Effects of pH on the Growth, Herbivory, and Chemical Defenses of Macrocystis pyrifera Apical ...

37 Pages·2014·0.88 MB·English

Effects of pH on the Growth, Herbivory, and Chemical Defenses of Macrocystis
pyrifera Apical Meristems
Erin Dillon
May 2014
EFFECTS OF PH ON THE GROWTH, HERBIVORY, AND CHEMICAL
DEFENSES OF MACROCYSTIS PYRIFERA APICAL MERISTEMS

An Honors Thesis Submitted to
the Department of Biology
in partial fulfillment of the Honors Program
STANFORD UNIVERSITY

by
ERIN DILLON
MAY 2014
EFFECTS OF PH ON THE GROWTH, HEKBIVORY, AND CHEAIIICAL DEtrENSES OF
MAC ROCYSTI S PYRIFERA AP ICAL MERI STF:UTS
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EN]\r DILLON
Approved.for submittal to the Department af Biologlt
for consideratian of granting graduation with honors:
Research Sponsor €. t, 11" \ llulz"q
Fiorenza Micheli i L\W^^A^.y',\^}AA/{ Date
(signature)
Second Reuder
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George Somero
(signature)
Acknowledgements

Thank you to Steve Litvin and Fiorenza Micheli for helping me develop and revise the
experimental design and for reviewing the manuscript, Jody Beers and the Somero Lab
for making it possible to run the Folin-Ciocalteu assays, the Palumbi Lab for allowing me
to use their aquaria and deacidification system, and George Somero for his invaluable
comments and revision of the manuscript. Also, thank you to Sarah Lummis for helping
me collect the apical meristems and being a reliable dive buddy. This research was
funded by a UAR Major Grant.
Table of Contents

Abstract 1
1. Introduction 2
2. Materials and Methods 6
2.1 Experiment 1 - Apical meristem growth rates 8
2.2 Experiment 2 - Rate and impact of herbivory 8
2.3 Experiment 3 - Effect of pH on kelp defense 10
2.4 Statistical Analysis 10
3. Results 10
3.1 Kelp Growth 10
3.2 Herbivory by Strongylocentrotus purpuratus 12
3.3 Herbivory by Chlorostoma brunnea 15
3.4 Phenolics 16
4. Discussion 18
5. References 24
6. Appendix A: Relevant ANOVA Statistics 30
List of Tables

Table 1. Average±SD of pH measurements between time points (T) in each pH treatment.
Table 2. Average pH values of each treatment during each S. purpuratus herbivory trial.
Table 3. Average pH values of each treatment during each C. brunnea herbivory trial.
List of Figures

Figure 1. Map of the collection site in the Hopkins Marine Life Refuge.
Figure 2. Schematic representation of the M. pyrifera young blade types.
Figure 3. Effects of pH on M. pyrifera apical meristem growth per week.
Figure 4. Average M. pyrifera apical meristem blade width relative to short-scale
temporal changes in the pH treatments.
Figure 5. Rate of consumption by S. purpuratus in each treatment over time.
Figure 6. Rate of consumption by C. brunnea in each treatment over time.
Figure 7. Average polyphenol concentrations of blades as a function of pH at each time
point.
Figure 8. Average polyphenol concentration in each pH treatment as a function of blade
age.
Abstract
Ocean acidification has the potential to reshape the structure of kelp forest communities
dominated by giant kelp (Macrocystis pyrifera). Whereas decreasing pH has been shown
to enhance the growth of kelp, acidification may also influence the grazing activity of
common herbivorous species that feed on kelp. The shift in balance between changes in
the rate of growth and herbivory can determine whether a phase shift from a kelp-
dominated to a turf algae-dominated ecosystem will occur. This study investigated the
effect of pH on the growth rate of M. pyrifera apical meristems as well as how alterations
in their chemical defenses due to acidification influence the rate of herbivory. Although
prior studies have documented increased algal growth under low pH conditions, few have
examined whether changes in blade palatability govern the amount of grazing. Moreover,
little is known about how the apical meristems, which are responsible for the vertical
growth essential to the survival of kelp in their light-limited environment, are affected by
changes in seawater pH. We exposed apical meristems to two different pH treatments –
naturally acidified upwelled seawater from Monterey Bay, for which pH oscillated
between pH 7.6 and 7.9, and a control treatment around pH 8.01 – in outdoor flow-
through aquaria and measured the rate of blade growth and the polyphenol concentration
to quantify chemical defense at one week intervals. Reciprocal transplant herbivory
experiments were run with juvenile purple sea urchins (Strongylocentrotus purpuratus)
and brown turban snails (Chlorostoma brunnea) to determine how the rate of herbivory
of these two ecologically important invertebrates was influenced by pH. Kelp growth was
found to be elevated under low pH conditions, while herbivory and polyphenol levels
were not significantly altered. The varied response of kelp to pH highlights the dynamic
balance between algal growth and herbivory and has long-term implications for the
health, recruitment, and ecological underpinnings of kelp forest ecosystems as the ocean
continues to acidify.
Key words: apical meristem, growth, herbivory, Macrocystis pyrifera, ocean
acidification, phase shift, polyphenols

1
Introduction
Ocean acidification is the decrease in seawater pH associated with enhanced absorption
of anthropogenic CO from the atmosphere (Sabine et al. 2004). Since the start of the
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industrial revolution, the average surface oceanic pH has dropped by 0.1 units and is
predicted to drop by another 0.3 units to reach 7.8 by the end of the century as CO
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emissions continue to rise (Hofmann, Straub, & Bischof, 2012; The Royal Society,
2005). Ocean acidification has enduring ramifications for the health of kelp forests and
their continued provision of ecosystem services, as it can disrupt the distribution and
recruitment of the canopy-forming giant kelp Macrocystis pyrifera (Henríquez et al.
2011, Olischläger et al. 2012, Harley et al. 2012). Macrocystis is the main source of
primary productivity in many kelp forests, sustaining their rich trophic structure both
through the production of phytodetritus and the provision of substrates for direct grazing
(Graham 2004). Moreover, as an ecosystem engineer, kelp provides the physical, three-
dimensional structure of the community, which can act as a nursery for economically and
culturally valuable species of fish (Graham 2004). However, the survival, growth, and
reproduction of kelp have been shown to vary with environmental factors, suggesting that
global warming and ocean acidification have the potential to reorganize local
communities and alter species interactions by disrupting the structure of kelp forests
(Harley et al. 2012).
Specifically, ocean acidification could potentially trigger a phase shift from a kelp-
dominated to a turf algae-dominated ecosystem, upsetting community dynamics and
altering herbivore density and abundance (Russell et al. 2009, 2011, Gorman and Connell
2009, Connell and Russell 2010, Hepburn et al. 2011, Harley et al. 2012). Ocean
acidification favors the growth of turf algae, which compete with kelp for available
seafloor substrate and inhibit kelp recruitment. It thereby amplifies the susceptibility of
kelp canopies to anthropogenic and natural disturbances and diminishes their resilience in
the wake of such events, consequently increasing the likelihood of a phase shift if
sections of the kelp canopy are removed by a stressor (Harley et al. 2012).
Apical meristems – the regions toward the end of the stipe where new plant tissue is
produced through cell division – help establish the competitive dominance of kelp by
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acting as the centers of vertical growth (Cerda et al. 2009, Harley et al. 2012). This
upward growth is critical for both light capture and canopy development. Canopy growth,
in turn, limits through shading the horizontal expansion of turf algae in the understory,
which can hinder kelp sporophyte recruitment by reducing the amount of available
substrate for settlement (Connell and Russell 2010, Russell et al. 2011, Falkenberg et al.
2012). Therefore, the continued growth and protection of apical meristems can help guard
against phase shifts by maintaining the canopy cover necessary to keep turf algae in
check.
However, acidification is predicted to have differential effects on algae depending on
their CO acquisition mechanism. Although the CO enrichment responsible for ocean
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acidification is expected to enhance the growth of fleshy macroalgae, turf algae will also
benefit. For example, whereas species that utilize carbon-concentrating mechanisms
(CCMs) may gain little if any benefit from higher dissolved CO levels, non-CCM
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species such as turf algae that rely solely on the diffusion of CO as a carbon source for
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photosynthesis may exhibit increased activity and gain an advantage in light-limited
environments such as kelp forests (Russell et al. 2009, Connell and Russell 2010,
Hepburn et al. 2011, Cornwall et al. 2012, Koch et al. 2013).
Herbivores play a key structuring role in algal communities by exerting top-down control
on kelp populations, regulating population size and diversity (Sala and Graham 2002,
Henríquez et al. 2011, Sala and Dayton 2011). The rate of herbivory is influenced by the
extent of morphological or chemical defenses produced by an alga as well as by its
nutritional value. Algal palatability, combined with population growth rates and
abundances of both the algae and herbivores, determine the strength of the overall effect
of herbivory on the algal population (Harley et al., 2012; Sala & Dayton, 2011; Sala &
Graham, 2002). Climate change is predicted to alter these algae-herbivore interactions
(Harley et al. 2012). For example, while reduced oceanic pH has been shown to stimulate
growth in fleshy macroalgae, it has also been demonstrated to cause a loss of polyphenols
– which act as natural herbivory deterrents – in some species of algae, thus increasing
their palatability (Kroeker et al. 2010, Arnold et al. 2012, Cornwall et al. 2012).
Therefore, while Macrocystis is expected to grow faster under future high-CO
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