Markham 2
Effects of the loss of the Apical Meristem on Growth and Tissue Composition in
Macrocystis pyrifera
Abstract
Changes to the physiology or chemistry of basal producers can have direct consequences
for consumers and the transfer of energy between trophic levels. As a foundation species, giant
kelp Macrocystis pyrifera sustains high growth rates and primary productivity under dense
shading canopies through an efficient system of translocation that provides energy and nutrients
to growing tissues. This study investigated what impact removing the growing point or apical
meristem from M. pyrifera, as occurs in storms, commercial harvest and historically in grazing
by the Stellar's sea cow, has on the physiology of the remaining immature sub-apical blades.
Blades from fronds experienced increased growth and erosion rates within the first week after
removal of the apical meristem as compared with controls. Äfter two weeks growth and erosion
rates were no longer significantly different between manipulated blades and control but
substantial differences in concentrations of the sugar mannitol as well as nitrogen and carbon
content persisted. The study revealed physiological effects of apical meristem loss that merit
further investigation as to their causal mechanisms and suggest the potential for meristem
removal to alter interactions with primary consumers.
Markham 3
Introduction
In many different ecosystems changes to the physiology or chemistry of basal producers
can have direct consequences for consumers and the transfer of energy between trophic levels
(Moe et al. 2005). Changes in tissue chemistry for autotrophs particularly have the potential to
alter palatability to herbivores through shifts in concentrations of secondary metabolites,
nutritional content, and structural stability (Hemmi & Jormalainen, 2002; Poore & Steinberg,
1999). Understanding changes in basal producers that may take place as a result of
environmental shifts or anthropogenic impacts can yield important insights into the flow of
energy through and nutrient cycling between trophic levels (Graham 2004).
The giant kelp Macrocystis pyrifera functions as a foundation species forming dense
forests upon which diverse communities of organisms rely for food and shelter in temperate
coastal waters around the globe(Arkema, Reed, & Stephen C Schroeter, 2009; Dayton, 1985;
Graham, 2004; Mann, 2000; Steneck et al., 2003). Its astonishingly high rates of growth and
primary productivity form the basis for numerous natural food webs and support expansive
canopies that sustain commercial harvests for various human uses (Buschmann & Hernandez-
Gonzalez, 2005; Doty, 1987; Gutierrez et al., 2006; Mann, 1973). Kelp growth is sustained by an
efficient system of translocation that moves energy and nutrients from mature portions of the
kelp to the growing points at the end of the fronds—the apical meristems (Lobban, 1978b; North,
1971). Detailed studies with "C tracers and fluorescein dye demonstrated that photosynthates
move at rates of up to 78 cm/hr both up and down the fronds of Macrocystis (Parker, 1963;
1965). The translocated substances— the sugar mannitol, amino acids, and inorganic ions¬
follow a “source-sink" dynamic: fully developed blades export these materials while immature,
Markham 4
growing blades import them to aid in growth (Schmitz & Lobban, 1976; Schmitz & Srivastava,
1979).
Apical meristems serve as an important sink drawing metabolites up the fronds toward
the rapidly growing blades at the apex (Lobban 1978a; Schmitz & Srivastava 1979). Early work
suggested that fronds without apical meristems no longer translocate materials up the frond but
instead send them down toward the base (Lobban, 1978a). However, little work has been
conducted explicitly to understand how the loss of the apical meristem affects blades remaining
on Macrocystis fronds.
The apical meristems of Macrocystis are commonly lost to storm damage (Seymour, M
J Tegner, Dayton, & Parnell, 1989) and many more are removed during canopy cutting for
commercial harvest (Doty, 1987). Moreover, historically, canopy grazing by the immense
Stellar’s sea cow (once abundant from California to Japan, now extinct) would have frequently
removed Macrocystis apical meristems (Burger, 1995). Reduced translocation could potentially
result in physiological changes to the remaining blades with rippling ecological effects with
direct and indirect consequences for organisms that interact with Macrocystis blades such as
microbial biofilms (Bengtsson, Sjøtun, Storesund, & Ovreås, 2011; Duggins, Simenstad, & J.
Estes, 1989; Norderhaug, Fredriksen, & Nygaard, 2003), epiphytic sessile invertebrates (Dixon.
S.C. Schroeter, & Kastendiek, 1981; Hepburn & Hurd, 2005), and invertebrate mesograzers
(Duggins, Eckman, Siddon, & Klinger, 2001; Foster & Schiel, 1985; McMillan, 2010;
Norderhaug et al., 2003; Watanabe, 1984)
In this study we sought to address what effect the removal of the apical meristem has on
the growth rate and chemical composition of the remaining sub-apical blades. We hypothesized
that the loss of the apical meristem would halt translocation of mannitol to the remaining sub¬
Markham 5
apical blades, thereby slowing growth rates and reducing the C:N ratio as a consequence of the
nitrogen built up in the tissue relative to faster growing portions. We further postulated that a
reduced C:N ratio could make blades more palatable to microbes and grazers, thus resulting in
greater rates of erosion.
Methods
The experiment was conducted in the shallow kelp forests of the Hopkins Marine Life
Refuge in Monterey, CA (36° 36’ N, 121° 54' W). Pairs of kelp fronds of similar length were
selected from twenty Macrocystis pyrifera sporophytes. The apical meristems were removed
from one frond of each pair by severing the stipe 25cm below the first dividing pneumatocyst on
the apical scimitar (Figl). The paired un-cut frond was used as a control. Growth and
deterioration rates were determined by the commonly used hole-punch technique (Rothäusler et
al., 2009) in paired blades 30 cm below the apical meristem (Fig.1) and compared in situ after
seven days and in the laboratory after sixteen days. Tissue was collected from each blade from
three holes approximately 17.5mm in diameter punched consecutively proceeding from the
growth measuring hole toward the pneumatocyst. The algal tissue was dried in an oven at 120°C
for 48hours and then ground with a ball mill (will check name) for thirty seconds per sample to a
fine powder for use in chemical analyses.
A colorimetric method (sensu White et al. 2010) was employed in order to compare
concentrations of mannitol in fronds with and without apical meristems. Mannitol was extracted
by heating 30mg of powdered kelp in 1.5 ml of water at 80 °C, centrifuging at 14000rpm for
30min, and removing the supernatant. 100 uL of this mannitol extract was added to 500 uL
formate buffer (0.5 mol L", pH 2.85). After mixing, 300 uL of Reagent 1 (5 mmol L* sodium
periodate) was added followed by 300 uL of Reagent 2 (consisting of 0.1 mol L * acetylacetone,
Markham 6
2 mol L“ ammonium acetate and 20 mmol L-1 sodium thiosulfate) was added. Reagent 2 was
always added 15 s after Reagent 1. The tube was then closed and heated in boiling water for 2
min, cooled under running tap water and measured with a spectrophotometer at 412 nm. Each
sample was diluted with water at: 1:10, 1:15, 1:20, and 1:50 vol/vol. Mannitol concentrations
were determined for each sample by cross-referencing with standards of varied concentrations
from which a linear relationship between absorbance and mannitol concentrations were obtained.
Due to the relatively low concentration of mannitol in M. pyrifera as compared with those
reported for other kelps by White et al. (2010) the full strength solution was used to calculate
percent mannitol.
In order to quantify Carbon and Nitrogen content, dried kelp powder in duplicate samples
was weighed on a Sartorius supermicro balance, and assayed for total N and C with a Carlo Erba
Na-1500 elemental analyser calibrated with acetanilide.
All data were analyzed using two-tailed, paired T-tests between blades from fronds with
and without apical meristems from each sporophyte.
Results
Äfter one week of growth, blades from fronds where the apical meristem was removed
grew significantly more quickly than intact controls (t=2.332, n-20, p=.0308) (Fig. 2). However,
after between days 7 and 14 the difference in growth rates was no longer significant (t=1.1136,
n=17, p=.281). The measure of erosion revealed that elongation occurred between the punched
hole and the blade tip. Äfter one week, blades from fronds with the apical meristems removed
had an average increase of distance from the punched hole to the blade tip of 3.Scm which was
significantly less than the average 6.6 cm of controls (t-2.124, n-20, p=.0467) (fig. 3). After 14
days the difference was no longer significant (t=.7804, n-17, p=.4445).
Markham 7
Analysis of Mannitol concentrations revealed that blades from fronds without apical
meristems had a significantly lower percent mannitol by dry weight as compared with controls
=4.2079, n=10, p=.0018) (Fig.4). However, the average percent carbon of blades from
manipulated fronds was significantly higher than that of controls (t-3.9597, n=17,
p=.0011)(Fig.5). No significant difference in percent Nitrogen was found between blades from
manipulated fronds (t=1.1807, n=17, p=.2549). Accordingly, the C:N ratio was significantly
higher for blades from manipulated fronds than those of controls (t-2.1648, n-17, p-.0448)
(Fig.6).
Discussion
High growth rates (Fig. 1) and an increased C:N ratio (Fig. 6)in blades from fronds
without apical meristems as compared with controls contradicted our initial hypotheses. While
reduced mannitol (Fig. 4) and increased erosion in blades from manipulated fronds (Fig.3) were
consistent with initial predictions, the causes of these changes are likely different than those that
were previously anticipated.
The increased growth rates of blades from fronds without apical meristems may still be
consistent with results from Parker (1965) and Lobban (1978) where fronds without their apex
no longer had any acropetal translocation (solute movement up the frond) but only basipetal
translocation (toward the holdfast). Translocation in Macrocystis is driven by osmotic gradient
whereby mature, "source" blades with a relative excess of mannitol and amino acids uptake
water which then flows with the solutes to immature, "sink" blades which excrete water to
encourage the flow (Schmitz 1982). If translocation upwards were halted with the loss of the
apical meristems, it would follow that the higher growth rates in blades from manipulated fronds
resulted from the fact that the manipulated blade would receive no imports but also would no
Markham 8
longer have blades above them with to export mannitol and amino acids to. By contrast as
control stipes continued to add blades, the focal blades became more and more distant from the
apical meristem, and may have shifted from primarily importers to partial exporters. This
bidirectional translocation, both importing and exporting, for blades between.75-1.1m from the
apical meristem as the control blades rapidly grew to in distance would be consistent with
previous work (Lobban 1978a). By exporting a portion of their photo-assimilates and amino
acids to the faster-growing blades above them on the fronds, control blades may have
experienced reduced growth rates. Under these conditions whatever mannitol the blades from
manipulated fronds produced would be used in situ for growth or to a lesser extent be drawn
weakly toward the base and the distant sink of new fronds. This hypothesis of halted acropetal
translocation is consistent with the lower concentrations of mannitol found in blades from
manipulated fronds as compared with controls (fig. 4). In controls the powerful "sink"
represented by the apical meristem and immature blades above the blades of interest would draw
a flow of mannitol acropetally from both the mature blades below and the mid-maturity blades
we measured (Lobban 1978b). This flow could keep levels of mannitol high as was found in our
mannitol assays.
Alternatively it is possible that the findings of Parker (1965) and Lobban (1978a) that
blades without apical meristems have no acropetal translocation were not applicable to this
experiment because of spatial and temporal differences in the experimental setups. Parker
removed not only the apical meristem but the preceding 30 blades as well in order to demonstrate
that fronds without apical meristems had only basipetal translocation. In doing so, he likely
remoyed all immature blades and therefore the osmotic gradient driving translocation. The
blades measured in this experiment would have been amongst the immature blades Parker
Markham 9
removed in his experiment. Likewise, Lobban simply conducted his experiments bathing blades
of Macrocystis in the field with radio-labeled C-14, on fronds as he encountered them in the field
with or without apical meristems. Considering the growth rates of Macrocystis blades, it seems
quite likely that would not have conducted his experiments in the short period between fronds
losing their apical meristem and the remaining subapical blades becoming mature.
It remains a distinct possibility that the removal of the apical meristems may have caused
accelerated translocation of mannitol and amino acids into the immature sub-apical blades until
the osmotic gradient was dissipated. As the last blade on a severed stipe, the blades from
manipulated fronds in our experiment would be free from competing "sinks" higher on the stipe,
therefore having a considerably weaker draw to export mannitol than controls. These factors
may explain the accelerated growth of blades from manipulated fronds in the first week.
Parker’s work (1965) would have missed this pattern because he removed the immature portion
of the frond entirely. Likewise Lobban, could have failed to observe such translocation by
missing the narrow window in which accelerated acropetal translocation followed meristem loss
can be measured, before it halts as the blades mature and the osmotic gradient dissipates. Future
experimentation could easily resolve these conflicting hypotheses by testing concentrations of
mannitol and amino acids during the period of rapid growth in the week following apical
meristem removal.
Regardless of the cause of the accelerated growth rates in blades from fronds without
apical meristems, this change in growth rate was associated with further shifts in chemical
composition (fig. 5 & 6). The higher percent carbon (fig. 5) coupled with lower concentrations
of mannitol (fig. 4) in blades from fronds without apical meristems, suggest that another form of
carbon different from mannitol is more prevalent as compared with controls. Whereas, mannitol
Markham 10
is known to be the ephemeral photoassimilate used in translocation, laminarin is known to be a
long-term storage carbohydrate (Lee, 1989). Lee notes that "Laminarin may be formed from
mannitol and during active growth mannitol can be formed faster than its rate of conversion into
laminarin so that both substances increase in amount. When growth slows down or
stops...laminarin increases with loss of mannitol". As the blades from both treatment groups
slowed in their growth over the second week the blades from manipulated fronds may have
converted what mannitol they had to laminarin. This increased conversion may have been due to
longer retention times of mannitol in blades from manipulated fronds without a flow of mannitol
or due to the comparatively greater maturity of these blades compared with those of controls. In
either case, the accretion of the more stable storage carbohydrate laminarin would explain the
higher percent carbon in blades from manipulated fronds. Moreover, a halting of translocation
would mean that the standing stock of mannitol would not be as actively replenished in blades
from manipulated fronds consistent with the reduced concentrations of mannitol. A simple assay
of laminarin concentration should be able to resolve whether the difference in percent carbon can
be attributed to laminarin production (White, Coveny, Robertson, & Clements, 2010).
Despite being confounded by elongation, the measurements of changes in distance
between the punched hole and the blade tip seem to suggest higher rates of erosion in blades
without apical meristems as compared with controls. It seems unlikely that the growth trends
observed in the proximal portion of the blades would be reversed in the distal portions of the
blade since Macrocystis blades lack structural subdivisions and most differences in the tissue
occur in a gradient (Lee 1989). Therefore, the smaller change in average length between the
punched hole and blade tip observed in manipulated blades as compared with controls suggests
that greater erosion occurred in blades from fronds without apical meristems. Additionally, the
Markham 11
higher growth rates of blades measured at the base from manipulated fronds as compared with
controls (fig. 2) suggests that the differences observed in erosion may be fairly conservative.
However, contrary to our initial hypotheses it is unlikely that this increased erosion is caused by
greater palatability for microbes associated with a reduced C:N ratio since manipulated blades, in
fact, had an elevated C:N ratio and we would expect blades with high microbial abundance to
have a lower C:N ratio (Duggins et al. 1989). Future work should address whether microbes are
in fact responsible for this accelerated breakdown and whether it is perhaps associated with
lower concentrations of polyphenols or higher concentrations of laminarin. Alternatively
increased erosion may be associated with structural difference associated with more rapid growth
rates or higher concentrations of laminarin. Investigating the cause of this accelerated erosion
and whether it occurred in blades that were already mature when the meristem was severed could
reveal interesting insights into the ecological ramifications of apical meristem loss and whether
such loss leads to an accelerated degeneration of cropped fronds.
In focusing on the consequences of changes in translocation for Macrocystis pyrifera
associated with apical meristem loss, this study took a substantially different approach than
previous work focusing on patterns of translocation under typical growing conditions (Parker
1963, 1965; Schmitz & Lobban 1976; Lobban 1978 etc.). The study reveals surprising
ramifications of the removal of apical meristems that merit further investigation into both their
underlying physiological mechanisms and ecological consequences. Our results lead to fürther
questions of whether the changes in erosion rates and chemical composition occur throughout
larger portions of the frond and whether such changes affect interactions with organisms
associated with the kelp, such as microbial biofilms and invertebrate consumers. Answering
these questions may in turn reveal important insights into the mechanisms by which kelp carbon
Markham 12
is made available to consumers, the impacts of harvesting, and the historic influence of canopy
grazing by Sellar’s sea cow (Fig.7).
Acknowledgements
I would like to thank Drs. Sarah Lee and Vanessa Michelou for their tireless efforts and
support, as well as Dr. Steve Palumbi for his invaluable insight. Special thanks also to Walker
Clayton and Nicole Sarto for being excellent snorkel buddies and lifeguards. Thanks also to the
faculty and students of Hopkins Marine Station who contributed to my project along the way.
Markham 13
Arkema, K., Reed, D. C., & Schroeter, Stephen C. (2009). Direct and indirect effects of giant
kelp determine benthic community structure and dynamics. Ecology, 90(11), 3126-37.
Bengtsson, M., Sjøtun, K., Storesund, J., & Øvreås, J. (2011). Utilization of kelp-derived
carbon sources by kelp surface-associated bacteria. Aquatic Microbial Ecology, 62(2),
191-199
Burger, R. (1995). Competition, Predation, and the Evolution and Extinction of Stellar’s Sea
Cow, Hydrdamalis Gigas. Marine Mammal Science, 11(3), 391-394.
Buschmann, A., & Hernandez-Gonzalez, M. C. (2005). Seaweed cultivation, product
development and integrated aquaculture studies in Chile. WORLD AQUACULTURE-,
36(3), 51-53.
Dayton, P. K. (1985). Ecology of Kelp Communities. Annual Review of Ecology and
Systematics, 16, 215-245.
Dixon, J., Schroeter, S.C., & Kastendiek, J. (1981). Effects of the encrusting bryozoan,
Membranipora membranacea, on the loss of blades and fronds by the giant kelp,
Macrocystis. Journal of Phycology, 17(4), 341-345. Wiley Online Library.
Doty, M. S. (1987). Case studies of seven commercial seaweed resources (281-282 ed., p.
311). Food & Agriculture Org.
Duggins, D., Eckman, J., Siddon, C., & Klinger, T. (2001). Interactive roles of mesograzers
and current flow in survival of kelps. Marine Ecology Progress Series, 223, 143-155.
Duggins, D., Simenstad, C., & Estes, J. (1989). Magnification of Secondary Production by
Kelp Detritus in Coastal Marine Ecosystems. Science, 245(4914), 170. American
Association for the Advancement of Science.
Foster, M. S., & Schiel, D. R. (1985). Ecology of giant kelp forests in California: a community
profile.
Graham, M. H. (2004). Effects of Local Deforestation on the Diversity and Structure of
Southern California Giant Kelp Forest Food Webs. Ecosystems, 7(4), 341-357.
Gutierrez, A., Correa, T., Munoz, V., Santibanez, A., Marcos, R., Cáceres, C., et al. (2006).
Farming of the Giant Kelp Macrocystis Pyrifera in Southern Chile for Development of
Novel Food Products. Journal of Applied Phycology, 18(3-5), 259-267.
Markham 14
Hemmi, A., & Jormalainen, V. (2002). Nutrient Enhancement Increases Performance of a
Marine Herbivore via Quality of Its Food Alga. Ecology, 83(4), 1052. doi:
10.2307/307191
Hepburn, C., & Hurd, C. (2005). Conditional mutualism between the giant kelp Macrocystis
pyrifera and colonial epifauna. Marine Ecology Progress Series, 302, 37-48.
Lee, R. E. (1989). Phycology. Phycology (p. 146). New York: Cambridge University Press.
Lobban, C. S. (1978a). Translocation of C in Macrocystis pyrifera (Giant Kelp). Plant
physiology, 61(4), 585-9.
Lobban, C. S. (1978b). The growth and death of the Macrocystis sporophyte (Phaeophyceae,
Laminariales). Phycologia, 17(2), 196-212. The International Phycological Society
Phycologia Business Office, Allen Press, 810 East 10th Street, P.O. Box 1897, Lawrence,
KS 66044-889
Mann, K. (1973). Seaweeds: Their Productivity and Strategy for Growth. SCIENCE, VOL 182,
NO 4116, P 975-981, DECEMBER 7, 1973.
Mann, K. (2000). Ecology of coastal waters: with implications for management (2nd ed.).
Malden, Mass.: Blackwell Science,.
McMillan, S. (2010). Trophic interactions among Chlorostoma brunnea, Macrocystis pyrifera,
and fungi. Society.
Norderhaug, K., Fredriksen, S., & Nygaard, K. (2003). Trophic importance of Laminaria
hyperborea to kelp forest consumers and the importance of bacterial degradation to
food quality. Marine Ecology Progress Series, 255, 135-144.
North, W. J. (1971). The biology of giant kelp beds (Macrocystis) in California,. Lehre,: J.
Cramer,
Parker, B. C. (1963). Translocation in the Giant Kelp Macrocystis. Science, 140(3569), 891.
American Association for the Advancement of Science.
Parker, B. C. (1965). Translocation in the Giant Kelp Macrocystis I. Rates, direction,
quantity of C14-lablled products and fluorescein. Journal of Phycology, 1(2), 41-46.
Wiley Online Library
Poore, A. G. B., & Steinberg, P. D. (1999). Preference-Performance Relationships and Effects
of Host Plant Choice in an Herbivorous Marine Amphipod. Ecological Monographs,
69(4), 443-464. Eco Soc America.
Markham 15
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Temperature and Grazing on Growth and Reproduction of Floating Macrocystis Spp.
(Phaeophyceae) Along a Latitudinal Gradient. Journal of Phycology, 45(3), 547-559.
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(Phaeophyceae). Marine Biology, 36(3), 207-216.
Schmitz, K., & Srivastava, L. (1979). Long Distance Transport in Macrocystis integrifolia: I.
Translocation of C-labeled Assimilates. Plant Physiology, 63(6), 995-1002.
Seymour, R.J., Tegner, MJ, Dayton, P. K., & Parnell, P. E. (1989). Storm wave induced
mortality of giant kelp, Macrocystis pyrifera, in Southern California. Estuarine, Coastal
and Shelf Science, 28,277-292.
Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. a, et al.
(2003). Kelp forest ecosystems: biodiversity, stability, resilience and future.
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Watanabe, J. (1984). Food preference, food quality and diets of three herbivorous
gastropods (Trochidae: Tegula) in a temperate kelp forest habitat. Oecologia, 62(1),
47-52. Springer.
White, W. L., Coveny, a H., Robertson, J., & Clements, K. D. (2010). Utilisation of mannitol by
temperate marine herbivorous fishes. Journal of Experimental Marine Biology and
Ecology, 391(1-2), 50-56. Elsevier B.V.
Arkema, K. K., Reed, D. C., & Schroeter, Stephen C. (2009). Direct and indirect effects of giant
kelp determine benthic community structure and dynamics. Ecology, 90(11),3126-37.
Bengtsson, M., Sjøtun, K., Storesund, J., & Øvreås, J. (201 1). Utilization of kelp-derived carbon
sources by kelp surface-associated bacteria. Aquatic Microbial Ecology, 62(2), 191-199
doi: 10.3354/ame01477
Burger, R. (1995). Competition, Predation, and the Evolution and Extinction of Stellar’s Sea
Cow, Hydrdamalis Gigas. Marine Mammal Science, II(3), 391-394.
Buschmann, A., & Hernandez-Gonzalez, M. C. (2005). Seaweed cultivation, product
development and integrated aquaculture studies in Chile. WORLD AQUACULTURE¬,
36(3), 51-53.
Dayton, P. K. (1985). Ecology of Kelp Communities. Annual Review of Ecology and
Systematics, 16,215-245.
Markham 16
Dixon, J., Schroeter, S.C., & Kastendiek, J. (1981). Effects of the encrusting bryozoan,
Membranipora membranacea, on the loss of blades and fronds by the giant kelp,
Macrocystis. Journal of Phycology, 17(4), 341-345. Wiley Online Library.
Doty, M. S. (1987). Case studies of seven commercial seaweed resources (281-282 ed., p.311).
Food & Agriculture Org.
Duggins, D., Eckman, J., Siddon, C., & Klinger, T. (2001). Interactive roles of mesograzers and
current flow in survival of kelps. Marine Ecology Progress Series, 223, 143-155. doi:
10.3354/meps223143.
Duggins, D., Simenstad, C., & Estes, J. (1989). Magnification of Secondary Production by Kelp
Detritus in Coastal Marine Ecosystems. Science, 245(4914), 170. American Association for
the Advancement of Science.
Foster, M. S., & Schiel, D. R. (1985). Ecology of giant kelp forests in California: a community
profile.
Graham, M. H. (2004). Effects of Local Deforestation on the Diversity and Structure of Southern
California Giant Kelp Forest Food Webs. Ecosystems, 7(4), 341-357. doi: 10.1007/810021-
003-0245-6.
Gutierrez, A., Correa, T., Munnoz, V., Santibannez, A., Marcos, R., Cáceres, C., et al. (2006)
Farming of the Giant Kelp Macrocystis Pyrifera in Southern Chile for Development of
Novel Food Products. Journal of Applied Phycology, 18(3-5), 259-267. doi:
10.1007/8 1081 1-006-9025-y
Hemmi, A., and V. Jormalainen. (2002). Nutrient Enhancement Increases Performance of a
Marine Herbivore via Quality of Its Food Alga. Ecology, 83(4), 1052.
Hepburn, C., & Hurd, C. (2005). Conditional mutualism between the giant kelp Macrocystis
pyrifera and colonial epifauna. Marine Ecology Progress Series, 302,37-48. doi:
10.3354/meps302037.
Lee, R. E. (1989). Phycology. Phycology (p. 146). New York: Cambridge University Press.
Lobban, C. S. (1978a). Translocation of C in Macrocystis pyrifera (Giant Kelp). Plant
physiology, 61(4), 585-9.
Lobban, C. S. (1978b). The growth and death of the Macrocystis sporophyte (Phaeophyceae,
Laminariales). Phycologia, 17(2), 196-212. The International Phycological Society
Phycologia Business Öffice, Allen Press, 810 East 10th Street, P.O. Box 1897, Lawrence,
KS 66044-8897. doi: 10.2216/10031-8884-17-2-196.1.
Mann, K. (1973). Seaweeds: Their Productivity and Strategy for Growth. SCIENCE, VOL 182,
NO 4116, P 975-981, DECEMBER 7, 1973.5 FIG, 2 TAB, 57 REF., 182(4116).
Markham 17
Mann, K. (2000). Ecology of coastal waters : with implications for management (2nd ed.).
Malden, Mass.: Blackwell Science,.
McMillan, S. (2010). Trophic interactions among Chlorostoma brunnea, Macrocystis pyrifera,
and fungi. Society.
Norderhaug, K., Fredriksen, S., & Nygaard, K. (2003). Trophic importance of Laminaria
hyperborea to kelp forest consumers and the importance of bacterial degradation to food
quality. Marine Ecology Progress Series, 255, 135-144. doi: 10.3354/meps255135.
North, W. J. (1971). The biology of giant kelp beds (Macrocystis) in California,. Lehre,: J
Cramer,
Parker, B. C. (1963). Translocation in the Giant Kelp Macrocystis. Science, 140(3569), 891.
American Association for the Advancement of Science.
Parker, B. C. (1965). Translocation in the Giant Kelp Macrocystis I . Rates, direction, quantity of
C14-lablled products and fluorescein. Journal of Phycology, 1(2), 41—46. Wiley Online
Library.
Poore, A. G. B., and P.D. Steinberg. (1999). Preference-Performance Relationships and Effects
of Host Plant Choice in an Herbivorous Marine Amphipod. Ecological Monographs, 69(4),
443-464. Eco Soc America.
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Fig. 1: Experimental setup in which fronds were cut 30cm from the first division on the apical
blade. Growth and erosion were measured on the nearest blade 30cm from the first divison.
Figure modified from Hepburn et al. (2007).
Apical meristem

pe


ade
30cm
lenenenag
-

8
Tag 2
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Fig. 2: Average growth rates (cm/day) of kelp blades in the first and second week after removal
of the apical meristem. Error bars are standard errors bars of the mean. n=20
3.5
3
2.5
2
Control
515
Apex
- Removed
0.5
Week Two
Week One
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Fig. 3: Average change in distance (cm) between the punched hole and the kelp blade tip in the
first week after removal of apical meristem. Error bars are standard errors bars of the mean.
n=16
10
Apex Removed
Control
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Fig. 4: Average percent dry weight mannitol for blades from fronds with and without apical
meristem two weeks after cutting. Error bars are standard errors bars of the mean. n=10
-6
23
8
Control
Apex Removed
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Fig. 5: Percent carbon of dry weight for blades with and without apical meristems two weeks
after cutting. Error bars are standard errors bars of the mean. n=16
30.5
30
29.5
29
§ 285
28
27.5
27
26.5
26
AM Removed
Control
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Fig. 6: Carbon:Nitrogen ratio of tissue from blades with and without apical meristems two
weeks after cutting. Error bars are standard errors bars of the mean. n=16
10.5
10
—
9.5
8.5
AM Removed
Control
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Fig. 7: Stellar's sea cow (Hydrodamalis gigas)grazing on Macrocystis canopies. (Encyclopedia
Britannica)