recreational Users; hereafter ORUs. The year-round
presence of both ORUs and bottlenose dolphins in the coastal waters of this region
increases the likelihood of encounters between them.

Corresponding author: mbearzi@earthlink.net

1 Kreimann, S. H., Silverstrom, K. 2013. Beach and Marina Management Fact Sheet. County of Los
Angeles Department of Beaches and Harbors. County of Los Angeles Department of Beaches & Harbors.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

ORU presence has been proven to have adverse effects on dolphins in other areas
worldwide. The occurrence of any vessel type, motorized or non-motorized, caused
disturbances to dolphin behavior in Scotland (Pirotta et al. 2015). In New Zealand,
Constantine (2001) observed sensitization and increased levels of avoidance with
prolonged exposure to swimmers. Constantine (2002) also observed a decrease in
bottlenose dolphin resting behavior when swimmers approached them in the wild. In
Hawai’i, increased swimmer and kayak traffic led to decreased resting behaviors in
spinner dolphins ( Stenella longirostris; Samuels et al. 2000; Danil et al. 2005; Timmel
et al. 2008; Ostman-Lind 2009). Spinner dolphins in Hawai’i also exhibited increased
aerial behavior within their resting areas in correlation with the high number of swimmers
in the area (Courbis and Timmel 2009). Indo-pacific dolphins ( Tursiops aduncus) in
Zanzibar displayed more frequent erratic (non-directional) behaviors in response to the
increased presence of swimmers and boats (Stensland and Berggren 2007). Similarly,
a study in West Cracoft Island, British Columbia found that when kayakers were present,
killer whales ( Orcinus orca ) displayed avoidance behaviors, potentially resulting in
changes to time spent feeding (Williams et al. 2011). Variations in behavioral states and
decreased resting and feeding behaviors may cause a change in energetic demand, leading
to changes in the lifetime fitness of the animal (Pirotta et al 2015; Williams 2011).

Based on the negative effects of these encounters between ORUs and cetaceans
documented in other areas worldwide, the National Marine Fisheries Service (NMFS)
has expressed concern that humans swimming with wild dolphins in the U.S. may qualify
as harassment, leading to the disruption to their natural behavior (Spradlin et al. 1999).
In an attempt to curb this disruption, the NMFS has advised vessels and swimmers to
avoid approaching the animals at distance of less than 50 meters. Both ORUs and
bottlenose dolphins have been frequenting the Santa Monica Bay since the 1930s and the
tourism presence along this shoreline has increased, especially in recent times. The impact
of ORU activities on bottlenose dolphins, however, has not yet been investigated in this
area. This preliminary study describes the potential behavioral effects on coastal
bottlenose dolphins of encounters with ORUs in this region, and provides suggestions for
management and conservation measures aimed to mitigate the impacts on these animals.

Materials and Methods

Study area

The Santa Monica Bay study area (approximately 460km2, Fig. 1) is a shallow shelf
bounded by the Palos Verdes Peninsula to the south (33°45’N, 1 18°24’W), Point Dume to
the north (33°59’N, 1 18°48’W) and the edge of the continental shelf to the west. The bay
contains two shallow water submarine canyons (Dume and Redondo) and the deeper
Santa Monica Canyon. The Santa Monica Canyon begins at a depth of about 100m at
the edge of the continental shelf. The bay has a mean depth of approximately 55m and
a maximum depth of 450m. A shallow shelf between the Santa Monica and Redondo
Canyons extends as a plateau from the 50m contour. Mild temperatures, short rainy
winters and long, dry summers characterize the study area. Normal water surface
temperatures range from 1 1 to 22°C.

Data collection and analysis

This study utilizes data collected in the years 1997-2012 as a part of a long-term year-
round marine mammal research project. The data presented in this paper were analyzed
retrospectively and some of the reported information was opportunistic in nature.

EFFECTS OF OCEAN RECREATIONAL USERS ON BOTTLENOSE DOLPHINS

118°50'0"W 1 1 8°40'0"W 118°30'0"W 118°20'0"W

Fig. 1. Study area and locations of encounters between bottlenose dolphins and ORUs during surveys
conducted in 1997-2012.

Coastal surveys (distance <1 km from shore) were conducted from February 1997 to
September 2012 (excluding July 2002-August 2005, 2008 and 2010; Table 1), generally in
the morning and early afternoon and in good weather conditions (Beaufort scale 2 or less,
sea state 0 and visibility >300 m). Coastal surveys were conducted from 7m (1997-2000)
and 10m powerboats (2001- 2002, 2006-2007), and two 17m sailboats (2005-2006, 2009-
2012), at an average speed of 18km h-1. Boat speed was reduced in the presence of
dolphins, and sudden speed or directional changes were avoided. Trained research
assistants approximated the dolphins’ position (±30 m from the boat) and speed with
respect to the boat’s position using GPS. Focal follows were conducted on all dolphin
groups, each attempted for a minimum of 30 minutes and lasting up to 250 minutes. Prior
to potential encounters between ORUs and coastal dolphins and throughout observation,
the research vessel attempted to maintain a distance of 50m from ORUs and the dolphin
focal group, paralleling the school and allowing the undisturbed recording of encounters
(for full methodology: Bearzi 2003). Any boat disturbances, such as bowriding, were
recorded (for definitions of boat disturbance: Bearzi 2003). The survey area was divided
at the Marina del Rey harbor, and coastal surveys were conducted either to the north or
south of the harbor depending on favorable weather conditions.

Data for coastal and offshore bottlenose dolphins were divided exclusively based on
their distance from shore: all bottlenose dolphins observed during coastal surveys up to
1 km from shore were considered coastal; all bottlenose dolphins observed during surveys
at >lkm from shore were considered offshore. For this study, only data on coastal
bottlenose dolphins were analyzed. Behavioral data collected opportunistically from July

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Summary of research effort for coastal surveys in Santa Monica Bay conducted from 1997 to
2012. No data were collected: July 2002-August 2005, 2008, and 2010. BD=bottlenose dolphins.

1997

1998

1999

2000

2001

2002

2005

2006

2007

2009

2011

2012

Totals

N of surveys

220

N of sightings

209

Survey hours

123

214

155

119

121

937

Number of 5 min samples

722

345

212

273

147

135

182

2,281

Hours of BD observation

190

to December 1996 (58 hours of field observations) provided a framework of information
to design the behavioral sampling procedures systematically adopted from January 1997
onward (Bearzi 2003). Data were collected with laptop computers and occasionally with
tape recorders. Throughout all focal follows, the number of animals, behaviors of the
dolphin group, and aggregation/associations with other marine mammal species were
recorded at 5-minute intervals (Bearzi 2005). Behavioral data collected without ORUs
present and before focal groups encountered ORUs were used as controls for the
behavioral data in which ORUs were present. When more than one ORU was present in
the study area, each ORU was recorded as one ORU. The number of dolphins was later
verified through photo-identification and video analyses.

When coastal bottlenose dolphins were observed within 50m of ORUs, behavioral data
continued to be recorded at 5-minute intervals to determine changes in school size,
behavioral state, group formation, and surfacing mode as a result of their encounters
with ORUs. Observed responses to potential disturbances to the bottlenose dolphins (i.e.
the research vessel) and approximate distances between dolphin focal groups and ORUs
were recorded. Data analyses were performed using R and Microsoft Excel 2011. A
general linear model (GLM) was conducted in R and used to analyze which factors were
most likely to be correlated with behavioral changes. All other data analyses on sighting
length, number of dolphins involved in encounters, distances between dolphins and
ORUs, rates of dolphins’ behavioral changes were performed in Microsoft Excel 2011.
Species distribution data were plotted with ArcGIS 10.2.1.

Definitions

For the purposes of this study, the following definitions were used:

Dolphin school, dolphins in continuous association with each other and within visual
range of the survey team (Weller 1991);

Focal group : any group of animals observed in association, moving in the same
direction and usually engaged in the same activity (Shane 1990). Groups of animals not
belonging to the observed focal group and spotted at distance were recorded, but their
number was excluded from group size calculation;

Behavioral state : a broad category of activities, such as feeding behavior, which
integrates several individual behavior patterns into a recognizable pattern (Weaver 1987;
for additional definitions see Bearzi 2005);

Encounter, any instance in which at least one bottlenose dolphin was observed within
50 meters of any type and number of ORU;

Association (A): an encounter between one or more dolphin and one or more of the
four ORUs at a distance of 10-20 meters;

EFFECTS OF OCEAN RECREATIONAL USERS ON BOTTLENOSE DOLPHINS

Close Association ( CA ): an encounter between one or more dolphins and any ORU at
a distance of 3 meters up to 10 meters;

Potential Interaction (PI)', an encounter between one or more dolphins and any ORU
at a distance equal to or less than 3 meters;

Interaction (I): observed physical contact between an ORU and one or more dolphins.

Changes in behavioral states of the dolphin were defined as follows:

Avoidance - when one or more dolphins altered behavior to prevent a closer encounter
with an ORU;

Change in direction - when one or more dolphins maintained the same speed but
altered direction of approach to ORUs;

Dive - when one or more dolphins altered their behavior to display a dive longer than
15 seconds in the presence of ORUs;

Aerial reaction - when one or more dolphins displayed an aerial behavior (e.g., bow,
leap) in the presence of ORUs;

Vocal reaction - when one or more dolphins displayed an audible response such as
chuffing in the presence of ORUs;

Stationary reaction - when one or more dolphins displayed a motionless behavior on
the surface for more than five seconds (e.g., floating, rafting) in the presence of ORUs;

Percussive reaction - when one or more dolphins hit the water with any portion of the
body (e.g., breach, tail slap) in the presence of ORUs;

Neutral reaction - when one or more dolphins showed none of the above behavioral
changes in the presence of ORUs.

Results

Data were collected during 220 coastal surveys along the Santa Monica Bay coastline
in the years 1997-2012, with an average of three surveys per month (Table 1). A total of
937 hours were spent searching for coastal bottlenose dolphin resulting in 209 sightings,
82.78% of which were conducted in good weather conditions (Beaufort scale 2 or less). A
significantly higher number of surveys were carried out in the northern study area
(£=3.24, DF=26, P<0.005). Sightings lasted an average of 55.84 minutes (SD=37.74,
SE=2.61, range 5-250 minutes, fl=209).

During the study period, 145 encounters were recorded between 72 bottlenose dolphin
schools and ORUs throughout the survey area (34.45%, 72=209 sightings; Fig. 1,
Table 2). An average of nine dolphins were involved in each encounter (SD=4.66,
SE=0.03, range 2-19 individuals, 72=145 encounters). Few encounters lasted more than
five minutes (4.55%, 72= 176 encounters). It was common for a single bottlenose dolphin
focal group to experience two or more encounters with an ORU during observation
(40.28%, 72=72 schools; Table 2). Multiple ORUs were encountered by 16.67% of focal
groups (72=72), and surfers were the most common ORU encountered by focal groups
(77.93%, 72= 145 encounters; Table 2). Encounters occurred most commonly between
ORUs and bottlenose dolphins within 3 to 10 meters (close associations; 40%, 72=145
encounters; xi = 1 -41 , 72=22, p=0.02; Fig. 2, Fig. 3). Physical contact (interaction)
between an ORU and bottlenose dolphin occurred on only one occasion.

Bottlenose dolphins responded neutrally to 61.93% of encounters with ORUs (72 =176
behavioral responses, Fig. 4). Without ORUs present, behavioral changes occurred in
48.35% of 5-minute behavioral samples. When ORUs were present, however, behavioral
changes occurred in 31.43% of 5-minute samples. This difference in the rates of change
from one behavior to another was statistically significant (Fli20=4.799 p< 0.05),

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

ORUs

Fig. 2. Distances between different ORUs and bottlenose dolphin/s for each encounter.

suggesting that the presence of ORUs alters the rate of behavioral change in bottlenose
dolphins. The most common behavioral changes observed by a focal group were either
a change of surface mode (1 1.72%, a = 176 behavioral responses) or “other” reactions,
which included activities such as “chin up” (3.84%), “tail up” (0.57%), mating (0.57%),
circling (0.57%), splitting into subgroups (0.57%), or feeding (0.57%) (collectively: 6.25%,
n—\16). The least common response to an encounter with an ORU was one or more
dolphins displaying percussive or aerial behaviors (Fig. 4). Aerial reactions occurred
solely as a result of encounters with surfers (2.14%, n= 140 responses; Fig. 4).

Focal groups responded to the presence of the research vessel by bowriding during
4.17% of the 5-minute samples in which an encounter occurred. If the dolphin group was
bowriding in the 5-minute behavioral sample prior to the encounter, 75% of encounters
resulted in a behavioral change. Focal groups did not avoid or approach the vessel in any
5-minute interval in which an encounter occurred. However, throughout focal follows of
groups that encountered ORUs, 4.17% approached the vessel and 2.78% avoided the
vessel (w=72 schools). None of the focal groups that approached or avoided the vessel
exhibited a behavioral reaction to an encounter with an ORU.

Table 2. Number of schools and encounters per ORU type and number of schools that experienced
multiple ORU encounters.

Surfers

Swimmers

Kayakers

Paddle boarders

Total

N of schools

Percentage of total schools

66.67%

9.72%

15.28%

8.33%

100%

N of encounters

113

145

Percentage of total encounters

77.93%

5.52%

10.34%

6.21%

100%

Schools with > 1 encounter

Percentage of total schools

50.00%

14.29%

18.18%

33.33%

40.28%

Schools with >2 encounters

Percentage of total schools

31.25%

9.09%

16.67%

23.61%

Percentage of encounters

EFFECTS OF OCEAN RECREATIONAL USERS ON BOTTLENOSE DOLPHINS

118°50'0"W 118°40’0"W 118°30'0"W 118°20'0"W

The results of a general linear model indicated that the group form of the focal
dolphins during the 5-minute behavioral sample prior to the encounter might be a factor
in determining whether a behavioral change would occur as a result of an encounter.
Prior to encountering an ORU, dolphin groups that were at mixed distances (p<0.05,

* y

Behavioral responses

■ Surfer
Swimmer

■ Kayak

D Paddle
boarder

Fig. 4. Reactions (or lack of) to an encounter with one or more surfer, kayaker, stand-up paddle
boarder, and/or swimmer during a 5-minute behavioral interval.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 3. Number of encounters and schools in which an ORU approached a dolphin or a dolphin
approached an ORU.

ORU approach

Surfers

Swimmers

Kayakers

Paddle boarders

Total

Encounters

% of encounters

11.50%

12.50%

26.67%

22.22%

13.79%

Schools

% of schools

14.58%

14.29%

9.09%

22.22%

15.28%

Dolphin approach
Encounters

% of encounters

4.42%

6.67%

4.14%

Schools

% of schools

8.33%

9.09%

6.94%

SE=0.153), widely dispersed with more than 50 meters between individuals (p<0.05,
SE=0.171), or in a tight form with less than one adult body length between individuals
(p<0.05, SE= 0.462), were more likely to exhibit a behavioral change as a result of that
encounter. Only one focal group involved in an encounter was described as being widely
dispersed in the 5-minute behavioral interval prior to the encounter. No other behavioral
data for this 5-minute interval were correlated with a behavioral change as a result of an
encounter.

Bottlenose dolphins were approached by one or more ORU in 13.79% of all
encounters, and dolphin focal groups approached ORUs in 6.94% of recorded encounters
(>7=145 encounters; Table 3). When ORUs approached dolphins, behavioral changes
occurred in 50% of encounters (77=20), compared with 75% when dolphins approached
an ORU (n= 4). When dolphins approached ORUs, all behavioral changes were changes
in direction.

The distance between dolphins and an ORU during an encounter was an important
factor in determining whether a behavioral change would occur as a result of the
encounter (Fig. 5). This factor was more important than the type of ORU involved in the
encounter (Fig. 5). Encounters classified as potential interactions were significantly more
likely to lead to behavioral changes than encounters at distances greater than 3 meters
(p<0.001, SE= 0.126). The type and number of ORUs present and whether a human or
dolphin approached during the encounter were not significant when added to the model.
Because the addition of these variables increased the AIC score of the GLM (177.76 to
187.15), they were excluded from the final version.

Discussion

Surfers were the most common ORU encountered by dolphins in the study area. This
result is likely due to the fact that Southern California has been a top US surf destination
since the 1930’s (Irwin 1973) and the sport continues to grow in popularity. On the
contrary, swimmers were only occasionally involved in encounters with dolphins along
this coastline. This may be explained by the presence of these ORUs close to the beach
while coastal bottlenose dolphins tend to move slightly more offshore. In other areas
where dolphins are found in extremely shallow waters, encounters with swimmers appear
to be more likely, making these animals prone to being subjected to swim-with-the-
dolphins programs and food-provisioned encounters. For instance, in Florida (Samuels
and Bejder 2004; Cunningham-Smith et al. 2006), Tonga (Kessler et al. 2013), and New
Zealand (Neumann and Orams 2006), dolphins are frequently exposed to swim-with

EFFECTS OF OCEAN RECREATIONAL USERS ON BOTTLENOSE DOLPHINS

Catl-

CatPI -

CatU-

CatCA-

ORUPaddleboard

CatM-

ORUSurfer-

ORUSwimmer-

(Intercept) =1.23, R% S = 0.G28, RjJ = 0.153. -2X= 157.17. x2 = 0.85, AIC = 177.17

0.5 1 T5 2 2.5 3 3^ 4 4^5 5

Odds Ratios

Fig. 5. Visualized results of a GLM depicting the effect of ORU type and distance from the focal
group on dolphin behavioral responses. Cat I: Interactions, Cat PI: Potential Interactions, Cat U:
Unknown Cat CA: Close Associations, ORU P: Paddle boarders, Cat M: More than 20 meters, ORU S:
Surfers, ORU W: Swimmers.

dolphins programs and food-provisioned encounters with humans. In these situations,
swimmers actively pursued dolphins. Based on this study, bottlenose dolphins in the
Santa Monica Bay were neither discouraged (by frequent ORU encounters) nor
encouraged (through food-provisioning) from interacting with ORUs. Because encoun-
ters in this region occurred by chance, there were likely fewer total encounters between
dolphins and humans compared to those in incentivized or active pursuit settings like
Australia and Brazil (Samuels et al. 2000).

Encounters between stand-up paddle boarders and bottlenose dolphins were recorded
least often, and were observed mainly in the last few years of research. Stand-up paddle
boarding was introduced in California in 2002, and by 2009 it was the fastest growing
paddle-sport in North America2. This study shows that multiple encounters between
ORUs and dolphins were common, but few encounters lasted more than five minutes.
This could be attributed to several factors such as oceanographic conditions, specific
behavioral patterns displayed by dolphins in this area (e.g., large amounts of time spent
foraging; Bearzi 2005), and U.S. regulations such as the Marine Mammal Protection Act.
As a comparison, in areas where swim-with-the-dolphin programs are allowed, this type
of encounter typically was 35-60 minutes in duration (Constantine and Baker 1996;
Samuels et al. 2003).

2 Addison, Corran. 2010. The History of Stand Up Paddling. Editorial. SUP World Mag 2010.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Our results indicated that dolphins changed their behavior more often when no ORUs
were present. The research vessel appeared to have a negligible effect on dolphin
behavior. This suggests that the presence of ORUs may be altering dolphin behavior by
preventing behavioral changes rather than increasing the amount of change. However, far
more data were collected when no ORUs were present. The opportunistic nature of the
study may have affected the number of ORU encounters observed. More targeted data
collection on dolphin behavior in the presence of ORUs is needed to further elucidate this
phenomenon.

In the Santa Monica Bay, only 20% of the dolphins approached by ORUs changed
their direction of travel, compared to 40% in a New Zealand swim-with program
(Constantine and Baker 1996). In several cases, dolphins that were highly habituated to
ORUs and actively sought out human interaction displayed high rates of aggression
toward ORUs (Samuels and Bedjer 2004, Scheer 2010) or have sustained an
anthropogenic injury (Samuels and Bedjer 1998). On one occasion, aggressive behavior
by a dolphin resulted in a human death (Santos 1997). Our study did not reveal any
instances of bottlenose dolphin aggression toward ORUs or vice versa, but as dolphins
become increasingly habituated to ORU presence, aggression may become a concern.

As expected, our preliminary results indicated that the proximity of ORUs to dolphins
during encounters was the best predictor of whether a behavioral reaction would be
elicited from the dolphin. If one or more dolphin and an ORU came within three meters
of one another during an encounter, a behavioral change was likely to occur. Increased
dolphin behavioral changes as a result of close encounters with ORUs are consistent with
Bedjer et al. (1999) findings, which determined that the distance between an ORU and
dolphins during an encounter was the most reliable predictor of a change in dolphin
behavior. Williams (201 1) also found that orcas ( Orcinus orca ) were more likely to exhibit
avoidance behaviors when approached by kayaks at close range. Kayakers may be of
particular interest for looking at these types of interactions, as they can elicit the same
response from a dolphin school as a powerboat (Lusseau 2003), and have been found
to associate with dolphins more often than motorized vessels in the same area (Nichols
et al. 2001).

Conclusions

This preliminary study shows that coastal bottlenose dolphins in the Santa Monica Bay
are not subjected to prolonged encounters with ORUs, and these dolphins appear to be
generally “habituated”3 to ORU presence. The apparent reduction in behavioral changes
in response to ORUs, as well as the high occurrence of “no reactions,” are in accordance
with Filby et al. (2014) findings that habituated dolphins display reduced avoidance
behaviors.

Coastal bottlenose dolphins are now well recognized as a sentinel species4 and key
indicators of coastal habitat health (Simberloff 1998; Wells et al. 2004; Bossart 2011; Reif
2011). Although the current impact of ORU activities on bottlenose dolphin behavior
does not appear to be significant in Santa Monica Bay, there is a need to adopt
a precautionary approach in view of: a) the increasing presence of ORUs along this

3 Thorpe (1963) defines habituation as “the relative persistent waning of a response as a result of
repeated stimulation, which is not followed by any kind of reinforcement.”

4 Barometers for current or potential negative impacts on individual-and-population-level animal health
(Bossart 2011)

EFFECTS OF OCEAN RECREATIONAL USERS ON BOTTLENOSE DOLPHINS

coastline, and b) studies in other regions showing the adverse effects of human
recreational activities on coastal bottlenose dolphins.

Dolphin responses to increased human presence can have lasting population effects.
For instance, habituation due to increased human presence may have intensified the
probability of boat strike mortality in Hector’s dolphins (Stone and Yoshinaga 2000). In
New Zealand, the Hector’s dolphin population decreased due to a rise in dolphin
ecotourism (Bejder et al. 2006), and dolphins abandoned previously favored habitat
(Bedjer 1997) as a result of encounters with humans. Martinez et al. (2011) suggested that
encounters that seem positive (i.e. dolphins approaching swimmers) can ^still cause
a reduction in crucial behavior such as feeding. Additionally, it has been demonstrated
that dolphin presence can cause a significant increase in ORUs, thereby increasing the
disturbance (Ostman-Lind 2009). Kayakers in Hawaii changed their behavior when
dolphins were present in an attempt to get closer to the dolphin school (Timmel et al.
2008). Considering the growing popularity of recreational activities along the Santa
Monica Bay coastline, there could be a risk of a similar response in this area. Efforts
should be directed to ensure that ORUs are aware of marine mammal observation
guidelines, such as the requirement to maintain a minimum distance of 50 meters during
an encounter with a dolphin.

Educational programs conducted in marine protected areas to inform the public of the
importance of marine mammals have been shown to aid in the enforcement of the
parameters of the Marine Mammal Protection Act and decrease disturbances to marine
mammals (Gunvalson 2011). Similar educational programs designed to explain marine
mammal observation guidelines to ORUs along the Santa Monica Bay coastline could
further minimize the effects of ORU presence on bottlenose dolphins.

In conclusion, this preliminary investigation suggests the need of regular monitoring of
coastal bottlenose dolphins and encounters with ORUs to determine potential changes in
these animals’ behavior. Also, it suggests the necessity of implementing public education
program and management measures to ensure that dolphins remain undisturbed by the
growing number and diversity of anthropogenic presence in the bay.

Acknowledgements

Field research was funded by Ocean Conservation Society. Special thanks to the Los
Angeles Dolphin Project volunteers and researchers. Special acknowledgments to IFAW
for the Logger software. Fieldwork was carried out under the current laws of California
and the General Authorization for Scientific Research issued by NOAA (Files No. 856-
1366 and No. 5401811-00 and No. 16381).

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114(2), 2015, pp. 76-88

Salt Marsh Reduces Fecal Indicator Bacteria Input to Coastal
Waters in Southern California

Monique R. Myers1 and Richard F. Ambrose2’*

1 California Sea Grant Extension Program, University of California Marine Science
Institute, Santa Barbara, CA USA

2Department of Environmental Health Sciences, University of California, 46-078 CHS,
Box 951772, Los Angeles, CA 90095-1772 USA

Abstract. — We investigated fecal indicator bacteria (FIB) concentrations in water
and sediment from Carpinteria Salt Marsh, a medium-sized (93 ha), mostly natural
southern California coastal wetland. High FIB concentrations, exceeding recrea-
tional water quality standards, were found at inlet sites after winter storm events and
during a summer dry weather sampling event. Runoff entering the wetland had the
highest concentrations of FIB after large rain events and after rain events following
extended periods without rain. The watersheds with the greatest agricultural and
urban development draining into the wetland generally contributed the highest loads
of FIB, while the largest and least developed watershed contributed the lowest FIB
concentrations. Surface water exiting the wetland at the ocean contained relatively
low concentrations of FIB and only exceeded recreational water quality standards
after the largest rain event of the year. Bacterial concentrations in sediment were
only elevated after rain events, suggesting wetland sediment was not a reservoir for
bacteria. Our results provide evidence that moderate-sized tidal wetlands at the base
of moderately urbanized watersheds can attenuate FIB, improving coastal water
quality.

Runoff from coastal watersheds carries bacteria to the ocean, causing human health
risks. Fecal indicator bacteria (FIB), including Enterococcus (ENT) and Escherichia coli
(EC), are natural components of human and other mammal, reptile and bird intestinal
fauna used to indicate the likely presence of human pathogens that cause unhealthy
conditions for people recreating in coastal water (Balarajan et al. 1991; Haile et al. 1999).
Sources of FIB include faulty or overflowing sewage systems, homeless populations and
domestic and wild animals (including birds) (Mallin et al. 2001; Crowther et al. 2002).
FIB are generally present in high concentrations in sewage and in urban and agricultural
runoff during wet weather conditions (Wyer et al. 1994, 1996, 1998; Kay et al. 2005).
They may be concentrated on fine (<6pm) particles (Brown et al 2013), and can come
from streambed sediments (Wilkinson et al. 1995; Solo-Gabriele et al. 2000), intertidal
sediments (Obiri-Danso and Jones 2000; Ferguson et al. 2005) and watershed stores that
are flushed by rainfall (Sanders et al. 2005).

For example, stormwater runoff from the Santa Ana River in California was identified
as a significant source of near-shore pollution, carrying sediment, FIB, fecal indicator
viruses, and human pathogenic viruses (Jeng et al. 2005). FIB concentrations are used as
a guide to determine when Southern California beaches should be closed to recreational

* Corresponding author: rambrose@ucla.edu

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

activities. In one of the only epidemiological studies of coastal ocean bathing water, Haile
et al. (1999) determined that thresholds of 10,000 cfu of total coliform (TC), 104 cfu of
E. coli (EC) and 400 cfu of enterococcus (ENT) per 100 ml of sample had potentially
harmful human health effects at southern California beaches. These values are
incorporated in California Department of Health Services regulations, which furthermore
state that if the TC/EC ratio is <10, then TC must be <1000 cfu/ 100ml.

Coastal tidal wetlands could mitigate the risk of bacterial contamination. It is well
known that freshwater wetlands perform water treatment functions (Kay and
McDonald 1980; Breen et al. 1994; Kadlec and Knight 1996; Davies and Bavor
2000). Constructed freshwater wetlands may remove over 85% of FIB (Kadlec and
Knight 1996; Davies and Bavor 2000). While tidal wetlands may perform similar
functions, few studies have addressed this topic. Dorsey et al. (2010) found bacterial
loads were significantly reduced in a southern California coastal wetland during daylight
hours. A tidal wetland behind a flood defense wall reduced flux and concentration of
fecal indicator bacteria (FIB) in coastal waters by 97% (Kay et al. 2005). An analysis of
32 years of coliform data for Newport Bay wetland and tidal embayment in southern
California revealed a gradient of reduced bacterial concentration between inland sites
and the ocean (Pednekar et al. 2005). The highly urbanized Talbert Salt Marsh
watershed had a gradient of high to low FIB during dry weather run off, with highest
concentrations in the upstream watershed and lowest at adjacent coastal waters (Reeves
et al. 2004).

Coastal wetlands are a potential source of FIB since animals, such as birds, attracted
by the wetland produce FIB-laden feces. Bacteria either from within wetland or outside
sources may settle in slow-moving wetland waters where they can accumulate in sediment
and possibly re-grow (Solo-Gabriele et al. 2000; Desmarais et al. 2002; Ferguson et al.
2005). Bacteria harbored in the sediment may be tidally flushed out to coastal bathing
waters (Sanders et al. 2005). High concentrations of FIB were observed in California
coastal wetlands when sediments were resuspended during strong ebb flows (Dorsey et
al., 2010; Dorsey et al., 2013). At Talbert Salt Marsh, a small (10 ha), restored southern
California tidal wetland, outflow from the wetland increased bacterial concentration in
coastal waters (Grant et al. 2001). The reduced size of this wetland, less than l/100th its
original 1200 ha, and restored condition likely affected its ability to attenuate bacterial
populations. This study and others pointed to bird populations as a potentially important
bacteria source (Abulreesh et al. 2004). However, a modeling study of the same wetland
by Sanders et al. (2005) indicated that bird feces were a minor contributor to surface
water contamination, although they suggested that feces contributed to sediment FIB
loads and tidal flushing deposited bacteria in coastal waters.

Water entering the ocean from coastal wetlands is most likely to cause poor ocean
water quality after large rain events, when runoff flowing into the wetland has high
volume and FIB concentrations, or when water has been stored for long periods in the
wetland without tidal flushing (Reeves et al. 2004; Gersberg et al. 1995). For example,
immediately following the breaching of San Elijo Lagoon in San Diego County, water
quality close to the wetland mouth at an adjacent marine bathing beach was unhealthy
(Gersberg et al. 1995); the authors predicted healthy bathing conditions would return to
coastal waters within two weeks after breaching and one week after any large rain events.
Jeong et al. (2008) found that as the volume of runoff entering Talbert Salt Marsh
declined, the wetland was better able to attenuate FIB loads and coastal water quality
improved.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Land uses, areas and elevations of subwatersheds that drain into Carpinteria Salt Marsh.
Table adapted from Page and Court (unpublished data).

Subwatershed

Drainage area

Maximum elevation

Greenhouse

Orchard

km2

Western Creek

3.41

1175

36.7

10.8

26.7

Franklin Creek

11.60

533

63.3

5.4

68.8

5.9

Santa Monica Creek

15.61

1192

6.1

0.4

8.1

0.5

The capacity of a wetland to remove FIB is affected by a variety of physical and
ecological factors including: wetland size, sediment size, tidal flow, bird and other animal
populations, vegetation type, size and abundance and tidal creek length and shape.
Larger, more pristine wetlands, with longer tidal creeks for runoff to travel through and
longer residence time of bacteria and sediment-attached bacteria, likely are better at
reducing FIB loads to the coastal ocean. Carpinteria Salt Marsh (CSM) was selected as
the study location because it is a moderate-sized, mostly natural southern California
wetland. To determine if CSM acted to attenuate or exacerbate FIB loads to coastal
waters, we evaluated FIB concentrations at all the inlet sites where watershed runoff
entered the wetland and at the wetland-ocean interface where watershed runoff flowed to
the ocean after passing through the wetland. Our purpose was to investigate whether this
wetland protected coastal water quality.

Materials and Methods

Study Area

CSM is a 93 ha (230 acre) wetland of pickleweed habitat [Sarcocornia pacifica
( =Salicornia virginica)]. Located at 34°24’N and 119°31’30"W in Santa Barbara County,
California, it is influenced by a Mediterranean climate with heavy, intermittent rainfall in
the winter and dry, usually rainless summer months. Nearly 90% of average annual
rainfall occurs between November and April, carrying materials stored during the
summer from the watershed into the wetland1. The bird population, estimated by
monthly two-hour bird counts at high and low tides in 2003, is estimated to be between
150 (June) and 1000 (October) including all bird species (shorebirds, water fowl etc.)2

The watershed of CSM is composed of three subwatersheds that are drained by
Franklin and Santa Monica creeks and a western coastal plain area (Table 1; Fig. 1).
Land use cover within sub-watersheds was delineated by Page and Court3 using
a Geographic Information System (GIS) and a USGS 30 m digital elevation model
(DEM). By combining the GIS with a 1999 aerial photograph of the study area, they
divided land use within each sub-watershed into five categories, 1) greenhouse agriculture,
2) open-field agriculture, 3) orchard, 4) urban/residential and 5) undeveloped (Table 1).

Franklin and Santa Monica Creeks originate in the Los Padres National Forest,
a mountainous area whose foothill communities are composed of chaparral vegetation.

^erren, W.R, Page, H.M. and Saley, P. 1997. Carpinteria Salt Marsh: Management Plan for
a Southern California Estuary, Environmental Report No. 5, Museum of Systematics and Ecology,
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara.

2 Brooks, A.J. 2003. Unpublished data. Marine Science Institute University of California, Santa
Barbara, CA 93106-6150

3 Page, H.M. and Court, D. 1997. Unpublished data. Marine Science Institute University of California,
Santa Barbara, CA 93106-6150

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

Table 1. Extended.

Open field

Total agriculture

Urban

Undeveloped

Total

26.3

7.7

154

45.1

50.9

14.9

136.4

341

45.6

3.9

177.4

15.3

270.7

23.3

714.9

61.5

1163

5.5

0.4

19.7

1.3

32.5

2.1

1509

96.7

1561

with several kilometers of downstream coastal plain that are covered by a mixture of
urban and agricultural development, including greenhouses and fields for commercial
flower production and lemon and avocado orchards. The Franklin Creek sub-watershed
(1107 ha) is the furthest east and has the lowest elevation, lying partially in the foothills
but primarily within the coastal plain, where a large portion of the land is developed with
multi-use agriculture, residential areas and light commercial facilities4. The Franklin
Creek watershed is the most developed of the three subwatersheds, with 271 ha of urban
development and 177 ha of agricultural land. Most of Franklin Creek (75%) is concrete
lined with a concrete bottom (Robinson et al. 2002). Franklin Creek provides water to
a restored section of CSM. Both Franklin and Santa Monica creeks have been dredged by
County Flood Control, creating wide, deep, straight channels through the wetlands. The
Santa Monica Creek sub-watershed (1561 ha) is the largest and least-developed sub-
watershed, with over 90% composed of undeveloped land in the foothills and southern
slopes of the Santa Ynez Mountains. The portion of Santa Monica Creek flowing from
the northern edge of the city of Carpinteria into the salt marsh is channelized and
concrete lined with a concrete bottom.

The Western creeks drain a much smaller area (340 ha) that lies entirely within the
coastal plain. The Western subwatershed is nearly 50% agricultural and 15% urbanized
(Robinson et al. 2002). The creek water is entirely from coastal plain runoff, flowing
through a riparian corridor before entering the western side of CSM at three locations.
Two of these creeks (Creeks B1 and B2) flow together, but upon intersecting with the
railroad track located just outside the wetland border, Creek B1 diverges and flows
easterly until it enters the salt marsh at a separate location. The most northwestern creek
(Creek A) primarily drains greenhouse runoff. Degradation of the salt marsh due to
anthropogenic pollutants entering from urban and agricultural runoff has been
documented since the 1970s5 (Page et al. 1995; Hwang et al. 2006).

Field Sampling

To investigate the change in FIB concentrations as water moves through CSM, we
sampled water and sediment at the main water inlet and outlet sites to the wetland. Inlet
sites included one site each from Franklin Creek and Santa Monica Creek and three sites
from the Western subwatershed (Fig. 1). The mouth was sampled approximately 100 m
upstream from the wetland/ocean interface.

4Ferren, W.R. 1985. Carpinteria Salt Marsh: Environment, History, and Botanical Resources of
a Southern California Estuary, Santa Barbara, CA: Herbarium, Dept, of Biological Sciences, University of
California, Santa Barbara.

5 MacDonald, K. 1976. The natural resources of Carpinteria Marsh. Their status and future. Report to
the California Department of Fish and Game. Coastal Wetland Series #13.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Fig. 1. Carpinteria Salt Marsh with inlet sites where creeks drain into the marsh and the mouth site
identified. (Image from Google Earth.)

Tidal cycle may affect ENT loads, with highest populations occurring during spring
ebb tides (Boehm and Weisberg 2005), so collection of all samples was initiated within an
hour after the tide had changed from in-coming to out-going. Samples were always
collected during daylight but at different times of day to accommodate the tide. Thus,
different samples may have been exposed to UV radiation for different lengths of time on
different sampling dates. This would have had little influence on differences among sites
for a sampling date since all samples were collected within a few hours of each other, but
could potentially lead to differences between dates. However, UV exposure did not
appear to have an overriding influence on results since high FIB concentrations exceeding
health standards occurred in samples taken in the afternoon after extended UV exposure.
There were also differences in cloud cover, stream flow, and other environmental
variables that could have led to variability in FIB concentrations.

One surface water sample was collected at each site except on February 26, 2004 and
March 3, 2004 when five water samples were collected, and July 8, 2004 when three water
samples were taken in Franklin Creek (site F). No water sample was collected from
Franklin Creek in December. Samples were placed in sterile 50 ml Falcon tubes and
maintained on ice in a dark container immediately after collection until they were processed
within 6-8 hours. Water column salinity was measured at each site using a YSI 85 meter.

Samples were collected three times during dry weather between Nov 30, 2003 and Dec
10, 2003 and during dry weather on July 8, 2004. Samples also were taken seven times
during the winter rainy season in 2003/2004. Samples were taken immediately following
significant rain events of 0.5” or greater on Feb 3 (0.85”), Feb 19 (0.5”), Feb 26 (2.8”)
and Mar 3 (0.5”) in 2004; on Dec 16, 2003, one day following a small 0.12” rain event
that occurred after a month without rain; and on Jan 16 and 17, 2004 during the wet
season but not following a significant rain event. Precipitation measurements were taken
from the Carpinteria Fire Station (34°23’53” N, 119°3F06”W) (Santa Barbara County
Flood Control District 2004; http://www.countyofsb.org/pwd/water/hydro.htm).

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

Table 2. Salinity during water and sediment sampling. Dashes indicate no salinity reading was taken.
Bold text indicates 5 sediment samples taken, normal text indicates 3 sediment samples were taken, and
sites with grey text boxes were not sampled for sediment. Asterisk indicates that lab tests failed on Dec 4
for Western Creek B2 although salinity was measured.

Dry weather

Wet weather

Station

Nov 30

Dec 4

Dec 10

Jul 8

Dec 16

Jan 16

Jan 17

Feb 3

Feb 19

Feb 26

Mar 3

Mouth

Franklin Creek
Santa Monica

■

Creek

Western Creek B2

25*

Western Creek B1

Western Creek A

Sediment samples of at least 5 g of material were scraped from the top 1-3 cm of the
tidal creek substrate closest to the water’s edge during an outgoing low tide. In an
unpublished experiment, we found no difference in sediment bacterial concentrations at
different lateral locations on the tidal creek bank. The samples from each location were
stored in individual plastic bags. In general, three sediment samples one meter apart were
collected at each site, although this varied somewhat with five sediment samples taken at
most sites on Nov 30, 2003 and no samples on Feb 26 and Mar 3, 2004 (see Table 2).

Sample Analysis

Each sediment sample was homogenized and a 5 g sample was suspended in 35 ml of
phosphate buffer solution (0.3mM KH2P04, 2mM MgCl2) based on Standard Method
9221 A-3 (Greenberg et al. 1992). Samples were shaken by hand for one minute and then
centrifuged at 4°C for five minutes at 1000 rpm (Evanson and Ambrose 2006). Three
sediment samples and one water sample were processed per site. Using standard
procedures for Idexx Colilert®-18 and Enterolert® 97-well Quanti-trays, ten ml of each
sample of sediment supernatant and water were added to 90ml of dilution water and
analyzed for TC, EC and ENT. The highest value of FIB that could be measured was
2500 MPN/100 ml since sample dilutions were not made; bacteria levels exceeding this
maximum detection limit were not quantified.

Results

The Santa Monica Creek subwatershed, which was the largest (15.6 km2) but least
developed (97% undeveloped) catchment draining into Carpinteria Salt Marsh (Table 1),
generally had the cleanest water and sediment (Fig. 2 and 3). Santa Monica Creek water
EC levels were below health standards at all times and TC was relatively low. The
subwatersheds with high amounts of urbanization and agricultural development
(Table 1), Franklin Creek and the Western subwatersheds, had runoff with higher FIB
concentrations. Franklin Creek subwatershed was the most developed and had the
highest FIB in runoff entering the wetland. High levels of TC and ENT were present in
Franklin Creek water during wet and dry weather, with ENT exceeding health standards
during each sampling event except on December 10 and 16, 2003. The Western
subwatershed also had high FIB levels with water exceeding ENT health standards on at
least one occasion at each site during both wet and dry weather.

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Dry Weather

Wet Weather

M F SM B2 B1 A

Fig. 2. Concentrations of total coliform (TC), E. coli (EC) and Enterococcus (ENT) bacteria in
Carpinteria Salt Marsh water samples. Five inlet sites [Western Creek A (A), Western Creek B (B1
and B2), Franklin Creek (F), Santa Monica Creek (SM)] and one mouth (M) site were sampled
during two dry weather (Dec 10 and Jul 8) and three wet weather (Dec 16, Feb 26 and March 3)
sampling events. No water sample was collected from Franklin Creek in Dec. Error bars indicate
MPN confidence interval based on SE of five method replicates for Feb 26 and Mar 3, three for Jul
8. Horizontal lines indicate the single-sample water quality standards for EC and ENT; the single-
sample standard for TC (10,000 cfu) is above the maximum detection limit (2,500 MPN/100 ml) for
the samples.

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

Sediment

0.12" rain 0.85" rain 0.5" rain

1000
100
10
1

0.1

Dec 1 Jan 1 Feb 1 Mar 1 Jul 8

Water

Date

Fig. 3. Concentrations of total coliform (TC), E. coli (EC) and Enterococcus (ENT) bacteria in
sediment samples taken between November 30, 2003 and July 8, 2004 and in water samples taken between
November 30, 2003 and March 3, 2004. Five inlet sites [Creek A (A), Creek B (B 1 and B2), Franklin Creek
(F), Santa Monica Creek (SM)] and one mouth (M) site were sampled. For sediment samples, error bars
are based on SE of three replicate samples; where error bars do not show, the error bar is smaller than the
symbol except for B2 for July 8, when only one replicate analysis was successful. Arrows indicate rainfall
events, with amount of rain noted. Horizontal lines indicate the single-sample water quality standards for
EC and ENT; the single-sample standard for TC (10,000 cfu) is above the maximum detection limit for the
samples (2,500 MPN/100 ml). Standards have not been established for sediment.

The largest winter rain event [7.1 cm (2.8”) on February 26, 2004] produced the highest
ENT and TC values at all sites (Fig. 2). The ENT health standard was exceeded at all
sites. This was the only occasion when site B2, which generally had the lowest bacteria
concentrations in the Western subwatershed, had similar or higher FIB levels than A and

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

B 1 . Only after this largest rain event did Santa Monica Creek water entering the wetland
exceed ENT standards. It also was the only occasion when water draining from the
wetland mouth into the ocean exceeded health standards and had concentrations of TC
over 2500 MPN/100 ml (Fig. 2).

Generally, FIB levels were low during dry weather and EC levels were low, not
exceeding health standards, during both wet and dry weather (Fig. 3). On December 10,
2003, both creek flow rates and FIB levels were low. Health standards were not exceeded
and TC was low compared to wet weather values. However, on July 8, 2004 after several
months without rain, FIB values were relatively high. ENT water quality standards were
exceeded at all Western and Franklin Creek sites and TC values were over 2500 MPN/100
ml for Creeks A and B1 and Franklin Creek (Fig. 2). During this time creek flow rates
were also high, indicating an upstream water source other than rainwater, likely from
agricultural irrigation of greenhouses and/or field crops.

FIB loads in sediment were affected by rain events, although the pattern of increased
FIB concentrations following storms was not as pronounced as in water samples,
possibly due to generally low bacteria concentrations, particularly for EC and ENT
(Fig. 3). At site B1 sediment mean values of EC varied between 1 and 166 MPN/g and
ENT values varied between 4 and 215 MPN/g, while in water mean EC and ENT values
at the same sites were as high as 1396 and 1848 MPN/g, respectively. Elevated TC was
detected in both water and sediment after rain events (Fig. 3). While EC and ENT in
sediment were generally low, relatively high values of ENT occurred at Western creek
sites after the Dec 15 rain event, when values in water were also high. (Sediment data were
not available following the largest winter rain event on February 26, 2004). Santa Monica
Creek sediment also had a relatively high ENT value during dry weather (Fig. 3).

At the wetland mouth, where water entered the ocean, FIB concentrations were usually
low, not exceeding recreational water quality standards (Fig. 2). FIB concentrations were
only elevated at the mouth following the largest winter rain event (on February 26, 2004),
when TC and ENT were over 2500 MPN/100 ml, vastly exceeding ENT health standards.

Salinity varied widely by sampling location and time (Table 2). The mouth site had
near-seawater salinity during all sampling times except February 26, 2004, which was
after the largest rain event. Franklin and Santa Monica Creeks also were usually close to
seawater salinity, but salinities were reduced after rainfall. The Western Creek sites had
lower salinities, even during dry weather, indicating their influence by persistent
freshwater inflow not related to storms.

Discussion

Watershed Input to Wetland

FIB concentrations entering CSM were related to the amount of watershed urbanization
rather than watershed size. The largest, least-developed watershed draining into the marsh
had water with low FIB, while the smaller, more highly developed watersheds produced
much higher FIB concentrations. Watershed land use has been correlated with FIB
concentrations in coastal waters around the United Kingdom (Crowther et al. 2002; Kay
et al. 2005). Urbanization was the primary predictor of EC concentrations in popular
bathing beaches around Clacton, UK as well as for EC and ENT concentrations in surface
waters of the 1583 km2 Ribble drainage basin (Kay et al. 2005).

In CSM, high FIB values occurred after rain events, as has been found in other
southern California wetlands. For example, TC in Santa Monica Bay and the Santa Ana
river wetlands peaked on the same day as the rain event and decreased within one day

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

(Haile et al. 1999; Evanson and Ambrose 2006) and ENT and EC in the Santa Ana river
wetlands peaked on the day of the storm or within several days (Evanson and Ambrose
2006). Overall the highest FIB values occurred following the largest rain event of the year
on February 26, 2004 (2.8”) and after the December 15, 2003 rain event that followed
over a month without precipitation, the longest dry period preceding a rain event during
this study. The 7.1 cm (2.8”) rain event likely was large enough to saturate soil and
produce field runoff as well as high volumes of impervious surface runoff. Although the
December 15 rain event was small 0.3 cm (0.12”), it likely flushed bacteria that had
accumulated over a long duration (relative to the dry period duration preceding other
storms sampled).

Western Creek flow rates in July, while not quantified, appeared similar to those that
occurred the day after rain events rather than the typical dry weather flow, likely due to
agricultural and greenhouse irrigation runoff from facilities as close as a kilometer
upstream of the wetland (Page et al. 1995). Some July dry weather values of TC, EC and
ENT in water were similar to or higher than bacterial concentrations from creek water
sampled directly following rain events.

Bacteria Removal

While surface waters entering CSM often had high FIB concentrations (during both
wet and dry weather), they generally exited the wetland with low FIB values. Although
the number of samples taken during this study was relatively low, sediment and water
samples were collected simultaneously at five inlets sites and the wetland mouth,
providing a synoptic view of FIB inputs and output over a season that included both wet
and dry weather sampling. The lower FIB concentrations at the wetland mouth
compared to water entering the wetland suggest that bacteria populations decreased as
a result of flowing through the wetland.

Bacteria removal from CSM waters likely was the result of processes such as predation,
destruction by ultraviolet light, and sedimentation (i.e. adsorbing to particles that then
settle to the bottom) (Alkan et al. 1995; Noble et al., 2004; Dorsey et al., 2010, Dorsey et al.,
2013). While an estimated 65-85% of the total fecal coliform, EC and ENT remain free-
floating in the water column and do not settle (Jeng et al. 2005; Schillinger and Gannon
1985), the low flow rate within CSM tidal channels allows for sedimentation and increased
exposure of FIB to harmful solar radiation, thereby reducing FIB concentrations in
a similar manner to a reservoir system or a constructed wetland (Kay and McDonald 1980;
Kay et al. 1999). As with freshwater wetlands, UV was probably important for FIB
destruction since sunshine is abundant year-round in southern California and CSM tidal
creeks are shallow, allowing high UV exposure. FIB concentrations also may have been
reduced due to dilution by tidal water, although this factor was minimized by sampling
during an outgoing tide.

FIB loads at site B2 in the Western subwatershed were generally lower than at sites A
and Bl, possibly because this water travelled approximately 100 yards along the wetland
fringe before entering the wetland. This area beside the railroad track, while not wetland
habitat, was a dirt ditch lined with plants. The extra amount of both travel time and
exposure likely contributed to FIB removal.

Within-wetland sources, such as bacterial growth in the sediment or feces from bird
populations, did not appear to significantly contribute to surface water FIB loads. Storm
flow re-suspension during winter could have contributed to increased bacterial
populations in the water (Steets and Holden 2003), but sediment FIB were generally

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

low and unlikely a large contributor during our study. Low values of bacteria in the
sediment indicated FIB were not stored there nor did they re-grow to high concentrations
in wetland sediment. Grant et al. (2001) suggested that Talbert Marsh, a small (10 ha)
southern California wetland with a similar bird population (1180 individuals) to CSM
(a population maximum of 171-2200 individuals6), exacerbated FIB concentrations in
coastal runoff, pointing to bird populations as an important within-wetland FIB source.
A subsequent model of FIB loads to Talbert Marsh, which included urban runoff,
erosion of contaminated sediments, bird feces, and combinations of these factors,
indicated that direct runoff of bird feces was not likely to be a major source in this small
wetland (Sanders et al. 2005). The low FIB concentrations at the mouth (wetland-ocean
interface) of CSM suggest that birds in CSM were not significantly increasing FIB loads
entering the ocean, despite the frequent concentration of birds near the wetland mouth
(personal observations).

Besides removal of bacteria, lower FIB concentrations could be due to dilution by
seawater. Salinity varied widely during sampling (range 2-37). Some dilution undoubtedly
occurred at times because salinity was over 30 at many stations during at least some
sampling times, particularly during dry weather and at the mouth. We minimized dilution
effects by sampling on the falling tide. Nonetheless, reductions in FIB concentrations
would have been due to a combination of dilution and removal processes.

The capacity of a wetland to remove contaminants is related to the volume of water
flowing through the wetland and wetland size. Not surprisingly CSM, at 93 ha at the base of
a 3,000 ha watershed, of which 350 ha was urbanized, was better able to attenuate FIB than
Talbert Marsh, a small 10 ha marsh located at the bottom of a highly developed 3,400 ha
watershed. Jeong et al. (2008) indicated that Talbert Salt Marsh was able to remove FIB
more efficiently as the volume of storm water runoff entering the marsh decreased. They
concluded that a wetland may have a maximum capacity to attenuate contaminants; when
loads exceed this value the wetland becomes a net source of contaminants to coastal waters.

Our work suggests that a moderate-sized wetland was able to attenuate FIB during
most rain events. Reducing the size of a wetland, such as occurred at Talbert Salt Marsh
(historically 1200 ha, now 10 ha), reduces its capacity to remove contaminants.
Expansion of existing wetland area through restoration may partially restore its capacity
for attenuating FIB, although this possibility remains to be tested.

Conclusions

This work provides evidence that a 93 ha southern California wetland is an adequate
size to allow for natural removal of FIB when the contributing watershed(s) have low to
moderate levels of development. With relatively little loss of original wetland habitat and
only moderate levels of development in its watershed, CSM is able to provide a valuable
ecosystem service of improving the quality of water before it reaches the coastal ocean.
Coastal water quality appeared to only be compromised by runoff during a large storm
event when high volumes of bacteria-laden water overwhelmed the wetland’s ability to
reduce loads through sedimentation, die off, and/or dilution.

Acknowledgements

We thank Dr. Andrew Brooks for permission to work in the Carpinteria Salt Marsh
Reserve of the University of California Natural Reserve System. Dr. Patricia Holden

6Gaede, P. 2007. Unpublished data. 918 Fellowship Road, Santa Barbara, CA 93109.

SALT MARSH REDUCES FECAL INDICATOR BACTERIA

provided lab space at the University of California, Santa Barbara. Support was
provided by a grant from the University of California Marine Council (Stanley Grant,
Principle Investigator). The manuscript benefitted from comments by two anonymous
reviewers.

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Bull. Southern California Acad. Sci.

114(2), 2015, pp. 89-97

Asian Fish Tapeworm ( Bothriocephalus acheilognathi )
Infecting a Wild Population of Convict Cichlid (. Archocentrus
nigrofasciatus) in Southwestern California

Victoria E. Matey,1 Edward L. Ervin,2 and Tim E. Hovey3

1 Department of Biology, San Diego State University, 5500 Campanile Dr., San Diego,

CA 92182-4614

2 Merkel & Associates, Inc., 5434 Ruffin Road, San Diego, CA 92123
3 California Department of Fish and Wildlife, 21729 Canyon Heights Circle,

Santa Clarita, CA 91390

Abstract. — In September 2007 and May 2014, the Asian fish tapeworm, Bothrioce-
phalus acheilognathi Yamaguti,1934 (Cestoda: Bothriocephalidea), was found in
populations of the non-native convict cichlid {Archocentrus nigrofasciatus) and
mosquitofish {Gambusia affinis) collected from the discharge channel of a water
treatment plant in Los Angeles County. Prevalence and mean intensity of infection
of 450 convict cichlids and 70 mosquitofish were 55.3%/9.3 and 11%/1.4,
respectively. Overall prevalence and mean intensity of infection in the convict
cichlid was higher in 2007 (92%/12.3) than in 2014 (37%/5.4). In 2007, parameters of
infection were size-dependent. The highest prevalence/mean intensity of infection
was revealed in small fish (100%/15.5) and the lowest in large fish (66.7%/1.5). No
statistically significant differences in infection parameters were found in convict
cichlids of different size classes in 2014. This paper provides the first documented
record of the Asian fish tapeworm infecting a wild population of the convict cichlid
in the U.S.

Introduction of exotic fish into novel aquatic ecosystems is sometimes accompanied by
the unintentional transmission of additional species dangerous to populations of endemic
fish, commercial fish and aquaculture (Bauer et al. 1973, Hoffman and Shubert 1984,
Scholz 1999, Salgalo-Maldonado and Pineda-Lopez 2003). One such invader, the Asian
fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Bothriocepha-
lidea), was imported from East Asia to Europe and the Americas during the 1960s and
1970s with herbivorous cyprinids, predominantly grass carp {Ctenopharyngodon idella ),
to control growth of aquatic vegetation in freshwater ecosystems (Hoffman 1999,
Williams and Jones 1994, Choudhury and Cole 2012). The Asian fish tapeworm
(hereafter, Asian tapeworm) has a simple life cycle that requires only two hosts:
a definitive host, a fish in which larval stages develop into adult worm producing eggs,
and an intermediate host, a cyclopoid copepod, which is a transmitter of the early larval
stage (Liao and Shin 1956). The entire life cycle is temperature-dependent, and under
optimal temperature, 25° C, can be completed in eighteen days (Bauer et al. 1973).

Due to low specificity for both intermediate and definitive hosts, and by colonizing
other cyprinid as well as poeciliid hosts, the Asian tapeworm easily became established
within native fish populations in new regions and continents, eventually resulting in its

Corresponding author: vmatey@mail.sdsu.edu

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

current global distribution (Hoffman 1999, Font 2003, Choudhury and Cole 2012).
Presently, it has been reported in 104 fish species in 14 families and seven orders from
almost every continent except Antarctica (Salgado-Maldonado and Pineda-Lopez 2003).
It is pathogenic to wild fish and aquaculture stock and may cause disease and even
mortality events (Bauer et al. 1973, Scott and Grizzle 1979, Hoffman 1980, Granath and
Esch 1983c, Hoole and Nissan 1994, Heckmann 2000, Hansen et al. 2006, Han et al.
2010, Britton 2011). In the U.S., after the initial discovery of the Asian tapeworm in
Florida in 1975 (Hoffman 1980), it has been reported from 13 additional states (Arizona,
California, Colorado, Hawai’i, Kansas, Michigan, Nevada, New Hampshire, New
Mexico, North Carolina, Texas, Utah and Wisconsin), both in the wild or in fish
hatcheries (Hoffman and Schubert 1984, Heckmann and Deacon 1987, Riggs and Esch
1987, Heckmann et al. 1993, Brouder and Hoffnagle 1997, Kuperman et al. 2002, Bean
et al. 2007, Pullen et al. 2009, Archdeacon et al. 2010, Choudhury and Cole 2012). In
California, the Asian tapeworm was first discovered in 1987 in grass carp, collected from
irrigation reservoirs in Riverside and Imperial counties and in golden shiners
(Notemigonus crysoleucas) collected from a fish farm in San Diego County (Chen 1987).

Surveys conducted in 1999-2001 revealed seven additional fish species (six cyprinid, one
poecillid) in southern California infected by the Asian tapeworm (Kuperman et al. 2002).
Of the six infected cyprinids, the arroyo chub ( Gila orcutti ) and Mojave tui chub
(Siphateles bicolor mohavensis ) are native, while the other four, common carp ( Cyprinus
carpio ), golden shiner, goldfish ( Carassius auratus) and fathead minnow ( Pimephales
promelas ), are introduced. The single infected poecillid is the introduced mosquitofish. In
June 2007, a population of convict cichlids ( Archocentrus nigrofasciatus ) was reported
from the perennial discharge channel of a water treatment plant in Los Angeles County
(Hovey and Swift 2012). The convict cichlid is native to Central America and is a tropical
thermophilic species with a minimum temperature tolerance of 20 C (Conkel 1993,
Bussing 1998). The first U.S. records of the convict cichlid were in Nevada where the fish
were discovered in two natural warm springs (Deacon et al. 1964, Hubbs and Deacon
1965). In Mexico, introduced convict cichlids (as, Cichlasoma nigrofasciatus ) were found
to be infected by the Asian tapeworm (Salgado-Maldonado and Pineda-Lopez 2003), but
no information on fish infection by this parasite was known for the U.S. The goal of the
present study was to investigate whether the recently discovered population of the convict
cichlid in California was infected by the Asian tapeworm.

Materials and Methods

Fish were collected for parasitological examination from a discharge channel with
elevated water temperature 26° C [±1.5° C]. The source of the thermally elevated water
was the treated discharge from the Rio Vista Water Treatment Plant that feeds directly
into the Santa Clara River, Los Angeles County (34.423806, -1 18.540511; WGS84). The
willow riparian scrub vegetation supported by the perennial discharge channel is
restricted to the southern bank of the much wider, dry sandy river bed of the Santa Clara
River. The outflow travels approximately 800 m before flowing subsurface. It is believed
that the established convict cichlid population at this location originated from released
aquarium fish (Hovey and Swift 2012). Other fish species that occurred at the study site
were the native arroyo chub, and the non-native mosquitofish, prickly sculpin ( Cottus
asper ), black bullhead ( Ameiurus melas), goldfish, and common carp (var. koi) (Hovey,
unpub. field notes). Of them, only mosquitofish were available for parasitological
examination.

ASIAN FISH TAPEWORM INFECTING CONVICT CICHLIDS IN CALIFORNIA

Table 1. Prevalence and mean intensity of infection of convict cichlids ( Archocentrus nigrofasciatus )
and mosquitofish ( Gambusia affinis) by the Asian fish tapeworm ( Bothriocephalus acheilognathi) in 2007
and 2014.

Sample

Fish total length

Intensity

Size class

size (N)

(TL) range, mm

Prevalence (%)

Mean ±SD Range

Convict cichlids
September 2007

Entire sample

150

25 - 130

92.0

12.3 ± 12.8

1 - 101

Class 1, small fish

100

25 - 59

100A*

15.5 ± 13. 7B*

1 - 101

Class 2, medium fish

61 - 86

80. 0C*

3.9 ± 4.5d*

1 - 22

Class 3, large fish

88 - 1303

66. 6e*

1.5 ± 0.7F**

1 - 3

May 2014

Entire sample

300

39-112

37.0

5.4 ± 5.2

1 - 24

Class 1, small fish

39 - 59

32.4°

4.8 ± 4.5h

1 - 19

Class 2, medium fish

155

60 - 80

41.9°

5.7 ± 5.4h

1 - 24

Class 3, large fish

88 - 112

25.4°

3.9 ± 3.5h

1 - 14

Mosquitofish

May 2014

Entire sample

43 - 65

15.7

1.4 ± 0.7

1 - 3

A-H: Within the category, mean values sharing the same letter are not significantly different (P < 0.05)
*/?-value <0.001
**/?-value >0.05

A total of 450 convict cichlids and 70 mosquitofish were used for this study. On 1 1
September 2007, only three months after the discovery of convict cichlids in the channel,
150 convict cichlids were collected to be examined for the presence of the Asian
tapeworm. A second fish collection took place on 1 May 2014 and included 300 convict
cichlids and 70 mosquitofish. Fish were captured by seine net and placed into 5-gallon
buckets containing channel water. Within three hours of being captured, the fish were
removed from the water, transferred into plastic bags and placed into a freezer. The fish
were then transported while still frozen, and stored at San Diego State University in
a freezer until the commencement of parasitological examinations. After being thawed,
total length (TL) of each individual was measured to the nearest mm. The TL of convict
cichlids collected in 2007 ranged from 25 mm to 130 mm and in 2014 ranged from 39 mm
to 112 mm (Table 1). To calculate infection parameters, convict cichlids were separated
into three size classes: class 1 (small), class 2 (medium) and class 3 (large) (Tables 1, 2).
We arbitrarily selected the range for each of the three size classes based on the clustering
of sizes. The body cavities were opened and digestive tracks removed. After a longitudinal
incision of the intestine, tapeworms were carefully teased from the intestinal wall, rinsed
in 0.85% saline and placed into Petri dishes with the same solution. Tapeworm
identification was made using the reference keys by Bykhovskaya-Pavlovskaya et al.
(1964) and Hoffman (1999). Tapeworms from each fish were enumerated to determine
the prevalence, the proportion of the hosts infected, and mean intensity of infection, the
mean number of parasites in the infected hosts (Bush et al. 1997). The number of fish
sampled, prevalence and mean intensity are provided in Table 1. A total number of
tapeworms found in fish collected in 2007 and 2014, number of tapeworms in each size
class of fish and the percentage of immature and mature tapeworms are presented in
Table 2. Images of immature and mature tapeworms were obtained by light microscopy
(LM) and scanning electron microscopy (SEM). For LM, 10 tapeworms and several

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 2. Number and percentage of immature and mature Asian fish tapeworms ( Bothriocephalus
acheilognathi) recovered from convict cichlids {Archocentrus nigrofasciatus) in 2007 and 2014.

Stage of tapeworm development, %

Size class of convict cichlids Number of tapeworms Immature Mature

Entire sample

September 2007
1710

43.2

56.8

Class 1, small fish

1558

45.3

54.7

Class 2, medium fish

137

24.1

75.9

Class 3, large fish

13.3

86.7

Entire sample

May 2014
597

83.9

16.1

Class 1, small fish

133

86.5

13.5

Class 2, medium fish

393

86.1

13.9

Class 3, large fish

64.8

35.2

pieces of intestinal wall with tapeworms attached were examined with a Nikon Eclipse
E200 microscope (Melville, NY) and photographed under magnification x40. For SEM,
eight mature tapeworms fixed in 70% alcohol were rinsed in phosphate buffer saline,
post-fixed in 1% osmium tetroxide, dehydrated in ascending concentrations of ethanol
from 50% to 100%, critical-point dried, sputter-coated with platinum, and examined
using a FEI Quanta 450 scanning electron microscope (Hillboro, OR). A series of
10 preserved Asian fish tapeworms collected from the convict cichlids was deposited into
the Harold W. Manter Laboratory of Parasitology, University of Nebraska, Lincoln,
Nebraska (HWML 64742).

Prevalence of infection in convict cichlids was tabulated by fish size (small, medium,
large) for 2007 and 2014 separately. The resulting 2x3 contingency table was analyzed
using a Pearson’s chi-squared test. Mean intensity in fish from three size classes in 2007
and 2014 were estimated using the two-sample independent Mann-Whitney U test.

Results

The Asian tapeworm was the only intestinal parasite found in the 450 convict cichlids
collected from the discharge channel of a water treatment plant in September 2007 and
May 2014. The prevalence and mean intensity of fish infections were higher in the 2007
sample than in the 2014 sample (Table 1). In the 2007 sample, parameters of infection
were different among fish from the three size classes (Table 1). The highest prevalence
and mean intensity of infection was found in small fish while the lowest were found in
large fish (Table 1). Intensity of infection in fish from different size classes varied widely
(Table 1). The highest parasite loads in small, medium and large fish were 101, 22, and 3,
respectively. Both mature and immature Asian tapeworms were recovered from fish.
Mature Asian tapeworms had a heart-shaped scolex with deep long bothria, a flattened
attachment disc (Fig. 1A), and a perfectly segmented strobila composed of wide
proglottids containing rosette-shaped ovaries filled with eggs (Fig. IB, C). Immature
tapeworms were represented by individuals at various developmental stages, ranging
from worms having a small scolex and non-segmented body, to worms with a well-shaped
scolex but still poorly segmented strobila and an underdeveloped reproductive system
(Figs. ID, E). In 2007, almost 60% of tapeworms recovered from the convict cichlids
were represented by mature worms (Table 2). The highest percent of mature tapeworms
was found in large (class 3) fish, and small (class 1) fish contained an almost equal

ASIAN FISH TAPEWORM INFECTING CONVICT CICHLIDS IN CALIFORNIA

Fig. 1. Representative scanning electron microscope micrographs (A, B) and light microscope
micrographs (C-E) of the Asian fish tapeworm Bothriocephalus acheilognathi. A) Mature worm - heart-
shaped scolex with long bothria and flatten attachment disc; B) Mature worm - segmented strobila with
mature proglottids and uterine pores; C) Mature worm - segmented strobila with mature proglottids and
rosette-shaped ovaries; D) Immature worm - small scolex with short bothri, pre-proglottid formation of
strobila; E) Immature worm - well developed scolex and early stage proglottid formation of strobilla. Ad -
adhesive disk; lw - intestinal wall; Ov - ovary; Pr - proglottid; Sc - scolex; St - strobila. Black-head arrows
indicate bothria, white-head arrow indicates uterine pore. Scale bars: 20pm.

number of mature and immature tapeworms (Table 2). In the 2014 sample, overall
prevalence and mean intensity of infection in convict cichlids were 2.5 times and 3 times
lower, respectively, than the 2007 sample (Table 1). Contrary to the 2007 results, no
significant difference was found in the infection parameters of fish from the three size
classes (Table 1). The highest load of Asian tapeworms at 24 individuals was found in
a medium (class 2) fish. In contrast to 2007 results, about 84% of Asian tapeworms
recovered from convict cichlids were immature (Table 1). The highest percent of mature
Asian tapeworms was found in large (class 3) fish (Table 2). Of the 70 mosquitofish, also
collected in May 2014, only eleven were infected by Asian tapeworms, with the lowest
infection level being one tapeworm (Table 1). Of the fifteen Asian tapeworms found, 87%
were immature (Table 2).

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Discussion

The present paper documents the first record of the Asian tapeworm in a wild
population of the convict cichlid in the U.S. Finding the Asian tapeworm in years 2007
and 2014 indicates the presence of a persistent reservoir of infection in the channel
conveying the thermally elevated discharge from the Rio Vista Water Treatment Plant in
Los Angeles County. As only convict cichlids and mosquitofish were available for
parasitological examination, we have no information on the infection in five other species
of fish inhabiting this channel. We cannot exclude that three fish species, arroyo chub,
goldfish and common carp, all well-known for their susceptibility to Asian tapeworm
(Kuperman et al. 2002), could contribute to the persistence of the parasite at this site.

The artificially elevated water temperature of 26° C [±1.5° C] was optimal for the
growth and development of the Asian tapeworm. Stimulating effect of high temperature
on parasite transmission, infectivity, development and infrapopulation structure has been
previously reported (Bauer et al. 1973, Sankurathri and Holmes 1976, Granath and Esch
1983a, b, c, Dobson and Carper 1992, Khan 2012). In our study, the overall infection rate
in the autumn sample (2007) was higher than in the spring sample (2014). These results
appear to be largely in agreement with the most common pattern of the seasonal
dynamics of populations of the Asian tapeworm, in which elevation of water temperature
was considered a critical factor controlling infectivity, development and infrapopulation
structure (Bauer et al. 1973, Granath and Esch 1983a, b, c).

However, the water temperature at our collection site remained nearly constant
throughout the year. Our sampling effort, separated by seven years, is long enough for
significant changes to have occurred in the ecosystem we examined. Based on our limited
sampling effort we were unable to identify alternative abiotic factors that, acting singly or
synergistically with biotic factors, might affect fish infection by the Asian tapeworm. The
last ones may include fluctuations in the biomass of zooplankton including cyclopoid
copepod community (the intermediate host of the Asian tapeworm), shortage in biomass
of phytoplankton (the food web for copepods), copepod species diversity (not all
copepods are an efficient intermediate host for the Asian tapeworm) and changes in the
structure of the fish community inhabiting the collection site. Water quality may also
contribute to the rate of fish infection. It is possible that the chemical composition of the
discharged water from the water treatment plant may affect both fish and cyclopoid
copepods known for their high sensitivity to water chemistry (Ferdous and Muktadir
2009). It is also known that in the case of fish infected by the Asian tapeworm, the pattern
of high prevalence of infection may be followed by low prevalence (Heckmann and
Deacon 1987, Archdeacon et al. 2010), and we cannot exclude the possibility that our
samplings do not fit this seasonal pattern because of the different seasons and years of
sampling.

Different parameters of infection were recorded in convict cichlids in the autumn 2007
and spring 2014 samples; overall values varied among size classes. In the 2007 sample,
both prevalence and mean intensity of infection were size-dependent. Prevalence of
infection reached 100% in small (class 1) fish but only 66.7 % in large (class 3) fish
(Table 1). There was an inverse relationship between the size class of fish and the number
of worms they harbored (Table 1). The highest parasite load of 101 Asian tapeworms was
carried by one of the smallest fish (TL 31 mm). Lower values of infection rate in larger
fish may be associated with the elimination of heavily infected individuals, the expelling
of a number of worms due to their competition for food source, or stronger immunity of
large fish compared to the smaller fish. The stage of worm maturation was inverse to the

ASIAN FISH TAPEWORM INFECTING CONVICT CICHLIDS IN CALIFORNIA

intensity of infection, and consequently to fish size (Table 2). For example, large fish
carried a maximum of three Asian tapeworms, most of them mature, while in the heavily
infected smaller fish, the percent of mature and immature worms were nearly equal at
45.2% and 54.7%, respectively. Based on the rate at which the Asian tapeworm developed
at 26° C [±1.5° C], the predominance of mature tapeworms infecting fish in 2007
indicates that this infection was at least one month old (Bauer et al. 1973, Williams and
Jones 1994). In the spring sample (2014) we documented comparatively low infection
levels in convict cichlids, regardless of fish size (Table 1). The highest parasite load of
24 Asian tapeworms was found in a medium (class 2) fish (TL 73 mm). There was an
inverse relationship between the size class of fish and the number of worms they harbored
(Table 1). In contrast to the fall sample (2007), the percent of mature tapeworms for all
three fish size classes was lower (Table 2). Approximately 86% of the tapeworms
recovered from the small (class 1) and medium (class 2) fish were immature,
predominantly in the early stages of development, while 64.8% of the tapeworms from
the large (class 3) fish were immature (Table 2). The predominance of immature stages of
the Asian tapeworms infecting convict cichlids in the spring season (2014) indicates that
the intermediate host, a cyclopoid copepod carrying infective larval stage of the
procercoids, had been recently consumed. Low infection parameters and the same pattern
of worm development were recorded in the mosquitofish. The seasonal patterns of
infection levels and development stages of the Asian tapeworm discussed above are in
agreement with previous reports of mosquitofish infections (Kuperman et al. 2002).
Although we advocate for the removal of introduced and deleterious species when
possible, this thermally isolated population of an infected tropical fish species in an
artificially elevated and nearly constant temperature environment, provides a unique
opportunity to study alternative factors influencing the seasonal population dynamics
and ecological relationships of the intermediate host (cyclopoid copepods), the Asian
tapeworm, and the final host, infected fish.

Acknowledgements

We thank N. Betchel, M. Cardenas, A. Kierzek, E. Miller, J. Mulder, J. O’Brien and L.
Reige for assistance with the collection of fish, and Steven Barlow for microscopy images.
We extend our gratitude to two anonymous reviewers and Catherine MacGregor for
comments that improved the manuscript.

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Bull. Southern California Acad. Sci.

114(2), 2015, pp. 98-103

Food Selection of Coexisting Western Gray Squirrels and
Eastern Fox Squirrels in a Native California Botanic Garden in

Claremont, California

Janel L. Ortiz and Alan E. Muchlinski

Department of Biological Sciences, California State University, Los Angeles, 5151
State University Drive, Los Angeles, CA 90032, USA

Southern California is home to one native and one introduced species of tree
squirrel. The native Western Gray Squirrel ( Sciurus griseus; here on gray squirrel), is
a highly arboreal tree squirrel that can be found inhabiting mixed oak and pine forest
habitats and tree dominated parks and gardens in suburban areas within California
(King 2004; Muchlinski et al. 2009). Gray squirrels feed primarily on fungi, pine nuts,
acorns, and bay fruit. They have also been documented to feed on Eucalyptus seeds,
samaras, and berries ( Morus and Phoradendron spp.) along with bird eggs and nestlings
(Carraway and Verts 1994). Fungi are one of the gray squirrel’s most highly utilized
food items. By consuming fungi, gray squirrels assist in providing a healthy soil
environment for the development and growth of oak-woodland communities (Maser
et al. 1981).

The introduced Eastern Fox squirrel ( Sciurus niger; here on fox squirrel) is an invasive
generalist species (Tatina 2007) typically found in upland areas, open forests, or areas
neighboring open spaces such as agricultural lands and pastures (Sexton 1990). The
presence of the fox squirrel in California has been a concern of the general public, land
managers, and researchers. The Los Angeles County Agricultural Commission considers
the fox squirrel a pest species and potentially aggressive. In their native range, the fox
squirrel has been important ecologically in the succession of grasslands to forests by
caching their food within open grasslands (Stapanian and Smith 1986). Seeds cached and
fed on by the fox squirrel come from persimmon, blue gum Eucalyptus , cottonwood,
pines, and many others (Koprowski 1994). Fox squirrels incorporate animal foods in
their diet such as insects, butterflies, ants, birds, and bird eggs (Koprowski 1994). It is
reported that the fox squirrel takes advantage of fruits found within backyards such as
avocados, oranges, and strawberries, an activity often disliked by human occupants
(Becker and Kimball 1947; Salmon et al. 2005).

Very little is known regarding food preferences of the two species within Southern
California and detailed information is limited. This study sought to gain information on
what foods each species selects, and which food items overlap and differ between gray
and fox squirrels. Knowledge of food preferences among species promotes making
management decisions that sustain their populations. For example, improving habitat by
adding particular plants or trees preferred by the gray squirrel can aid in the recovery of
its population (Linders and Stinson 2006). Information on food selection may also reveal
a high degree of overlap such that competition is possible in years of food shortage.
Competition could lead to extirpation of the gray squirrel where food selection is limited.
Muchlinski et al. (2009) established that fox squirrels replace gray squirrels at locations

Corresponding Author: ortizjanel@gmail.com

FOOD SELECTION OF WESTERN GRAY AND EASTERN FOX SQUIRRELS

within Southern California. Food availability could be a factor in the replacement of gray
squirrels from habitats invaded by the fox squirrel.

Observations on food selection were conducted at Rancho Santa Ana Botanic Garden
(RSABG) in Claremont, California. RSABG is a native California garden of
approximately 35 hectares containing a heterogeneous mixture of trees, shrubs, and
grasses. Food available within the garden is all natural with very little human influence
(e.g. trash, birdfeeders). Tree species present include but are not limited to Quercus,
Juglans, Pinus, Umbellularia, and Sequoia. The study was conducted March’ 2013 to
February 2014. Three transect lines and surrounding trails within the garden were visited
in the same order for each observation period. Observations occurred as follows for
a total of 124 hrs: (1) every other week from 14:00 to 17:00 hrs (72 hrs, 6 hrs/month,
24 observational days), (2) during a monthly census of the squirrels (36 hrs, 3 hrs/month,
12 observational days), and (3) during general behavioral observations conducted as
a separate study (16 hrs total, 2 observational days per species). Data were collected using
binoculars (8x30mm) and recorded creating a list of food items consumed by each species
per observation day. The number of individuals consuming the food item was not
recorded; however, the total number of days a food item was selected by each species was
documented (Table 1). Food items were recorded only if the squirrel was eating at the
time of the encounter.

Twenty-nine food items were consumed during the year by gray and/or fox squirrels
(Fig. 1). In instances when observations are separated by at most three months it is
assumed the species utilized that food item during the time between observations. Eleven
food items including Pinus spp. (female cone), Sequoia spp. (female cone), Quercus spp.
(acorn, flower bud, leaf/insect, and catkin), Juglans spp. (walnut and catkin), Fragaria
spp. (fruit), Aesculus spp. (fruit/husk) and bark/insects from various species were
consumed by both gray and fox squirrels (Table 1). Abundantly available acorns were
utilized by both species the entire year while less abundant pine cones were utilized
the first half of the year (January-July). Walnuts off the branch or from cached stores
were utilized by both species most of year. Remaining food items were consumed
seasonally, prior to spoilage or drying out (personal observation), when alternative food
items were unavailable.

Gray squirrels consumed 7 food items that fox squirrels did not (Table 1), including
Fremontodendron spp. (flower bud, flower/nectar, and fruit), Umbellularia californica
(flower bud, fruit), Arctostaphylos spp. (fruit) and fungi. Gray squirrels utilized fruits
from the California Bay Laurel ( Umbellularia californica) from July to February. Fungi
were documented as a food item for the gray squirrel October through January.

Fox squirrels consumed 11 food items not consumed by the gray squirrel (Table 1).
Food items eaten by fox squirrels included Washingtonia spp. (leaf), Liquidambar spp.
(fruit), Heteromeles spp. (fruit), Arctostaphylos spp. (flower), Rosa spp. (flower bud),
Mahonia spp. (fruit), Comar ostaphylis spp. (fruit), Cornus spp. (fruit), Berberis nevinii
(fruit), Pinus spp. (male cone), and Allium spp. (bulb). Such foods fill the fox squirrel’s
diet when acorns or pine seeds were unavailable. Many food items were utilized for only
one to two months. Fruits of the American Dogwood ( Cornus ) served as a food source
for a majority of the year.

Both species preferred a variety of food items at RSABG, yet observations at several
urban/suburban parks indicated gray squirrels were limited in food choices (Ortiz 2014).
Gray squirrels at these parks ate acorns, female and male cones ( Pinus spp.), black
berries from an unknown ornamental tree, and fruit from the California Bay Laurel

100

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

Table 1. Number of days food items were selected by Sciurus griseus and Sciurus niger out of 38 total
observational days at Rancho Santa Ana Botanic Garden in Claremont, California from March 2013 to
February 2014.

Food item

S. griseus*

S. niger*

Fragaria spp. (Fruit)

Washingtonia spp. (Leaf)

Fungi

Umbellularia calif ornica (Fruit)

Umbellularia californica (Flower Bud)

Mahonia spp. (Fruit)

Liquidamba spp. (Fruit)

Heteromeles spp. (Fruit)

Cornus spp. (Fruit)

Comarostaphylis spp. (Fruit)

Berber is nevinii (Fruit)

Arctostaphylos spp. (Fruit)

Arctostaphylos spp. (Flower)

Aesculus spp. (Fruit/Husk)

Pinus spp. (Male Cone)

Pinus spp. (Female Cone)

Fremontodendron spp. (Fruit)

Fremontodendron spp. (Flower Bud)

Fremontodendron spp. (Flower/Nectar)

Rosa spp. (Flower Bud)

Sequoia spp. (Female Cone)

Juglans spp. (Walnut)

Juglans spp. (Catkin)

Various spp. (Bark/Insect)

Allium spp. (Bulb)

Quercus spp. (Flower Bud)

Quercus spp. (Leaf/Insect)

Quercus spp. (Catkin)

Quercus spp. (Acorn)

* Total number of food items consumed by each species.

( Umbellularia calif ornica). Gray squirrels expanded their diet in the city of Redlands to
include oranges from neighboring orchards. Fox squirrels had a broader diet in the parks
including fruits and buds of Eucalyptus spp., fruit of the Plantanus spp., bark and leaves
from various tree species, samaras ( Ulmus spp.), peaches, cones from Casuarina, legumes,
seed pods ( Jacaranda spp.) and Arecaceae fruits. Fox squirrels also supplemented their diet
with peanuts and dry dog food supplied by park visitors and food in trash cans (personal
observation). In contrast, King (2004) found gray squirrels did not supplement their diet
with food from trash cans during her study in a park with a high level of human activity.

Food choices of gray and fox squirrels within their native and non-native ranges have
been documented through observation and stomach analyses (Ingles 1947; Cross 1969;
Steinecker and Browning 1970; Byrne 1979). Many of these food studies show an overlap
in diet between the species. Each species also consumed unique food items. Food
preferences found at RSABG are in line with many published works (Cross 1969; Wolf
and Roest 1971; Steinecker 1977; Byrne 1979; Carraway and Verts 1994; Crabtree 2008);
however, this study was the first to document several native plants of California.

FOOD SELECTION OF WESTERN GRAY AND EASTERN FOX SQUIRRELS

101

'■ 5. griseus

l ]s. niger

Both

Fragaria spp

Washingtonia spp.

Fungi

Umbellularia californica

Flower Bud

Mahonia spp.

Liquidambar spp.

Heteromeles spp.

Cornus spp.

Comarostaphylis spp. Fruit

Berberis nevinii

Arctostaphylos spp

Pinus spp.

Fruit

Fremontodendron spp. Flower Bud
Flower/Nectar

Rosa spp.

Flower Bud

Sequoia spp. Female Cone
Walnut
Catkin

Juglans spp.

Various spp. Bark/Insect
Allium spp.

Bulb

Flower Bud
Leaf/Insect
Quercus spp. Catkin

Acorn

—

IlfellSi

— B

Jan Feb Mar Apr

1 May 1

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Fig. 1. Food items consumed by Sciurus griseus and Sciurus niger from March 2013 to February 2014
at Rancho Santa Ana Botanic Garden in Claremont, California. Black bars indicate food items consumed
by S. griseus, white bars indicate food items consumed by S. niger, and gray bars indicate food items
consumed by both species.

Fox squirrels consumed a wider variety of foods including fruits/seeds of RSABG
natives and exotic species at local parks. A broader diet allows the fox squirrel a more
stable, year-round food supply. Even with California’s on-going drought affecting the
production of fruits, fox squirrels are able to supplement their diet with birdseed and
hand-feeding from humans (King 2004). Food items previously documented include
fruits of Eucalyptus globulus (Boulware 1941; King 2004), Ulmus parvifolia flowers (King
2004), samaras of Acer macrophyllum (King 2004; personal observation), plus other food
items unique to the fox squirrel.

Gray squirrels continued to be restricted in food choices based on the habitat in which
they were found. Although there were alternative trees with additional food items
available, gray squirrels still fed almost exclusively on acorns and pine nuts. Gray
squirrels move away from acorns and pine nuts when seasonally unavailable. They have
been documented to eat bay fruit, pecans, almonds, cypress, mulberry, maple, and elm in

102

SOUTHERN CALIFORNIA ACADEMY OF SCIENCES

other locations (Ingles 1947). Yet none of these food items, with the exception of bay
fruit, were emphasized in publications as part of gray squirrels’ diet in Southern
California. Gray squirrels in South Pasadena were found to have consumed seeds of
Eucalyptus (Little 1934), which has only been observed once in Trabuco Canyon,
California where oaks were drastically affected by a drought, producing little to no acorn
crop (personal observation). Cross (1969) showed the importance of fungi in their diet,
with specialty in subterranean fungi but also epigeous fungi and gill mushrooms
(Steinecker 1977; Byrne 1979).

Although gray and fox squirrels overlap in many food choices including fungi
(Carraway and Verts 1994; Koprowski 1994), fox squirrels were not observed consuming
fungi during our study. The population of fox squirrels at RSABG may not need to
utilize fungi since the garden contains a variety of food items such as fruits and catkins to
consume instead. Utilization of fungi by the gray squirrel is reported to occur most
during spring and summer (Carraway and Verts 1994), whereas fox squirrels utilize fungi
during the summer and winter (Koprowski 1994). Timing of fungi consumption by the
gray squirrel varies from year-long usage (Cross 1969) to primarily late summer (Byrne
1979). The benefit of fungi to their diet remains unknown.

Conserving the native Western Gray Squirrel will prove to be a complex issue. As of
now, the best conservation method in urban/suburban habitats is to preserve isolated
populations of gray squirrels that currently exist. Habitat improvements such as planting
trees like the California Bay Laurel and conifers and shrubs like Fremontodrendon may
sustain the isolated populations of gray squirrels for a longer period of time.

Acknowledgements

The authors wish to thank the staff at Rancho Santa Ana Botanic Garden for their
support in conducting this work as well as Drs. Andres Aguilar and Paul Narguizian for
their review of an earlier draft. Also, thank you to the three anonymous reviewers whose
comments helped improve this research note.

Literature Cited

Boulware, J.T. 1941. Eucalyptus tree utilized by fox squirrel in California. American Midland Naturalist,
26:696-697.

Becker, E.M. and M.H. Kimball. 1947. Walnut growers turn squirrel catchers. Diamond Walnut News,
29(3): 4-6.

Byrne, S. 1979. The distribution and ecology of the non-native tree squirrels Sciurus carolinensis and Sciurus
niger in northern California. University of California, Berkeley, Ph.D. Dissertation, 190 pages.
Carraway, L.N. and B.J. Verts. 1994. Sciurus griseus. Mammalian Species, 474:1-7.

Crabtree, K.M. 2008. Habitat and resource use of western gray squirrels ( S . griseus) in suburban southern
California parkland. California State Polytechnic University, Pomona, M.S. Thesis, 59 pages.
Cross, S.P. 1969. Behavioral aspects of western gray squirrel ecology. University of Arizona, Tucson,
Ph.D. Dissertation, 168 pages.

Ingles, L.G. 1947. Ecology and life history of the California gray squirrel. California Fish and Game
Bulletin, 33:139-157.

King, J.L. 2004. The current distribution of the introduced fox squirrel ( Sciurus niger ) in the greater Los
Angeles metropolitan area and its behavioral interaction with the native western gray squirrel
(Sciurus griseus ). California State University, Los Angeles, M.S. Thesis, 135 pages.

Koprowski, J.L. 1994. Sciurus niger. Mammalian Species, 479:1-9.

Linders, M.J., and D.W. Stinson. 2006. Draft Washington state recovery plan for the western gray
squirrel. Washington Department of Fish and Wildlife, Olympia, Washington. 91 pages.

Little, L. 1934. Seeds of the eucalyptus tree a new food for the Anthony gray squirrel. Journal of
Mammalogy, 15:158-159.

FOOD SELECTION OF WESTERN GRAY AND EASTERN FOX SQUIRRELS

103

Maser, C., B.R. Mate, J.F. Franklin, and C.T. Dyrness. 1981. Natural history of Oregon coast mammals.
USD A Forest Service, Pacific Northwest Forest and Range Experiment Station, General Technical
Report, 496 pages.

Muchlinski, A.E., G.R. Stewart, J.L. King, and S.A. Lewis. 2009. Documentation of replacement of native
western gray squirrels by introduced eastern fox squirrels. Bulletin Southern California Academy of
Sciences, 108:160-162.

Ortiz, J.L. 2014. Behaviors of the native western gray squirrel {Sciurus griseus) and the invasive eastern fox
squirrel ( Sciurus niger) in Los Angeles and surrounding counties. California State University, Los
Angeles, M.S. Thesis, 78 pages.

Salmon, T.P., D.A. Whisson, and R.E. Marsh. 2005. Wildlife Pest Control Around Gardens and Homes.
2nd ed. Oakland: Univ. California Agric. Nat. Res. Publ. 21385.

Sexton, O.J. 1990. Replacement of fox squirrels by gray squirrels in a suburban habitat. American
Midland Naturalist, 124:198-205.

Stapanian, M.A. and C.C. Smith. 1986. How fox squirrels influence the invasion of prairies by nut-bearing
trees. Journal of Mammalogy, 67:326-332.

Steinecker, W.E. 1977. Supplemental data on the food habits of the western gray squirrel. California Fish
and Game, 63:11-21.

— and B. M. Browning. 1970. Food habits of the western gray squirrel. California Fish and Game,
56:36^48.

Tatina, R. 2007. Optimal Foraging in the eastern fox squirrel: food size matters for a generalist forager.
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Wolf, T.F. and A. I. Roest. 1971. The fox squirrel ( Sciurus niger) in Ventura County. Calif. Fish and
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SMITHSONIAN LIBRARIES

3 9088 01816 7825

CONTENTS

Effects of Ocean Recreational Users on Coastal Bottlenose Dolphins ( Tursiops
truncatus) in the Santa Monica Bay, California. Amber D. Fandel, Maddalena
Bearzi, and Taylor C. Cook

Salt Marsh Reduces Fecal Indicator Bacteria Input to Coastal Waters in Southern
California. Monique R. Myers and Richard F. Ambrose

Asian Fish Tapeworm ( Bothriocephalus acheilognathi ) Infecting a Wild Population
of Convict Cichlid ( Archocentrus nigrofasciatus) in Southwestern California.
Victoria E. Matey, Edward L. Ervin, and Tim E. Hovey

Food Selection of Coexisting Western Gray Squirrels and Eastern Fox Squirrels in
a Native California Botanic Garden in Claremont, California. Janel L. Ortiz
and Alan E. Muchlinski

Cover: Western gray squirrel ( Sciurus griseus ). Photo courtesy of Alan Muchlinski.

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