Abstract In this study, I examined predation by two species of whelk on bay
mussels (Mytilus trossulus) to determine whether a northern-occurring species (Nucella
ostrina) and a southern-occurring species (Nucella emarginata) differed in absolute
feeding rate and thermal dependence of feeding. I also examined the respiration rates of
these congeners. Each species was held in three temperature treatments: 21°C,-16°C
(ambient), and 10.5°C for 28 days. Across all temperatures, N.emarginata usually had
higher feeding rates than N.ostrina for the first 14 days, but, after 21 and 28 days,
N.ostrina tended to have higher feeding rates. Feeding by both species displayed classical
physiological responses to temperature (Qios 2) for the first 14 days. By the twenty-first
day, when satiation seemed to occur, Q1o values increased to 4.49 and 5.35 for
N.emarginata and N.ostrina, respectively. In particular, both species at 10.5°C
demonstrated considerably reduced feeding rates upon satiation. This suggests that
metabolic costs were much lower at 10.5°C and, therefore, the animals required less
energy input after satiation. While N.ostrina’s Qjo value declined to 1.67 after an
additional 7 days, N.emarginata’s Qjo value declined to 3.40. Total consumption rates for
the entire experimental period were not significantly different between species at any
temperature. These results suggest that, while N.ostrina feeding rates may be lower after
a starvation period, N.ostrina is able to maintain similar levels of energy input over the
long-term by having a shorter satiation phase. In the respirometry experiment,
N.emarginata had significantly higher O2 consumption rates (0.16% 02 consumed/mI
seawater/hr/g) than N.ostrina (0.050% O2 consumed/mL seawater/hr/g). The
physiological results of this study correlate with the thermal habitats of N.emarginata and
N.ostrina and may have implications for global warming.
Introduction
The latitudinal temperature variability of coastal waters of the North American
Pacific coast can furnish intertidal organisms with different thermal habitats. The effects
of ocean temperatures on predatory behavior and metabolic activity have long been
recognized (Broekhuysen, 1940; Sanford, 1999; Hochachka and Somero, 2002), but little
study has been dedicated to two recently differentiated congeneric species of rocky
intertidal whelk. The Southern species (Nucella emarginata) resides in warmer waters
than its Northern counterpart (Nucella ostrina) yet both species prey on a variety of the
same animals, such as barnacles (Balanus glandula) and mussels (Mytilus trossulus,
Mytilus californianus, Mytilus galloprovincialis), in the mid-to low- intertidal zone.
Utilizing a proboscis to drill through the exterior shells of their prey, the whelks ingest
tissue via a drilled borehole. In addition, the shell morphology of these species is often
indistinguishable. Because of the behavioral and phylogenetic similarities between these
species, N.emarginata and N.ostrina provide useful models for comparing the effects of
temperature on physiology.
In 1990, Palmer et al. were the first to suggest that N.emarginata may actually
comprise two reproductively isolated cryptic species. Marko (1998) later concluded that
N.ostrina and N.emarginata were allopatrically speciated by physical isolation in
different zoogeographic provinces. The dramatic 4°C increase in sea surface temperatures
south of Point Conception established the physical boundary that separated these
populations.
In laboratory studies, changes in water temperature have been shown to
dramatically alter the feeding behavior of intertidal organisms. For the oyster drill
Urosalpinx cinerea, Hanks (1957) investigated predation rates on Mytilus edulis and
noted that increases in temperature considerably increased feeding rates (Qjo value of
5.06 between 15°C and 20°C). Largen (1967) performed similar experiments with Thais
(Nucella) lapillus, a species more closely related to Nemarginata and N.ostrina, and sav
a Q1o value of 3.2 between 15°C and 20°C. Sanford (2002) conducted experiments with
Pisaster ochraceus and Nucella canaliculata preying on Mytilus trossulus to determine
the effects of small temperature changes (9°C to 12°C) and episodic upwelling on the
predation rates of these organisms. Again, increased temperature caused significant
increases in predation rates. (Qio's ranging from approximately 2.4 to 7.1 for
N. canalicuata and 2.5 to 4.3 for Pisaster ochraceus).
Metabolic activity, measured as a respiration rate, has been determined for other
Nucella species, but little has been done to compare N.emarginata and N.ostrina. Bayne
and Scullard (1978) investigated the respiration rates of Thais (Nucella) lapillus at
different temperatures and starvation conditions. Stickle and Bayne (1982) extended this
analysis to include salinity effects on oxygen consumption. Recently, Dahlhoff et al
(2001) have tested respiration rates of N.ostrina in Oregon field sites that experience
different seasonal temperatures. VO2 ranged from -2 to 4 mmol O/hr/g wet weight for
unfed whelks at Boiler Bay, OR, during the summer.
In order to assess physiological differences between N.emarginata and N.ostrina,
I investigated the feeding rates, thermal dependency of feeding, and respiration rates of
each species. I attempted to address the following questions: (1) Do feeding rates differ
between species and change over time? (2) Are feeding rates thermally dependent and
does thermal dependency change over time? (3) Do respiration rates differ between
species? (4) Do respiration rates correlate with feeding rates? The results suggest that
N. emarginata has higher maximal feeding rates than N.ostrina. For both species, feeding
rates were thermally dependent, and thermal dependency changed over time. At a
constant 12.2°C, N.emarginata had significantly greater respiration rates than N.ostrina.
The physiological results correlate with the thermal environments occupied by each
species. As climate change occurs, N.emarginata may have a selective advantage in
regions where the congeners have overlapping populations.
Materials and Methods
Experimental Design
In order to assess physiological differences between N.emarginata and N.ostrina,
1 first investigated feeding rates for each species under three different temperature
regimes: (1) 10.5°C, (2)-16°C (ambient), and (3) 21°C. All whelks were kept submerged
during the experimental period except during weekly mussel counting.
Six glass tanks (77 L, 76cm x 31.Scm x 36.Scm) filled with seawater were placed
in an outdoor pavilion at Hopkins Marine Station in Pacific Grove, CA, for the controlled
treatments. The closed tanks were covered with fiberglass sheets and kept well-shaded.
The light/dark cycle for the experimental period coincided with daily shifts at Pacific
Grove from April 25, 2003, to May 29, 2003.
For the ambient treatment, two 77L tanks were placed on the floor of the outdoor
pavilion. For the 10.5°C treatment, two tanks were placed in a larger tank (770L, 180cm
x 88cm x 36cm) whose temperature was controlled with a custom freon-based chiller and
affixed temperature controller (Digital Temperature Controller, Aqua Logic, Inc.). The
final two tanks were placed in a 770L tank containing an immersion heater (112 Silica
Glass Power heater, 500 W, with temperature controller), which served as a water bath
for the 21°C treatment (Fig. 10). Each water bath contained two water pumps (Via Aqua
1300) to maintain a continuous flow of freshwater around the glass tanks. Water
temperatures in the glass tanks were raised for the 21°C treatment and lowered for the
10.5°C treatment over the course of approximately 7 hours and self-regulated by
temperature sensors which maintained the set temperatures within +0.5°C.
Each 77L glass tank contained a filter and water pump (Duetto DJ-100) to
cleanse, circulate, and oxygenate the seawater. In addition, approximately 50 percent of
the tank volume of seawater was changed every 4 to 7 days. Using temperature data-
loggers (Optic StowAway, Onset Computer Corp., Pocasset, MA) submerged in each
tank, water temperatures were recorded every 10 minutes during temperature ramping
and every 30 minutes during the rest of the experimental period.
Organisms
On 23 April, 2003, N.emarginata were collected from the Coal Point rocky
intertidal zone at the University of California, Santa Barbara. N.ostrina were collected on
April 24, 2003, from wave-exposed areas at Soberanes Point, CA. Whelk lengths were
measured for both species, and those with similar size ranges were used in the feeding
experiment. N.ostrina had a size range of 19.9- 26.8 mm, and N.emarginata had a size
range of 18.2-26.0 mm. Bay mussels (Mytilis trossulus) were collected from Strawberry
Hill, Oregon, on April 23, 2003. The mussels were cleaned, sorted for a size range of 15.
25 mm, and then placed in flowing ambient seawater.
Feeding Experiment
Whelks were placed in identical plastic containers (975 mL, Berry Plastics Corp..
Evansville, IN) drilled with small holes (8mm diameter). Each tank held two containers
with four N.ostrina per container and two containers with four N.emarginata per
container. Thus, each tank contained eight whelks of each species, and each temperature
treatment included 16 whelks of each species. The entire experiment comprised forty-
eight N.emarginata and forty-eight N.ostrina.
Whelks were then acclimated at ambient temperature without food for 4 days. On
April 30, 2003, temperatures were ramped down for the 10.5°C treatment and ramped up
for the 21°C treatment. Once the desired temperatures were attained, 25 mussels were
added to each plastic container.
Feeding Rate Measurements and Calculations
After 7 days, the numbers of dead mussels with drilled boreholes were counted
and replaced with live mussels. Dead mussels without boreholes were also replaced but
were not included in whelk feeding rates. In addition, live mussels with partially drilled
boreholes were neither replaced nor included in feeding rate measurements. The process
was repeated for three more weeks to obtain data for 4 time periods over the course of 28
days. Feeding rates were calculated by dividing the number of mussels consumed by the
total number of whelks per container. If whelk mortality took place over the course of a
7-day time period, then the factor (0.5)X(number of dead whelks) was subtracted from
the total number of whelks in a particular container. This factor calculated the number of
dead whelks between two time points since I could not be certain when a whelk died
during 7 day time period. For the following time period, assuming no more whelks
perished, the number of whelks in the container would equal the number alive at the
previous time point.
Qio Calculations
Qio values between each temperature interval (10.5°C - 16°C, 16°C - 21°c.
10.5°C -21°C) were determined for each species at each time point by using the Q10
equation (Q10 (ki/k2)""2) from Hochachka and Somero (2002). For an overall Q1o
value that incorporated all three temperature intervals at a given time point, inputs for the
equation were derived from a regression curve that fit a line of feeding rate versus
temperature.
Respirometry
Respirometry trials were conducted in order to assess differences between the two
species at a constant temperature. Whelks used in these trials were maintained in ambient
seawater and left unfed for at least 5 days. Äfter puncturing the plastic corks of glass
chambers (134mL) with a 10mL syringe (B-D 10mL Latex-free Syringe, Becton
Dickinson and Co., Rutherford, NJ) and a PrecisionGlide needle (18G1 ½, Becton
Dickinson, NJ), whelks were placed into several sealed chambers filled with ambient
seawater. To allow the whelks to equilibrate to the assay temperature of 12.2°C, the
chambers were then placed in a 12.2°C water bath for 40 minutes. The assay temperature
was chosen to approximate ambient seawater temperatures experienced by the whelks at
that time. Data were recorded using PowerLab (model 8SP, ADInstruments, Mountain
View, CA) and the PowerLab Chart Program. Seawater aerated with an air pump was
used to calibrate the oxygen electrode to 100% saturation, and sodium sulfite was used to
calibrate the electrode to 0% saturation.
After a 40 minute equilibration, a gas-tight syringe was used to remove 1mL
seawater from each chamber and, then, to inject the seawater into the electrode unit. The
1OmL syringe served as a reservoir of seawater to replace the ImL fraction and prevent
the build-up of negative pressure inside the chamber. Further 1mL fractions were
removed at 30 minute intervals for 120-150 minutes. Each trial included an empty
chamber as a control. At the end of each trial, whelks were dissected and weighed to
determine wet weights. Also, the volume of seawater in each chamber was measured.
Change in percent O2 saturation over the time course was calculated using a
regression curve fitting the percent O2 saturation at each interval. The slope of the contro
was subtracted from the slope of an experimental chamber to determine actual percent
change in O2 saturation in a given chamber. Using the resulting slopes, the mass-specific
oxygen consumption rates were calculated.
Statistical Analysis
Replicate plastic containers were the experimental unit and, as such, average
feeding rates were measured per container. Temperature data-loggers within each tank
confirmed that each container experienced the same temperature range in any tank
undergoing the same temperature regime. Thus, each container was treated as an
independent unit. With two different species at three temperature treatments over 4 time
points, the experiment involved 96 combinations of feeding rates per treatment per
container. Thus, a factorial ANÖVA was used to determine the effect of period, species,
and temperature on feeding rate. In addition, the interactions among period and species.
period and temperature, and species and temperature were tested. Finally, the interaction
10
between all three factors, period, species, and temperature, was tested via factorial
ANÖVA. Systat Version 8.0 was used for ANÖVA analyses. By utilizing the Student-
Newman-Keuls test for differences among means, statistically significant differences
among species at the same time point and under the same temperature treatment were
determined. At the end of the experiment, again using a Student-Newman-Keuls test,
differences between total consumption rates were identified. In the respirometry
experiment, a one-way ANOVA was used to calculate the effect of species difference on
respiration rates.
Results
Several interspecific, thermal, and temporal comparisons will be delineated in the
following section. First, feeding rates will be compared between species at specific
temperatures and time periods and between time periods for each species at a particular
temperature. Feeding rate ranges for the entire experiment will then be compared
between species for each temperature. Second, for each time period, overall Qjo values
will be presented for each species. Qio ranges of each temperature interval for each
species will be given. Third, total consumption rates at each temperature treatment and
total Qjo values for the entire experimental period will be compared between species.
Finally, the respiration rates of each species will be given.
Temperature Treatments
Temperatures for the 10.5°C and 21°C treatments were within +0.5°C of desired
values throughout the experimental period. Ambient temperatures were more variable but
averaged -16°C. (Fig. 1)
Absolute Feeding Rates
N.emarginata tended to have higher feeding rates than N.ostrina during the first
14 days while N.ostrina appeared to have greater feeding rates after 21 and 28 days. At
21°C, N.emarginata had significantly higher feeding rates than N.ostrina during periods
and 2 (Fig. 2., Student-Newman-Keuls Test, px0.05). N.emarginata feeding rates were
again significantly greater at 10.5°C during period 1, while N.ostrina had significantly
greater feeding rates at 10.5°C during period 4 (Student-Newman-Keuls Test, pæ0.05).
Under ambient conditions for all time points, no significant interspecific differences in
feeding rate were present (Student-Newman-Keuls Test, p20.05)
N.emarginata displayed more temporal variation in feeding rate than N.ostrina.
At 21°C and 10.5°C, Nemarginata had a significant decrease in feeding rate between the
second and third period (Fig. 3, Student-Newman-Keuls Test, p«0.05). N.ostrina,
however, had no significant changes in feeding rate over time across all temperatures
except for a significant increase in feeding rate at 10.5°C between period 3 and 4 (Fig. 4,
Student-Newman-Keuls Test, p20.05).
In the 21°C temperature treatment, N.emarginata exhibited feeding rates in the
range 1.56 to 3.63 mussels per whelk per 7 days (Fig. 3). In contrast, Nostrina’s range of
feeding rates at 21°C was 1.94 to 2.29 mussels per whelk per 7 days (Fig. 4). At ambient
temperature, N.emarginata demonstrated a feeding rate range of 1.16 to 2.56 while
N.ostrina’s range was 1.103 to 2.25 at the same temperature. N.emarginata had a range
of 0.357 to 2.25 in the 10.5°C temperature treatment while N.ostrina had a range of 0.452
to 1.40.
Thermal Dependence: Qjo Values Between Time Periods
Feeding rates of both N.emarginata and N.ostrina were sensitive to changes in
water temperature (ANÖVA, F-ratio= 28.405, p50.001). Overall Qjo values, derived
from regression curves (see Materials and Methods), showed that N.emarginata had
Qjo’s of 1.64 and 2.77 for periods 1 and 2, respectively (Table 1). After 21 days, the Q1o
climbed to 4.49 and then decreased slightly to 3.40. N.ostrina presented a similar pattern.
Qio values increased from 1.57 to 2.15 during the first 14 days. By day 21, the Qjo spiked
at 5.35 and then rapidly declined to 1.67 by the end of the experimental period.
Thermal Dependence: Q1o Values Between Temperature Intervals
With the notable exception of the 10.5°C -16°C temperature interval,
N.emarginata and N.ostrina had similar ranges for Qjo values in each temperature
interval over the course of 28 days. In the 10.5°C -16°C temperature interval, Qjo values
of N.emarginata ranged from 1.30 to 13.5 (Table 1). In contrast, the 16°C - 21°C interval
was less varied with a Qjo range of 1.43 to 3.19. Finally, a gradual increase in Q10
occurred in the 10.5°C - 21°C interval with a range of 1.61 to 4.39. For N.ostrina, the
10.5°C - 16°C interval again displayed a relatively large Qio range (0.91 to 5.97). The
16°C -21°C interval had a Q1o range of 0.84 to 3.29 while the 10.5°C -21°C interval had a
range of 1.63 to 4.43.
Total Consumption Rates and Total Q1o Values
Total consumption rates increased with increasing water temperature but were not
significantly different between species at any temperature (Fig. 5, Student-Newman-
Keuls Test, p20.05). N.emarginata’s total consumption rates were 1.06, 1.71, and 2.48 at
10.5°C, 16°C, and 21°C, respectively. Similarly, N.ostrina’s total consumption rates were
0.994, 1.58, and 2.07 at 10.5°C, 16°C, and 21°C, respectively. The overall Qio value for
the entire 28-day period was 1.96 for N.emarginata and 1.92 for N.ostrina (Fig. 6).
Respirometry
N.emarginata had a significantly greater average respiration rate (0.16% 02
consumed/mL seawater/hr/g) than N.ostrina (0.050% O2 consumed/mL seawater/hr/g)
(Fig. 7, one-way ANÖVA, p#0.001). N.emarginata also showed greater within-species
variation in respiration rate than N.ostrina.
Discussion
The results of this study suggest that Nemarginata is capable of feeding and
respiring at much higher rates than N.ostrina and that N.emarginata is also more likely to
decrease feeding rates in response to satiation. While N.ostrina may not reach
N.emarginata’s high feeding rates, N.ostrina tends to be less sensitive to satiation.
Alternatively, changes in feeding rates over time may have been distorted by stressful
laboratory conditions. In addition, since the feeding history of either species could not be
ascertained, changes in feeding rates may have also been due to different initial energy
stores. Nevertheless, over the long-term, both species exhibit similar average feeding
rates at all temperatures. Both Nucella congeners also have feeding rate sensitivity to
water temperature. Though fluctuations in Qjo occur for both species between 7-day
intervals, N.emarginata and N.ostrina have Qjo’s close to 2 over a longer time period (28
days).
Average Feeding Rates: N.emarginata
Observed feeding rates for N.emarginata over the first two time periods tended to
be higher than expected given feeding rates from related experiments on thermal
dependence of feeding for drilling whelks. Studies performed on N.canaliculata used
larger size ranges of mussels and mussels were counted every 14 days (Sanford, 2002).
Thus, in such experiments, fewer mussels would provide the same energy input.
Over time, N.emarginata seemed to ramp down feeding rate more quickly at 16°C
and especially 10.5°C. Perhaps, between periods 1 and 2, satiation had a more
pronounced effect at lower temperatures because of lower metabolic costs associated
with lower temperatures. Alternatively, the reductions in feeding rates at lower
temperatures may have been due to stress associated with laboratory conditions. In this
alternative scenario, N.emarginata at the lower temperatures responded to stress by
reducing feeding rates more rapidly.
By period 3, feeding rates at lower temperatures again declined. However, in this
case, N.emarginata at 21°C finally responded to satiation by considerably decreasing
feeding rates. The higher metabolic rates at higher temperatures may have required
N. emarginata to maintain elevated feeding rates for a longer time period. N.emarginata’s
potential for high feeding rates is consistent with its designation as a southern
thermophilic species by Marko (1998). Living in habitats with higher water temperatures
one would expect N.emarginata to have a higher feeding rate capacity in order to
compensate for the greater metabolic costs.
Between the third and fourth period, N.emarginata feeding rates remained
relatively constant at all temperatures. This suggests that either N.emarginata reached a
minimum feeding rate associated with satiation or that, even under stress, N.emarginata
had minimum feeding requirements. Since Nucella species have been shown to live for
months without food (Sanford, personal communication), the latter explanation may be
less likely. Also, if stress is playing the major role, then one might expect that feeding
rates would decline further by period 4, but this does not occur. In addition, despite
having no mortality at 21°C, N.emarginata showed a significant reduction in feeding rate
at that temperature between periods 2 and 3.
Average Feeding Rates: N.ostrina
While feeding rates at 21°C remained quite constant for N.ostrina over all time
periods, feeding rates at 16°C and 10.5°C declined from period 1 through period 3. Again.
lower metabolic costs at the cooler temperatures may have allowed a more significant
response to satiation. By period 3, N.ostrina feeding rates closely matched those of
N.emarginata, but, by period 4, N.ostrina had increased feeding at both temperature
extremes. These results suggest that feeding rates during satiation for both species are
similar in absolute terms, but N.ostrina is not as far from its maximum feeding capability
In addition, N.ostrina seemed to rebound from a sated state more quickly, implying that
N.ostrina has a shorter satiation phase to compensate for a lower maximum feeding rate.
At 21°C, N.ostrina’s metabolic processes may be operating at rates that preclude
satiation. Feeding rates may not be able to increase further because N.ostrina may already
be close to the maximum rate of feeding that is physically permissible for the whelk.
Thus, feeding rates stay at a high level to keep up with metabolic costs. This is consistent
with Marko’s (1998) conclusions that N.ostrina do not live south of Point Conception.
where a 4°C increase in temperature occurs. N.ostrina in 21°C water temperatures may be
close to their thermal limit for feeding.
Total Consumption Rates
Since total consumption rates were not significantly different between species at
any temperature, N.ostrina may use a shorter satiation phase to compensate for lower
feeding capacity and thus maintain comparable energy input to N.emarginata over the
long term. On the other hand, N.ostrina might be better equipped to adapt to stress (e.g.
re-circulated water flow, bacteria) since it returned to higher feeding rates by the end of
the experiment.
Q1o Effects
The results of this study suggest that N.emarginata and N.ostrina have similar
feeding rate responses to temperature over the long term. Qjo values for the 28-day
experiment were 1.96 and 1.92 for N.emarginata and N.ostrina, respectively. The thermal
dependence of feeding for N.emarginata changed considerably over time. The increase in
Q1o value from 2.77 at period 2 to 4.49 at period 3 was driven primarily by sharp
reductions in feeding rate at 10.5°C. In fact, the Q1o value for the 10.5°C- 16°C interval
climbed sharply from 1.91 to 10.6. This is not unusual since much higher Qio values have
been observed for 10°C- 15°C intervals (Q10= 25) in temperature-dependent feeding of
the oyster drill Urosalpinx cinera on mussels (Hanks, 1957). Sanford (2002) showed
comparable Qjo effects for N.canaliculata (Qio’s ranging from approximately 2.4 to 7.1
between 9°C and 12°C). N.emarginata may have experienced much lower metabolic
costs at the lower temperature. Also, N.emarginata’s thermal dependence of feeding may
decrease with increasing temperature as satiation ensues. N.ostrina also showed a peak in
Q1o (5.35) at period 3, again driven by lower feeding rates at 10.5°C and a high Q1o
between 10.5°C and 16°C (5.97). Thus, Nostrina exhibited similar thermal dependence
patterns as N.emarginata until period 3. By period 4, the overall Q1o value returned to a
level similar to period 1. This suggests that, whether as a recovery from satiation or
stress, N.ostrina can decrease its thermal dependence of feeding more rapidly than
N. emarginata.
Respirometry
Surprisingly, N.emarginata, the southern thermophile, showed higher oxygen
consumption rates than N.ostrina. Inhabiting the warmer waters south of Point
Conception, one would expect N.emarginata to have lower metabolic activity at a given
temperature. Further study needs to be conducted to confirm the results found here and to
determine the thermal dependency of respiration for both species.
N.emarginata’s high maximum feeding rates might be required to replace the
energy lost through its higher metabolic costs. Respirometry showed that N.emarginata
tended to have more variable respiration rates at 12.2°C than N.ostrina. Thus,
N.emarginata might also have a greater ability to alter metabolic activity in response to
temperature changes. Greater metabolic plasticity in N.emarginata might help explain
N.emarginata’s prolonged response to satiation and thus also clarify why N.emarginata
and N.ostrina had similar total consumption rates by the end of the experiment.
Alternatively, the N.emarginata sample size may have been too low to reduce variation in
respiration readings.
Conclusions
The physiological results of this study correlate with the thermal environments
inhabited by N.emarginata and N.ostrina. Though both species show similar patterns of
thermal dependency of feeding, N.emarginata exhibits greater maximum feeding rates
and greater O2 consumption rates. Living at higher temperatures, N.emarginata might
have higher feeding rates in order to cover the costs of higher metabolic activity. As the
climate warms, N.emarginata may be able to take advantage of its temperature
adaptations to out-compete N.ostrina in regions of overlapping populations. Both species
of Nucella showed feeding rates that changed over time, but N.emarginata had a
prolonged satiation phase compared to N.ostrina. In contrast, N.ostrina’s lower maximal
feeding rates were more consistent over time. Thus, in habitats where food can be scarce,
N.emarginata could rapidly increase feeding rate when food is available but then wait in
its longer satiation phase when food is in short supply. Net energy input would be greater
for N.emarginata, especially at temperatures near or above 21°C. Though Marko suggests
that N.emarginata’s northward range expansion was probably not due to climatic change,
the results here suggest that climatic change could potentially accelerate the process.
Acknowledgements
First and foremost, I would like to thank George Somero for his guidance, support, sense
of humor, and belief. His passion for marine biology was truly infectious. Jim Watanabe
also provided insightful advice and was incredibly helpful with experimental design and
statistical analysis. I would also like to thank the entire Somero Lab for supporting this
work through thoughtful advice and technical assistance. Though not currently at
Hopkins Marine Station, Eric Sanford provided much of the inspiration behind this
project and never failed to answer even the most naïve queries via lengthy email
correspondence. In addition to Eric, Brad Buckley of UC Santa Barbara and colleagues
from Oregon State University helped obtain organisms required for this work. Also, I
owe much to my fellow Bio 175H students who provided a wonderful atmosphere for
learning and research in an idyllic setting. I could not have completed this project without
their help and support. Finally, I would like to thank all the instructors involved in 175H
who carry on the venerable tradition of turning wide-eyed undergraduates into budding
researchers. This course has been challenging and laden with unforeseen obstacles, and
yet it has also been one of the most rewarding of my Stanford career.
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simulating episodic upwelling. J. exp. Mar. Biol. Ecol. 273: 199-218.
Sanford, E. 1999. Regulation of keystone predation by small changes in ocean
temperature. Science 283: 2095-2097.
Stickle, W.B., and B.L. Bayne. 1982. Effects of temperature and salinity on oxygen
consumption and nitrogen excretion in Thais (Nucella) lapillus (L.). J. exp. Mar.
Biol. Ecol. 58: 1-17.
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Figure Legend
Fig. 1. Water Temperatures during the 28-day N.emarginata and N.ostrina feeding rates
experiment. Whelks were held in three treatments: constant 10.5°C,-16°C (ambient), and
21°C. Temperatures were recorded every ten minutes during temperature ramping and
every thirty minutes for the rest of the experimental time period.
Fig. 2. N.emarginata and N.ostrina feeding rates in three laboratory treatments over a
four week time period. Bars are mean number of mussels eaten per whelk per 7 days (n-
4 containers per treatment). Ästerisks above bars indicate statistical differences between
species (Student-Newman-Keuls Test, px0.05
Fig. 3. N.emarginata in three laboratory treatments over a four week time period. Bars
are mean number of mussels eaten per whelk per 7 days (n= 4 containers per treatment).
Identical letters above bars indicate statistical differences between time periods at a given
temperature treatment (Student-Newman-Keuls Test, p£0.05). Qjo values for a given
period are indicated above each set of bars.
Fig. 4. N.ostrina in three laboratory treatments over a four week time period. Bars are
mean number of mussels eaten per whelk per 7 days (n= 4 containers per treatment).
Identical letters above bars indicate statistical differences between time periods at a given
temperature treatment. Qio values for a given period are indicated above each set of bars.
Fig. 5. N.emarginata and N.ostrina total feeding rates in three temperature treatments.
Bars are mean number of mussels eaten per whelk over 28 days (n= 4 containers per
treatment). Ästerisks above bars indicate statistical differences between species (Student-
Newman-Keuls Test, p50.05)
Fig. 6. N. emarginata and N.ostrina total feeding rates in three temperature treatments.
Colored lines indicate actual feeding rates at each temperature over 28 days, and dashec
lines indicate regression curves. Qjo values calculated from regression curves are noted.
Fig. 7. N.emarginata and N.ostrina respiration rates. Bars are mean respiration rates of
%02 consumed per mL seawater per hour per gram wet weight. The star indicates a
statistical difference between respiration rates of the two species (one-way ANÖVA.
p50.001, N.emarginata n-9, N.ostrina n= 12)
t
Temperature (°C)
3




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