Download The inability of northern whelks to drill the range extending barnacle

The inability of northern whelks to drill the range extending barnacle Tetraclita rubescens
Daniel S. Swezey
Eric Sanford
Introduction:
Materials and methods:
Recent studies have documented geographic range extensions in a variety of systems and taxa (Parmesan and Yohe 2003). As species
expand into new regions, interactions with predators and competitors may play an important but understudied role in determining the
success of the range extension. The volcano barnacle Tetraclita rubescens was historically reported on rocky shores from Baja
California to San Francisco but has recently extended northward to Cape Mendocino, CA (40°24’N) (Connolly and Roughgarden 1998).
Field: We conducted an experiment to test: (1) whether whelks differ in their preference for Tetraclita relative to two other species of intertidal
barnacles, and (2) whether whelks from a southern population prey more intensely on Tetraclita than whelks from a northern population. In June
2005, we attached 20 stainless steel mesh cages (measuring 20 x 20 x 5cm, l x w x h) in the low intertidal zone at Bodega Marine Reserve (latitude:
38º19’N). Each cage contained a plastic plate (15x15 cm) to which we epoxied 10 barnacles (basal diameter = 7-10 mm) from each of three species:
Balanus glandula, Semibalanus cariosus, and Tetraclita rubescens. Juvenile Semibalanus cariosus were collected on mussel shells (Mytilus
californianus) at Shelter Cove, CA (latitude: 40º01’N), juvenile Tetraclita rubescens were collected on the wall plates of larger Tetraclita from
Soberanes Point, CA (latitude: 36º26’N ), and Balanus glandula were collected on mussel shells from Bodega Marine Reserve. For barnacles
attached to mussel shells, we cleaned the shells of tissue and used a band saw to cut out the small piece of mussel shell that included the barnacles.
We then used marine epoxy (Z-spar) to attach the 30 barnacles in a random distribution across each plate. Each cage was randomly assigned to
either a treatment group (containing 5 whelks, shell length 16-19.6 mm) or a control group (no whelks). For cages with whelks, 8 contained Nucella
ostrina collected from Soberanes Pt. (in an area of dense Tetraclita populations), and 8 contained Nucella ostrina collected in the Bodega Marine
Reserve (a site only recently colonized by sparse numbers of Tetraclita). Whelks were held in the laboratory in flowing sea water and without food for
9 to 11 days and were then placed in field cages. After 21 days, the cages were opened and barnacle mortality was recorded.
Thaid gastropods (whelks) are the primary
predators on intertidal barnacles and may
have driven an evolutionary reduction in
the number of plates making up the
barnacle shell (Palmer 1982). Because
whelks often target sutures between plates
for drilling, having fewer plates might
reduce the number of successful attacks.
Tetraclita is unique on the California coast
in that it has only 4 parietal plates as
opposed to the 6 parietal plates of most
other barnacles. Along with its narrow
opercular opening and “thatched” external
plates, Tetraclita may have morphological
features that defend it from whelk
predation. The two most common
intertidal whelks along the California coast
also differ in drilling strategies;
N. canaliculata typically drills barnacles
through the parietal walls, whereas
N. ostrina often drills through the opercular
plates (Palmer 1982). Thus, barnacle
morphology and whelk drilling behaviors
may interact to determine barnacle
susceptibility to whelk predation.
Nucella ostrina
Cape Mendocino
Present Range Limit (2005)
Shelter Cove
Nucella canaliculata
Kibesillah
Bodega
San Francisco
Old Range Limit (1980)
Soberanes Pt.
CALIF.
Pacific
Ocean
Tetraclita rubescens
As Tetraclita populations expand northward, this species will likely compete for space with other resident barnacle species including
the northern barnacle Semibalanus cariosus. However, Tetraclita’s morphology may reduce whelk predation and thus give Tetraclita
an advantage when competing for space. In addition, northern whelks encountering Tetraclita for the first time may not be genetically
(Sanford et al. 2003) or behaviorally predisposed (West 1986) to recognize and prey upon Tetraclita.
We used field and laboratory experiments to address the following questions:
1) Do whelks prefer to drill other barnacles (Balanus glandula, Semibalanus cariosus) more than Tetraclita?
2) Is predation on Tetraclita lower among northern whelk populations than among more southern whelk populations that have a
longer history of co-occurrence with this barnacle species?
3) Do whelk species with different drilling strategies (Nucella ostrina versus N. canaliculata) differ in their ability to prey upon
Tetraclita?
4) Do differences in shell morphology make Tetraclita less vulnerable to drilling predation than Semibalanus cariosus?
Barnacle plates
Cages in the field
Laboratory: Studies were conducted at BML to test whether: (1) whelk species differ in their ability or propensity to drill Tetraclita and Semibalanus, and
(2) barnacle shell morphology influences the success of whelk predation. The experiment used 180 plastic containers (1-liter), each of which contained
one barnacle (Semibalanus cariosus or Tetraclita rubescens) and one whelk (Nucella ostrina or Nucella canaliculata). The containers were randomly
placed across two sea tables and each container was supplied with flowing seawater from an independent water line. Tetraclita were collected on
intertidal mussels from Soberanes Pt. and the S. cariosus were collected on intertidal mussels from Kibesillah Hill (latitude: 39º36’N). Whelks were also
collected from Kibesillah Hill from a patch of mussels covered with barnacles (S. cariosus), and were held in the laboratory without food for 10 days
prior to the start of the experiment. Barnacles collected on mussel shells were isolated using a band saw (as described above), and were epoxied onto
5 x 5 cm squares of lexan plastic. All barnacles used had a basal diameter of 13-23 mm.
To test the role of barnacle morphology in defense versus whelk predation, we filed down the tops of some barnacles. Barnacles were randomly
assigned to three treatments: filed, “pseudo-filed” (a procedural control), or untouched. In the filed treatment, we removed excess shell at the top of
each barnacle to increase exposure of the opercular plates (see below). To simulate possible stress due to the filing treatment, barnacles within the
pseudo-filed group were lightly filed along the sides of their parietal plates for the same length of time used in the filing treatment. Whelks and barnacles
were assigned to plastic containers (2 whelk species x 2 barnacle species x 3 barnacle treatments x 15 replicates = 180 containers total) Whelks and
barnacles were left undisturbed in their containers for 10 days and then barnacle mortality was recorded in each container.
Lab Barnacle Treatments
Treatment Group
Barnacle
Top filed to expose
opercular plates
Whelk
Results:
Field: N. ostrina from both Soberanes Point and Bodega Marine Reserve consumed significantly higher quantities of B.
glandula and S. cariosus than Tetraclita after 21 days in the field (Figures 1 & 2). Mortality in control cages was minimal
(Figure 3) suggesting that most mortality in the cages was caused by whelks.
80
60
40
60
40
20
20
0
0
S.
cariosus
100
% Mortality
80
% Mortality
% Mortality
100
B.
glandula
Figure 3. Control (No Whelks)
Figure 2. Soberanes Whelks
Figure 1. Bodega Whelks
100
Barnacle Species
80
60
40
20
0
B.
glandula
T.
rubescens
S.
cariosus
T.
rubescens
B.
glandula
Barnacle Species
S.
cariosus
T.
rubescens
Barnacle Species
Laboratory: After 10 days, roughly twice as many N. canaliculata than N. ostrina had consumed the barnacle in their
containers (n=27 versus 13, respectively). Of the 27 barnacles consumed by N. canaliculata only 3 were Tetraclita.
N. ostrina did not consume any Tetraclita after 10 days. Filing seemed to show no significant effect on the attractiveness of
S. cariosus to both whelk species (Figure 4+5).
Figure 5. N. canaliculata Lab Drilling
100
80
80
% drilled
% drilled
Figure 4. N. ostrina Lab Drilling
100
60
40
20
60
40
20
0
0
Control
Filed
Pseudo
Tetraclita
Control
Filed
Pseudo
Semibalanus
Control
Control
Filed
Tetraclita
Pseudo
Control
Filed
Pseudo
Filed
Sea tables at Bodega Marine Lab
Inside of each container
Discussion:
1) Do whelks prefer to drill other barnacles more than Tetraclita?
In both lab and field studies, N. ostrina and N. canaliculata demonstrated a clear preference for barnacle species other than Tetraclita (Figures 15). N. ostrina from Kibesillah Hill and Soberanes Point were unable or unwilling to drill any Tetraclita during initial observations of the lab and field
experiments (to date).
2) Is predation on Tetraclita lower among northern whelk populations than southern whelk populations co-occurring with Tetraclita?
Interestingly, we found that N. ostrina from Soberanes Point collected among high densities of Tetraclita did not drill Tetraclita in the field after
3 weeks while those from Bodega drilled Tetraclita at a low level (Figures 1 & 2). This may be due to a lower barnacle consumption rate of the
Soberanes whelks (only half that of the Bodega whelks). N. ostrina from Soberanes Point may need to further deplete other barnacle species
before they begin to drill Tetraclita.
3) Do whelk species with different drilling strategies (Nucella ostrina versus N. canaliculata) differ in their ability to prey upon Tetraclita?
The difference in overall consumption rates between N. ostrina and N. canaliculata may be a result of species specific behavior differences in
predation rate. No Tetraclita have been drilled by N. ostrina in the lab, and this may reflect a size escape in Tetraclita or different drilling strategies
and abilities of the two whelk species.
4) Do differences in shell morphology make Tetraclita less vulnerable to drilling predation than Semibalanus cariosus?
Continuing lab studies will investigate the difference in rate of suture recognition between N. canaliculata and N. ostrina on drilled barnacles in the
lab. Filing of the barnacle shells in the lab did not appear to influence barnacle attractiveness thus far (Figure 4+5). Ongoing lab and field trials will
indicate whether or not the whelks can drill Tetraclita as a last resort given enough time.
Conclusions: In the field, juvenile Tetraclita are preferred less than other barnacles, and as they increase in size, they may be nearly invulnerable
to predation pressure from northern whelks. As we continue to see species shift their ranges at an increasing rate globally, it will be become
increasingly important to understand the interactions between established predators and competitors with newly arriving species. Our results
suggest that intertidal barnacle assemblages along the north coast of California may experience significant changes in species composition over
the coming decades.
Semibalanus
Acknowledgements: We would like to thank the National Science Foundation REU program (Grant # DBI0453251) for funding.
We are grateful to Rachael Dickey, Amanda Newsom, Arunima Kolekar, and Jackie Sones for their contributions to this project.
We would also like to thank the staff at BML for all of their guidance and support throughout the course of the project.
References:
Connolly, S.R., J. Roughgarden. 1998. CA Fish and Game 84, 182.
Palmer, A.R. 1982. Paleobiology 8, 31.
Parmesan, C., G. Yohe. Nature 421, 37.
Sanford, E., et al. 2003. Science 300, 1135.
West, L. 1986. Ecology 67, 798.