CALIFORNIA STATE UNIVERSITY, NORTHRIDGE
THE EFFECTS OF OCEAN ACIDIFICATION ON BIOEROSION IN THE
BACK REEF OF MOOREA, FRENCH POLYNESIA
A thesis submitted in partial fulfillment
of the requirements for the degree of
Master of Science in Biology
By
Lauren Michele Valentino
August 2014 The thesis of Lauren M. Valentino is approved:
______
Peter J. Edmunds, Ph.D. Date
______
Mark A. Steele, Ph.D. Date
______
Robert C. Carpenter, Ph.D., Chair Date
California State University, Northridge
ii ACKNOWLEDGEMENTS
I would like to thank my advisor Dr. Robert Carpenter for believing in me and providing opportunities that will continue to foster my abilities as a student, writer, and scientist. Dr. Carpenter’s guidance and unwavering patience helped me become a more confident and independent researcher. I will never forget all of the delicious dinners, boat lunches, and round-island adventures surveying the reefs of Moorea. I truly can’t thank him enough for making me an additional member of the Carpenter lab family, something that I will carry proudly as I continue my career in marine science.
I am grateful to Dr. Peter Edmunds who met with me countless times to help me work through many different questions I had regarding my thesis. His attention to detail and ability to streamline the most complicated processes always left me with a deeper understanding and enthusiasm for my research. Any self-doubt was immediately met with the mantra, “You’re good enough. You’re smart enough. And doggone it, people like you.” This and many other Pete-isms will help remind me of the importance of my confidence as a scientist (and a good coffee buzz) throughout my research and life.
I would also like to thank Dr. Mark Steele for being an incredible teacher and committee member. He always made me feel comfortable being myself, while still taking my research and me seriously. I used to think that stats were abstract and arduous, but Dr. Steele has a way of explaining it in a simple, straightforward way that makes it seem so practical and useful. His paper discussions and pragmatic approach to marine research helped me look at science with a more critical eye. I feel very lucky to have learned from the diverse perspectives of Bob, Pete, and Mark who have all made me the scientist I am today, and for that I am forever thankful.
Also, thanks to my Mom, Lindsay, and Johnnie for being patient and understanding throughout my grad school experience. Going home always helped put things in perspective and reminded me that where I am from is as important as where I am going. Thanks to Heather Hillard, the ‘eather in Leather, who was my lab partner in crime beginning to end. I have her to thank for getting me through what I once thought was not possible. Merci bien to the rest of the Carpenter lab, especially Amy, Carolina, Vinny, Anya, Coulson, Steeve, and Stella who were always positive, helpful, and improved my quality of life both on campus and in the field. For all their love and support, thanks to my adoptive LA family, Sylvia (Stout), Cecilia (Harley), and Lauren M. for giving me a home away from home. I am so grateful to my friends Camdilla, Sara, Lareen, and Mark. The countless dinners, adventures, and work parties I shared with them helped me though the most challenging times, kept me sane, and most importantly made me laugh.
This research was made possible with funding from the US National Science Foundation to the Moorea Coral Reef Long Term Ecological Research MCR-LTER (1026851 and 1236905), R. Carpenter and P. Edmunds (1041270), and from generous donations made by the Gordon and Betty Moore Foundation. Additionally, this research was supported by California State University Northridge Graduate Studies, Associated Students, California State University’s Thesis Support Grant, and California State University’s Gradate Equity Fellowship.
iii TABLE OF CONTENTS
Signature Page ii
Acknowledgements iii
List of Tables v
List of Figures vi
Abstract vii
Chapter 1 General Introduction 1
Chapter 2 Distribution and Abundance of Internal and External Bioeroders Across the Back Reef of Moorea, French Polynesia
Introduction 9 Methods 15 Results 19 Discussion 21 Tables 26 Figures 30
Chapter 3 Effects of Ocean Acidification on Calcification, Bioerosion, and Respiration Rates of Lithophaga laevigata within Massive Porites in Moorea, French Polynesia
Introduction 35 Methods 40 Results 47 Discussion 50 Tables 56 Figures 59 Chapter 4 Summary 64
Literature Cited 69
iv LIST OF TABLES
PAGE
2.1 - Results from a two-factor analysis of variance (ANOVA) testing for 26 differences in external bioeroder densities upstream and downstream.
2.2 - Results from a two-factor analysis of variance (ANOVA) testing for 27 differences in internal bioerosion on bommie and rubble substrate at upstream and downstream locations.
2.3 - Results from the mixed model analysis of variance (ANOVA) testing for 28 differences in Lithophaga abundance at upstream, top, downstream locations on a Porites colony.
2.4 - Results from Tukey’s honestly significant difference tests of the mixed 29 model analysis of variance (ANOVA) testing for differences in Lithophaga abundance at upstream, top, downstream locations on a Porites colony.
3.1 - Results from the simple linear regression of the major axis of the borehole 56 and the length of the valve (n=38).
3.2 - Summary of carbonate chemistry measurements in 6 randomly assigned 57 tanks throughout a 28-d incubation period in elevated and ambient pCO2 treatments. Mean ± SE. N=28 sampling days for all parameters.
3.3 - Results from the mixed model analysis of variance (ANOVA) testing 58 effects of Core Type (Porites with and without Lithophaga) and CO2 (ambient and elevated treatments) on area-normalized net calcification rates.
v LIST OF FIGURES PAGE
2.1 - Study site on the north shore of Moorea, French Polynesia. 30 Upstream and downstream locations shown for transects conducted on external bioeroders, internal erosion, and Lithophaga abundance. Arrows depict the unidirectional flow across the back reef.
2.2 - External bioeroder abundance on bommies and rubble in upstream 31 and downstream locations. Location P=0.214, Substrate type P=<0.001, L x S P=0.636.
2.3 - Percent bioerosion in bommie and rubble pieces collected at 32 upstream and downstream locations. Location P=0.337, Substrate type P=<0.001, L x S P=0.010.
2.4 - Lithophaga abundance in upstream and downstream locations. 33 Location P=0.912.
2.5 - Spatial Abundance of Lithophaga on Porites on upstream, top, and 34 downstream sides of a Porites colony. Zone P=0.002, Upstream P=0.001, Top P=0.008, Downstream P=0.002, (n=10).
3.1 - Correlation between the major axis of the borehole opening of 59 Lithophaga laevigata and valve length (n=38).
3.2 - Area-normalized net calcification rates of Porites with and without 60 Lithophaga in ambient and elevated treatments (n=28).
3.3 - Weight-normalized net calcification rates of Lithophaga in burrow 61 mimics in ambient and elevated treatments (n=20).
3.4 - Estimated bioerosion rates of Lithophaga in Porites in elevated and 62 ambient pCO treatments (n=28). 2
3.5 - Respiration rates of Lithophaga in burrow mimics after 28 days in 63 elevated and ambient pCO treatments (n=12). 2
vi ABSTRACT
Effects of ocean acidification on bioerosion in the back reef of Moorea, French
Polynesia.
By
Lauren M. Valentino
Master of Science in Biology
Coral reefs are among the most diverse ecosystems on the planet and have been compared to rainforests because of their complexity and high species diversity. Tropical reefs have relatively nutrient-poor waters, but they are one of the most productive ecosystems providing benefits and ecosystem services to society in the form of coastal protection, food, and economic resources such as tourism. Rising carbon dioxide emissions by humans will have serious environmental implications for the ocean environment. Coral reef ecosystems are particularly vulnerable to this unprecedented increase of CO2 due to their carbon chemistry and thermal sensitivity. Anthropogenic
CO2 is predicted to decrease ocean surface pH by 0.14–0.35 units by 2100 causing ocean acidification (OA). Most studies have focused on how OA will affect rates of calcification of coral reef organisms. However, bioerosion also could be sensitive to rapid changes in ocean carbonate chemistry. I tested the effects of decreased pH on the distribution of bioeroders in the field and on the boring capacity of the mollusk
Lithophaga laevigata living within corals, massive Porites spp. (a complex of three species: P. lobata, P. australiensis, and P. lutea) in the lab. Field studies showed higher
vii external bioeroder abundance on coral bommies, and higher internal bioerosion in coral rubble, however, there was no differences in bioerosion between variable pH environments found at upstream and downstream transects. L. laevigata, a boring bivalve, is abundant within massive Porites sp. on the back reef of Moorea, French
Polynesia. L. laevigata abundance in massive Porites across the back reef ranged from 3 to 95 ind/m2. Size analysis of L. laevigata showed a significant correlation of the borehole opening and the size of the bivalve, which allowed for a non-destructive method for collection of uniformly sized bivalves as a way to standardize bioerosion rates for analyses. I conducted a month-long mesocosm experiment where massive Porites cores with and without L. laevigata, were incubated in ambient (400 µatm) and elevated (850
µatm) pCO2 treatments held at a constant temperature. Net calcification rates of Porites cores significantly decreased in the elevated treatment. Presence of L. laevigata decreased net calcification rates of Porites regardless of CO2 treatment. I also compared the bioerosion rate of L. laevigata in coral cores (based on changes in buoyant weight) and tested the hypothesis that OA increases the ability of bivalves to bioerode in elevated pCO2 conditions. For this experiment, there was no significant effect of OA on bioerosion rates of L. laevigata. However, respiration rates of L. laevigata increased under elevated pCO2 conditions. These results provide a better understanding of this abundant and active bioeroder under simulated future environmental conditions and give insight to the poorly understood effects of OA on bioerosion.
viii Chapter 1
General Introduction
Tropical coral reefs are among the most diverse ecosystems on the planet and have been compared to rainforests because of their complexity and high species diversity
(Reaka-Kudla 1997). While coral reefs occur in relatively nutrient-poor waters, they are among the most productive ecosystems, providing invaluable ecosystem services to society in the form of shoreline protection, food, material, medicine, cultural services, and appealing environments for tourism (Grigg et al. 1984, Moberg and Folke 1999).
Approximately 275 million people reside adjacent to coral reefs and directly benefit from the ecosystem services they provide (Burke et al. 2011). French Polynesia is one example of a multi-island nation that depends on their coral reefs. A case study of Moorea, French
Polynesia by Charles (2005) revealed that residents consider education, cultural services, and lagoon fisheries among the most important functions and services of the coral reefs, while 98% of tourists surveyed expressed aesthetic value as the most important. The significance of these services, principally tourism, is reflected in its total economic value estimated at $85.5 million/year (Charles 2005).
The ongoing rise in carbon dioxide emissions by humans from fossil fuels and net land use will have serious environmental implications for the oceans. The ocean is a carbon sink for approximately 33% of anthropogenic CO2 emissions (Sabine et al., 2004).
While oceanic absorption of CO2 is a naturally occurring process, a 40% increase in carbon dioxide (CO2) concentrations since pre-industrial times is reducing the oceans capacity to buffer and adapt to these rapid changes (IPCC 2014). Scleractinian corals and other calcifiers that build coral reef framework, are sensitive to this unprecedented
1 change in seawater chemistry due to their calcium carbonate skeletons, changing both the biological and geological components of the reef (Kleypas and Yates 2009).
Ocean acidification (OA) is the uptake of atmospheric CO2 causing a reduction in ocean pH and carbonate saturation (Ω) over an extended period of time with no change in total alkalinity (AT) (Gattuso and Hansson 2011). Saturation state (Ω) is the degree to which seawater is saturated with both calcium and carbonate minerals, and as OA continues, surface ocean Ω values will decrease. Total alkalinity describes the capacity of water to neutralize acids. The net result of adding CO2 to seawater is an increase in
+ – hydrogen ions [H ] and bicarbonate ions [HCO3 ], but a reduction in available carbonate
2– ions [CO3 ]. The decrease in carbonate ions reduces the overall buffering capacity as
CO2 increases, resulting in proportionally more hydrogen ions, therefore increasing acidity with no change in total alkalinity. Relative to preindustrial times, anthropogenic
st CO2 is predicted to decrease ocean surface pH by 0.14–0.43 units by the end of the 21 century, causing ocean acidification (OA) (IPCC 2014). This change in carbon chemistry of seawater will have an impact on marine calcifiers and noncalcifiers, and studies have shown a negative trend in organism performance under OA (Kroeker et al. 2010). While fundamental seawater chemistry of OA is well understood and agreed upon by scientists
(IPCC 2014), there are still many questions to investigate to provide a more complete understanding of the effects of OA on ecological interactions between organisms in the marine environment. More research providing evidence and agreement on the impacts of
OA is needed to better predict the vulnerability of future coral reefs.
In the open ocean, the effects of OA are linked closely to atmospheric CO2 concentrations, however, as water flows over a coral reef, biological processes of the
2 coral reef community can alter carbon chemistry of the seawater as well (Smith & Pesret,
1974; Gattuso et al., 1993, Anthony et al., 2011, Kleypas et al. 2011). Lagoonal reefs are typically low-energy environments with high seawater-residence time. Reef metabolism and calcification are influenced by flow-mediated flux of carbon and nutrients (Wyatt et at 2010, Zhang et al. 2012). Benthic primary producers and calcifiers alter the seawater chemistry as water flows over reef communities (Anthony et al., 2011; Kleypas et al.
2011). As ocean acidification continues to threaten coral reefs, it is of particular interest to study how community structure modifies seawater chemistry across shallow reef flats, which could in turn influence the effects OA. Some shallow reef flats already experience natural diel fluctuations in seawater pH that exceed values predicted for the future
(Hofmann et al. 2011). A study in Moorea, French Polynesia, illustrated that calcification of corals and calcifying algae cause a drawdown of total dissolved inorganic carbon due to photosynthesis and calcification that exceeds the drawdown of total alkalinity, resulting in a net increase in aragonite saturation state (Kleypas et al. 2011). The carbon flux of corals and macroalgae can increase or decrease aragonite (a crystalline form of calcium carbonate found in corals) saturation state. Seawater with aragonite saturation state above one are considered to be above the saturation horizon, but values below one result in dissolution of calcifying organisms. In an algal-dominated reef, increases in the ratio of photosynthesis to calcification could potentially compensate for ocean acidification of reef communities located downstream, while coral dominance could elevate pCO2 and decrease aragonite saturation state (Anthony et al. 2011; Kleypas et al.
2011). In Moorea, unidirectional water flow over the reef crest changes seawater chemistry from upstream to downstream habitats across the back reef (Hench et al. 2008).
3 Measurements of seawater chemistry across the back reef of Moorea revealed an increase in pCO2 from upstream to downstream with higher values in the downstream location at night (Johnson et al. 2014). While the effects of flow and reef metabolism on local carbonate chemistry are complex, it is important to design experiments that take into account local and spatial variability exhibited by shallow reefs in order to accurately predict the effects of OA on coral reefs.
At the whole-reef scale, there is a delicate balance between constructive processes
(calcification) and destructive processes (dissolution and bioerosion), where coral reef persistence depends on the rate of reef accretion being faster than or equal to erosional processes (Glynn 1997). Climate change and anthropogenic activities threaten to tip the balance from coral reef construction to reef destruction causing net reef loss. A decrease in available carbonate and saturation state of aragonite (Ωarag) in the ocean can have negative effects on calcifying organisms, which are an integral component of coral reef ecosystems (Hoegh-Guldberg et al., 2007, Kleypas and Yates 2009). As a result, most studies have focused on how the rapid rate of decline in ocean pH predicted for 2100 by the IPCC will affect marine calcifiers. However, OA also will affect bioerosion, which is carbonate erosion by living organisms. For example, some studies predict that bioerosion rates of chemical eroders such as sponges and microscopic algae will increase under future climate change conditions (Tribollet et al. 2006, Wisshak et al. 2012, Duckworth and Peterson 2013).
Bioeroders contribute to the high species diversity found on coral reefs (Glynn,
1997). The most prominent bioeroders include parrotfish, sponges, bivalves, sea urchins, and microscopic algae (Glynn, 1997). The natural breakdown of CaCO3 into rubble, sand,
4 and silt happens via chemical dissolution and mechanical abrasion. Parrotfish and sea urchins bioerode externally and use mechanical means to break down the reef during grazing by abrading carbonate substrata to consume algae growing on the surface.
Bivalves, sponges, and microscopic algae are internal eroders, and primarily use chemical means to dissolve and penetrate carbonate substrata, which is also referred to as biocorrosion (Kleeman 1996). While there are a limited number of studies on the effects of OA on bioerosion on coral reefs, it has been shown that reducing the Ωarag will facilitate bioerosion of macroborers (macroscopic organisms that bore into carbonate) and microscopic algae due to increased calcium carbonate dissolution and increase skeletal porosity of coral over time (Manzello et al., 2008, Tribollet et al., 2009, Chen et al., 2012). Endolithic (living embedded in the surface of rocks) bioeroders are much less studied than more conspicuous benthic organisms on coral reefs due to their existence within carbonate substratum. These endoliths are thought to have evolved during the
Mesosoic as a response to increasing predation and competition (Vermeij 1987). The effects of both internal and external eroders increase greatly on dead carbonate surfaces, while bioeroders that erode directly thru living coral tissues are less common.
Lithophaga, an endolithic bivalve, was found associated with living coral from a fossil record that dates back to the middle Miocene (Kuhnelt 1931). Kleeman (1980) suggested that Lithophaga larvae that settle on living coral tissue have host-specificity, unlike Lithophaga that settle on dead carbonate where many different species may overlap. The macroborer Lithophaga laevigata (Quoy & Gaimard, 1835) is abundant within massive Porites (a complex of three species: P. lobata, P. australiensis, and P. lutea) in Moorea (Peyrot-Clausade et al. 1992). Veligers (bivalve larvae) settle on the
5 tissue of their host coral and eventually establish a borehole within the coral skeleton
(Scott 1988b). The dumbbell shaped borehole opening of Lithophaga is easily recognizable on the surface of massive Porites tissue. Fang and Shen (1988) suggested that Lithophaga is a mechanical borer, however numerous studies have demonstrated that this is not possible due to the delicate structure of their valves, therefore it is accepted generally that the dominant method of dissolution for this species is biocorrosion
(Kleemann 1984, 1986, 1990a, 1990b, 1996). Dissolution by Lithophaga affects the calcium carbonate substratum, followed by removal of the loose particles using ciliary currents and expulsion of pseudofaeces (Kleemann, 1973, 1996).
While the coral host survives the invasion of Lithophaga, an increase in bivalve abundance decreases the compressive and bending strength of the coral skeleton (Scott and Risk 1988). Some species of Lithophaga line their boreholes, making them denser and stronger than the surrounding coral skeleton, and it has been argued that this could increase the coral skeleton strength, but this is not the case for Lithophaga laevigata, which does not line their borehole. Studies have shown that as anthropogenic influence increases on coral reefs so will the number of coral associates such as lithophagid bivalves, hermit crabs and vermetid snails. Elevated nutrient concentrations provide favorable habitat for these filter-feeding heterotrophs, therefore Lithophaga abundance could be an indicator of reef health (Scaps and Denis 2008, Scaps et al. 2008). In live coral, Lithophaga can be a large contributor to bioerosion on coral reefs. In the Eastern
2 Pacific, bioerosion rate of Lithophaga can reach up to 9,000 g CaCO3/m /yr with bivalve densities as high as 1,879 ind/m2 (Glynn, 1997).
Massive Porites is the favored host of Lithophaga laevigata in Moorea, and it is
6 likely that OA will have an effect on both of these calcifying organisms. Massive Porites is an important reef builder and contributes to a large portion of living coral cover across the back reef of Moorea (Lenihan et al. 2011). A study looking at the combined effects of temperature and OA on massive Porites demonstrated a 20% decrease of calcification in elevated pCO2, and no effect of temperature (Anthony et al., 2008). However, Comeau et al. (2013) found no effect of OA on net calcification of massive Porites exposed to high pCO2 under high light conditions. Due to a thick tissue layer and minimal response to increased temperature and pCO2 relative to other corals; massive Porites is considered to be a ‘winner’ on future coral reefs (Edmunds 2011, Edmunds et al., 2012, Comeau et al.,
2013, Fabricius et al. 2011).
Organisms have the ability to raise and lower their metabolism between certain limits. A review by Pörtner et al. (2004) demonstrated that hypercapnia elicits metabolic depression in several species of marine animals. However, it has been hypothesized that
OA could also increase metabolic rates in bioeroding organisms (Wisshak et al., 2012), which could in turn affect their ability to bioerode. Within carbonate substrata, respiration of bioeroders such as endolithic phototrophs and cyanobacteria increase the concentration of CO2, which decreases the pH and facilitates carbonate dissolution (Ferran, 2006,
Tribollet et al., 2006). Lithophaga laevigata bioerode by producing acids to dissolve the skeleton of massive Porites, but respiration rates of these infaunal organisms could accentuate carbonate dissolution. Increased respiration rates in hypercapnic conditions have been observed for Mytilus edulis, in elevated pCO2 levels (243 Pa pCO2) (Thomsen and Melzner 2010). The arctic pteropod Limacina helicina also increased respiration rate
-1 -1 by 0.25 µmol O2 (g wet weight) h for each 0.1 pH unit decrease at elevated
7 temperatures (4°C), but was unaffected by pCO2 at ambient temperature (0°C) (Comeau et al. 2010). In a recent review on the impacts of OA on marine shelled mollusks, several species of oysters and clams were found to have increased respiration rates with OA, although the majority of experiments reported no effect of OA on respiration (Gazeau et al., 2013). Lithophaga is unique to other marine shelled mollusks due to its infaunal lifestyle, so increased respiration rates under OA could alter the internal environment of their burrow.
The focus of this thesis was first to quantify the abundance of the bioeroding community across the back reef of Moorea, French Polynesia, where pH exhibits natural diel oscillations due to reef metabolism (Anthony et al., 2011; Kleypas et al. 2011).
Secondly, to investigate how the balance between calcification and dissolution due to bioerosion could change under OA conditions using the unique symbiosis between
Lithophaga laevigata on living massive Porites as a model system. While the majority of studies of OA on coral reef have focused on reef construction (calcification), bioeroders play a key role in carbonate cycling, therefore the present study examines the effects of decreasing pH on both of these processes to better understand how OA may affect the reef carbonate balance.
8 Chapter 2
Distribution and Abundance of Internal and External Bioeroders Across the Back
Reef of Moorea, French Polynesia
Introduction
Physical and biological features of coral reefs are formed by the production and destruction of CaCO3 framework. The persistence of coral reef framework depends on the balance between calcification and erosion/dissolution (Glynn 1997). As long as accretion rates remain above erosion/dissolution rates, net reef growth will occur. Shallow reef environments are home to a broad diversity of species that are responsible for maintaining this balance (Reaka-Kudla 1997). Human induced climate change, such as global warming and ocean acidification, threaten to tip the balance in favor of destructive processes. In order to better understand how climate change will affect coral reefs, studies need to consider the influence of various biological, chemical, and physical processes.
Reef metabolism and calcification are influenced by the flow-mediated flux of carbon and nutrients (Wyatt et at 2010, Zhang et al. 2012). Across the back reef from the reef crest to the fringing reef, there are physical and chemical changes that occur daily in this dynamic environment. As ocean acidification continues to threaten coral reefs, it is of particular interest to study how community structure influences variability in shallow reef flats where natural diel fluctuations cause changes in local carbon dioxide partial pressures (pCO2). Some shallow reef flats already experience natural daily minima in seawater pH that are lower than values predicted for the future (Hofmann et al. 2011).
Studies have shown that local variability of carbonate chemistry is affected strongly by
9 spatial patterns in benthic community structure (Anthony et al. 2011; Kleypas et al.
2011). Aragonite (the crystalline form of calcium carbonate found in corals) saturation state is frequently quantified in ocean acidification (OA) studies, and seawater must be supersaturated (Ωarag>1) in order for net precipitation to occur. In shallow tropical reef environments, the carbon flux of corals and algae can drive aragonite saturation state in opposite directions. Shallow-water coral reefs dominated with calcifying organisms elevate pCO2 and decrease Ωarag for organisms living downstream, while an algal- dominated area with high productivity decreases pCO2 and increases Ωarag potentially compensating for the negative effects of OA in areas downstream of the macroalgae
(Anthony et al. 2011; Kleypas et al. 2011). Upstream locations have more stable pCO2 levels and they are consistently exposed to ocean source water from the open ocean onto the reef crest, while downstream sites have a higher residence time and more pCO2 variability from day to night (Anthony et al. 2009). Data collected recently across the back reef of Moorea has shown an increase in pCO2 at night from upstream (~421.0µatm) to downstream locations (~700.4µatm) (Johnson et al. 2014).
Benthic organisms influence seawater chemistry through a variety of processes including primary production, respiration, calcification, and dissolution. Of these processes, dissolution has received the least attention in the OA literature, particularly carbonate dissolution caused by living organisms, which is referred to as bioerosion, a term coined by Neumann (1966). Processes of carbonate erosion by living organisms occur continuously. Natural breakdown of CaCO3 into rubble, sand, and silt occurs via chemical dissolution and mechanical abrasion. External eroders predominantly use mechanical means and organisms such as parrotfish, surgeonfish, limpets, chitons,
10 vermetid gastropods, and echinoids scrape or excavate the surface during grazing and burrowing. Done et al. (1996) recognized parrotfish and echinoids as keystone species of coral reefs due to their grazing activities by controlling algal abundance and bioerosion of carbonate framework. Parrotfish (family Scaridae), for example, play a key role in the production and distribution of coral sands. Their highest bioerosion rates occur on dead substrata infested with endolithic algae, while ingestion of living coral tissue is less common (Bruggemann et al. 1996). While size and abundance play an important role in the extent of carbonate destruction caused by external bioeroders, benthic eroders can bioerode at much higher rates than fish grazers. Rates of bioerosion by parrotfishes are
−2 −1 approximately 2-7 kg CaCO3 m yr , whereas sea urchin bioerosion rates can exceed 22
−2 −1 kg CaCO3 m yr (Glynn, 1988; Bruggemann, 1994; Reaka-Kudla et al., 1996).
Internal eroders, also known as endoliths, predominantly consist of boring sponges, sipunculids, bivalves, and microscopic algae and generally use chemical means to bioerode (Glynn 1997). Organisms that employ chemically-mediated dissolution of
CaCO3 framework do so by producing metabolic acid or by excretion of ligands and enzymes (Kleemann 1996). Boring sponges mostly use chemical means to bioerode and can influence the alkalinity and dissolved silica of reef-water chemistry (Zundelevich et al. 2007). Endolithic phototrophs (cyanobacteria and algae) dissolve calcium carbonate using organic acids or chelating fluids and/or boring organelles (Le Campion-Alsumard et al. 1995, Tribollet et al. 2006).
While rates of bioeroder settlement and limestone dissolution are greater on dead substrata, there are several organisms that can settle and erode thru living coral tissue.
One of the most significant contributors to the bioerosion of living coral is the
11 macroborer Lithophaga, a boring bivalve. Kuhnelt (1931) was the first to discover
Lithophaga in living coral, where coral fossils revealed the association of these endolithic bivalves and their live coral host (Kleemann 1994). Many different lithophagids erode into dead substrata, but there are several species that specifically settle on the living tissue of certain species of coral. As larvae, Lithophaga are thought to use chemoreception to migrate to a specific living coral host, unlike dead coral, where several species may be found beside each other (Kleemann 1980). Once settled in the coral polyp, Lithophaga begin to grow into and erode the coral skeleton (Scott 1988). Due to their fragile valves and structure of their burrow, it is generally accepted that the dominant method of erosion is chemical, also known as biocorrosion (Kleemann 1996,
1984, 1986, 1990a, 1990b). Even though Lithophaga bore into the coral skeleton, a conspicuous figure-eight-shaped borehole on the surface of the coral colony makes them easy to recognize on the reef.
Lithophaga spp. inhabiting living coral generally are well protected from predation and can use coral mucus for nutrition (Shafir and Loya 1983). While the colonization of Lithophaga does not result in coral mortality, an increase in abundance decreases the compressive and bending strength of the coral skeleton (Scott and Risk
1988). Lithophaga residing in coral can significantly contribute to the bioerosion of coral reefs, with densities as high as 1,879 ind/m2 in some parts of the Pacific (Glynn 1997).
On an individual scale they erode less carbonate compared to larger bioeroders such as parrotfish. However, when coral structure is compromised at its base due to Lithophaga burrows, this could cause an entire coral colony to topple or overturn in a single storm event, and their impact on reef degradation increases considerably.
12 Several studies have focused on how Lithophaga abundance could be an indicator of reef status as a “degraded” or “healthy” reef. Coral reefs with higher anthropogenic influence supported significantly higher number of coral associates (Scaps and Denis
2008, Chen et al. 2012). Elevated nutrient concentrations provided favorable habit for coral associates, particularly filter-feeding heterotrophs (Scaps and Denis 2008, Scaps et al. 2008). It also has been shown that coral boring bivalves prefer to settle in massive corals over branching corals, with Lithophaga densities almost ten times higher in massive than branching habitat (Moretzsohn et al. 1992).
In Moorea, massive Porites is the specific host of Lithophaga laevigata.
Lithophaga laevigata occurs only in living Porites (G. Paulay personal communication).
On the north shore of the island, there is predominately unidirectional water flow that moves across the reef into the lagoon (Hench 2008). On a smaller scale, there is considerable spatial variability as water moves across and around an individual coral colony. This spatial variability can affect where planktonic larvae settle when transported through this heterogeneous environment. Studies have shown that as water moves over and around a coral mound the flow accelerates at the top and then slows down and forms a recirculation zone (eddy) downstream, which could promote larval settlement and attachment (Reidenbach et al. 2009; Brown 2012; Hench and Rosman 2013).
Climate change and anthropogenic impacts threaten to tip the balance between coral reef construction (calcification) and destruction (dissolution and bioerosion). While there are limited studies on the effects of decreasing aragonite saturation state on bioerosion, it is projected that bioerosion rates will increase due to increased CaCO3 dissolution and increased skeletal porosity. The negative effects of climate change will
13 increase coral mortality, which will in turn increase invasion of bioeroders. Erosion of scleractinian corals, both living and dead, is an integral part of reef dynamics, therefore investigation of how bioerosion intensity varies across the back reef will be important in predicting potential outcomes in a changing environment.
In January 2012, I quantified the internal and external bioeroding community across the back reef and examined differences between upstream and downstream locations. For external erosion, I focused on benthic eroders (excluding fishes) and quantified the abundance of external bioeroders across partially dead massive Porites bommies and coral rubble fields. To quantify internal erosion at upstream and downstream locations, I collected subsamples of coral rubble and portions of dead massive Porites within the same transects. As discussed above, differences in pCO2 levels at upstream and downstream locations likely could influence the extent of bioerosion, which correlates with the bioeroding community found at those two locations. Also, it has been shown that faster growing perforate corals, such as Porites, have faster passive dissolution rates (dissolution of bare skeletal carbonates) than imperforate coral skeletons under ocean acidification, which also could have implications for dead massive Porites bommies at upstream and downstream locations (van Woesik et al. 2013). I hypothesized that downstream locations exposed to higher pCO2 would have more bioeroders and experience greater internal bioerosion relative to upstream coral bommies and rubble.
During summer 2012, Lithophaga surveys were conducted in upstream and downstream locations. In addition to quantifying their abundances across the back reef, abundance was quantified within the microhabitats of individual massive Porites colonies and on the upstream, top, and downstream zones of the coral bommie. These surveys
14 helped inform future work that involved collection and experimental manipulation of these organisms. It is difficult to predict differences in bioeroder abundance and the extent to which they erode due to the numerous confounding influences found in a coral reef environment. However, the influence of reef metabolism and flow dynamics and their role in climate change is still a relatively new area of investigation and may play a larger role than considered previously.
The goal of the external bioeroder surveys was to explore differences in benthic bioeroding communities in upstream and downstream locations. The second portion of this research was to determine the extent of internal erosion in rubble and dead Porites portions in upstream and downstream locations. For all bioeroder surveys in upstream and downstream transects, my hypothesis was that there would be more bioerosion in downstream locations due to the daily occurrence of lower aragonite saturation (at night) due to reef metabolism. The final part of this research was to determine lithophagid abundances across the back reef as well as their spatial distribution on individual coral bommies. The hypothesis for their spatial distribution is that there would be greater lithophagid settlement and therefore abundance, on the downstream side of bommies.
Methods
Study Site
This study was conducted across the back reef on the north shore of Moorea,
French Polynesia (17º 30’ S, 149º 50’ W) located in the central South Pacific. In January
2012 (austral summer) and May 2012 (austral winter) surveys were conducted in the back reef habitat, between the reef crest and the boat channel. This area is dominated by large
15 coral bommies (mounding colonies) mostly comprised of massive Porites >1 meter in diameter, separated by patches of rubble and sand. The unidirectional flow across the back reef from the fore reef into the lagoon was used to determine the two locations examined during this study (Hench et al. 2008). Upstream refers to parallel transects located ~20 meters behind the reef crest and downstream refers to parallel transects located ~400 meters from the reef crest (Figure 1). This site was selected based on the location of previous work that demonstrated chemical differences at these two locations
(Johnson et al. 2014). Water depths in both upstream and downstream locations were between 2–3 meters.
Benthic surveys
To quantify external bioeroder abundance, benthic transects were conducted in
January 2012 on the back reef. All external bioeroders were counted within four, randomly assigned 0.25 m2 quadrats (based on study by Peyrot-Clausade et al. 2000) along a 15 m transect. A total of 20 transects were placed parallel to reef crest in both upstream and downstream locations. Five transects were placed across areas dominated with rubble fields or coral bommies in upstream and downstream locations. The reasoning for including both types of substrata was to cover the most common type benthic components in this area excluding sand patches. When one transect was complete, the next transect was conducted further along the upstream/downstream location at least 15 meters from the previous transect so there was no overlap. Only partially dead coral bommies were surveyed due to the species considered and to avoid confounding effects of bioeroding community differences associated with living versus
16 dead coral bommies that have greater heterogeneity in structure and associated fauna.
Species abundance was recorded for: Diadema savignyi, Echinostrephus aciculatus,
Echinometra mathaei, Echinothrix diadema, Echinothrix calimaris, Spirobranchus giganteus, and Dendropoma maxima. This species list includes conspicuous borers, grazers, and excavators, which were common external bioeroders on the back reef.
Collection and Analyses for Internal Erosion
During transects conducted at upstream and downstream locations, two pieces of coral rubble (approximately 30-mm length) were collected from bottom right hand corner of quadrat from each rubble transect and two fragments of dead coral chiseled from the nearest dead coral bommie from each bommie transect were collected using a random number assignment (n=40). Rubble and bommie portions were dried at 60 °C and then bisected using a handheld Dremel tool with a diamond grit cutting wheel. A cross section of each sample then was photographed and ImageJ software was used to measure total area of the cross section and area that was bioeroded.
Lithophaga surveys
To quantify Lithophaga abundance, benthic transects were conducted on the north shore back reef in May 2012. A similar transect configuration was used in upstream and downstream locations. All Lithophaga were counted within five randomly assigned (by number and alternating sides: left, right) 0.25 m2 quadrats (due to the small size of
Lithophaga) along a 15 m transect. If the transect did not run directly through a living
Porites colony, the quadrat was placed on the nearest bommie. Only living Porites
17 bommies were surveyed since this species specifically inhabits living coral tissue. A total of ten transects were placed parallel to reef crest with five located upstream and five in downstream locations.
Lithophaga abundance on individual Porites colonies
In addition to quantifying Lithophaga abundance at upstream and downstream locations, I conducted a separate survey where I looked at the distribution of Lithophaga on individual Porites bommies. In May 2012, Porites bommies scattered throughout the back reef on the north shore were selected haphazardly for this survey. I divided the coral colony into three zones: upstream, top, and downstream. Considering the dominant unidirectional flow pattern, surveys were conducted close to the reef crest in order to determine the upstream versus downstream face of the bommie as accurately as possible.
Once determined, a weighted transect was placed across the middle of the bommie bisecting the upstream and downstream zones. Since the tops of bommies are typically flat or mildly convex, the top zone was surveyed from above and careful attention was given to not count individuals more than once. The number of Lithophaga laevigata was totaled in each of the three zones. For this study, a total of ten Porites colonies were surveyed. Only living massive Porites bommies were considered since this species specifically inhabits living coral tissue.
Statistical Analyses
All analyses were completed using SYSTAT 12 software (Systat, Inc., Illinois,
USA). To determine differences of the external bioeroder abundance across the back reef
18 on rubble and bommie transects, a two-way ANOVA with Location and Substrate type as fixed factors was used. For examining differences of the internal bioerosion across the back reef on rubble and bommie samples, a two-way ANOVA with Location and
Substrate type as fixed factors was used. Internal erosion percentages were arcsine transformed. Differences in Lithophaga abundance in upstream and downstream locations across the back reef were compared with a simple t-test, with location a fixed factor and Lithophaga densities as the response variable. A two-factor mixed model
ANOVA was used to compare the spatial abundance of Lithophaga across an individual
Porites colony with zone (upstream, top, and downstream) as a fixed factor and coral colony as a random factor. Significant differences between zones were further analyzed with Tukey’s HSD post-hoc tests between each of the three zones. A graphic analysis of residuals was used to test assumptions of normality and homoscedasticity.
Results
External Eroder Abundance
External bioeroder density did not differ on upstream and downstream locations
(F1, 76 = 1.569, p = 0.214). Substrate type was significant (F1, 76= 82.686, p = <0.001) and bommies upstream 68 ± 12.2 (mean ± SE) individuals 0.25 m2 or downstream 66 ± 12.1
(mean ± SE) individuals 0.25 m2 had significantly more external eroders than rubble upstream 4 ± 2 (mean ± SE) individuals 0.25 m2 or downstream 7 ± 2.1 (mean ± SE) individuals 0.25 m2. There were no significant interactive effects of location and substrate type (p =0.636) (Table 2.1, Figure 2.2).
19 Internal Erosion
Internal bioerosion percent area did not differ between upstream and downstream locations (F1, 34 = 0.948, p = 0.337). Again, substrate type was significant (F1, 34= 27.472, but was opposite to external bioeroder abundance, internal erosion in rubble pieces collected upstream 12.5% ± 3.4 (mean ± SE) or downstream 4.9% ± 1.7 (mean ± SE) was significantly higher than bommie pieces upstream 23.4% ± 4.5 (mean ± SE) or downstream 34.6% ± 6.4 (mean ± SE). There was a significant interactive effect of location and substrate type (F1, 34 = 7.364, p = 0.010) (Table 2.2, Figure 2.3).
Lithophaga abundance
Densities of Lithophaga did not differ across upstream and downstream transects on the back reef. Lithophaga abundance in upstream habitats were on average 27 ± 4.1
(mean ± SE) individuals 0.25 m2 and downstream 26 ± 5.2 (mean ± SE) individuals 0.25
2 m locations (F1,48 = 0.912) (Figure 2.4).
Lithophaga abundance on individual Porites colonies
There was a significant effect of zone on Lithophaga abundance across Porites colonies surveyed (F2, 18 = 8.752, p = 0.002). Lithophaga abundance also differed significantly among bommies (F9, 18 = 3.695, p = 0.009) (Table 2.3). Pairwise comparisons showed significant differences in Lithophaga density between top and downstream zones (p = 0.018). Top and upstream zones (p = 0.717) and downstream and upstream zones (p = 0.099) were not significantly different (Table 2.4). The downstream side of the coral bommie had the highest number of Lithophaga with 27 individuals per
20 m2. The upstream side had on average 11 individuals per m2, and the tops of bommies had the lowest number of Lithophaga with only 3 individuals per m2 (Figure 2.5).
Discussion
Species abundance and diversity will have a direct impact on the regulation of coral reef growth (Peyrot-Clausade et al. 2000). As anthropogenic CO2 emissions increase, the effects of ocean acidification will have negative effects on marine calcifiers and noncalcifiers responsible for maintaining coral reef balance (Kroeker et al. 2010). In this study, there were no significant differences in bioerosion and bioeroder abundance at upstream and downstream locations, ~20 meters and ~400 meters from the reef crest. A similar study conducted on Tiahura reef in Moorea, also determined no significant differences in erosional activity of sea urchins (external eroders) between three sites across the back reef, however there was an increasing trend of average bioerosion rates from the reef crest into the fringing reef (Peyrot-Clausade et al. 2000). External and internal erosion both were significantly related to substratum type whether on partially dead coral bommies or in rubble fields. External bioeroder survey results showed greater abundances on bommies than on rubble fields (Fig. 2.2). Inversely, the extent of internal erosion was higher in rubble than within portions of dead coral bommies (Fig. 2.3).
External eroders considered for these surveys included several species of sea urchins and burrowing epifauna that bore, graze, and excavate the surface of dead coral.
While there were no significant differences in their abundance between upstream and downstream transects, significantly higher abundances on coral bommies could be influenced by habitat preference of these organisms. Individuals on coral bommie
21 transects mostly consisted of Echinometra mathaei, Spirobranchus giganteus, and
Dendropoma maximum, all of which are very common in the back reef of Moorea.
Echinometra mathaei is a significant contributor to bioerosion on reef flats and is commonly seen on massive stony corals where it uses robust spines to excavate long burrows throughout the surface layer. Similar to lithophagids, sea urchin abundance has been shown increase on highly degraded reefs where fish predators have been removed.
A study of Kenyan reefs demonstrated that reef lagoons with greater fishing pressure had higher sea urchin abundances and less coral cover. Echinometra mathaei increased five- fold over the course of 15 years on the most exploited lagoon. (McClanahan & Muthiga
1988). The tube-building polychaete Spirobranchus giganteus, was found in high abundance embedded into the skeleton of Porites, and usually is surrounded by living tissue only in colonies of living coral. Dendropoma maximum, a worm snail in the family
Vermetidae, also are very abundant in Moorea. They typically live on the surface of coral bommies, and one experiment conducted in the same area as this study, showed that increased densities of these vermetids significantly reduced the percent cover of live coral and skeletal growth (Shima et al. 2010). The most common individuals found on rubble transects mostly consisted of Diadema savignyi and Echinostrephus aciculatus. These two types of urchins have very fine spines and are common on rubble. D. savignyi bioerodes through the process of grazing and hides in crevices during the day, while E. aciculatus creates a circular burrow and embeds itself into dead skeleton. Knowing the substratum preference and relative abundance of this diversity of organisms provides a better understanding of the external bioeroder community present on the back reefs of
Moorea.
22 Results for the internal erosion analysis demonstrated that there were no differences between locations, but there was a significant increase in bioerosion within rubble samples compared to the portions of dead bommies. This potentially is due to the fact that rubble represents an older piece of coral rock than recently dead portions of substratum that were extracted from Porites bommies. This result agrees with a study on the Tiahura reef in Moorea that showed a positive correlation between bioerosion rates and time elapsed since death of a colony (Peyrot-Clausade et al. 1992). Increasing degradation of a coral bommie not only changed the extent of erosion but also the dominant agents of bioerosion. In samples collected for the present study, the main bioeroders included sponges, worms, and bivalves, all of which are known to be important bioeroders in the latter stages of degradation of massive Porites colonies
(Peyrot-Clausade et al. 1992). Studies looking at bioerosion over time on experimental blocks of carbonate have demonstrated that external bioerosion pressure is greater than internal bioerosion during the first year (Kiene and Hutchings, 1994; Peyrot-Clausade et al., 1995). High grazing pressure can limit the settlement and survival of internal eroders; therefore borers play a more important role on older portions of dead coral substrates and under lower grazing intensity (Hutchings 1986, Kiene 1988).
In addition to quantifying bioerosion in dead substrata, I quantified abundances of
Lithophaga laevigata, which occur only in living massive Porites (Peyrot-Clausade et al.
1992). Similar to the previous studies conducted in January 2012 on dead coral substrata, there were no differences in Lithophaga laevigata abundance across the back reef between upstream and downstream locations. There was however an interesting pattern when examined on a microhabitat level of individual Porites colonies. The heterogeneous
23 flow environment across a coral bommie generally shows high flow on the upstream, even higher flow over the top, and slower flow consisting of turbulent eddies in the recirculation zone downstream (Brown 2012; Hench and Rosman 2013). The downstream sides of the coral bommies had the highest number of Lithophaga, the tops of bommies had the lowest number of Lithophaga, and upstream abundance was intermediate. These results are consistent with studies conducted in other environments where slower water flow promoted attachment of epibionts such as foliose algae and planktonic larvae downstream (Ferrier and Carpenter 2009, Reidenbach et al. 2009). The downstream side of a coral colony does not seem ideal for a filter feeding heterotroph considering the diffusive boundary layer is thicker on this side of the bommie and therefore would have less efficient exchange of nutrients and particles to the surface.
Potentially there is a bottom-up effect, and the physical environment is more influential to larval settlement than the biological advantage of food availability. These physical and biological interactions may provide important information about the larval phase of
Lithophaga.
While the majority of this research was mensurative, it is important to examine natural patterns of coral reef communities in varying pH environments (as seen in upstream and downstream transects) to help predict the effects of OA. Even subtle differences, such as changing seawater chemistry across a back reef can have significant impacts on benthic community structure. Reef areas that have a lower pH, lower aragonite saturation, and higher pCO2 have less cementation, which strengthens the reef framework and decreases porosity. Exposed parts of the reef such as the upstream transect that experiences higher flow usually are more cemented than downstream as
24 water flow decreases into the lagoon (Manzello et al. 2008). Higher flow environments can also reduce echinoid densities, which would affect bioerosion rates in the lagoon
(McClanahan and Muthiga, 1988). Negative anthropogenic effects such as overfishing have already been shown to increase destructive processes as a result of increasing echinoid populations (Carpenter, 1984; McClanahan and Muthiga, 1988). However, the effects of ocean acidification on coral reef balance still are largely unknown, therefore more studies need to examine the distribution and intensity of external and internal bioerosion across different habitat types in naturally variable pH environments.
25 Table 2.1. Results from a model I two-factor analysis of variance (ANOVA) testing for differences in external bioeroder densities upstream and downstream.
Source MS df F p Location (L) 0.51 1 1.569 0.214 Substrate Type (S) 24.22 1 82.686 <0.001 L x S 0.10 1 0.225 0.636 Error 0.34 76
26 Table 2.2. Results from a model I two-factor analysis of variance (ANOVA) testing for differences in internal bioerosion on bommie and rubble substrate at upstream and downstream locations.
Source MS df F p Location (L) 0.018 1 0.948 0.337 Substrate Type (S) 0.508 1 27.472 <0.001 L x S 0.136 1 7.364 0.010 Error 0.018 34
27 Table 2.3. Results from the mixed model II analysis of variance (ANOVA) testing for differences in Lithophaga abundance at upstream, top, downstream locations on a Porites colony.
Source MS df F p Zone (Fixed) 1459.55 2 8.752 0.002 Bommies (Random) 616.23 9 3.695 0.009 Error 166.77 18
28 Table 2.4. Results from Tukey’s honestly significant pairwise difference tests for differences in Lithophaga abundance at upstream, top, downstream locations on a Porites colony.
Location 1 Location 2 Difference p Downstream Top 23.33 0.018 Downstream Upstream 17.11 0.099 Top Upstream -6.22 0.717
29
Figure 2.1. Study site on the north shore of Moorea, French Polynesia. Upstream and downstream locations shown for transects conducted on external bioeroders, internal erosion, and Lithophaga abundance. Arrows depict the unidirectional flow across the back reef.
30 90
80
70 2 60
50 Bommie 40 Rubble 30 Individuals per 0.25m per Individuals 20
10
0 Upstream Downstream
Figure 2.2. Mean (±SE) external bioeroder abundance on bommies and rubble in upstream and downstream locations (n=5).
31 45
40
35
30
25 Bommie 20 Rubble % Bioerosion % Bioerosion 15
10
5
0 Upstream Downstream
Figure 2.3. Percent (±SE) bioerosion in bommie and rubble pieces collected at upstream and downstream locations (n=5).
32 35
30
25 2
20
15 Individuals per m per Individuals 10
5
0 Upstream Downstream
Figure 2.4. Mean (±SE) Lithophaga abundance in upstream and downstream locations. Location (n=10).
33 40 35
2 30 25 per m per 20 15 Lithophaga 10 5 0 Upstream Top Downstream Zone on Bommie
Figure 2.5. Mean (±SE) spatial abundance of Lithophaga on Porites on upstream, top, and downstream zones of a Porites colony (n=10).
34 Chapter 3
Effects of Ocean Acidification on Calcification, Bioerosion, and Respiration Rates of
Lithophaga laevigata within Massive Porites in Moorea, French Polynesia
Introduction
Tropical coral reef ecosystems are dynamic shallow water environments built by scleractinian corals and encrusting macroalgae. They provide a complex, hard, and stable substratum for a large diversity of marine organisms. This CaCO3 reef framework supports one of the most diverse ecosystems on the planet and has been compared to rainforests because of their complexity and high species diversity (Reaka-Kudla 1997,
Bellwood and Hughes 2001). Coral reefs typically occur in within relatively nutrient-poor waters, yet they are one of the most productive ecosystems, providing invaluable benefits and services to society in the form of coastal protection, food, and economic resources such as tourism (Grigg et al. 1984, Moberg and Folke 1999). Human induced carbon dioxide emissions into the atmosphere are increasing over time and the effects of climate change associated with these emissions are predicted to negatively alter the ocean environment. Currently, more than half of coral reef ecosystems worldwide are at risk of degradation (Burke et al. 2011).
According to the fifth assessment report of the IPCC, carbon dioxide (CO2) concentrations have increased by 40% since preindustrial times from fossil fuels and net land use emissions. The ocean is carbon sink for approximately 33% of these anthropogenic emissions (Sabine et al., 2004). The absorption of CO2 into the ocean is a naturally occurring process and the ocean serves as a source or sink of CO2 through
35 carbon cycling. However, the unprecedented increase of anthropogenic CO2 entering the world oceans reduces its capacity to buffer it. The net result of adding CO2 to seawater is
+ – an increase in hydrogen ions [H ] and bicarbonate ions [HCO3 ], but a reduction in
2– available carbonate ions [CO3 ]. The decrease in carbonate ions reduces the overall buffering capacity as CO2 increases, resulting in proportionally more hydrogen ions, therefore increasing acidity with no change in total alkalinity. From preindustrial times, anthropogenic CO2 causing ocean acidification (OA) is predicted to decrease ocean surface pH by 0.14–0.43 units by the end of the 21st century (IPCC 2014). Evolutionary rates of marine organisms may not allow them to adapt fast enough to these rapid changes in ocean chemistry.
Ocean acidification (OA) poses a threat to the growth and maintenance of the coral reef framework. Calcifying organisms depend on available carbonate ions, and the decrease in the saturation state of aragonite (Ωarag) due to ocean acidification will have negative for calcifying organisms, which are an integral to coral reef ecosystems (Hoegh-
Guldberg et al., 2007, Kleypas and Yates 2009). As a result, most studies to date have focused on how this rapid rate of decline in ocean pH could affect marine calcifiers directly. However, an equally important but opposing process, bioerosion, also will be affected by OA. Bioerosion is essentially carbonate erosion by living organisms. On coral reefs, bioerosion is accomplished by a diversity of organisms. Bioeroders are found within families such as Scaridae (parrotfish), Clionaidae (sponges), Mytilidae (bivalves), and Echinometridae and Diadematidae (sea urchins). Each of these contributes to the break down of coral into rubble and sand via mechanical abrasion or via chemical dissolution. Parrotfish and sea urchins use mechanical means to break down the reef
36 during grazing activities by abrading the surface to consume algae growing on carbonate substrata. Bivalves and sponges primarily use chemical means to dissolve and penetrate the surface, which is also referred to as biocorrosion. At the whole reef scale, there is a dynamic balance between constructive processes (calcification) and destructive processes
(dissolution and bioerosion). Coral reef growth depends on the rate of reef accretion being faster than erosional processes (Glynn 1997). It generally has been predicted that bioerosion rates will increase under future climate change conditions. While there are very limited studies on the direct effects of OA on bioerosion, it has been shown that reducing the saturation state of aragonite (Ωarag) will facilitate bioerosion by macroborers and endolithic algae due to increased calcium carbonate dissolution and increase skeletal porosity over time (Manzello et al., 2008, Tribollet et al., 2009, Chen et al., 2012).
The effects of bioerosion are more rapid and common within dead carbonate substrata, however, there are several organisms that can settle and erode living coral tissue and the underlying skeleton. The bivalve Lithophaga laevigata (Quoy & Gaimard
1835) is a macroborer that is abundant within massive Porites spp. throughout the Pacific region (Peyrot-Clausade 1992). The dumbbell shaped borehole opening of Lithophaga is easily recognizable on the surface of massive Porites tissue. Veligers (bivalve larvae) settle on the living tissue of their host coral and eventually establish a borehole within the coral skeleton (Scott 1988b). Fang and Shen (1988) suggested that Lithophaga is a mechanical borer, however numerous studies have demonstrated that this is not possible due to the delicate structure of their valves, therefore it generally is accepted that the dominant method for this species is biocorrosion (Kleemann 1984, 1986, 1990a, 1990b,
1996). Dissolution by Lithophaga affects the substrate matrix and embedded grains, and
37 is followed by removal of the loose particles using ciliary currents and expulsion of pseudofaeces (Kleemann, 1973a, 1996). While the coral host survives the invasion of
Lithophaga, an increase in their abundance significantly decreases the compressive and bending strength of the coral skeleton (Scott and Risk 1988). Lithophaga in high densities are sometimes referred to as an “infestation”. In live coral this bivalve can be a significant contributor to bioerosion on coral reefs. The bioerosion rate of Lithophaga can
2 2 reach up to 9000 g CaCO3/m /yr with densities as high as 1879 ind/m (Glynn, 1997).
Massive Porites coral contributes to the three-dimensional structure of coral reefs providing habitat for a diversity of organisms. Porites is a relatively slow growing coral with a thick tissue layer and is considered more resistant to environmental disturbances such as crown of thorn (corallivore) outbreaks and elevated temperature and pCO2 exposure (Done 1987; Done and Potts 1992; Edmunds 2011; Edmunds et al. 2012;
Fabricius et al. 2011). Comeau et al. (2013) found no effect of OA on net calcification of massive Porites exposed to high pCO2 under high light conditions. However, Anthony et al. (2008) examining the combined effects of temperature and OA on massive Porites resulted in a 20% decrease of calcification in elevated pCO2 and no effect of temperature.
As anthropogenic influence increases on coral reefs so will the number of coral associates such as snails (Drupella cornus), vermetid gastropods (Dendropoma maxima), scallops
(Pedum spondyloideum), and bivalves (Lithophaga spp.). Filter-feeding heterotrophs are known to thrive in these elevated nutrient conditions (Scaps and Denis 2008, Scaps et al.
2008). As anthropogenic disturbances continue to change the reef, it is important to investigate how the effects of OA will influence massive Porites containing Lithophaga.
This study examined how the balance between calcification and dissolution due to
38 lithophagid erosion could change under OA conditions using the unique symbiosis between Lithophaga laevigata on living massive Porites as a model system.
Within carbonate substrata, respiration of bioeroders such as endolithic phototrophs and cyanobacteria increases the concentration of CO2, which decreases pH and facilitates carbonate dissolution (Ferran, 2006, Tribollet et al., 2006). Lithophaga laevigata bioerode by producing acids to dissolve the skeletal layers of massive Porites, but respiration rates of these infaunal organisms could contribute to dissolution as well, similar to endoliths, which could have an indirect effect on bioerosion rates. Closely related mussels in other studies have shown no effect of OA until a pH of 7.4 (Berge et al., 2006). In a recent review on the impacts of OA on marine shelled mollusks, several species of oysters and clams increased respiration rates with OA, while the majority of experiments exhibited no effect of on respiration (Gazeau et al., 2013). Lithophaga is unique in that it is an infaunal organism, so increased respiration rates under OA could alter the internal environment of their burrow and exacerbate the effects of external OA on coral colonies.
The purpose of this study was to test the effect of OA on bioerosion rates of the macroborer Lithophaga laevigata in massive Porites spp. I tested the effect of OA on net calcification rates of coral with and without Lithophaga and on Lithophaga alone, as well as the effect on bioerosion rates, and respiration rates. Since different sized bivalves could have varying erosive capability, I took an initial sampling to account for the size of the bivalve and therefore the burrow by measuring the borehole opening. A collection of
Lithophaga was used to see if there is a correlation of the “figure 8” borehole opening dimensions and shell dimensions modeled after a study by Schiaparelli et al. (2005) that
39 found a highly significant correlation in a closely-related species, Gastrochaena dubia.
The expectation was that a significant correlation between the apertures major axis
(length of the opening) and valve length would provide a nondestructive method to selectively collect similarly- sized Lithophaga. To investigate bioerosion rates, I conducted a month-long mesocosm experiment using massive Porites samples with and without Lithophaga, and Lithophaga in burrow mimics under ambient and elevated pCO2 conditions. I first hypothesized that OA would have no effect on net calcification of massive Porites with and without Lithophaga. I also hypothesized that net calcification of
Lithophaga would decrease under OA. Lastly, I hypothesized that bioerosion rates by
Lithophaga in living massive Porites would increase in elevated pCO2 conditions.
Following the first experiment, respirometry chambers filled with seawater from the ambient and elevated mesocosms were used to compare respiration rates of Lithophaga.
For this experiment, I hypothesized that respiration rates of Lithophaga in burrow mimics would increase under elevated pCO2 conditions. Increased respiration rate could reveal an indirect effect OA may have on dissolution of the coral due to change in metabolic activity of this infaunel bioeroder. To my knowledge, this is the first attempt to quantify in-situ bioerosion rates of a macroborer in living coral and the first experiment to test the effects of OA on net calcification and respiration rates of Lithophaga laevigata.
Methods
Lithophaga Morphometrics
Collections were conducted from June-July 2012, on the north shore of Moorea,
French Polynesia (17º 30 S’, 149º 50’ W). Portions of massive Porites (P. lobata and P.
40 lutea) containing multiple Lithophaga were collected in the back reef at ~1–2 m depth.
Samples were collected using a hammer and chisel and brought to the Richard B. Gump
South Pacific Research Station for processing. A photo was taken of the borehole before the Lithophaga was extracted from the coral using a hand-held Dremel tool with a diamond-grit cutting wheel. Care was taken to avoid damaging the bivalve during this process. Once extracted, a photo was taken of the valves through a stereo microscope.
The photos then were analyzed using ImageJ software to measure the major and minor axis of the borehole opening and the length and height of each valve.
Bioerosion Sample Collection
Massive Porites samples containing one Lithophaga were collected in the back reef on the north shore of Moorea, French Polynesia at ~1–2 m depth using a pneumatic drill with a diamond-grit hole saw attachment (32 mm diameter, 38 mm cutting depth,
McMaster-Carr). The hole saw allowed for standardization of the area of each coral core during the sampling effort. For each sample collected with a Lithophaga, an additional core was collected nearby for the same parent colony with no Lithophaga inside to serve as a control for calcification rates used to calculate bioerosion. One hundred and twelve coral cores (half with Lithophaga, half without) were drilled from adult colonies, placed in plastic bags with seawater, and immediately transported back to the Richard B. Gump
South Pacific Research Station. Coral cores collected from the same parent colony were paired throughout the duration of the experiment. Coral cores were trimmed using a hand-held Dremel tool with a diamond-grit cutting wheel to remove excess skeleton at the base and standardize the volume of the CaCO3 core. All exposed portions of the
41 skeleton were sealed using Z-spar marine epoxy (A788 epoxy) to avoid dissolution of the newly exposed carbonate skeleton and the core was attached to plastic bases. These samples remained in a seawater table with high flow for two days to leach any toxic chemicals and allow time for the epoxy to set.
Using the same coring method mentioned above, additional coral cores were removed containing Lithophaga. These cores then were bisected using a chisel and hammer to extract Lithophaga from the coral and were transferred into burrow mimics
(PVC aquarium tubing and Parafilm) to use later for respiration trials as well as control for net calcification of the bivalve during the course of the experiment. Core pairs and
Lithophaga in burrow mimics all were transferred to a 1000-L flow through acclimation tank (Aqualogic) for approximately two weeks to allow time to heal from the collection process. Temperature and light (75 W LED, Sol White LED Module; Aquaillumination) conditions were set to mimic ambient conditions as close as possible to the back reef of
Moorea. A temperature controller maintained the seawater at 27 ºC and lights delivered
~500 µmol quanta m−2 s−1 on a 12:12 hour light:dark cycle. To remove position effects within the acclimation tank, samples were placed on a rotating table at the base of the tank that rotated once every 12 hours under the LED lights that were set to a 12:12 hour light:dark cycle.
Mesocosm Treatments and Maintenance
To test the effects of OA on bioerosion, a mesocosm experiment was conducted where cores with and without Lithophaga, and Lithophaga alone, were assigned randomly to six, 150-L tanks (Aqua Logic, San Diego, CA) for a month-long incubation
42 period. Seawater for the tanks was pumped directly from Cook’s Bay and passed through a sand filter (100 µm mesh). This size filter, along with LED lights, is sufficient to provide both autotrophic and heterotrophic nutrition to the coral and filter-feeding bivalve. Filtered seawater is stored in a header tank and gravity fed to the mesocosms.
Flow was maintained in each tank with submersible pumps (Rio 8HF, ~2,000 L h-1). The same lighting system (Sol White LED Module; Aquaillumination) used in the acclimation tank was used for the mesocosms and were also run on a 12:12 hour light:dark cycle. Samples were rotated every other day within each tank to avoid position effects.
Three tanks were held at present-day pCO2 concentrations ~400 µatm (ambient) and the remaining three were held at the predicted value for the end of the century ~850
µatm (SRES A2, IPCC 2014). All mesocosms were held at constant temperatures (~27
−2 −1 °C) and light levels (~500 µmol quanta m s ). To achieve the elevated pCO2 treatment, pCO2-enriched air was bubbled into the tanks using a solenoid-based controller (Model
A352, Qubit Systems, Ontario, Canada) and an infrared gas analyzer (IRGA model S151,
Qubit). LabPro software was run on a laptop to log the pCO2 output (Vernier Software and Technology, Beaverton, OR). Ambient or CO2-elevated air was delivered to the appropriate tanks using Gast pumps (Model DOA-P704-AA, Benton Harbor, MI).
Seawater Chemistry Analyses
Seawater samples were collected from each tank at 0900 hours local time daily and transferred to the lab and processed immediately for total alkalinkty (AT), salinity
(YSI 3100 Conductivity Meter), and pH. Dickson et al. (2003) certified reference
43 materials were used to determine the accuracy and precision of the titrations (CRM Batch
105 and 122, Dickson Lab, Scripps). In situ temperature and pH measurements were monitored in the tanks twice daily using portable meters (Fisher Scientific digital thermometer #15-077-8, ± 0.05 °C, Orion 3 star meter, DGI115-SC probe, Mettler
Toledo, Port Melbourne, Australia) throughout the 28-day experiment.
Total alkalinity and pH on a total scale (pHT) were measured using open-cell potentiometric titration with an automatic titrator (T50, Mettler Toledo, Port Melbourne,
Australia). The titrator probe (DGI115-SC probe, Mettler Toledo, Port Melbourne,
Australia) was 3-point calibrated using pH 4, 7, and 10 buffers (Fisher Scientific) and the titrator was filled with certified acid titrant (~0.1N HCl and 0.6M NaCl, Dickson Lab,
Scripps). Seawater chemistry was analyzed with LabX titration software (Mettler Toledo,
Port Melbourne, Australia). The AT, pHT, temperature, and salinity values were used in
CO2SYS (Lewis & Wallace, 1998) to calculate DIC parameters. pHT was measured additionally spectrophotometrically using m-cresol indicator dye (SOP, Dickson et al.
2007).
Net Calcification Rates
The buoyant weight technique (Spencer-Davies 1989) was used to estimate net calcification rates of the cores (with and without Lithophaga) and of Lithophaga alone.
Buoyant weights of each sample were recorded at the beginning and end of the 28-day incubation in the mesocosms. After 28 days, all samples were removed from the mesocosm treatments, weighed, and net calcification rates were determined using the change in buoyant weight between the initial and final values with a precision of ± 1 mg.
44 The change in buoyant weight was converted to dry weight using the density of seawater and aragonite (2.93 g cm-3). Surface area of each core was measured using the aluminum foil technique (Marsh 1970) and net calcification rates were normalized to surface area.
Lithophaga net calcification rates were normalized to tissue dry mass and expressed as mg/g/day.
Bioerosion Rate Calculation
To calculate bioerosion rates, the change in dry weight (ΔDW) from the initial and final measurements were converted from buoyant weights of massive Porites with and without Lithophaga. The change in dry weight of massive Porites core without
Lithophaga was subtracted from massive Porites with Lithophaga the same parent colony
(ΔDW Coral+Lith – ΔDW Coral) and then divided by surface area of each core (Area Core) times duration of the experiment. The change in buoyant weight of the Lithophaga alone was considered negligible; therefore it was not included in the calculation. This resulted in the bioerosion rate in milligrams of calcium carbonate removed per cm2 per day.
ΔDW Coral+Lith – ΔDW Coral 2 Area Core * Time = mg CaCO3 removed / cm / Time
Lithophaga Respiration
Lithophaga in burrow mimics were incubated in mesocosms at ambient and elevated treatments using methods listed above. Respiration trials were conducted toward the end of the experiment using Lithophaga in burrow mimics after an 18-day incubation period. Lithophaga were selected randomly from elevated and ambient treatments and
45 were used in dark respiration trails in confined 160-mL respirometry chambers. One
Lithophaga in a burrow mimic was placed on a perforated plate overlying a stir bar. Flow was maintained using a submersible magnetic stir-bar below the perforated plate. The chamber was surrounded by a temperature-controlled water jacket held at 27 °C. Each chamber was filled with water from the source tank for each Lithophaga and all air bubbles were removed through the ports on the lid. Each animal was given time to acclimate and open their valves and extend their siphons before beginning the trial.
Oxygen depletion was recorded over time using a calibrated PreSens fiber optic oxygen sensor (PreSens Precision Sensing GmbH, Germany). The oxygen probe was calibrated using water-saturated air (100%) and zero oxygen seawater (supersaturated sodium dithionite, Na2S2O4). To avoid hypoxia, oxygen saturation was maintained between 85-
100%. Additional controls were run to account for any change in oxygen concentration in the filtered seawater alone. At the conclusion of the experiment the bivalve tissue was removed, rinsed with fresh water, and dried at 60 °C to a constant weight with a precision of ± 1 mg. Respiration rates were calculated by using the oxygen solubility table
-1 (Unisense, Ramsing and Gundersen) to convert from % saturation to µmol O2 mL and values were normalized to the soft tissue dry weight resulting in normalized rates in µmol
-1 -1 O2 mg hr .
Statistical Analysis
All analyses were completed using SYSTAT 12 software (Systat, Inc., IL, USA).
A linear regression was used to determine if there was a relationship between the major axis of the borehole opening and the valve length. To analyze the area-normalized net
46 calcification rates of coral cores with and without Lithophaga in elevated and ambient treatments, a mixed model ANOVA was run in SYSTAT with CO2, core type (Porites with and without Lithophaga), and the interaction of CO2 and core type as fixed factors.
Random factors included: Pair ID (core set collected from the same coral bommie) nested within tank, nested within CO2 treatment; tank nested within CO2 treatment; and the interaction of core type with tank nested within CO2 treatment (Table 3.2). For bioerosion and respiration rates, a one-way between subjects ANOVA was conducted to compare the effect of the CO2 treatment in elevated and ambient conditions. A graphic analysis of residuals was used to test assumptions of normality and homoscedasticity.
Results
Lithophaga Morphometrics
There was a positive linear relationship between the two variables, major axis of borehole and valve length (r2 = 0.52, P<0.001). This information allowed a nondestructive method to be used to selectively collect similarly sized Lithophaga based on the major axis of the borehole opening (Table 3.1, Figure 3.1).
Tank Conditions
Ambient and elevated experimental treatment conditions were maintained at 388
± 3 µatm (pH 8.05 ± 0.01) and 842 ± 8 µatm (pH 7.77 ± 0.01) respectively (mean ± SE, n=84). Temperature, total alkalinity, and salinity were similar across all treatments. The average temperature in ambient conditions was 27.0 ± 0.1 °C and 27.0 ± 0.1 °C in the elevated treatment. Total alkalinity was 2306 ± 3 µmol kg-1 in ambient and 2312 ± 2
47 µmol kg-1 in elevated treatments. The salinity was on average 36.1± 0.04 ppm across all treatments (Table 3.1). The same seawater (ambient and elevated) was used for the respiration trials.
Net Calcification Rates
Net calcification rates of cores were analyzed by CO2, core type, and the interaction of CO2 and core type as fixed factors. Random factors included: Pair ID nested within tank, nested within CO2 treatment; tank nested within CO2 treatment; and the interaction of core type with tank nested within CO2 treatment. Results demonstrated a significant effect of CO2 (F1, 50= 12.221, P=0.024), where cores in the elevated treatment exhibited a 12% decrease in calcification. There also was a significant effect of
Lithophaga presence on net calcification rates (F1, 50= 56.614, P=0.002), and massive
Porites cores with Lithophaga calcified 15% less than corals alone. There was no significant interaction of CO2 and core type (F1, 50 = 0.158, P=0.711). There were also no significant nested effects of tank nested within CO2 treatment (F4, 50 = 0.265, P=0.899) or the interaction of core type with tank nested within CO2 (F4, 50 = 0.396, P=0.811).
However, there was a significant effect of pair ID nested within tank, nested within CO2 treatment (F50, 50 = 5.473, P<0.001) (Table 3.3).
In ambient treatments, area-normalized net calcification rates of Porites without
-2 -1 Lithophaga had a mean of 1.1 ± 0.07 mg CaCO3 cm day (± SE, n=28) and Porites with
-2 -1 Lithophaga had a mean of 0.97 ± 0.06 mg CaCO3 cm day (± SE, n=28). In elevated treatments, area-normalized net calcification rates of Porites without Lithophaga were a
48 -2 -1 mean of 1.0 ± 0.05 mg CaCO3 cm day (± SE, n=28) and Porites with Lithophaga were
-2 -1 a mean of 0.85 ± 0.04 mg CaCO3 cm day (± SE, n=28) (Figure 3.2).
Net calcification rates of Lithophaga in burrow mimics were measured for ambient and elevated treatment. Results of a t-test were not significant (P=0.437, n=20), so there were no changes in net calcification rates of the bivalve itself under elevated pCO2 conditions (Figure 3.3).
Bioerosion Rates
There was no significant pCO2 treatment effect on bioerosion rates in this experiment (P=0.747, n=28). Bioerosion rates in ambient and elevated conditions were
-2 -1 approximately 0.15 mg CaCO3 cm day and represented about 15% of the net calcification rates. Average bioerosion rates in the ambient treatment were 0.158 ± 0.043
-2 -1 -2 -1 mg CaCO3 cm day (mean ± SE, n=28), and 0.139 ± 0.042 mg CaCO3 cm day (mean
± SE, n=28) in the elevated treatment (Figure 3.4).
Respiration Rates
Respiration rates of Lithophaga in burrow mimics after 18 days in elevated and ambient pCO2 treatments differed significantly (P=0.0439, n=12). Mean respiration rates were approximately 26% higher in the elevated treatment. The mean respiration rate in
-1 -1 the ambient treatment was 0.16 ± 0.012 µmol O2 mg hr (mean ± SE, n=12) and 0.22 ±
-1 -1 0.024 µmol O2 mg hr (mean ± SE, n=12) in the elevated treatment (Figure 3.2).
49 Discussion
The main focus of this study was to test the effect of the macroborer Lithophaga laevigata in massive Porites under ocean acidification. The effects of OA were analyzed on net calcification, bioerosion, and respiration rates to understand how bioerosion by
Lithophaga will impact massive Porites under future predicted pCO2 levels. In addition to testing coral cores containing Lithophaga, it was important to isolate the effects of OA on the growth and physiology of Lithophaga laevigata alone to better understand their association with, and potential impact on massive Porites.
The initial morphometric analysis of Lithophaga was similar to results found by
Schiaparelli et al. (2005). Unlike Lithophaga, the bivalve used in the study by
Schiaparelli et al. (2005), Gastrochaena dubia, has an aragonitic chimney surrounding its siphons, burrow lining, and it erodes into dead skeletal material and shells. Yet, results of the simple linear regression exhibited an analogously strong linear relationship between the major axis of the borehole opening and valve length. While these results were expected, it was important to measure the dimensions of Lithophaga laevigata specifically due to its differences with Gastrochaena. The correlation found between the borehole opening and bivalve length provided a nondestructive method to collect similarly sized Lithophaga for the experiments. Not only were these data useful in the context of this experiment, but it also provided insight on their population structure without having to extract the bivalve from its coral host. Ideally, there would also be a correlation between the borehole opening and the burrow volume of Lithophaga laevigata, which could then be used to estimate the extent of bioerosion in the field.
However, I was unable to accurately quantify burrow volume and perhaps using more
50 advanced techniques, such as a computed tomography scan of coral with Lithophaga, would provide the precision needed to accurately quantify burrow volume.
Contrary to my hypothesis, net calcification rates of Lithophaga laevigata were not affected by high pCO2 conditions in the elevated treatment. Effects of OA on calcifying marine invertebrates are variable, however a study on a closely related species,
Mytilus edulis, also exhibited no response to elevated pCO2 levels on net calcification over a 60-day experiment (Ries et al. 2009). There is a potential for marine organisms to regulate their extracellular pH (pHE) allowing them to maintain calcification under OA.
Organisms can respond to decreased pH by accumulating bicarbonate, which is thought to directly increase Ωarag at the calcification site or modify the delivery of bicarbonate to the calcifying epithelium (Pörtner et al. 2004, Thomsen and Melzner 2010). Additionally,
Lithophaga is an infaunal organism and potentially has evolved a higher capacity to buffer seawater due to its adaptation to the relatively low pH environment thought to be experienced by burrowing organisms (Gattuso and Hansson 2011).
Net calcification rates of massive Porites cores with and without Lithophaga, are within the range similar to those reported in previous studies (Anthony et al., 2008,
Edmunds et al., 2011). Net calcification results for massive Porites exhibited a 12% decrease in net calcification rate for cores incubated in elevated pCO2 conditions regardless of the presence of a bioeroder. This is consistent with the study by Anthony et al. (2008), which reported a 20% decrease in calcification of massive Porites in elevated pCO2. However, other studies have reported minimal to null effects of OA on massive
Porites, but these studies used juvenile colonies, which could respond differently than the portions of coral extracted from parent colonies (Edmunds 2011, Edmunds et al., 2012).
51 Results of the mesocosm experiment exhibited a 15% decrease in net calcification rates of massive Porites containing Lithophaga regardless of treatment. These results not only demonstrate the negative consequence of OA on massive Porites growth, but also that
Lithophaga presence resulted in a decrease in net calcification rates. While a similar depression in net calcification of massive Porites with Lithophaga occurred in both ambient and elevated treatments, this has considerable implications when Lithophaga heavily colonizes a Porites colony, which is common occurrence inshore Cook’s Bay where the environment is favorable for Lithophaga abundance (personal observation).
While these results do not affect bioerosion rates directly, the separate negative effects of
OA and Lithophaga presence on net calcification rates of massive Porites provide critical insight on accretion and erosion balance between these macroboring organisms and their live coral host.
The mesocosm experiment tested the hypothesis that OA would increase bioerosion rates of Lithophaga laevigata in massive Porites. Contrary to that hypothesis, there was no effect of OA on bioerosion rates. Several studies to date have shown that bioerosion rates of endolithic algae and boring sponges increased with decreasing pH
(Tribollet et al. 2006, Wisshak et al. 2012, Duckworth and Peterson 2013). The effect of
OA on bioerosion rates of boring algae and sponges on dead strata may not apply to the unique association of Lithophaga laevigata in living massive Porites. Other studies used macroborer abundance to provide a rough estimate of bioerosion rates in naturally varying pH environments, however, it is difficult to isolate pH effects on bioerosion in the field (Manzello et al. 2008, Chen et al. 2012, Crook et al. 2013). It has been predicted that bioerosion rates will increase for carbonates accreting under an OA regime like those
52 found in sites of upwelling. For example, in the Eastern Tropical Pacific, the carbonate substratum is poorly cemented due to the naturally low pH conditions from upwelling and is subject to severe bioerosion (Manzello et al. 2008). Other field studies also found greater bioerosion of lithophagids in massive Porites growing in lower pH and higher sea surface temperature (SST) conditions (Chen et al. 2011, Crook et al. 2013). It is important to note that these were all field studies, so they did not isolate the direct effect of OA on bioerosion and there are potentially confounding effects of nutrients, temperature, location, flow, and depth. Bioerosion rates are much faster on dead carbonate substrata versus living portions of a coral colony, so this could be a limitation of measuring changes in living coral for a month-long experiment. Therefore, my results are conservative considering the timescale of this natural process. Since Lithophaga is a chemical bioeroder, the null effect of OA on bioerosion rates could also be a response to the lower pH by decreasing production of the acid used to biocorrode the interior of the coral skeleton.
Animals have the ability to raise and lower their metabolism between certain limits. A review by Pörtner et al. (2004) demonstrated that hypercapnia elicits metabolic depression for several different species of marine organisms. However, it has been hypothesized that decreasing pH also could increase metabolic rates in bioeroding organisms (Wisshak et al., 2012), which could, in turn affect their ability to bioerode. In the present study, there was a 26% increase in respiration rates of Lithophaga under elevated pCO2 after 18 days of exposure. Similar effects of hypercapnia on respiration rates have been observed for Mytilus edulis for comparable pCO2 levels (Thomsen and
Melzner 2010). The arctic pteropod Limacina helicina also significantly increased
53 respiration rate in elevated pCO2 level at elevated temperature, but was unaffected by pCO2 at ambient temperature (Comeau et al. 2010). The significant increase in respiration rate does not necessarily indicate metabolic stress. Throughout the experiment, there was zero mortality, organisms remained active, and there was sufficient acclimation time during the mesocosm experiment before respiration trials were conducted. How these organisms are allocating their energy was not tested directly in this study, therefore results need to be interpreted with caution. Yet, hypercapnia increased respiration rates, which could explain why there was no change in bioerosion rates of Lithophaga. Their acids are metabolically expensive to produce; therefore increased aerobic metabolic rates could be at the cost of acid production. Whether Lithophaga can maintain increased respiration rates under chronic OA conditions is still unknown. Over longer periods of time than the present study, increased respiratory CO2 release could conversely increase bioerosion rates by decreasing Ωarag and increasing carbonate dissolution inside the skeletal burrow.
Studies have suggested that massive Porites will become a dominant benthic space holder in the future due to its marginal negative responses to climate change and
OA (Edmunds 2011, Edmunds et al., 2012, Fabricius et al. 2011). Carbon dioxide emissions by humans into the atmosphere are on the rise, and this could have serious implications for massive Porites containing this ubiquitous coral associate. In addition to
OA, coastal development, nutrient enrichment, and increased storm events also can affect
Lithophaga bioerosion, which is known to compromise the structural integrity of this important reef builder (Scott and Risk 1988). This study reveals that Lithophaga is additionally slowing the calcification rates of massive Porites, which could further
54 compromise this predicted “winner” in the face of climate change. Erosion of scleractinian corals is an integral part of reef dynamics, therefore an investigation of the impacts of OA on bioerosion was important in predicting potential outcomes of our changing environment. Lithophaga is considered a significant contributor to bioerosion, yet they remain understudied and there is a dearth of detailed information on their basic biology and natural history. Results gained from this study provide critical information needed to predict future responses to ocean acidification. Future OA studies should be longer-term experiments that include multiple environmental parameters that will have direct effects on bioerosion such as temperature, flow, and nutrient concentrations.
55 Table 3.1. Results from the simple linear regression of the major axis of the borehole and the length of the valve (n=38).
Effect MS df F p Regression 150.5 1 38.96 0.000 Residual 3.86 36
56
Table 3.2. Summary of carbonate chemistry measurements in 6 randomly assigned tanks throughout a 28-d incubation period in elevated and ambient pCO2 treatments. Mean ± SE. n=28 sampling days for all parameters.
pCO A Salinity Treatment Tank T (°C) 2 T pH (µatm) (µmol kg-1) total (ppm)
Ambient 1 26.9 ± 0.1 390 ± 7 2299± 4 8.05 ± 0.01 36.0 ± 0.03 Ambient 2 27.3 ± 0.1 396 ± 6 2304± 4 8.04 ± 0.01 36.1 ± 0.04 Ambient 10 26.9 ± 0.1 385 ± 4 2315 ± 2 8.05 ± 0.003 36.0 ± 0.03 Elevated 7 27.8 ± 0.1 846 ± 13 2311 ± 2 7.77 ± 0.01 36.2 ± 0.04
Elevated 8 27.5 ± 0.1 852 ± 14 2316 ± 3 7.77 ± 0.01 36.0 ± 0.03 Elevated 12 27.1 ± 0.1 829 ± 13 2311 ± 2 7.78 ± 0.01 36.0 ± 0.04
57 Table 3.3. Results from mixed model analysis of variance (ANOVA) testing effects of Core Type (Porites with and without Lithophaga) and CO2 (ambient and elevated treatments), Tank, and Pair ID (colony of origin) on area-normalized net calcification rates.
Source Effect MS dfnum F p
CO2 Fixed 0.428 1 12.221 0.024 Core Type Fixed 0.608 1 56.614 0.002 CO2 x Core Type Fixed 0.002 1 0.158 0.711 Tank (CO2) Random 0.035 4 0.265 0.899 Core Type x Tank (CO2) Random 0.011 4 0.396 0.811 Pair ID (Tank (CO2)) Random 0.148 50 5.473 <0.001 Error 0.027
58 16
14 y = 2.2311x + 2.587 R² = 0.5197 12
10
8
6 Shell length (mm) (mm) length Shell
4
2
0 0 1 2 3 4 5 6 Siphonal aperture major axis (mm)
Figure 3.1 Predictive relationship between the major axis of the borehole opening of Lithophaga laevigata and valve length (n=38).
59 1.4
1.2 -L +L
-1 1.0 day
-2 0.8 cm 3 0.6
mg CaCO mg 0.4
0.2
0.0 400 µatm 850 µatm Treatment
Figure 3.2 Mean (±SE) area-normalized net calcification rates of Porites with and without Lithophaga in ambient and elevated treatments (n=28).
60 0.0035
0.0030
0.0025
0.0020
0.0015 mg/g/day mg/g/day
0.0010
0.0005
0.0000 400 µatm 850 µatm
Figure 3.3 Mean (±SE) weight-normalized net calcification rates of Lithophaga in burrow mimics in ambient and elevated treatments (n=20).
61 0.25
0.20 -1 day
-2 0.15 cm 3
0.10 mg CaCO mg 0.05
0.00 400 µatm 850 µatm Treatment
Figure 3.4 Mean (±SE) estimated bioerosion rates of Lithophaga in Porites in elevated and ambient pCO2 treatments (n=28).
62 0.30
0.25
-1 0.20 hr -1 mg
2 0.15
mol O mol 0.10 µ
0.05
0.00 400 µatm 850 µatm Treatment
Figure 3.5 Mean (±SE) respiration rates of Lithophaga in burrow mimics after 28 days in elevated and ambient pCO2 treatments (n=12).
63 Chapter 4
Summary
Increasing carbon dioxide emissions into the atmosphere by humans will have serious consequences for the world oceans. Coral reefs have been identified as one of the most vulnerable marine ecosystems (Burke et al. 2011). While consequences of ocean acidification on coral reefs are well studied for marine calcifiers, bioeroders have been largely ignored until recently, despite their important role in affecting the coral reef framework (Wisshak et al. 2012, Duckworth and Peterson 2013). More than a century ago, Darwin recognized the importance of biologically mediated dissolution in reef development and maturation (Darwin, 1842). The goal of this research was to examine the effect of lowered pH on bioerosion in living and dead coral with a specific focus on
Lithophaga laevigata inhabiting living massive Porites.
Findings presented in Chapter 2 suggest that habitat type had a greater influence on internal and external bioeroder abundance than physical and chemical differences across the back reef. No patterns were found between upstream and downstream transects for any of the bioeroders examined. External bioeroder abundance was higher on coral bommies than on rubble fields. However, internal erosion was higher in rubble than portions of dead coral bommie. These patterns may not only be influenced by habitat preference, but also modes of bioerosion employed by external and internal eroders
(grazers versus borers). In a long-term study by Kiene and Huchings (1992) on the Great
Barrier Reef, experiments using dead coral samples concluded that internal borers played a minor role on reef environments dominated by grazing. Similar patterns were observed in the combined results from the present study of external and internal erosion, where
64 coral bommies that had higher grazing pressure from sea urchins exhibited lower internal erosion. Coral rubble that had lower grazer abundance was more susceptible to boring activity. Without the indirect protection provided by external grazers on partially dead coral bommies, the substratum would likely become heavily bored in their absence
(Kiene and Huchings 1992). Grazing activities of external eroders also may affect borer recruitment by modifying the available substratum for infaunal organisms (Hutchings
1986, Sammarco et al. 1987). Results in the present study also complement an experiment on Tiahura reef that demonstrated a positive correlation between bioerosion rates and the time elapsed since death of a coral branch or colony (Peyrot-Clausade et al.
1992). Increasing degradation (bommie to rubble) of coral not only changed the extent of erosion but also the dominant agents of bioerosion. Lithophagids, sponges, and worms were common in rubble, which are known to be important bioeroders in the latter stages of degradation of massive Porites (Peyrot-Clausade et. al. 1992).
It is well known that lithophagid bivalves are important contributors to bioerosion, and in high densities can lead to rapid reef loss (Glynn 1997). Therefore, I was interested in investigating Lithophaga laevigata, which only occurs in living massive
Porites, and is common in Moorea, French Polynesia (G. Paulay personal comm., Peyrot-
Clausade et. al. 1992). While no differences were observed in Lithophaga laevigata abundance across the back reef at upstream and downstream locations, a notable pattern was revealed when their abundance on the scale of an individual colony was examined.
On average, the downstream sides of Porites bommies had higher numbers of Lithophaga than the upstream side, and the top, which had the lowest abundance. This pattern is similar to patterns found in other studies where slower water flow on the downstream
65 side of a benthic boulder promoted attachment of epibionts such as foliose algae and planktonic larvae (Ferrier and Carpenter 2009, Reidenbach et al. 2009). The heterogeneous flow environment across a coral mound described by Hench and Rosman
(2013) helps to explain the spatial variation of Lithophaga abundance on massive Porites colonies. However, these results are also counter-intuitive considering the thicker diffusive boundary layer found on the downstream side of a colony provides less efficient exchange of nutrients and particles to this sessile filter-feeding heterotroph (Brown 2012,
Hench and Rosman 2013). These results suggest a bottom-up effect, where the physical environment may have a stronger influence on larval settlement /adult abundance than the biological advantage of food availability. These physical and biological interactions provide important information about the population of Lithophaga inhabiting shallow coral reefs. The extent and type of bioerosion examined in Chapter 2 likely are a result of various physical and ecological processes, and further in situ studies of bioeroders are needed to increase the understanding their influence on benthic community structure.
The morphometric analysis of Lithophaga, modeled after Schiaparelli et al.
(2005), revealed a strong linear relationship between the major axis of the borehole opening and valve length. This predictive relationship provided a nondestructive method to collect similarly sized Lithophaga for experiments. Not only were these data useful in the context of my experiment, but it can also be used to gather information on their population size structure without having to extract the bivalve from its coral host.
The goal of Chapter 3 was to explicitly test the effect of ocean acidification on bioerosion of macroborer Lithophaga laevigata in massive Porites. Lab conditions were set up to mimic future predicted pCO2 levels of ~850 µatm (SRES A2, IPCC 2014). Net
66 calcification, bioerosion, and respiration rates were measured to understand how bioerosion by Lithophaga would impact massive Porites under OA. Contrary to my hypothesis, net calcification rates of Lithophaga laevigata itself were not affected by hypercapnic conditions. These results agree with a study on a closely related species,
Mytilus edulis, which also exhibited no response to elevated pCO2 levels on net calcification (Ries et al. 2009). While OA had no effect on net calcification rates of the bivalve itself, a different result was found for the living coral they inhabit. Net calcification rates for massive Porites exhibited a 12% decrease when exposed to elevated pCO2 conditions regardless of the presence of a bioeroder. This is consistent with a study that also documented a slight decrease in calcification of massive Porites in elevated pCO2 (Anthony et al. 2008). There was a 15% decrease in net calcification rates of massive Porites containing Lithophaga regardless of treatment. These results not only demonstrate the negative consequence of OA on massive Porites growth, but also that
Lithophaga presence results in a decrease in net calcification rates. Even without the negative consequences of OA on massive Porites alone, these results show that colonies containing Lithophaga, particularly ones that have high densities, could be calcifying slower than colonies free of this infaunal organism.
To my knowledge, this study is the first attempt to quantify bioerosion rates in situ with living coral. Findings presented on bioerosion rates in Chapter 3 suggest that there is no effect of OA on bioerosion rates of Lithophaga laevigata in massive Porites.
These results are contrary to other studies that found increased macro- and microboring with decreasing pH (Tribollet et al. 2006, Chen et al. 2012, Wisshak et al. 2012).
However, these studies examined bioerosion in dead carbonate portions or made rough
67 estimates of bioerosion rates based on abundance data and pH variations in the field.
Bioerosion rates are much faster on dead carbonate substrata versus living portions of a coral colony, so this could explain the contradicting results. One hypothesis that could elucidate the lack of an effect of OA on bioerosion rates is that Lithophaga responds to lower pH by decreasing production of the acid used to biocorrode the interior of the coral skeleton.
The metabolic rate of an organism increases and decreases between certain limits as a response to environmental conditions. Decreasing pH could increase metabolic rates in bioeroding organisms (Wisshak et al., 2012), which could in turn affect their ability to bioerode. In the present study, respiration rates of Lithophaga in burrow mimics increased by 26% under elevated pCO2. Similar effects of hypercapnia on respiration rates have been observed for Mytilus edulis in comparable pCO2 levels (Thomsen and
Melzner 2010). How these organisms are allocating their energy could explain why there was no change in bioerosion rates of Lithophaga. Acids are metabolically expensive to produce; therefore increased aerobic metabolic rates could be at the cost of acid production.
Overall, results from this study begin to illustrate effects of OA on the symbiosis of Lithophaga laevigata inhabiting living massive Porites spp. This information is important to predict future responses to ocean acidification and how these responses could influence coral reef framework. As climate change continues to influence coral reef communities, there is much more to be learned about the effects of OA on bioerosion and future studies should include multiple parameters such as temperature, flow, and nutrient concentrations to accurately represent what is happening in the natural environment.
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