INTRODUCTION
The world’s fisheries are in dire straits; over 65% have been classified as heavily
exploited, overexploited, or depleted (NRC 1999). It is thought that marine reserves could help
mitigate this problem, serving as reproductive sources to replenish nearby systems, including
fisheries (Murray et al. 1999, Crowder et al. 2000, Dayton et al. 2000). Unfortunately, there are
few documented success stories of fisheries enhancement through the establishment of marine
reserves (Tegner 1993). There are many possible reasons for this. For example, the general lack
of unexploited marine ecosystems to serve as baseline controls results in relatively low statistical
power when trying to detect any changes in the system under scrutiny. The policies governing
marine reserves are also fairly weak. Definitions of marine reserves are vague, the regulations
they impose on the public are few, and the enforcement of those regulations is virtually
nonexistent (Allison et al. 1998). Socioeconomic pressures often cause marine reserves to be
placed in suboptimal habitat, since fishermen naturally recognize productive systems and
strongly oppose any restrictions applied to those areas.
Even if these logistical and political difficulties are overcome, however, the question
remains of where to site marine reserves. Understanding source-sink dynamics is necessary to
ensure that the effort involved in setting up a reserve is not wasted, or worse yet, detrimental to
the system. Crowder et al. (2000) showed that a reserve sited in sink habitat could actually result
in a reduction in the overall population if total fishing effort were displaced rather than reduced.
putting heavier fishing pressure on remaining unregulated marine areas, some of which may be
source habitat. Identifying appropriate source habitats, then, becomes a crucial step in successful
design of marine reserves.
Traditionally, sources have been defined as net exporters of individuals, and the
convention for identifying them in marine systems has been to backtrack larvae to their physical
sources based on dispersal patterns mediated by ocean currents and factors such as length of
planktonic development and larval swimming ability (Crowder et al. 2000). This definition has
recently been augmented with another approach that focuses on habitat quality by tracking
growth, mortality, and reproduction patterns for a given population. Finding habitats where
reproduction is optimized could be a first step in applying source-sink dynamics to marine
reserve design. Different aspects of habitat may influence both the quality and quantity of
larvae produced, thereby differentiating habitats from each other in terms of their value as
reproductive sources.
Using the acorn barnacles Balanus glandula as a model system, questions concerning
what determines larval quantity and quality can be addressed. B. glandula is found in the mid
and high intertidal zone from Alaska to Baja California. This species broods developing
embryos for approximately four weeks (Hines 1976) prior to their release as planktonic larvae
(nauplii). Larvae then spend two to four weeks in the water column before attaching to rocky
substrate on the shore and metamorphosing into juvenile barnacles. Crisp and Patel (1960)
found that barnacle nauplii (Semibalanus balanoides) hatch at a larger size when they developed
at colder temperatures, and it was later shown that larger larvae tend to grow faster following
settlement and metamorphosis (Jarrett and Pechenik 1997). Due to the increased chance of
survival for larger settlers, larger larvae may be of higher quality. According to this information,
larval size would be expected to vary with temperature along a latitudinal gradient (Barnes and
Barnes 1965); that is, if temperature varies inversely with latitude, larvae should increase in size
from Southern California northward.
Additionally, differences between bay and open coast habitat provide an opportunity to
test the effect of temperature on reproduction over a much smaller geographic scale. Water
temperatures within Monterey Bay are 2 to 3°C warmer than on the nearby open coast during
periods of spring upwelling, which coincides with B. glandula's brooding season. Thus, larger
larvae may be exported from open coast sites than from locations within the bay. Furthermore, it
is possible that bay habitat may be at an advantage over open coast habitat as far as larval
quantity is concerned. Higher food availability (measured in terms of chlorophyll-a) was found
in Narragansett Bay, Rhode Island than on the open coasts, and as a result, bay barnacles had
higher growth rates and allocated more resources to reproduction (Bertness et al. 1991). Similar
conditions may exist in Monterey and other bays since these areas often receive high nutrient
input. If this is true, then barnacles in Monterey Bay may produce and export more larvae per
adult than those living on the open coast. The goal of this study was to test whether the patterns
of reproduction described above hold true for Central California bay and open coast habitat, and
whether any overlap in habitat type exists that would make it possible to optimize both larval
quantity and quality in siting marine reserves within this region.
MATERIALS AND METHODS
Field collections. Balanus glandula were collected on the central coast of California
from three open coast sites (Soberanes Point and Mal Paso Creek south of Monterey Bay, and
Pigeon Point in the north) and three sites within Monterey Bay (Hopkins Marine Station, Moss
Landing, and Santa Cruz) (Appendix, Fig. 1). To extend the geographic comparison of embryo
size, barnacles were also collected from Fogarty Creek, Oregon, and the Scripps Pier in San
Diego. Fifteen individuals (basal diameters ranging from 6-12mm) with ripe lamellae were
collected haphazardly from each site by removing adults from the rock with a screwdriver. At the
Central California sites, barnacles were collected from mid-intertidal, wave-exposed areas near
the lower limit of the mussel bed (Mytilus californianus). Barnacles from San Diego and Oregon
were collected on M. californianus shells from the upper part of the mussel bed and sent to
Hopkins Marine Station. Intertidal data loggers (Optic Stowaway, Onset Computer Corporation,
Pocasett, MA) recorded water temperature every 30 minutes at Fogarty Creek, Soberanes Point,
and Hopkins; AVHRR satellite images of Southern California were obtained to determine mean
water temperature at San Diego during the brooding period.
Lab analysis. Barnacle size (maximum basal diameter of the shell) and embryo size
were quantified for each barnacle collected. Only individuals with the darkest egg masses were
sampled to ensure that embryos were in the latest stage of development. In fact, upon inspection
under a microscope, most of the embryos in the sampled egg masses had already hatched.
Variation in embryo size among individuals due to developmental stage was thus eliminated.
since all embryos were at the same stage of development. For each individual, the length of 15
haphazardly selected embryos was measured (to the nearest 0.002mm) under a raised coverslip
using a 40x power objective and an ocular micrometer. To compare differences in reproductive
allocation between bay and open coast barnacles, the dry weights of the shell, soft body, and egg
masses were quantified. The shells, bodies and egg masses were dried at 70°C for 24 hours until
they reached a constant mass. Approximately 2% of each egg mass (90-200 of 5,000-10,000
embryos) was sampled to measure embryo length, and the rest (except for the Oregon and San
Diego samples) was dried for weighing. The dried mass of even 500 embryos was undetectable
(20.Img), so this amount was considered insignificant in the measurement of the overall mass of
the embryos.
Reproductive effort was calculated by dividing the number of embryos by the dry mass of
the soft body (normalized to 10 mg, a typical dry body weight for barnacle samples). The total
number of embryos in an egg mass was estimated from five individuals from Moss Landing
(representing bay sites) and five from Soberanes Point (representing the open coast sites) by
diluting the egg mass homogenously in ImL of a 100:3 solution of distilled water and ethanol,
averaging the counts from five sub-samples of 0.002mL each, and multiplying by the total
volume. The solution was then dried at 70°C for 24 hours until only the dried egg mass
remained. From the weights of these dried egg masses, separate conversion factors (number of
embryos/gegg mass) were calculated for bay and open coast barnacles, and all dried egg weights
were converted to number of embryos per individual.
RESULTS
Embryo size
As predicted, embryo length from barnacles within Central California was correlated with
temperature. Embryos were on average 10% longer (ANOVA, p0.01, Table la) in the colder
open coast sites (Fig. 2a) than the bay sites, with means of 233um and 212um, respectively (Fig.
2b). Embryo size was not significantly related to barnacle size (p#0.33) at any of the study
sites, at least within the relatively narrow range of barnacle sizes collected. The latitudinal
comparison, however, did not coincide with the predicted outcome. Fogarty Creek in Oregon,
being the farthest north, was expected to be the coldest site and as a result have the largest
embryos. However, among all embryos from open coast sites, those from Central Calfornia were
the largest (233um), followed by Oregon (226um), and then San Diego (223um). The only
significant difference in embryo size (p0.01, Table 1b) that existed between these populations
was Central Cailfornia vs. San Diego (Fig. 3a). The 0.3°C temperature difference between
Soberanes Point and Fogarty Creek (Fig. 3b) should not have substantially affected embryo size.
San Diego water temperature, however, was an average of 7°C warmer (Fig. 3c) than the sites to
the north of it.
Reproductive effort
Reproductive effort was not correlated with habitat type (bay or open coast); instead, a
division was seen between northern and southern sites (p#0.01, Table 1c). The barnacles at the
northern sites, Moss Landing (bay), Santa Cruz (bay), and Pigeon Point (coast), had roughly half
the reproductive effort (from 6.6 to 10 thousand embryos/ lOmg dry soft body mass) of those at
Soberanes Point (coast), Mal Paso Creek (coast), and Hopkins (bay) (from 16.8 to 21 thousand
embryos/ lOmg dry soft body mass) (Fig. 4). Again, there was no significant correlation
between barnacle size and reproductive effort (p20.37).
DISCUSSION
These data suggest that there are significant differences in the reproduction between
Balanus glandula populations within Monterey Bay and on the open coast. These differences in
embryo size and reproductive effort may have important consequences for the replenishment of
local populations in Central California.
Embryo size
While temperature appears to play an important role in embryo size within the Central
California populations, this trend seems to disappear on a wider geographic scale. The reliability
of this comparison is somewhat uncertain because the barnacles collected from Oregon and San
Diego were sent to me from sites I never visited. Consequently, I am unfamiliar with the
characteristics of these sites, and cannot confirm that they are truly representative of the areas
from which they came. Also, the barnacles from San Diego and Oregon were collected from
slightly higher tidal heights than those from Central California, which could influence embryo
size. Fürthermore, one site representing the north and one representing the south may simply not
provide enough spatial replication to document any latitudinal trend that might exist.
Nevertheless, these data suggest that temperature is not the sole factor determining embryo size
over such a wide spatial scale. Although larger embryos were observed in colder environments,
à survey of Semibalanus balanoides embryo sizes also revealed the lack of a consistent
latitudinal trend (Barnes and Barnes 1965). In any case, the observation that open coast (rather
than bay) habitat produces larger, and thus perhaps higher quality embryos is arguably more
important to marine reserve design than specifying the desirable latitude at which to site reserves
for a given species.
An unanswered question is why temperature has the effect it does on embryo
development (Crisp and Patel 1960). It has not yet been determined whether the difference in
embryo size resulting from development at different temperatures actually signifies a difference
in embryo dry weight. If embryos developing at colder temperatures are not only greater in size,
but in mass, how is additional mass gained? Are embryos at colder temperatures simply more
metabolically efficient, using up less of what they start out with? Or is it possible for nutrients to
diffuse into embryos? Hines (1976) and many others have reported that barnacle embryos
developing at colder temperatures take longer to hatch. This would seem to suggest the latter of
the two above possibilities, since a longer period of development would mean more time to
acquire nutrients through diffusion. Beyond affecting larval size and development rate, little is
known regarding the effects of colder temperatures on other larval qualities. Lab and field
studies of larval survival and performance, which may include measurements of respiration.
feeding, and swimming rate, would create a more complete description of larval quality,
Reproductive Effort
The hypothesis that higher reproductive effort would be found in bay barnacles was
based on the assumption that conditions of food availability in the bay were higher than on the
open coast, as reported in Bertness et al. (1991) for Narragansett Bay. However, no measure of
food availability within or outside the Monterey Bay was made for this study. Narragansett Bay
has significant amounts of estuarine input responsible for higher productivity in the bay. On the
west coast, upwelling, which is a factor that does not come into play on the east coast, may be
providing additional nutrients to local open coast phytoplankton populations, thus increasing
food availability to filter feeders such as barnacles in those areas. Thus, one might expect to see
à pattern on the west coast opposite to that on the east coast: higher food availability on the open
coast due to upwelling, resulting in higher reproductive effort in barnacles at open coast sites.
But unless Pigeon Point has anomalously low levels of upwelling for an open coast site, this
explanation may only partially account for the results in this study. Reproductive effort at
Pigeon Point was more similar to bay sites than it was to the other open coast sites. However,
upwelling and subsequent phytoplankton blooms do not always have immediate effects on
barnacle growth. Sanford and Menge (200 1) reported that short-term growth rates in B. glandula
along the Oregon coast were not well correlated with chl-a abundance. They suggested this may
be due to the influence of zooplankton abundance, an additional food source for barnacles. The
added complexity of another trophic level to this system could certainly account for fluctuations
in growth rates and possibly in reproductive effort.
Ultimately, higher food availability should correspond to higher growth rates. Whether
there is as strong a correlation between growth rates and reproductive effort in Monterey Bay as
was seen in Narragansett Bay remains to be seen. Barnacle growth rates at all six sites must be
quantified to confirm whether food availability alone could account for the dramatically higher
levels of reproductive effort seen in the three southern sites.
Factors other than food availability could also be affecting reproductive effort, such as
differences in energy partitioning due to crowding. Wu et al. (1977) noted that a decrease in the
degree of crowding was associated with an increase in reproductive effort in B. glandula.
Crowded barnacles expend a greater proportion of their total energy on building a taller shell,
presumably in an effort to increase their surface area for food acquisition in the face of limitec
space and intense competition with neighboring barnacles. Population density must therefore be
taken into account when formulating hypotheses concerning reproductive effort. Areas of higher
food availability would not necessarily result in higher reproductive effort if settlement rates
were also high, leading to crowding as the barnacles grew. A measure of population density for
each site was not made for this study, but such information would be useful.
Another confounding factor is the possibility of asynchronous release of larvae at
different sites. B. glandula may have up to 6 broods per brooding season (Hines 1976) and data
suggest that the earliest brood is composed of the most embryos (Barnes and Barnes 1956). It is
not known whether each brood after that is successively smaller, but the possibility should be
considered. It could be that barnacles from the three northern sites are on an earlier reproductive
schedule than barnacles from the southern sites. For example, when secondary collections were
made in late May at Soberanes Point and Moss Landing, it seemed that a much greater
abundance of barnacles were brooding or had ripe ovaries at Soberanes Point than at Moss
Länding. If southern sites are one or more broods behind northern sites and brood size is
dependent on how many times the adult has already reproduced that season, the perceived
difference in brood size from these populations may be an artifact of this asynchronous release.
Of course, the assumed asynchronous release at Soberanes Point and Moss Landing could be
representing a difference in bay vs. open coast populations rather than northern vs. southern.
Asynchronous release may also be distorting data on larval quality, since similar patterns of
embryo size declining with later broods have been described for Balanus glandula and other
barnacles (Barnes 1953, Stathmann 1987). The possibility of asynchronous release must be
more explicitly examined
Achieving an understanding of reproductive effort and factors that contribute to its
magnitude would be a huge stride for marine reserve design. Combining this quantitative
measurement of reproduction with more qualitative measurements such as embryo size, as well
as performance and survival rates, would greatly augment the steadily growing base of
knowledge about source-sink dynamics in the coastal ocean. This study addresses only a few of
the complications involved in considering reproduction in a model organism, and reproduction is
only one facet of the problem of identifying source habitat, but it is a good starting point for
fürther research. The observed differences in reproductive effort and embryo size among such
closely spaced sites is surprising and adds further complexity to the design of marine reserves;
careful research and planning are necessary, since it has been shown here that it cannot be
assumed that sites in a fairly narrow geographic region are of equivalent habitat quality. The
prospect of designing reserves for multiple species with different life histories complicates
matters further, and raises an unknown question: do species share common source habitat? Only
through constant reevaluation and extension of ideas such as those presented here will progress
be made toward more successful implementation of marine reserves as reproductive sources.
Acknowledgements
I would first like to thank Michelle Phillips for cheerfully accompanying me on trips into the
intertidal at four in the morning to catch the low tide. I am also indebted to George Somero for
the freedom he has afforded me in his lab, to Mark Denny for his critical thinking that kept some
of my more outrageous claims grounded in reality, and to Jim Watanabe for his patience with me
and my rather rudimentary understanding of statistics. I thank my fellow students in 175H for
their support and commiseration after long nights in the lab, and for reminding me that many
things may look better in the morning. Finally, I am eternally grateful to my primary advisor,
Eric Sanford, for generously lending his expertise and his time in the field during my collection
process, for offering insight and encouragement all along the way, for his shrewd (if painfully
thorough) editing skills, and for sparking my interest in this project in the first place.
13
Literature Cited
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sufficient for marine conservation. Ecological Applications 8: S79-S92.
Barnes, H. 1953. Size variation in the cyprids of some common barnacles. Journal of the
Marine Biological Association of the United Kingdom 32: 297-304.
Barnes, H. and M. Barnes. 1956. The general biology of Balanus glandula Darwin. Pacific
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Barnes, H. and M. Barnes. 1965. Egg size, nauplius size, and their variation with local,
geographical, and specific factors in some common cirripedes. Journal of Animal
Ecology 34: 391-402.
Bertness, M.D., S.D. Gaines, D. Bermudez, and E. Sanford. 1991. Extreme spatial variation in
the growth and reproductive output of the acorn barnacle Semibalanus balanoides.
Marine Ecology Progress Series 75: 91-100.
Crisp, D.J. and B. Patel. 1960. Environmental control of the breeding of three boreo arctic
cirripeded Balanus balanoides, Balanus balanus, and Balanus crenatus. Marine Ecologi
2: 283-295.
Crowder L.B., S.J. Lyman, W.F. Figueria, and J. Priddy. 2000. Source-sink population
dynamics and the problem of siting marine reserves. Bulletin of Marine Science 66: 799-
820.
Dayton P.K., E. Sala, M.J. Tegner, and S. Thrush. 2000. Marine reserves: parks, baselines, and
fishery enhancement. Bulletin of Marine Science 66: 617-634
Hines, A. 1976. Comparative reproduction ecology of three species of intertidal barnacles. Ph.D.
Thesis, University of California, Berkeley.
Jarrett, J.N and J.A. Pechenik. 1997. Temporal variation in cyprid quality and juvenile growth
capacity for an intertidal barnacle. Ecology 78:1262-1265.
Murray, S.E., R.F. Ambrose, J.A. Bohnsack, L.W. Botsford, M.H. Carr, G.E. Davis, P.K.
Dayton, D. Gotshall, D.R. Gunderson, M.A. Hixon, J.Lubchenco, M. Mangel, A.
MacCall, D.A. McArdle, J.C. Ogden, J. Roughgarden, R.M. Starr, M.J. Tegner, and
M.M. Yolavich. 1999. No-take reserve networks: sustaining fishery populations and
marine ecosystems. Fisheries Management—Perspective: 11-25.
NRC (National Research Council). 1999. Sustaining marine fisheries. National Academy Press,
Washington, DC.
Sanford, E. and B.A. Menge. 2001. Spatial and temporal variation in barnacle growth in a
coastal upwelling system. Marine Ecology Progress Series 209:143-157.
Strathmann, M.F. 1987. Reproduction and development of marine invertebrates of the Northern
Pacific Coast. University of Washington Press, Seattle.
Tegner, M.J. 1993. Southern California abalone: can stocks be rebuilt using marine harvest
refugia? Canadian Journal of Fisheries and Aquatic Sciences 50: 2019-2028.
Wu, R.S.S., C.D. Levings and D.J. Randall. 1977. Differences in energy partition between
crowded and uncrowded individual barnacles (Balanus glandula Darwin). Canadian
Journal of Zoology 55: 643-647.
Fig. 1.
Fig. 2a.
Fig. 2b.
Fig. 3a.
Fig. 3b.
Fig. 3c.
Fig. 4.
Figure Legends
Map of study sites in Central California.
Water temperatures at Soberanes Point and Hopkins Marine Station, from April¬
May 2001. High tide water temperatures were calculated as the mean temperature
during a four-hour period centered around each high tide.
Balanus glandula embryo sizes at Central California study sites. Light gray
represents bay sites, dark gray represents open coast sites; sites are arranged in
order of increasing latitude from left to right. Error bars are the standard error for
embryo size for n=15 individuals at each site.
Balanus glandula embryo sizes at open coast study sites across a latitudinal
gradient. Sites are arranged in order of increasing latitude from left to right. Error
bars are the standard error for embryo size for n-15 individuals at each site.
Water temperatures at Fogarty Creek, Oregon, and Soberanes Point, California
from April-May 2001. High tide water temperatures were calculated as the mean
temperature during a four-hour period centered around each high tide.
Satellite image of Southern California representing water temperature on an
average day in May. The star in the lower right corner denotes the location of
Scripps Pier.
Balanus glandula reproductive effort at Central California study sites. Light gray
represents bay sites, dark gray represents open coast sites; sites are arranged in
order of increasing latitude from left to right. Error bars are the standard error for
reproductive effort for n-15 individuals at each site.
18
-
8.
a
6.

58
0
5
8
885
88
5
0 a
80
5u
Table 1a: Analysis of variance for egg size in bay vs. open coast populations
Source of Variation
MS
F crit P-value
5 0.002254 30.76919 2.323127 1.18E-17
Between Groups
Within Groups
84 7.32E-05
Total
SNK post-hoc analysis
SNK value
for k-6
4.125 0.0091148
for k=5
3.943 0.0087127
MPC
3.707 0.0081912
for k=4
0.205 0.214 0.218 0.233 0.233 0.235
3.374 0.0074554
for k=3
for k-2
2.812 0.0062136
Table 1b: Analysis of variance for egg size for populations from different latitude
Source of Variation
MS
P-value
Fcrit
Between Groups
0.000391 4.269444 2.502659 0.003779
Within Groups
70 9.15E-05
Total
SNK post-hoc analysi:
SNK value
for k=5
3.96 0.0097814
MPC
for k=4
3.722
0.0091935
0.223
0.226
0.233 0.233 0.235
for k=3
3.387 0.0083661
2.821
0.006968
for k-2
Table 1c: Analysis of variance for reproductive effort for 6 sites in Central California
MS
Source of Variation
ECI
P-value
Between Groups
5 4.52Et08 18.33949 2.323127 2.88E-12
Within Groups
84 24620245
Total
SNK post-hoc analysis
SNK value
4.125
for k=6
5284.7507
for k=5
MPC
3.943 5051.5811
for k-4
665976 979635 1002610
3.707 4749.2293
1681276 1687620 2095408
for k=3
3.374 4322.6058
2.812 3602.5985
for k-2
igeon Pt
Fig. 1
Santa Cruz
M
anding
Ma
Soberanes
15.00
14.00
13.00
12.00
5 11.00
10.00
9.00
8.00

0.24
0.23
0.22
0.21
0.2
0.19
0.18
Fig. 2a
14


K




Fig. 2b
Moss
Soberanes Mal Paso
Hopkins
Creek
Landing
Location
14
e


—D-Soberanes
——Hopkins
Santa Pigeon Pt.
Cruz
0.24
0.235
0.23
5 0.225
0.22
0.215
0.21
12.5
11.5
10.5
9.5
8.5
Fig. 3a
San Diego Soberanes Mal Paso Pigeon Pt. Fogarty
Creek
Creek, OR
Location
Fig. 3b
4
——Oregon
— Soberanes


He



Date
NOA-12 MSST SLIT 2001/05/04 17:37:17 F0
3

19.0
18.5
18.0
17.5
-17.0
16.5
16.0
15.5
-15.0
14.5
14.0
13.5
+13.0
Fig. 30
25000
20000
15000
10000
5000
Soberanes Mal Paso
Creek
Fig. 4
Hopkins
Moss
Landing
Location
Santa Cruz Pigeon Pt.