This document is a contribution of the Moorea Coral Reef LTER (OCE 04-17412)

June 8, 2007 Schedule for MCR LTER Site Visit Sunday, July 8 Check into Sheraton Moorea Lagoon & Spa Afternoon Optional Moorea Terrestrial Tour 4:30-5:00 Gump Station Tour/Orientation 5:00-5:30 Snorkel Gear Setup for Site Team/Observers – Gump Dock 5:30-6:30 Welcome Cocktail – Gump House 6:30-7:30 Dinner – Gump Station 7:30-9:30 NSF Site Team Meeting – Gump Director’s Office 9:30 Return to Sheraton Monday, July 9 6:45 Pickup at Sheraton 7:00-7:45 Breakfast – Gump Station 7:45-11:45 Field Trip (Departing Gump Station; Review Team Dropped at Sheraton) 12:15 Pickup at Sheraton 12:30-1:30 Lunch – Gump Station 1:30-4:30 Research Talks – Library • MCR Programmatic Research Overview (Russ Schmitt) o Time Series Program (Andy Brooks) o Bio-Physical Coupling (Bob Carpenter) o Population & Community Dynamics (Sally Holbrook) o Coral Functional Biology (Pete Edmunds & Roger Nisbet) • Concluding Remarks (Russ Schmitt) 4:00-5:00 Grad Student/Post Doc Demonstrations – MCR Lab & Gump Wet Lab 5:00-6:30 Grad Student/Post Doc Hosted Poster Session/Cocktails – Library 6:30-7:30 Dinner – Gump Station 7:30 Return to Sheraton Tuesday, July 10 7:15 Pickup at Sheraton 7:30-8:30 Breakfast – Gump Station 8:30-12:00 Site Talks - Library • IM (Sabine Grabner) • Site Management & Institutional Relations (Russ Schmitt) • Education & Outreach (Michele Kissinger) • Network, Cross Site & International Activities (Sally Holbrook) 12:00-1:00 Lunch – Gump Station 1:00-5:30 Executive Session – Gump Director’s Office 5:30-6:45 Exit Interview - Library 6:45-9:30 Tahitian Feast & Dance Performance – Gump Station 9:30 Return to Sheraton Wednesday, July 11 7:00-8:00 Breakfast – Gump Station 8:00-12:00 Optional Field Trips 12:00-1:00 Lunch – Gump Station

i

ii Volume I. Program Overview

Table of Contents

Schedule for MCR LTER Site Visit…………………………………………………………….. i

Introduction…………………………………………………………………………………….. 1 Physical Setting and Major Environmental Drivers………………………..………………. 3

Programmatic Area Research Summaries……………………………………………………… 7 Spatially Explicit Time Series Program……………………………………………………. 7 Bio-Physical Interactions and Coupling…………………………………………………… 21 Population and Community Dynamics…………………………………………………….. 29 Coral Functional Biology……………………………………….………………………..... 41

Information Management……………………………………………………………………… 51 Objective…………………………………………………………………………………… 51 Data Acquisition and Processing…………………………………………………………... 51 Approach…………………………………………………………………………………... 52 System Architecture……………………………………………………………………….. 52 Database Interfaces………………………………………………………………………… 53 Future Directions…………………………………………………………………………… 54

Site Management and Institutional Relations…………………………………………………. 57 Site Management…………………………………………………………………………... 57 Institutional Relations……………….…………………………………………………….. 58

Education and Outreach………………………………………………………………………. 61 Education………………………………………………………………………………….. 61 Outreach…………………………………………………………………………………… 64

Network, Cross-Site and Collaborative Activities……………………………………………. 67 LTER Network Activities………………………………………………………………… 67 LTER Cross-Site Interactions…………………………………………………………….. 67 Other National and International Collaborations…………………………………………. 69 List and Brief Description of Collaborators and Organizational Partners……………….. 71

References…………………………………………………………………………………….. 77

iii

iv Introduction

The Moorea Coral Reef (MCR) LTER site was established in 2004 as an interdisciplinary, landscape-scale program to provide better understanding of the processes that modulate ecosystem function and structure of coral reefs, one of the most diverse and productive of all ecosystems (Muscatine and Porter 1977, Hatcher 1990). Coral reefs increasingly are being affected by perturbations that range from short term, relatively localized disturbances (where return to the original state is possible) to more chronic, widespread influences of shifts in climate that may fundamentally alter the ecosystem (Connell 1997, Knowlton 2001, Gardner et al. 2003, Lesser 2007). Indeed, coral reefs are thought to be especially sensitive to changes in environmental drivers associated with climate, leading to concern that climate forcing may cause sweeping, worldwide changes in this ecosystem in the coming decades (Knowlton 2001, Lesser 2007). Hence, a fundamental goal of the MCR LTER is to elucidate the mechanistic basis of change in coral reef ecosystems by (i) identifying major controls over reef dynamics and (ii) determining how they are influenced jointly by disturbance and climate. Such mechanistic understanding should allow more accurate forecasts of how coral reef ecosystems will respond to perturbations that operate across different spatial and temporal scales, which in turn can inform policy makers and resource managers.

The conceptual framework for the initial 6 years of the MCR science program is shown in Fig. 1; the components and initial research questions of our science program are described more fully in the next section, and a brief summary of our activities to ‘operationalize’ the framework is given in Box 1 below. While research by MCR investigators addresses each of the five core LTER focal areas1 (which will facilitate cross-site comparisons), we self-organized three broad but interrelated thematic areas that are internally integrated and informed by our time series program (Fig. 1). Briefly, the three areas that we are exploring are: (a) the interactions and coupling between physics and biology; (b) population and community dynamics; and (c) the functional biology of stony corals, the foundational group of the ecosystem. There are, of course, critically important linkages among these three thematic areas. Integration of our research program is further enhanced by a modeling and synthesis component intended to refine forecasts of long term change, to yield major conceptual advances, and to inform existing and produce new theory. Findings from our modeling and synthesis, process-oriented and time series activities will feed back to each other (e.g., long term projections become hypotheses) to make linkages among our science components both tight and dynamic.

General issues of scale and scale dependency connect much of our science program. Disentangling cause and effect relationships and forecasting responses of coral reef ecosystems require that we understand several types of scaling issues. For a start, most reef organisms have a bipartite life cycle and hence have demographically open local subpopulations that are connected to others via dispersal of early developmental stages. Many critical biological processes on the reef are influenced, for example, by the flow of fluid, and relevant hydrodynamic and oceanographic processes operate at spatial scales that range from the sub- millimeter to thousands of kilometers and temporal scales that range from milliseconds to

1 (i) Dynamics and control of primary production; (ii) population dynamics of key groups; (iii) pattern and control of organic recycling; (iv) pattern of inorganic input and nutrient dynamics; (v) consequences of disturbance.

1 decades. Further, it is imperative to know how results found at one space or time frame can (or cannot) be extrapolated to others. For instance, field experiments that explore such important regulatory processes as density dependence almost inevitably must be conducted at relatively small spatial (~ m2) and brief temporal (~ days to months) scales; furthermore, space almost invariably is substituted for time in such explorations of regulatory processes with the assumption that the underlying mechanisms operate similarly in both domains (Schmitt and Holbrook 2007). These illustrate the general problem in ecology of predicting, in this case, large-scale dynamics from small-scale processes (Chesson 1998). Often local scale interactions do not provide insight into regional scale processes, which has led to recent developments in scale transition theory (Melbourne and Chesson 2006).

Contemporary studies on coral reefs have underscored the wide array of spatial and temporal scales necessary to attain ecologically relevant understanding of coral community dynamics (Edmunds and Bruno 1996, Sebens et al. 1997, 1998, Murdock and Aronson 1999, Bellwood and Hughes 2001). They also have revealed the need to understand the functional linkages across levels of biological organization - from molecules to the ecosystem - as well as the nature of feedbacks across multiple ecological scales (Agrawal et al. 2007). An elegant example of this is provided by coral bleaching episodes, which can be evaluated best through studies operating at landscape scales (sensu Mittelbach et al. 2001) and spanning years to decades. Studies of the mechanistic basis of bleaching have revealed profound connectivity among the molecular and bio-physical aspects of photochemistry (Warner et al. 1999, Jones et al. 2000), the molecular genetics of the algal symbionts (LaJeunesse et al. 2003), the interactive effects of light and temperature (Hoegh-Guldberg 1999), and the bleaching pattern within and among colonies (Rowan et al. 1997). Thus, our LTER

Figure 1. The conceptual research program is designed to explore to the extent possible framework for the MCR LTER relevant functional, spatial and temporal scales.

Achieving our science goals also requires a sufficient understanding of important nonlinearities in ecological responses of coral reef ecosystems, and this broad theme is threaded through our science program. Understanding the causes and consequences of such nonlinearities as threshold responses and the nature of their reversibility (e.g., alternate stable states) are of great importance to ecology in general (Scheffer and Carpenter 2003) and to coral reef ecosystems in particular (Hughes 1994). The rapid phase transition from coral to algal dominance observed in some coral reef systems (Gardner et al. 2003) serves as a stark example [albeit one that appears reversible (Carpenter and Edmunds 2006, Idjadi et al. 2006)], and is just one of the potentially catastrophic state changes that are forecast to occur in this ecosystem during the present century (Kleypas et al. 1999, Knowlton 2001, Lesser 2007). In this general context, we also will explore how short term (pulse) disturbances interact with long term environmental forcing (press disturbances) to shape ecological responses in this ecosystem.

2 Box 1: Actions and activities MCR investigators, postdocs, graduate students and technical staff have taken to ‘operationalize’ our conceptual Science Framework (Fig. 1)

1. Time series Program: a comprehensive set of spatially explicit time series measurements was designed and implemented (during Year 1) to describe decadal trends in the reef ecosystem and forcing functions on a landscape scale. 2. Interdisciplinary Working Groups: MCR investigators, postdocs and graduate students self-assembled into three, interdisciplinary working groups to enhance collaboration and integration. 3. Process-Oriented Field Studies: a series of process-oriented field studies motivated by our initial focused questions have been initiated to explore gaps in our understanding of physical and biological processes and events that affect structure, function and dynamics of the reef ecosystem of Moorea; additional integration is achieved by focusing on common model systems. 4. Ecological Modeling and Synthesis: quantitative modeling approaches are being developed to address our focus on the biological basis for variation in performance of stony corals; additionally, a collaborative meta-analysis project has been initiated. 5. Information Management System: a web-accessible, EML-compliant information management system has been designed and implemented.

Physical Setting and Major Environmental Drivers

Moorea is located in the central south Pacific (17o30’S: 149o50’W), about 4,400 km south of Honolulu and 6,600 km southwest of Los Angeles (Fig. 2). The Moorea Coral Reef LTER site is the complex of coral reefs that surrounds the 60 km perimeter of the island of Moorea in the Society Islands of French Polynesia, 20 km west of Tahiti (Fig. 3). It is a small, triangular volcanic ‘high’ island (Figs. 3 - 5) with an offshore barrier reef that forms a system of shallow (mean depth ~ 5 to 7 m), narrow (~ 1 to 1.5 km wide) lagoons that encircle the island. The MCR site itself encompasses all of the area around the island bounded inshore by the shoreline and, except for certain oceanographic measurements, offshore by the 20 m depth isocline on the fore reef slope (Fig. 4). The site contains the three major coral reef habitat types (fringing

Figure 2. Location of Moorea in reef, back reef, and fore reef) and twin bays on the north the central south Pacific shore, all of which are easily accessible by small boat (Figs. 6 & 7).

The fore reef slopes rapidly to depths of several hundred meters, with substantial cover of stony coral (Fig. 7) growing as deep as 40 m. Moving shoreward from the crest of the barrier reef, the domination of the bottom by ‘pavement’ and comparatively small coral ‘bommies’ (patch reefs formed by coral) grades into rubble and sandy areas with much larger bommies that eventually

3 give way to dominance by fine sand bottom (Fig. 8). Coral grows right up to the shoreline (Fig. 6). Twin deep bays formed by two rivers bisect the north shore, and are a source for some non- marine organic and inorganic materials to the coral reef itself. These and smaller watersheds produced three to five passes in the barrier reef on each of the three sides of Moorea (Fig. 4).

Figure 3. False color satellite image of the triangular Figure 4. Outline of the island of Moorea showing shaped island of Moorea (left), 20 km west of Tahiti the offshore barrier reef (black line) that encircles (right), in the Society Island archipelago of French the island to form 1.5 km wide lagoons; blue Polynesia (north toward top) denotes the spatial extent of the MCR LTER Site

10 km

Figure 5. Aerial photograph of Moorea (looking to the Figure 6. View from above the Gump Research southwest) showing the steep volcanic topography, Station (lower left) to the northeast showing a narrow coastal plain and offshore barrier reef fringing reef next to shore, deep bay, shallow back reef (turquoise), crest of the barrier reef (white waterline), and the open ocean beyond

The reefs are in excellent condition and have been subject to relatively few natural disturbances in the last several decades, such as outbreaks of crown-of-thorns seastar (Acanthaster planci) in the 1970s, cyclonic storms in the early 1980s and in 1991, and some coral bleaching. The cover of coral (~ 50% live coral cover on fore reefs of the north shore) and abundance and diversity of reef fishes are high (~ 250 species of lagoon and fore reef fishes in our samples; the Moorea Biocode Project sampled > 600 fish species from Moorea). Reefs in this region have not

4 undergone a phase shift from coral to algal domination. Bottoms typically are dominated by corals in the genera Porites, Pocillopora, Acropora, and Montipora. Reef fishes have been subjected to moderately low fishing pressure, although large pelagic species are rare (presumably due to fishing pressure). The Territorial Government recently set aside large tracts of reefs around Moorea as Marine Protected Areas (where manipulative research is allowed).

Figure 7. MCR Co-PI Edmunds photographing Figure 8. A small work boat in the MCR fleet corals at 17 m on the fore reef for quantitative anchored in a shallow back reef area of Moorea analysis

Moorea also is ideal for our focus on the dynamics of a physically forced system. For example, with respect to local flow, ocean waters enter lagoons over the reef crest and exit through the passes in the barrier reef on each side of the island. Offshore wave climate is a major driver of current speeds within the lagoon. Swell prevails from the southwest in the Austral winter and from the north in the summer, resulting in seasonality in exposure of different sides of Moorea to large waves and high flows.

Because Moorea lies near an amphidromic point with respect to semidiurnal tides, tidal amplitudes are exceedingly small (~ 30 cm maximum). Except for strong El Nińo Southern Oscillation (ENSO) events, the Tahiti – Moorea area rarely is affected by strong atmospheric disturbances; analysis of a 16 yr time series indicated the Tahiti region had the lowest variability of sea level on daily, monthly and annual time scales of any of the localities examined in the tropical south Pacific (Bongers and Wyrtki 1987).

The climate in the Society Islands is tropical with two distinct seasons; a cooler (19/25oC low/high), drier winter between May and November (Austral winter) and a hotter (21/29oC low/high), more humid Austral summer from December through April. Rainfall (~ 230 mm/month) occurs principally during the Austral summer months although southeasterly winds blowing northward from the Antarctic during the southern winters can give rise to mara’amus, strong winds that bring much cooler temperatures and periods of intense rainfall.

Long term changes in at least three major environmental drivers associated with global climate change are predicted to have substantial effects on coral reef ecosystems (Smith and Buddemeier 1992). These include long term rises in sea surface temperature, ocean acidity (related to ocean [CO2]) and sea level. Both temperature and [CO2] strongly affect calcification rates of reef corals, and the mutualism between reef-forming coral and photosynthetic zooxanthellae breaks

5 down in response to several types of stressors, particularly temperature; coral death can occur when the stressor is extreme, repeated, prolonged or combined with another. Temperature varies on a number of time scales, and so can be both a pulse and press disturbance.

Another major abiotic source of pulse disturbance includes large waves associated with strong storms. Although Moorea lies outside of the Southern Pacific cyclone belt, it occasionally experiences the effects of strong cyclonic storms. In addition, storm waves damaging to reefs on Moorea can be generated as far away as the Antarctic Southern Ocean to the southwest and the Bering Sea to the north. Hence, decadal-scale climate phenomena such as the Pacific Decadal Oscillation (PDO) in the northern hemisphere and the Antarctic Oscillation (AAO; also called the Southern Annular Mode (SAM)) can influence the reef ecosystem in Moorea. Higher- frequency climate variation such as El Nińo Southern Oscillation (ENSO) events also cause pulse disturbances by, for example, modifying the strength of local trade winds and intensity of the Equatorial Counter Current.

Coral reef ecosystems are influenced by constituents in runoff, such as sediments, freshwater and nutrients, and changes in land use can become important press drivers on a local to landscape scale at Moorea. Other potentially important drivers associated with human activities include fishing; in Moorea most of the large pelagic fishes are rare, and removal of these top predators may have had cascading effects on the reef. Both predatory and herbivorous fishes on the reef also are exploited. One response by local institutions to this exploitation was to designate a network of Marine Protected Areas around Moorea.

There are, of course, important pulse disturbances that are biotic in nature. These include periodic outbreaks of the predatory crown-of-thorns seastar (Acanthaster planci) (Fig. 9) and various types of coral diseases.

Figure 9. A crown-of-thorns seastar (Acanthaster planci) foraging on coral in a lagoon on the north shore of Moorea

6 Programmatic Area Research Summaries

Spatially Explicit Time Series Program

Introduction and Overall Goals

Programs designed to detect changes in coral reef ecosystems face several significant challenges. Many coral reef organisms are extremely long-lived; corals and some reef fishes may live for several decades. As previously discussed, environmental drivers affecting coral reef ecosystems can operate across a variety of spatial and temporal scales ranging from millimeters to kilometers and minutes to decades. Finally, aspects of coral reef community and ecosystem dynamics may exhibit a strong degree of inertia. Data obtained from studies conducted on the Great Barrier Reef have shown that areas heavily affected by hurricane damage required as much as a decade before any noticeable recovery was recorded (Connell 1997), and our data suggest that the abundance and diversity of reef fishes may be relatively insensitive to all but extremely large declines in the underlying coral community (see Population and Community Dynamics).

The MCR Time Series Program has been designed specifically to: (1) measure long term trends in the physical environment and coral reef biota as a means of increasing our understanding of the mechanisms underlying those changes, (2) provide a contextual basis for process-oriented studies and (3) meet the needs for comparative analyses within the greater LTER network. Our framework stresses the close integration of repeated physical and biological measurements made across several spatial scales and levels of biological organization, building from the sub- organismal to the ecosystem levels. Specific components of the Time Series Program are detailed in Box 2.

Box 2: Major components of the MCR LTER Time Series Program

1. Climate time series data including solar irradiance, atmospheric pressure, wind speed and direction, air temperature and rainfall 2. Physical oceanography time series data on ocean temperature, conductivity, turbidity, PAR, wave height and direction, current speed and direction, concentrations of organic and inorganic nutrients and pH 3. Ecosystem function time series data, including rates of reef and water column-based primary productivity, fluxes of nutrients, bacterioplankton production rates, DOM remineralization 4. Community structure time series data, including rates of settlement / recruitment of corals and fishes; abundance and size/biomass of major reef constituents including heterotrophic reef microbes, phyto- and zooplankton, algae, scleractinian corals, herbivores and other major reef invertebrates and fishes

7 Description of the MCR LTER Time Series Program

Background: Given the wide range of spatial and temporal variability in the physical and biological processes described above and the great variety of taxa and physical processes that are tracked, we have designed a hierarchical sampling program. Depending on the taxon or process under investigation, the scale and scope of the measurements taken encompass a variable number of sites, zones, depths, or frequencies of sampling. The most spatially inclusive sampling includes three habitat types [fore reef (10 and 17 m depth), back reef, fringing reef] at two localities on each of the three shores of Moorea (Fig. 10). We have continued the ongoing time series sampling efforts we had in place prior to the NSF award. Regional scale properties (e.g., sea-surface temperature, subsurface Chl a concentration, regional surface currents) are estimated via remote sensing using existing satellite sensors. Biotic factors surveyed within quadrats or along fixed transects include aspects of (i) ecosystem function (e.g., primary productivity), (ii) community-level attributes (e.g., trophic structure, diversity), (iii) population-level characteristics (e.g., abundance, dynamics), and (iv) individual-based characteristics (e.g., demography, functional metrics). In addition to collecting standard climate data, other Figure 10. Schematic diagram of Moorea showing abiotic factors that affect reef organisms locations of major habitat types: fringing reef, back reef, are sampled repeatedly through time. reef crest, fore reef, deep water passes and bays

During the first three years of the award, we have refined our sampling protocols, deployed our full suite of physical oceanographic instruments and conducted biotic surveys. Results from the first five years of the program will be used to calculate the power of our analyses to detect temporal effects of varying magnitudes. If necessary, the sampling protocols will be revisited in the sixth year to make sure we can achieve the level of statistical power required to detect effects given a pre-determined level of α = 0.05 and a specified minimal detectable difference. These analyses will produce a ranking of abiotic factors based on their likely influence on biotic traits, and will inform our experiments to establish cause-and-effect and will provide parameter values for analytical models.

Basic Sampling Design: We have established one heavily-instrumented site and one less- instrumented site on each of Moorea’s three shores (i.e., 3 primary sites and 3 secondary sites). These six instrumented sites are in extremely close proximity (< 25m) to the fixed quadrats or transects where biotic surveys are conducted (Fig. 11).

8 Figure 11. Map of Moorea showing approximate locations of meteorological stations, physical oceanographic instruments, and biotic surveys

Measuring Trends in Climate and Abiotic Conditions

Our primary physical data collection focuses on factors known to influence coral reef ecosystems (see Table 1): temperature, light (including UV), nutrient availability, and water flow (primarily wave-driven flow). In addition, salinity, turbidity, availability of inorganic nutrients, and the hydrographic structure and variability associated with the water column seaward of the reef sites are followed. Although changes in water pH that affect coral calcification due to increased atmospheric CO2 are unlikely to be detectable over a decadal time frame (Kleypas et al. 1999), we do measure water pH periodically as part of our routine hydrographic time series sampling program.

Large scale observations of current and water mass variability come from satellite remote sensing of currents Figure 12. Climate data suggest that air (TOPEX Poseidon, ERS, altimeter satellites), temperature temperature has risen (top) and rainfall (AVHRR), and ocean color (SeaWiFS, MODIS). Data on has declined (bottom) over the past 30 yrs deep, ocean swell impinging on Moorea and synoptic at Moorea; source: Meteo France scale meteorological variability come from ongoing monitoring programs in French Polynesia (Fig. 12).

9 Publicly available data from SeaWiFS, MODIS and AVHRR satellite sensors are used to measure spatial and temporal variation in such biogeophysical variables as subsurface concentration of Chl a, light absorption caused by dissolved and detrital matter, particulate backscattering and Sea-Surface Temperature (SST) at the scale of Moorea and up to larger scales (e.g., Society Archipelago, French Polynesia, central south Pacific; Fig. 13). Observations of large scale processes and their variations can be compared to local observations to explore links among scales. The spatial resolution of the imagery is 9 km for SeaWiFS data and 4.5 km for MODIS. SeaWiFS data have been collected since 1997 and MODIS data since 2000.

Water temperature is measured continuously at 2 min intervals at three locations per site, 10 and 20 m Figure 13. Ocean color remote sensing for the detection of long term trends in global and regional surface chlorophyll a as on the fore reef and on the back reef, observed by MODIS; data represent an 8 day composite with 4 using Seabird Electronics SBE-39 km resolution; data: Maritorena thermistors (0.01° C resolution) deployed 0.5 m above the bottom for up to 6 months per deployment. An additional four SBE-39 thermistors (Fig. 14) and two Seabird Electronics SBE 37 SMP Conductivity, Temperature and Depth (CTD) Recorders are deployed on vertical mooring lines anchored to the bottom in depths of 20 m at sites LTER 1, 4 and 5. Additional thermistor strings are deployed in depths of 30 m at LTER 1, the entrance to the Cook’s Bay pass and in the center of Cook’s Bay. A SBE 37 CTD and a Wetlab FLNTUSB fluorometer to measure concentrations of chlorophyll a and turbidity are deployed on the fringing reef next to the Gump Research Station and in the middle of the Viapahu lagoon.

Arrays of benthic instruments are deployed at 10 m depth at all three primary study sites. These arrays include Seabird Electronics wave height sensors (SBE 26+) that sample wave spectra for 5 min per hour at a sampling frequency of 2 Hz (Fig. 16), and acoustic Doppler current profilers to record water flow over a 3 month deployment. Simultaneous measurements of wave heights and currents are critical given that strong flows on coral reefs and in lagoons are driven by waves. Measurements of photosynthetically active radiation (PAR) levels on the reef itself have been measured at the three primary sites since 2005 using Li-Cor 1400 hand-held underwater PAR sensors. Beginning in 2007, we will extend these measurements to all six sites. Water column hydrographic profiling (Fig. 15) and collection of samples to estimate inorganic nutrient concentrations occur quarterly at LTER 1, at a site 5 km offshore of LTER 1 and at several sites within Cook’s Bay.

10

Figure 14. A Seabird SBE-39 Figure 15. Daily time series of temperature (oC)- depth (m) thermistor deployed on a T-string line profiles along a transect from the base of Cook’s Bay to Avaroa Pass as measured by CTDs; data: Hench

Figure 16. Wave spectra incident on Moorea’s three sides; note seasonal asynchrony among shores; data: Washburn

11 Oceanographic instrumentation is complemented by collection of surface environmental data at a weather station (recording solar irradiance, atmospheric pressure, wind, temperature) deployed at the Gump Station and by additional meteorological stations maintained by the French weather agency, Meteo France, at locations on all three shores of the island. Beginning in August 2006, data from the Gump met station and the CTD deployed on the fringing reef next to the Gump Research Station have been streaming data in near-real time to UCSB. These data are made available to the general public via the MCR LTER website (http://mcr.lternet.edu).

Measuring Trends in Biological Attributes

Net Annual Primary Production of Reef and of Reef Phytoplankton: Primary production of the reef community is estimated using upstream-downstream respirometry (Fig. 17). These measurements are made across a 150-200 m transect from just behind the reef crest extending downstream across the back reef. Wave setup on the reef crest creates a hydraulic head that drives nearly unidirectional water flow across the back reef. This flow varies with tidal stage, with higher velocities during high tides.

Instruments (In Situ RDO Optode Oxygen probe/meter, Nortek Aquadopp ADP, Li-Cor 1400 with 4π sensor) are bottom mounted at the upstream and downstream ends of the transect. Changes in dissolved oxygen are measured at 1-min intervals for a minimum of 48 h (2 complete tidal cycles). Velocity measurements are made throughout the water column sampling at 25 Hz every 60 s. Scalar irradiance (PAR) is sampled at 1 Hz and averaged for each minute. This method assumes that the water column is mixed fully so that oxygen generated / consumed at the benthos is mixed evenly in the water column. Estimates of mixing at meter scales using Figure 17. Instrument array to estimate reef-based primary productivity high resolution temperature measurements indicate that this assumption holds during typical wave climate conditions. Oxygen concentrations also have to be corrected for diffusion across the air-water interface, which is driven primarily by concentration differences across the interface and the degree of turbulence at the surface. Small-scale turbulence estimates have been made using a SCAMP in order to derive appropriate exchange coefficients.

. 2 Rates of net community primary production in January 2007 varied from 3 to 4.5 gO2/h m under relatively low light conditions. Previous measurements during high light were three-fold higher . 2 (13 gO2/h m ). These rates are comparable to NPP values quantified for other Pacific reefs. Efforts that are just beginning are investigations of the relative importance of light and water velocity as modulating factors for reef primary production. We plan to take advantage of the

12 varying hydrodynamic exposure of reefs around Moorea to test the hypothesis that increased velocity associated with offshore wave climate increases rates of reef community production as a result of enhanced mass transfer across thinned boundary layers. This phenomenon has been demonstrated at smaller spatial scales (from 10s of cms to several meters), but it is not clear whether these flow effects scale-up to reef flat spatial scales. Using a multiple regression approach, we should be able to decompose the relative strengths of the effects of light and water velocity on community primary production.

Additionally, we are interested in studying how substratum composition and roughness affect the relationships between light, water velocity, and primary production. We plan to exploit differences in reef community composition and in substratum complexity around the island to address these questions.

Vertical profiles of primary production of water column Figure 18. MCR investigators taking communities are measured using standard 14C water samples off Moorea tracer/bottle techniques offshore, inshore and on the reef flat at LTER 1. Because measure of primary production can be temporally variable, we have been sampling at a higher frequency (e.g., multiple times per week each quarter) for an extended period to determine the optimal sampling frequency (Fig. 18).

Rates of Nitrogen Fixation: Coral reefs exhibit some of the highest rates of nitrogen fixation of any biological community. Because coral reefs typically are located in oligotrophic oceans, a potential source of nitrogen from fixers is considered to be important to reef community function. The majority of nitrogen fixers on reefs are cyanobacteria associated with algal turf communities. To estimate rates of nitrogen fixation on Moorea reefs, we deployed sets of coral plates on the back reef where they have developed an algal turf community similar to the surrounding coral substratum. Plates are 10 x 10 x 1.5 cm, cut from dead colonies of the coral Porites lobata, and are attached to PVC platforms and affixed to the reef at a depth of 1 to 1.5 m.

Rates of nitrogen fixation are estimated by collecting plates from the field and placing them in a sealed Plexiglas chamber (volume ca. 11 L) that incorporates a headspace of air. The chamber provides unidirectional water flow at velocities of up to 30 cm/s. Fixation rates are estimated at saturating irradiances using the acetylene reduction technique. After plates are sealed in the chamber, acetylene gas is injected into the headspace and gas samples are taken over a time course of 90 to 120 min and analyzed for the presence of ethylene in a gas chromatograph.

Abiotic and Biotic Controls of Reef Primary Production: Concentrations of nutrients (ammonium, nitrate, phosphate, silicate) are estimated in water samples collected when water column primary production is estimated. Fluxes of nutrients across reef transects are obtained from combining estimates of cross-reef flow (m/s), water depth (m), and nutrient concentrations

13 (kg/m3) to give nutrient mass flux (kg/s/m width of reef). Nutrient concentrations in the environment provide discrete estimates of nutrient availability. However, growth of many primary producers is related to nutrient availability integrated over time. Estimates of integrated nutrient availability can be reflected in the C:N and C:P ratios in tissues of primary producers. In 2005 and 2006, we obtained estimates of C:N and C:P of algal turfs and selected macroalgae from algae collected from fore reef, reef flat, and fringing reef locations. All nutrient and macroalgal samples collected were frozen to -80 oC, packed on dry ice and returned to UCSB for analysis by the Marine Science Institute’s Analytical Lab.

Heterotrophic bacterioplankton are essential to the recovery of dissolved organic matter (DOM) and regeneration of inorganic nutrients lost from the reef community. Bacterial production estimates are elevated compared to the open ocean and large temporal variability in bacterial production is likely linked to availability of reef DOM. Like others, we have found that bacterial production is elevated in interstitial spaces within corals (Carlson and Morris, unpubl. data), suggesting that corals contain regenerative spaces for nutrients. We sample bacterioplankton biomass, production as well as DOC and DON concentrations where and when primary production is measured. Estimates of Figure 19. A Synechococcus bacterioplankton biomass and production rates include coral cyanobacterium interstices, where samples are drawn using sterile syringes. DOM remineralization experiments (Carlson et al. 2002) are used to assess the magnitude of available organic matter and growth efficiencies of the heterotrophic prokaryotes at offshore, above reef and reef interstitial sites.

Temporal and Spatial Variability of Benthic Algae: We quantify the abundances of benthic algae at each of the permanent habitat/site combinations on a yearly basis to detect temporal trends and spatial patterns in abundances, especially between shores, that may result from differential hydrodynamic forcing across shores. Within each habitat, stainless steel poles are epoxied into the reef to mark the ends of five, 10 m permanent transects. Sampling locations (initially located randomly, but fixed over time, n=10/transect) are identified by stretching a marked cable between the poles and the percent cover of benthic algae is estimated in 0.25 m2 quadrats.

The most abundant component of the benthic algal communities in Moorea is algal turf. This diminutive, multi-specific assemblage covers from 10 to 60% of the substratum across all habitats and sites and indicates that herbivory is an important component of Moorea reefs that maintains algal communities in a very low biomass, high turnover state. Algal turfs are consistently abundant in the fore reef and back reef habitats where herbivory is high. Algal turf abundance is lower in fringing reefs. There are no strong differences in algal turf abundance among sites or shores with the possible exception of reduced cover at fringing reef sites on the southwest shore.

Macroalgae are less common and range in abundance from 5 to 30%. The most common macroalgal species are Sargassum mangarevense (Fig. 20), Turbinaria ornata, Halimeda minima, Dictyota bartayresiana, and Amansia rhodantha. Among the fringing reefs, macroalgae are most common at LTER 6. This might be related to freshwater and/or nutrient input at this

14 site. In back reef and fore reef habitats, macroalgae are most common at LTER 2 and 3 and generally have cover of <10% at other locations.

Crustose coralline algae often are found in areas that are most heavily grazed or in areas of extreme wave action (e.g., reef crests), and their cover ranges from 5 to 25% across all habitats and sites. They are most common on the fore reef where they increase in Figure 20. Sargassum mangarevense abundance from sites on the north shore (LTER 1, 2) to sites on the southeast shore (LTER 3, 4), and are most common at sites on the southwest shore (LTER 5, 6). These patterns may be related to hydrodynamic exposure as suggested by emerging patterns in the physical oceanographic data. These site/shore patterns are not evident in fringing and back reef habitats, where crustose corallines are most common at north shore sites (LTER 1, 2).

With only two years of data, it is speculative to draw inferences about any apparent temporal ‘trend’ in the abundances of benthic algal components. One exception might be the increase in macroalgal abundance (from 12 to 23%) at the deep fore reef location at LTER 2. This reef has been impacted significantly by Acanthaster predation on coral and the increase in reef substratum due to dead coral skeletons may allow colonization by macroalgae, at least in the short term. A similar pattern is evident at the shallower fore reef location at LTER 2.

Overall, benthic algae occupy a significant proportion of reef substrata and are dominated by algal turf communities. The relatively modest cover of macroalgae suggests that herbivory is high enough to limit the abundance of macroalgae at these sites. Increased abundances at sites near the northeast corner of Moorea are intriguing but not explicable at the current time. Patterns of abundance of crustose corallines indicate that they are most common on fore reefs of hydrodynamically exposed sites.

Temporal and Spatial Variability of Invertebrate Herbivores: Estimates of abundances of invertebrate herbivores are made along the same transects as the benthic algal abundances (1 m2 quadrats, n = 4 per transect) on a yearly basis. All herbivorous echinoids and gastropods are counted along with the corallivorous echinoderms Culcita novaguineae and Acanthaster planci.

Abundances of most herbivorous invertebrates are <1 individual/m2. The most common species are the echinoids Echinometra mathaei, Diadema savigyni, D. setosum, Echinothrix diadema, Echinothrix calimaris, and Echinostrephus aciculatus (Fig. 21). These species tend to be more abundant in back reef habitats, although E. aciculatus is most common at fore reef locations. Abundances of the herbivorous gastropods Trochus maculatus and Tectus niloticus appear to be most common immediately shoreward of the reef crest, outside our areas of sampling. Culcita and Acanthaster are rare enough that they have not appeared in our Figure 21. A Diadema sea quadrats. However, Acanthaster are seen commonly at some sites, urchin particularly LTER 2 fore reef habitats and LTER 5 on the back reef.

15 Community Structure and Dynamics of Coral Populations: Since 2005, scleractinians, macroalgae, crustose coralline algae, algal turf, and bare space have been photographed digitally and analyzed for percentage cover. Where coral cover is low, larger photo-quadrats are used. Based on data collected to date, the coral communities on the fore reef are dominated by Pocillopora and Acropora. Each of the five dominant genera appears to be translating site and shore effects in different ways (Fig. 22). Because taxonomic issues are still being addressed, our current exploration of response of species diversity to environmental change is being addressed at the genus level. As advances in coral taxonomy are made, we can refine our measures of species richness and evenness through a re-analysis of our archived digital photographs. Figure 22. Differences between 3 shores, 6 sites and 2 depths in the percent cover of 5 dominant genera of corals found on the fore reefs in Moorea; data: Edmunds

Functional Metrics of Coral “Vitality”: We are still working out important logistical challenges to quantifying physiological condition of several coral species using PAM fluorometry to assess the functionality of the zooxanthellae symbionts and detect temporal patterns associated with environmental changes. Analyses of our initial measurements suggest that short-term temporal variability in the signal, as measured over several days, is too great to extrapolate to longer term (e.g., among year or decadal scales) without a much more intense sampling effort. We are assessing patterns of coral settlement and recruitment at both of our sites on the north shore and at several locations throughout the lagoons using settlement tiles deployed annually for a duration of six months on the Figure 23. MCR investigator measuring a fore reef (at 10 m depth) and within the lagoons. We permanently marked Porites rus are initiating additional sampling of coral recruitment on the fore reef by deploying cotton line suspended by buoys and anchored to the reef bottom at a depth of 15 m at all six LTER sites.

We have sampled the physical attributes and associated fishes of ~80 permanently marked Porites rus colonies along the north shore every year, beginning in 2000 (for detail, see Holbrook et al. 2002a, b). P. rus represents one of the major patch-forming corals in lagoons of Moorea, and the sampled group includes a range in size and exposure to waves and current flow (Fig. 23).

16 Corals as an Archive of Past Climate Variability: Coral skeletons contain information about past climate variability in their density, fluorescent banding and isotopic and trace element content. We plan to use climate and environmental records gleaned from corals in Moorea, using established techniques, to estimate baseline climate and environmental conditions as a reference for current conditions. Coral records can help identify past bleaching events using the isotopic composition and fluorescence. Finally, the year of mortality for dead corals can be identified by matching features in coral records to known climate events. Because these measures are not subject to change over short time periods, we plan to initiate this work in the second three years of our funding cycle.

Temporal and Spatial Variability of Zooplankton: Zooplankton abundance, biomass (dry weight and organic carbon), and community composition are assessed at LTER 1, a site 5 km offshore of LTER 1 and at several sites within Cook’s Bay two or three times per year and opportunistically throughout the year. Samples are collected using plankton nets (333 µm mesh for macrozooplankton; 100 µm for microzooplankton) in deeper waters and diver-positioned pump samplers close to the reef.

Temporal and Spatial Variability of Reef Fishes: The abundance and sizes (to nearest cm) of coral associated fishes are assessed annually along 4 permanently established 50 x 4 m transects within three habitat types, fore reef, back reef and fringing reef, at each of the six study sites seasonally. In the summer of 2005, observations at the two fore reef sites on the north shore, LTER 1 and 2, were repeated three times at approximately one week intervals in order to compare the strengths of temporal and spatial variability. A cluster analysis based on the species abundance data obtained from all sites surveyed suggested that while there was a small amount of temporal variability between survey dates, it was not enough to mask the strong spatial patterns that were evident in the data. Fish communities surveyed on the fore reefs regardless of site or sampling date were more similar to one another than they were to communities surveyed in either back reef/lagoon or fringing reef habitats. Communities from fore reef sites on the southeastern and the western shores (LTER Figure 24. An orange-fin anemonefish 4, 5 and 6) differed from those on the north and and juvenile three-spot dascyllus on northeastern shores (LTER 1, 2 and 3). There was also their host sea anemone a clear pattern of separation between the fishes inhabiting fringing reefs and those observed in the back reef/lagoon areas, but these differences were not as large as those between those two habitats and the communities observed on the fore reef (Fig. 25).

Finally, we continue our daily quantification of larval settlement of planktivorous fishes to the habitat on the fringing reef adjacent to the Gump Research Station from mid-June through August, which we have done annually since 1993.

17

Figure 25. Results from a cluster analysis of the species abundances observed in each of the three habitats (Reef=fore reef, Lagoon=back reef/lagoon, Fringe=fringing reef) sampled at the six MCR LTER sites. The first number after the habitat designation refers to the specific MCR LTER site, and the second number refers to the sampling event. Fore reef sites on the north shore were sampled on three different occasions at an approximately one week interval. Different colors group unique habitat/site combinations into statistically similar groups. Data: Brooks

Box 3: MCR LTER investigators participating in the MCR LTER Time Series Program and their principal roles

A Alldredge Phyto- and zooplankton, water column 1o productivity, organic and inorganic nutrient concentrations G Bernardi Abundance and biomass of fishes, population genetics A Brooks Abundance and biomass of fishes, community dynamics of fishes C Carlson Microbial consortia associated with corals and reef benthos R Carpenter Reef based 1o productivity, abundance of algae and major reef invertebrates P Edmunds Abundance and size distribution of tropical reef corals R Gates Abundance and community dynamics of zooxanthellae J Hench Lagoonal scale circulation patterns S Holbrook Population and community dynamics, fish settlement D Lea Paleoclimatology J Leichter Island scale patterns of current and wave climates, internal waves H Lenihan Abundance and size distribution of tropical reef corals and reef invertebrates S MacIntyre Net water transport, boundary layer dynamics, flow-benthos coupling S Maritorena Large scale patterns in oceanographic and atmospheric conditions R Schmitt Population and community dynamics, fish settlement L Washburn Island scale patterns of current and wave climates S Williams Reef based 1o productivity, organic and inorganic nutrient concentrations

18 Table 1. List of variables included in the MCR LTER Time Series Program

Measured Variable Locations Primary Measurement Method Frequency of Sampling

Large Scale: Climate (weather) data French Polynesia Satellites & Met. Stations (Meteo France) Daily Remote sensing (TOPEX-Poseidon, ERS) daily predictions Tides French Polynesia Pressure sensors around Moorea 5 minutes every 30 minutes Regional surface currents French Polynesia Remote sensing (TOPEX-Poseidon, ERS) few days to weekly Sea-surface temperature French Polynesia Remote sensing (AVHRR) daily (when clear) Ocean color French Polynesia Remote sensing (SeaWiFS, MODIS) daily (when clear) Subsurface [Chl a] French Polynesia Remote sensing (SeaWiFS, MODIS) daily (when clear) Light absorption/particulate backscattering French Polynesia Remote sensing (SeaWiFS, MODIS) daily (when clear) Small Scale: Climate (weather) data Moorea – all sides Gump weather station, Meteo France 15 minutes Waves (offshore pressure) Moorea – 1 site/side Seabird (SBE-26) pressure sensors 5 minutes/hour over 6 months Flow (lagoonal and island wide) Moorea – 1 site/side Acoustic Doppler current profilers Every 5 minutes over 6 month period Water temperature Moorea – all sites Seabird (SBE-39 and SBE 37) Every 2 minutes Salinity Moorea – 1o sites Seabird (SBE-37) Every minute over 6 month period Turbidity Moorea – 1o sites Seabird (SBE-37) Every minute over 6 month period Chlorophyll a Moorea – N. Shore WetLab (FLNTUSB) PAR Moorea – 1o sites Seabird (SBE-37) Every minute over 6 month period pH Moorea – 1 site/side Standard pH meter Quarterly Dissolved nutrients Moorea –N. shore Field collection and laboratory analysis Quarterly POC Moorea – N. shore Field collection and laboratory analysis Quarterly PON Moorea – N. shore Field collection and laboratory analysis Quarterly Biotic: Growth Moorea – all sites length/weight measures Variable Abundance, (Age/Size structure) Moorea – all sites Transects Variable Settlement/Recruitment (key species1) Moorea – all sites Settlement plates, recruit transects Variable Coral cores Moorea – all sites Cores Once every 5 years Diversity (key groups2) Moorea – all sites Transects Variable Primary productivity - Upstream-downstream respirometry Reef Moorea – all sites Semi-annually Lab measurements of key groups Water column Moorea – all sites 14C tracer/bottle techniques Quarterly Reef cover Moorea – all sites Remote imaging (Satellite/aerial photos) Once per three years

19 20 Bio-Physical Interactions and Coupling

Introduction

Many of the features defining coral reefs are products of the interaction of biological and physical processes acting over multiple spatio-temporal and functional scales. For instance, corallum morphology is determined by the biological process of mineralization, together with physical forcing that can create flow-dependent colony shapes and pCO2-dependent mass accretion. Not only does the corallum have a profound effect on the coral success (i.e., polyps and colonies), but also corallum-level effects scale up to modulate reef-scale responses to environmental conditions such as light and water velocity. In this working group, we have brought together biologists and physical oceanographers to work collectively on bio-physical coupling, with the goals of elucidating the scale-dependency of bio-physical coupling. The bio- physical coupling group is exploring the scale-dependence of physical processes around the island of Moorea, focusing initially on waves and water fluxes and temperature characteristics at several scales. The research exploits key biological processes to test experimentally the nature and importance of bio-physical coupling in this system and in coral reefs in general. The research outcomes of this group have relevance to both the Coral Functional Biology working group, by defining the role of the environment on coral performance, and the Population and Community Dynamics working group, by identifying potential physical processes that drive the dynamics of populations and communities.

Overview

The effects of physical forcing on coral reefs are evident over a continuum of scales ranging

104 yrs from small spatial scales and global climate rapid intervals (e.g., the 103 yrs change response of the zooxanthellae 100yrs basin scale variability photosynthesis and 10yrs El Nino Rossby community primary 1yr waves seasonal cycle production to changes in light mesoscale 1mon eddies and fronts levels caused by clouds 1wk coastal barotropic upwelling variability passing in front of the sun) to Time scale Time 1d internal tides surface tides oceanographic basins and internal waves 1 hr and millennia (e.g., global climate inertial motions

1 min vertical change). Although turbulent surface mixing gravity waves 1 s capillary categorical scales of waves molecular processes 0.1 s influence of physical factors 1mm 1cm 10cm 1m 10m 100m 1km 10km 100km 103km 104km 105km on coral reefs do not match Spatial scale Figure 26. A cartoon illustrating the relationship between scales of space the continuum of effects and time over which physical processes affect the structure and function of observed (Fig. 26), we have coral reefs (after Hench, Dickey). Importantly, the natural world acts on generated a thematic a continuum from small distances (mm) and rapid intervals (seconds) construct for the purpose of (lower left), to vast distances (1000s km) and great time scales (millennia) (upper right). We are using this relationship as a conceptual tool to studying bio-physical create a 3-domain construct consisting of (1) colony/local scale, (2) coupling in which three reef/seascape scale, and (3) island/regional scale, to facilitate progress in domains are defined: (1) forging links between the biological and physical processes driving coral reef structure and function.

21 coral colony/local scale effects, that act over centimeters to meters and occur within seconds to a year, (2) reef/seascape scale effects, that occur over hundreds of meters and occur within years to decades, and (3) island/regional scale effects that act over tens to hundreds of kilometers within centuries. A fourth domain, the basin scale (thousands of kilometers and millennia) also can be defined, but currently we are subsuming this into our island/regional scale (Fig. 26). Based on this three-domain construct, we have started to: (a) interpret our biological and physical data within domains of similar scale, and (b) identify links between biological and physical processes acting on similar or different scales.

Box 4: Key research questions within the area of bio-physical coupling that currently are being addressed by MCR LTER

1. What are the primary scales at which biophysical scaling acts to determine coral reef community structure? 2. To what extent do spatial patterns in coral, fish, and algal community structure map onto patterns of variation in physical oceanography? 3. What are the principal ecological and physiological mechanisms through which seawater temperature modulates coral recruitment and the success of individual coral colonies? 4. What are the interactive roles of predation and water flow in determining the success of early life stages of reef corals? 5. To what extent is spatial and/or temporal variation in larval settlement of reef organisms shaped by water flow and nearshore physical transport processes? 6. To what extent does wave climate modulate rates of mass exchange and metabolism of reef organisms and communities? 7. To what extent can spatio-temporal variation in the supply of zooplankton modulate the distribution and growth of suspension feeding taxa? 8. At what spatial scale are populations of Symbiodinium (“zooxanthellae”) structured, and how are the populations structured by flow regimes? 9. How do oceanographic, basin-scale processes affect the reefs of Moorea?

Figure 27. Underwater view of wave break on a reef crest off Moorea

22 Physical Processes

A central thesis of the MCR research program is that coral reefs are physically-forced systems. As part of our time series studies described above, the physical oceanographic setting within which the coral reefs in Moorea are located is being quantified. On an island scale, moored instruments record a variety of oceanographic properties (e.g., wave spectra, velocities, temperature, salinity). These data provide the physical oceanographic framework for transport and variability in physical parameters that impact these reefs. At the reef scale, more extensive instrumentation has been deployed (north shore) to elucidate the importance of episodic wave events in determining across-reef velocities, and in driving cells of circulation through the lagoon and out reef passes (Fig. 28). At a similar scale, high resolution temperature measurements at depth intervals have Figure 28. Wave spectra (top), across reef velocities (middle), and been used to quantify water flux up along channel velocities in the reef pass (bottom) associated with the slope of the fore reef. These flux lagoonal systems on the north shore of Moorea; data: Hench estimates are critical for quantifying dissolved and particulate nutrient subsidies to reef organisms (Fig. 29). At organism scales, several studies have been initiated to investigate the effects of small scale variation in temperature and water velocity on recruitment of corals, interactions between velocity, coral morphology and coral-associated fishes, and the effects of velocity and turbulence on the metabolic performance of reef organisms. Increasingly, our measurements of physical parameters are informing both our biological time series studies, and leading to the development of

Figure 29. Water temperatures on the fore reef (top) and in Avaroa testable hypotheses about the effects Pass; periodic excursions of colder water impinge on the deeper of bio-physical coupling across fore reef and may bring nutrient and particulate subsidies to reef spatial scales. organisms. Data: Leichter

23

Figure 30. (left) Seawater temperature recorded at two sites within the lagoon of Moorea (≈3-4 m depth), which were selected as representative of 10 sites scattered around the island. The loggers collecting these data were attached directly to the reef rock, and they record strong diurnal variation in temperature. (right) Coral recruitment to 10 x 10 cm tiles located at the same sites as those where lagoon temperature is recorded show strong among-site variation in densities. We are beginning to explore the role of variation in temperature in forcing (i.e., coupled with) rates of coral recruitment. Data: Edmunds, Leichter, Adjeroud

Biological Processes

Within the MCR LTER, analyses of biological processes are occurring in numerous sub-systems, with a wide diversity of taxa, and across multiple spatio-temporal scales. We next describe a subset of the studies we are pursuing to illustrate the broad range of research themes in the MCR.

An underlying approach for the MCR is to conduct time series and process-oriented studies

60 around the three sides of Moorea that experience different hydrodynamic conditions. The two years of time series 50 data show that there are differences in community 40 structure around the island. Our work focusing on the coral community structure shows that sites differ markedly % 30 within shores, without strong shore effects (Fig. 31), even 20 though multiple aspects of the physical oceanography vary

10 among shores. Similar patterns are beginning to emerge in the analyses of algal community structure and fish 0 1 2ABC3 4DE F5 6GH I populations. We also have started to examine the spatial NSESW Figure 31. Coral cover at 10 m depth distribution of symbiotic Symbiodinium (zooxanthellae), on the outer reef of Moorea based on and the results from this work will shed light on the photoquadrats recorded at the 6 LTER possibility of physical forcing of the genetic structure and sites (1-6, 2/shore), as well as three population connectivity of symbiont communities. other sites selected randomly along Specifically, we have photographed, collected and each shore (A-I) (mean ± SE, n = 40/site). A nested ANOVA reveals that extracted DNA from 185 corals representing 42 species there is no significant variation among and 15 genera collected at 2 depths at nearly all of our shores (P = 0.29), but strong variation time series sites. To characterize the Symbiodinium occurs at the level of sites (P < 0.01). populations in these corals, the Internal Transcribed We infer that biophysical coupling on Spacer Region 2 (ITS2) as well as the 23S large subunit of the spatial scale of sites is causing striking changes in the community the chloroplasts are being amplified, and shortly the work structure. Data: Edmunds will begin to clone and sequence this material to identify

24 the dinoflagellate symbionts. Together, data emerging from these integrated studies are providing the foundation on which several of the ongoing and planned process-oriented projects with the Bio- physical Coupling Group are built.

Examples of process-oriented studies at the smallest scale (colony/local) that are affected by physical forcing, comes from our analyses of coral recruitment

and seawater temperature, as well as the effects of Figure 32. Dark-adapted yield of Pocillopora meandrina exposed to simulated diurnal diurnal variations in temperature on coral fluctuations in temperature that are performance. Temperature loggers deployed in ecologically relevant for the lagoon of locations within the lagoon have revealed striking Moorea (Fig. 30). Importantly, for the two variation in seawater temperature that is matched by trials conducted, yield was suppressed in the differential rates of coral recruitment (Fig. 30). While experimental corals (open bars) to an extent comparable to that expected from a it is too early to determine whether these patterns are consistent (i.e., stable) temperature extreme related functionally, experimental analyses of the (shaded bars). These data suggest that coral effects of diurnal fluctuations in seawater temperature performance is coupled to diurnal variation reveal that they can have strong effects on coral in temperature. Data: Putnam performance, specifically photophysiology (Fig. 32). Working at a slightly larger spatial scale (at the interface of colony/local and reef/seascape), we have been investigating the extent to which the growth of juvenile corals is modulated by colony- and reef- scale variation in water velocities, zooplankton availability, and fish predation. Using a transplantation and caging experimental design, our studies have shown for Acropora elseyi that growth is highest: (a) on tops of bommies where velocities are greatest, (b) when predators are excluded, and (c) when zooplankton supply is high and predators are excluded (Fig. 33). Similar results have been observed in experiments conducted with other coral taxa (Pocillopora verrucosa and Acropora valida). This work provides a nice example of our Figure 33. Analysis of the growth of Acropora elseyi as a function of early-stage studies that are (a) habitat structure (on the seafloor vs. reef bommie), (b) caging, and revealing coupling relationships (c) location along a hydrodynamic gradient. The results demonstrate a between biological and physical strong coupling between growth and physical forces, with greatest processes. growth at high unidirectional flows but when fish predators are excluded. Corals grew less rapidly in areas with high wave energy and turbulence, even when fish predators were excluded. Zooplankton Members of our group have greatly enhance growth, but only when predators are excluded (not been gathering preliminary data shown in this graphic). Data: Lenihan, Brooks, Hench, Alldredge, on the delivery of zooplankton Monismith

25 at 6 sites across the back reef on the north shore as a function of flow velocity, and also on variation in zooplankton abundance with depth above the bottom. These data were gathered to determine if the magnitude of zooplankton flux impacted the growth of corals and food availability to planktivorous fishes. Additional impacts on the availability of food for other planktivores including fish may be inferred as well. Seasonal delivery rates at one of these sites also have been measured as part of the time series program. Using small plankton nets held horizontally over the reef at varying heights (Fig. 34), we have found that zooplankton abundance varies considerably across sites, and roughly is a function of flow speed (Fig. 35, exact flow velocity is yet to be analyzed). Companion analyses of coral growth rates have revealed that their growth is a function of the delivery rate of crustacean zooplankton. Interestingly, at a similar spatial scale, we have found the surprising result that zooplankton are greatly enhanced in the upper strata of the lagoon water compared to greater depths, even though the water column is ≤ 2.4 m deep (Fig. 36). This patchy distribution of zooplankton provides an intriguing Figure 34. Schematic of technique to estimate zooplankton flux dimension along which bio-physical coupling might greatly affect coral growth and performance. Additional research at the reef scale has demonstrated the combined effects of across-reef gradients in velocity and herbivory on carbon allocation in the macroalgae Sargassum mangarevense. These results suggest strong interactions between physical and biotic processes on the reef scale. We also have completed an analysis of the scale-dependency (m – km) of morphological plasticity in the coral Pocillopora verrucosa, with the results demonstrating that skeletal traits respond at differing spatial scales to the physical environment.

Currently the work of our group is only beginning to examine biological variation at the largest (and most challenging) spatial scale of island/ regions, although further studies in this domain are a clear goal of the next 3 years. Our initial efforts are focusing on the genetic analyses of reef fish and symbiotic Symbiodinium, as well as the remote sensing of biological phenomena (e.g., chlorophyll concentrations).

Medium resolution (1/24 to 1/12 of a Horizontal flux of zooplankton-day degree) satellite imagery is used to 150000 assess several physical and protoconchs biogeochemical variables at the 100000 eggs regional scale (~500 to ~2000 km) copepods around Moorea. Daily, weekly and 50000 other crustaceans

Number/m2/h other monthly estimates of sub-surface

0 chlorophyll concentration, colored P3 P4 P5 P6 P7 P8 dissolved organic material, Location particulate backscattering, PAR,

Figure 35. Mean horizontal flux of zooplankton across the back diffuse attenuation and Sea-Surface reef on one day in December, 2007. P3 was 5 m behind the reef Temperature are derived from crest and P8 was about 1 km behind the reef crest with other SeaWiFS, MODIS and AVHRR stations spaced intermittently between them; flow speeds data. The time series of satellite decreased from P8 to P3. Data: Alldredge

26 Horizontal zooplankton flux across the back reef estimates provide information number of zooplankton /m2 /h about the spatial and temporal variability of biogeochemical 25000 March 21,2007 March 27, 2007 variables and their covariations 20000 (coupling). They are also used to 15000 detect possible long term (decadal) 10000 trends in the oceanic waters in the 5000 vicinity of Moorea. These data

number of animals /m2/h of animals number 0 60 cm 115 cm 60 cm 115 cm 60 cm 115 cm 60 cm 115 cm should also be useful in assessing Site A Site B Site A Site B if and how the biogeochemical Mean Height of Net Above the Bottom state of the ocean influences reef

Figure 36. Availability of zooplankton at two heights above the sea responses and processes. We are floor in the lagoon of Moorea. Interestingly, more zooplankton is now also processing altimetry data found 1-1.3 m above the seafloor compared to 0.5-0.8 m above the to characterize surface current floor, thereby creating a context within which the performance of patterns and seasonal variability on suspension feeding organisms can be modulated by regional scales around Moorea. zooplankton/flow forcing. Data: Alldredge

Interaction with other working groups

The themes developing within the bio-physical coupling working group have a strong synergy with the time series core of the LTER project, as well as both the Population and Community Dynamics and the Coral Functional Biology working groups. The time series data are beginning to describe variation in corals around Moorea where sites differ more than shores, and community structure displays strong depth x site interactions. We believe these effects probably are manifestations of the effects of bio-physical coupling. Within the Population and Community Dynamics group, a well-developed theme is the analysis of trophic structure, and here there is a strong connection between velocity-dependent metabolism and carbon flux. Within the Coral Functional Biology group, it is clear that the emerging theoretical context created by combining studies of coral functional biology with a Dynamic Energy Budget (DEB) approach is both informed by, and interactive with, the physical environment at multiple scales. Although we only are beginning to identify the web of connectivity among these working groups and the Figure 37. An MCR investigator conducting dye studies to biological phenomena they represent, estimate water residence time within a Pocillopora coral it is clear that further explicit research in these areas will be productive.

27 Box : MCR LTER scientists affiliated with the Bio-Physical Interactions and Coupling working group and their principal interests († - faculty, * - postdocs, § - graduate students)

A Alldredge† Spatio-temporal variation in zooplankton A Brooks† Trophic structure of reef fishes, coral/fish/flow interactions R Carpenter† Dynamics of benthic algae; flow dependence of benthic metabolism P Edmunds† Coral population and community dynamics; physiological ecology of corals F Fram* Estimates of turbulence, reef metabolism measurements R Gates† Spatio-temporal variation in genetic structure of Symbiodinium in reef corals J Hench* Wave- and buoyancy driven circulation, reef scale physical oceanography J Leichter† Upwelling dynamics on reefs, lagoon/bay circulation H Lenihan† The interactive effects of biological and physical processes on benthic taxa S MacIntyre† Estimates of turbulence across the reef, reef metabolism measurements S Maritorena† Remote sensing from reef to basin scales M Maheigan§ Phenotypic plasticity in reef corals H Putnam§ Physiological response of reef corals to fluctuating temperatures M Stat* Genetic identity of Symbiodinium in reef corals S Talmage§ Carbon allocation in macroalgae across gradients in flow and herbivory L Washburn† Physical oceanography surrounding coral reefs S Williams† Nitrogen fixation in coral reef communities

Figure 38. Wave breaking over reef crest of Moorea Figure 39. Reef crest and a lagoon on the north shore of Moorea

28 Population and Community Dynamics Introduction

Compared with many other ecosystems, coral reefs have attributes that make them especially challenging to fully understand community dynamics. These include an exceptionally high biodiversity that potentially results in complex webs of interacting species and/or functional redundancy, and an unusually high occurrence of positive feedbacks in those webs that arise from the ubiquity of mutualisms in tropical systems. Coupled with these is another complicating factor common to marine ecosystems: reef species typically have complex life cycles where early developmental stages disperse in the plankton from the natal reef, which decouples local feedback on fecundity from local colonization of young but also connects spatially distributed subpopulations. The MCR LTER approach explicitly recognizes these challenges and our program in this area builds from one level of ecological organization to another. Our general aims are to: (1) elucidate the processes that shape population dynamics at local to landscape scales of major constituents of coral reef ecosystems, (2) evaluate the consequences to structure and function of important direct and indirect pathways in key webs of interacting species, and (3) explore issues related to the maintenance and consequences of diversity. Integration of our research efforts is facilitated by the use of common sets of model systems, which typically center on stony corals and associated fishes but also involve a wide array of other taxa (e.g., algae, sea urchins, zooplankton, and microbes). Box 6 gives our initial questions in this thematic area.

Box 6: Key questions in the area of Population and Community Dynamics currently being addressed by MCR LTER scientists

1. What are source localities of larval recruits to reefs at Moorea? 2. What are the causes and consequences of variation in settlement of reef organisms? 3. What are the causes and scales of spatial variation in strength of temporal density dependence? 4. What are the direct and indirect effects in webs of interacting species, particularly those involving mutualism? 5. How does habitat patchiness affect benthic–pelagic coupling? 6. What are the important feedbacks and flows of materials in the major reef sub-webs? 7. How does variation in the foundational group influence abundance and diversity of associated organisms?

Population Dynamics

Process-oriented studies conducted by MCR investigators in the initial three years primarily have focused on corals, reef fishes and to a lesser extent, algae. Presentation of our findings specifically for corals is brief here because many results on processes influencing their condition, abundance and dynamics are covered extensively in the next section (Coral Functional Biology). Data from annual photo-quadrats on condition and changes in colony size of several coral species (Montastrea curta, Acropora cerealis, Pocillopora verrucosa) will be used in size-based matrix models to project dynamics, and these projections will generate testable predictions and guide further process studies. Additional goals are to link the matrix models with physiological

29 analyses of such critical ‘life processes’ as the effects of temperature on calcification to create a mechanistic capacity to understand how changing environmental conditions will affect this foundational group, and in turn to project how changes in coral populations will affect the dynamics of other reef-associated species.

Because most reef species have a dispersing life stage, one of the most fundamental issues concerns connectivity among subpopulations, and the issue is drawing considerable attention by marine ecologists worldwide because of its ecological and practical importance. For coral reef fishes, for example, elegant models that couple models of ocean currents with important biological features (e.g., larval duration, swimming behavior) have provided insight into possible distances larvae travel to successfully recruit, although these ‘dispersal kernel’ estimates remain untested.

Our approach is to use powerful genetic tools to more definitively identify source populations of larval recruits of reef fish at Moorea, and to obtain robust estimates of the degree and spatial scale of ‘self’ Figure 40. A recently recruited cohort of three- spot dascyllus on Moorea all showing an recruitment. We previously found evidence that uncharacteristic vertical body bar indicates long-distance dispersal can occur in species whose larvae have comparatively modest planktonic durations (~ 3 weeks). Our forensic genetic studies have revealed that in French Polynesia, there are two distinct clades of the three-spot dascyllus (Dascyllus trimaculatus). Although the vast majority (96%) of individuals have haplotypes that only occur in French Polynesia, a second clade is comprised of haplotypes from a widely distributed Pacific Rim group far from French Polynesia, suggesting that a small number of larvae from reefs a thousand or more kilometers away have occasionally colonized reefs on Moorea (Bernardi et al. 2003). Our more recent work provides some tantalizing preliminary findings regarding larval dispersal of this damselfish. DNA sequences of the mitochondrial control region were obtained for a sample of recruit and adult three-spot dascyllus (378 recruits, 225 adults). Adults show extreme genetic diversity on a local spatial scale, but for recruits, many individuals were identical to each other and several of those were genetically identical to adults on Moorea. This suggests that self-recruitment within Moorea could be common. In three instances, Figure 41. An orange-fin anemonefish with its tailfin clipped for DNA analyses new recruits from the same host anemone, collected on being returned to its host sea anemone; the same day, were genetically identical, suggesting program headed by Bernardi that genetically related individuals can recruit together. The probability of this occurring for a species with a dispersing larval stage is diminishingly small unless they have been retained on an extremely localized scale or they are much more resistant to mixing while dispersing than previously thought, regardless of how far they have dispersed. We are pursuing these possibilities.

30 We are using a second species of fish, the orange-fin anemonefish (Amphiprion chrysopterus), as a model system to ‘map’ the spatial scale of possible self-recruitment in Moorea using sophisticated genetic techniques. The project, a collaboration with scientists from CRIOBE, focuses on the single species of anemonefish in Moorea because it lives in a discrete microhabitat (the giant sea anemone Heteractis magnifica), and the entire population on Moorea numbers around three hundred adults so most or all can be sampled (we already have done about half of the island wide population). Work on genetic tags of other members of the genus was successful and we have collected extensive ecological information on this species at Moorea. We are using genetic tags to determine the actual level of migration of larvae and to complete a spatially explicit set of family relationships for the island. Once microsatellite markers for adults have been completed, we can infer patterns of relatedness from the degree of homozygosity; more importantly, we can analyze parentage of new recruits, thus allowing us to calculate the number and spatial pattern of self-recruiting individuals. This approach has the advantage of being simple, unambiguous and less labor intensive than other alternatives. We have extracted DNA from tissue samples of 151 adults, and amplifications were made for 20 microsatellite loci. All individuals were scored for 18 out of 20 microsatellites. Results of the project to date indicate a very strong excess homozygosity, a hallmark of inbreeding depression due to self- recruitment. We believe that our study will result in one of the best estimates of the spatial pattern and extent of self-recruitment in a reef animal with dispersing larvae.

Building from the issue of connectivity, we also are exploring factors that influence early recruitment of young, including those that shape rates of settlement2 and subsequent performance (survivorship, growth). 0.35 Preferred The larvae of stony 0.30 Neutral Avoided corals and reef fishes 0.25 use qualitatively 0.20 different types of cues 0.15 to locate a place on the 0.10 reef to settle. The Figure 43. A recently Coral Settlement Selectivity Coral Settlement 0.05 larvae of many species colonized coral 0.00 T. prototypum P. conicum Hydrolithon sp. L. insipidum P. onkodes Bare tile of coral must come in Crustose Coralline Algae Species physical contact with a chemical (a Figure 42. Larval settlement preferences of polysaccharide) contained within the cell Pocilloporid corals for five common species of walls of crustose coralline algae that induces crustose coralline algae and free space. Data are settlement and metamorphosis. By contrast, Manly’s α selectivity indices; the solid line indicates random settlement; dashed lines are 95% confidence larvae of reef fishes can use such gradient sensed cues as odor and sound to locate a site to settle. MCR researchers have found that coral larvae have a strongly non-random pattern of settlement among species of crustose coralline algae at Moorea, with very high selectivity for one alga (Titanoderma prototypum), no preference for some, and strong avoidance of other coralline species (Fig. 42). Survival and colony growth of the coral following settlement mapped directly onto the settlement preference rank (post-settlement performance was greatest on the preferred coralline and lowest on the avoided coralline species). This suggests that coral larvae use coralline algae to discriminate benthic space with very fine spatial resolution (cm scale) to locate the most suitable microhabitats for early post-settlement success. We have begun some

2 Settlement is the brief event when a pelagic larva or spore makes the permanent transition to the reef environment.

31 process-oriented analyses of coral larvae and their settlement behavior through our growing international collaboration with Taiwanese scientists from the Kenting Coral Reef ILTER site in Taiwan (see Network, Cross-Site and Collaborative Activities section below). The Kenting ILTER site offers unique opportunities to harvest coral larvae on a known and predictable schedule, and to work with them in a sophisticated aquaculture facility. Earlier this year, a small team of MCR investigators worked at the facility and completed preliminary experiments to test the effects of temperature on the response of coral larvae to settlement cues contained in coralline algae.

Our comparable work on planktivorous damselfishes (Dascyllus spp.) that dwell in branching corals revealed that the relationship between the rate of settlement and density of conspecifics already present on a coral was hump-shaped; experimentation revealed that with increases in resident density, the hump-shaped settler-resident function arises from a Figure 44. A recently tension between increases in a cue (emanating from conspecifics) that settled three-spot attract larvae to the coral and increases in aggressive interactions with dascyllus (Dascyllus trimaculatus) residents that reduce successful colonization of those larvae.

Of course, the delivery of larvae to a reef typically fluctuates tremendously in space and from one reproductive cycle to another. As input of young is one of the critical dynamical rates, we have sought to understand some of the bio- physical linkages that influence the supply of larvae (see preceding Bio-physical Interactions and Coupling section). Indeed, one of the paradigms for reef animals with dispersing larval stages is that fluctuations in the supply of larvae are the major driver of local adult dynamics. For reef fishes, a large number of studies have found density dependence in the survival of new recruits, suggesting that at least some of the variation in settlement resulting from a fluctuating supply of larvae is dampened, although the issues of when and how regulation occurs in reef fishes remains surprisingly contentious. The most detailed studies we have undertaken on these issues so far involve the planktivorous damselfish model system; larvae of Dascyllus species recruit to branching corals or anemones following a three week planktonic phase, survivors reach Figure 45. Histograms of current speed (left scales) at adulthood in one year and the fish can live five reefs on Moorea; monotonically increasing curve in each panel is the cumulative distribution (right). Gray up to about five years. Like most species, curves on the Cooks 0 panel are the generalized larval settlement of these species in a settlement – flow functions from Schmitt and Holbrook reproductive cycle is highly variable over (2002) for three damselfish species: YT is yellowtail relatively small spatial scales (< km). Some (Dascyllus flavicaudus), HB is humbug (D. aruanus), and 3S is three-spot (D. trimaculatus). Data: Washburn

32 of this variation is driven by nearfield current speeds. The three species show different relationships between flow speeds and settlement, permitting prediction of the relative intensity of their settlement at any particular site (Fig. 45). The 10 findings imply that differences in larval abilities in the anemone) 2 8 nearfield can result in distinctly different patterns of larval colonization among species, even in the absence of 6 other sources of variation. It also is the type of 4 covariance between an environmental feature (here current flow) and competition that promotes coexistence 2 in Chesson’s (2000) lottery model.

Three-spot Dascyllus Settlement 0 1994 1996 1998 2000 2002 2004 2006

(mean no. per 14 d pulse per 400 cm (mean no. per 14 Year Most of the marine species with dispersing larvae that Figure 46. Inter-annual variation in have been examined show tremendous fluctuations in average size of a settlement cohort of settlement intensity over longer time frames, and our three-spot dascyllus to a fringing reef model damselfish three-spot dascyllus (D. trimaculatus) on Moorea. Data were collected on is no exception. The annual inputs of three-spot the same reef using the same methods (except for 1994). Data: Schmitt and dascyllus young to their anemone nursery habitat varied Holbrook among years by an order of magnitude over the past 14 years at the same fringing reef (Fig. 46). However, the free-living adult populations of this species did not carry a signature of these highly variable recruitment pulses; abundances of adults in a lagoon population remained relatively constant while that in a bay population doubled over this same time period (Fig. 47). Temporal trends of adults mirrored those of the juvenile nursery habitat (anemones) (Fig. 48), suggesting that adult abundances are limited by the throughput of juveniles and not by a limited supply of larvae. Strong density-dependent mortality of juveniles has been verified experimentally.

300

Bay 8 250 Lagoon Bay Lagoon

200 6 reef) reef) 2 2

150 4

100 per 1280 m 2 (m (no.1280 per m 2 50 Anemone Surface Area Surface Anemone

0 0 Adult Three-spot Dascyllus Abundance Dascyllus Three-spot Adult 1992 1994 1996 1998 2000 2002 2004 2006 1992 1994 1996 1998 2000 2002 2004 2006 Year Year Figure 48. Temporal trends in abundance of Figure 47. Temporal trends in abundance of free- nursery habitat (sea anemones) for juvenile three- living adult three-spot dascyllus in a bay and a lagoon spot dascyllus in a bay and a lagoon population; population for ~ 3 turnovers of individuals data both panels: Schmitt and Holbrook

Biotic Interactions and Webs of Interacting Species

The ability to forecast population and community dynamics requires understanding of the manner by which species interact, and the great biological diversity of coral reef systems makes it imperative that we understand the indirect as well as direct effects that arise from biotic

33 interactions. Further, highly coevolved symbiotic relationships are common in this system and, in comparison with competition and predation, the influence of mutualism on the abundance and dynamics of organisms is generally less well studied and understood. Of course, the best-known mutualism on tropical reefs – the coral- zooxanthellae interaction – is central to the existence of the coral reef ecosystem (see the following section, Coral Functional Biology). MCR research has revealed there are a rich number of additional mutualisms that involve coral. For example, trapeziid crabs (Fig. 49) gain shelter from their predators and in return certain species of the crabs are known to help defend the coral from its seastar enemies; we discovered that many trapeziid crabs remove sediment from their host branching coral Figure 49. A (Acropora, Pocillopora), which is imperative to the survival of corals in trapeziid crab areas prone to sedimentation (see Coral Functional Biology section). Our symbiont researchers also have discovered a completely new mutualism; tube- forming amphipods that associate with encrusting corals (Montipora) cause long finger-like projections to form. These provide shelter to the amphipods and their three-dimensionality helps protect the coral from its two major predators, the crown-of-thorns (COTS) and the pin cushion starfish (Fig. 50). In addition, our field studies of mutualisms are stimulating efforts in modeling and theory. For example, a study of a shrimp-goby mutualism at the MCR site led to development of models that explore the dynamics of mutualists with demographically open populations (Thompson et al. 2006); incorporating immigration in models of mutualisms is important because the majority of aquatic and many terrestrial organisms disperse from natal sites during at least one life-history stage. The models by Thompson et al. (2006) demonstrated that the consequences of immigration for the dynamics of the mutualists depend on which demographic rate is most strongly affected by the mutualism.

Figure 50. Left: Mean (± 95% CI) percent area successfully attacked on Montipora colonies with and without amphipod-induced fingers by crown-of-thorns (left) and pin cushion (right) seastars. Right: Photograph of a Montipora ‘finger’ formed by the presence of a tube-building amphipod (in feeding position at tip); data and image: Bergsma

34 Of course, webs of interacting species can frequently result in a species having an indirect positive (or negative) effect on another, and we are exploring sets of model ‘interaction webs’ in

80 this context. For example, juvenile three-spot dascyllus compete with orange-fin anemonefish

60 for shelter space on host sea anemones. The reef)

2 anemonefish is a strong competitor for space and 40 it can essentially exclude dascyllus from its

- 61 Fish + 41 Fish anemone host. However, this strong negative (no per 400 m 400 per (no 20 effect on dascyllus is offset by a strong indirect

Juvenile Dascyllus Abundance Dascyllus Juvenile positive interaction that counteracts about two 0 (- , 0) (- , +) (0 , 0) thirds of the competitive effect on dascyllus (Calculated) (Observed) (Observed) abundance (Fig. 51); anemonefish have a strong Treatment positive effect on anemone growth, which creates Figure 51. The separate effects of the direct more habitat space that is disproportionately negative and the indirect positive interaction with available to dascyllus. Thus the anemonefish is anemonefish on abundance of juvenile three-spot dascyllus; bars represent (left to right) the both a strong competitor and an indirect mutualist calculated abundance of juvenile dascyllus due with three-spot dascyllus (Holbrook and Schmitt solely to competition (- , 0), the observed 2004, 2005), and the indirect positive interaction abundance (mean ± 1 SE) when the direct enhances coexistence (Schmitt and Holbrook negative and indirect positive interactions both 2003). A similar example arises in the mutualism occurred (- , +), and the observed abundance (mean ± 1 SE) when neither interaction impinged described above involving amphipods that induce on dascyllus (0, 0). The downward pointing finger-like growth of encrusting Montipora coral; arrow represents the abundance cost due solely to small fishes shelter within the finger-like competition, and the upward pointing arrow the projections but they cannot associate with abundance gain due to the indirect mutualism; Montipora that lack the amphipod mutualist. Holbrook and Schmitt 2004.

Many positive (+,+) interactions on coral reefs are protection mutualisms, a class where models of mutualism reveal strong effects on dynamics when the partners have demographically open populations (Thompson et al. 2006). Predator-prey interactions can alter the benefits experienced by the mutualists. For example, planktivorous damselfishes (Dascyllus spp.) that shelter in branching coral enhance the growth rate of their host, and this benefit increases with biomass of fish associated with the coral (see following section, Coral Functional Biology). We found that once branching corals reached a sufficient size to harbor Figure 52. Arc-eye Hawkfish on a damselfish, about half had groups of damselfish and half did Pocillopora coral not. The young coral colonies that lacked damselfish instead were occupied by a single hawkfish (Fig. 52). MCR researchers found that predation by hawkfish prevents colonization of a colony via larval settlement. However, when branching corals reach larger sizes, they can be colonized by emigration of adult damselfishes, which hawkfish cannot consume. Thus, it is likely that predation on juvenile damselfish can indirectly harm branching coral when colonies are small, since the reduced group size of fish results in slower growth, thus increasing the period of time that the colony spends at a vulnerable small size.

35 Many reef organisms use reef structure as refuges from their predators, and competition for enemy-free space can be intense, giving rise to density dependent mortality. We used our damselfish model system (in this case, yellowtail dascyllus, D. flavicaudus, in branching coral) to explore the degree of

) 0.1 β spatial heterogeneity in the strength of temporal density dependence, together with spatial scale over which is varies and the underlying cause. Experiments revealed that the 0.01 strength of density dependence varied by more than an order of magnitude among six sites that all were within ~ 5 km, and the heterogeneity was well predicted by variation Per Capita Density Effect ( 0.001 in the local abundance of predators (Fig. 53). Although the 0102030 Predator Density predators strongly influence abundance of their prey, we 2 (no. per 500 m ) have no evidence that, at least on this spatial scale, yellowtail dascyllus have a Figure 53. Relationship between spatial variation in the strength of positive effect on predator temporal density dependence in abundance. This is another of a yellowtail dascyllus and in the density growing number of examples of their predators at an experimental that suggest weak or no site; error bars are 95% CI. Schmitt coupling in the dynamics of and Holbrook 2007 reef predators and fish prey Figure 54. A sand- (e.g., not a classical tightly coupled predator-prey interaction). In perch immediately Moorea, we have found that variation in local abundance of after capturing a predators is well predicted by heterogeneity in reef architecture juvenile yellowtail (which in turn is driven by the processes that affect distribution and dascyllus abundance of coral). This suggests there may be important trophic level interactions among predators and that the consumers of juvenile dascyllus may be selecting habitats based on protection from their predators rather than avail-ability of their prey (‘safety-matching’). This has important ramifications, particularly since top predators are frequently heavily exploited by fishers. These issues will be explored in the future.

Our studies of webs of interacting species also are helping reveal the linkages between benthic assemblages and processes in the water column. These studies arise naturally from the spatial patchiness afforded by the foundation species. Large colonies of corals such as Porites rus and P. lobata are especially abundant in the lagoons and on the fringing reef. They provide habitat for a wide variety of fish and invertebrates, and their distribution and abundance can be followed over time with satellite imagery (Fig. 55). The diversity and species composition of fish hosted by these structures are related to Figure 55. A remotely- sensed classification image of a lagoon on the north shore of Moorea; colors correspond both their size and structural complexity to particular habitat types; image classification: (e.g., Brooks et al. 2007). Occupants of Maritorena Porites and other large corals – and indeed the corals themselves - are linked trophically

36 to the water column via planktivory and absorption of nutrients (Fig. 56). They are also linked to the benthic community (algae, mobile invertebrates such as COT starfish, sea urchins, large crustaceans, etc.) via competition for space and consumer relationships. At all levels (benthos, water column, coral) microbial food webs engage in critical recycling processes and other important functions.

An aspect we are exploring concerns the scale of the interactions that link the water column and the coral- based community (Fig. 57). Preliminary studies of the water column in the shallow lagoons of Moorea reveal interplay between biological and physical processes. Recently-gathered zooplankton data indicate that their Figure 56. Patch-forming coral Porites rus horizontal flux was positively related to flow velocity, but there was a considerable degree of depth stratification, a novel finding for such a shallow lagoon environment (Fig. 36). The distribution of zooplankton in this shallow water column may result from a combination of zooplankton behavior (upward swimming) and/or consumption by zooplanktivores on the reef; passive particles did not show this pattern. On a slightly larger spatial scale, unique microbial communities are associated with sites offshore, in the lagoon, and in the interstitial spaces of branching coral. This pattern is consistent with a lack of mixing at this spatial scale, but it also raises interesting possibilities about spatial variation in microbial community function. Total cell counts for Bacteria, the SAR11 clade, and the unicellular cyanobacteria Synechococcus have been completed and a clone library is being constructed to identify unique microbial Figure 57. MCR investigator Alice Alldredge signatures associated with the different making a daytime plankton tow above coral communities.

To further integrate efforts, we have begun to focus on various aspects of structure and function using two more complex model food webs (Fig. 58); one contains major trophic linkages between the benthic and planktonic communities (coral – plankton –fish – predators – microbes), and the other is centered around benthic algae and herbivory (algae –grazers – predators - microbes). We will be exploring interactions among constituents, feedbacks within these sub- webs, and controls of structure and function. Our time series data will be used to inform some of these food web studies. For example, time series data indicate that abundances of bacteria and small crustacean zooplankton are lower in the lagoon than in waters offshore of the island, suggesting the possibility that a trophic cascade might be in effect, where microbial loop protists feeding on bacteria are released from predation by low zooplankton abundances in the lagoon.

37 zooplankton Fig 2: Proposed Grazing-based Foodweb phytoplankton Zooplankton Fish

Microzooplankton Detritus Microbes

Bacteria Herb. Inverts. Herb. Fishes Echinoids Scarids Gastropods Acanthurids Crabs Siganids ?

Detritus Turf Algae DEB model macroinvertebrates Algal turf Macroalgae

Light Nutrients Water flow

Figure 58. Two major sub-food webs that MCR investigators are focusing on to evaluate flows of materials, interactions and feedbacks among the constituents and linkages between structure and function. Left: The coral – zooplankton – fish – predator - microbe sub-web. Right: The algae – grazer – predator – microbe sub-web. We also will explore the nexus between the sub-webs.

Trophic Structure and the Maintenance and Consequences of Diversity We are collaborating with French scientists to establish the trophic structure of the fish assemblage in French Polynesia using stable isotope techniques (which represents the most extensive effort for reef fishes to date). Barcoding technology promises even greater resolution of food webs, 60 and we are in the early stages of collaboration with 40 scientists from the Moorea Biocode Project to analyze diets

20 of key consumer species. Our time series program will (number of species per plot) per species of (number Fish Species Richness

0 ultimately provide data to examine temporal patterns of 0 1020304050 diversity, particularly as the ecosystem undergoes 1000 plot) 2 disturbances and environmental forcing that affect corals, 800 the foundation group. MCR investigators initially have 600 focused on issues related to resistance and resilience of reef 400

200 fishes to changes in cover of live coral by coupling Total FishAbundance (number m of individuals per 500

0 experiments with surveys of large plots that ranged in cover 0 1020304050 of live coral from 1 to ~ 50 %. The results suggest that 1.00 total abundance, species richness and species composition 0.75 of the local fish assemblage varied nonlinearly with cover 0.50 of live coral (Fig. 59). The fish assemblage was relatively

0.25 insensitive to changes in coral abundance over a wide

Fish Taxonomic Similarity Taxonomic Fish 0.00 range, only declining precipitously when coral became rare 0 1020304050 Cover of Live Coral (< 5 percent cover). The same asymptotic relationship (percent of bottom) between fish species richness and coral cover was also Figure 59. Species richness, observed in a field experiment. Future research includes a abundance and taxonomic similarity of fishes in 500 m2 field experiment that tests the functional consequences of lagoon plots over the natural variation in species richness of corals to fish assemblages, range of live cover at Moorea; which is being initiated during 2007 in Moorea and Papua data: Holbrook, Schmitt, Brooks New Guinea by MCR and Australian scientists.

38 Box 7: MCR LTER scientists currently affiliated with the Population and Community Dynamics working group and their principal interests († - faculty, * - postdocs, § - graduate students)

T Adam§ Community ecology / fish ecology A Alldredge† Zooplankton population and community ecology R Beldade* Population genetics G Bergsma§ Community ecology G Bernardi† Population genetics A Brooks† Ecology of coral-fish interactions K Buenau§ Ecological modeling C Carlson† Microbial consortia associated with corals and reef benthos R Carpenter† Algal population and community ecology P Edmunds† Ecophysiology of tropical reef corals K Hanson§ Zooplankton community ecology S Holbrook† Population and community ecology H Lenihan† Effects of biological and physical processes on the success of coral recruits S MacIntyre† Net water transport, boundary layer dynamics, flow-benthos coupling S Maritorena† Marine optics and bio-optical modeling R Morris* Microbial consortia associated with corals and reef benthos R Nisbet† Dynamic energy budget modeling A Poray§ Algal population dynamics N Price§ Community ecology R Schmitt† Population and community ecology M Spitler§ Algal ecology H Stewart* Ecology of coral-invertebrate interactions; algal ecology L Washburn† Physical oceanography A Yau§ Population ecology

Figure 60. A patch reef in the back reef area of the Maharepa lagoon, Moorea

39 40 Coral Functional Biology Introduction

Even upon casual inspection, it is clear that a tropical coral reef is more than simply the sum of the parts. Thus, it is difficult, arguably impossible, to study the individual components and use the results to understand the function of the whole, yet typically this is the mechanism by which basic biological research is accomplished. The MCR LTER differs from this model by taking explicit steps to integrate results through a modeling approach embracing nonlinear relationships and feedback loops. Our goal is to understand how abiotic and biotic forcing functions affect the functional biology of corals, and to incorporate these effects into a model with the capacity to integrate the understanding of reef corals across spatial, temporal and functional scales. As a means to this end, we have started to apply Dynamic Energy Budget (DEB) theory to scleractinian corals, initially to understand coral colony-level functionality, but on a 3 to 6 year time frame, also to populations, communities and ecosystems. First, we are examining multiple aspects of the functional biology of corals with the goal of understanding how the flux of metabolites (C, Ca, and N) determines organism success in a physically forced environment. Second, we are developing DEB theory, extended largely from a mixotroph system, to model the empirical data derived from our studies of coral functionality. We plan to ground truth the model, test its predictive capacity against empirical data, and complete sensitivity analyses for the measured processes before scaling the organismic model to higher functional levels.

Overview

The biology of scleractinian corals is influenced strongly by their superficially simple design in which a diploblastic body plan is molded into a strongly three-dimensional structure that interfaces closely with a mineral skeleton of its own making. Nestled within the cnidarian cells, mostly in the oral endodermal layer, the symbiotic dinoflagellates provide many of the defining features of tropical corals, facilitating autotrophy with respect to carbon, greatly accelerating rates of mineralization, and creating the capacity both for tight nutrient recycling within the symbiosis, and nutrient scavenging from the surrounding water. There is growing evidence that microbial consortia greatly increase the capacity for mutualistic symbioses involving scleractinian hosts, creating for example, the capacity for nitrogen fixation either within the superficial mucous or even within the coral tissue itself. We are just beginning to explore these possibilities for corals in Moorea.

The classic features that define corals require access to biologically significant metabolites that must pass though multiple cell membranes and negotiate boundary layer dynamics at the outer margins of the organism. With such strong dependence on the transport and delivery of metabolites, and numerous potential pathways for feedback and metabolic cross talk between symbiotic partners, reef corals lend themselves well to modeling with a DEB approach, which classically places metabolite transport at its core.

41 We view DEB theory as providing a theoretical framework within the biotic domain created by the organismic biology of reef corals (Fig. 61). This domain incorporates the principal biological processes modulating coral success (e.g., symbioses with dinoflagellates and microbial consortia, growth rates, morphology, calcification, excretion, etc.), and in turn, this is modulated through interactions with the biological and the physical aspects of the environment. The principal tools of this interaction are agents of bio- physical coupling, including salinity, Figure 61. Conceptual model displaying the central role played the flux of metabolites, water by Dynamic Energy Budget (DEB) theory in unifying and motion, predation, etc. Some of the integrating advances in understanding the functional biology of major products of these interactions scleractinian corals. The aspects of functional biology displayed are the events that scale up to operate within a biotic realm defined by the organismic structure of corals, and all are unified through the common theme of population and community-level potential rate limitation through the flux of important metabolites processes. Together, the interactions such as C, N and Ca. The biotic realm of the coral organism among the coral biotic domain and interfaces with the abiotic and biotic realms of the environment, the environmental biotic/abiotic which in turn modulate organismic success through bio-physical domains, as well as the potential to coupling. DEB forms a mechanism through which organismic biology can be modeled to enhance both instantaneous and scale up to population and predictive understanding of corals, and importantly, creates the community level processes, illustrate capacity for scaling up to the analysis of populations and the strong interactions among the communities. On a 2 to 3 year time scale, we are concentrating working groups we have established on the development of the basic DEB theory at an organismic within the MCR. scale, then to scaling up our efforts on a 3 to 6 year time frame.

To illustrate our progress, here we first provide examples of studies of the functional biology of reef corals, and second, we present an outline of the DEB models that we are developing to utilize and build from the data.

Figure 62. The fore reef slope at ~ 8 m on the north shore of Moorea showing high cover and diversity of live coral

42 Box 8: Key questions in the area of Coral Functional Biology currently being addressed by MCR LTER scientists

1. How does seawater temperature affect the calcification rates of reef corals? 2. To what extent does skeletal morphology modulate the consequences of rising C02 on coral calcification? 3. How do temperature signals differing in magnitude and frequency of variation affect the physiology of corals? 4. How are tissue reserves of corals affected by thermal history, and to what extent do they affect the subsequent response to thermal stress? 5. What role does temperature play in determining the success of early life stages of reef corals? 6. How does bio-physical coupling between water flow, zooplankton supply, and predator availability, determine the growth and success of coral recruits? 7. How does the flux of energy determine the size of reef corals?

Functional Biology

Arguably the most significant feature defining reef corals and coral reefs is the ability of scleractinians to calcify at a prodigious rate. Although the ability for calcification is common to all scleractinians, regardless of their growth in warm or cold waters, it is only in the symbiotic corals that calcification rates are sufficiently fast to construct tropical coral reefs. Two of the leading physical factors (other than light) driving these high rates of mineralization are temperature and C02, both of which are expected to increase significantly with the effects of global climate change. We have begun to explore the effects of both temperature and C02 on the Figure 63. Growth rates (mg/cm2/d) of calcification rates of reef corals that are common Pocillopora meandrina (filled bars, red line) within the lagoons of Moorea. In these experimental and Porites rus (open bars, blue line) grown studies, the objective is to quantify the effects of in microcosms at eight different temperatures physical forcing on coral calcification, firstly to learn (mean ± SE, n = 3-5/bar). Curves are the best-fit, third order polynomials (R2 > 0.92), more about the basic biology of ecologically and show that both species have unusually important reef corals, and secondly, to improve our high thermal optima for calcification (≈29 ability to predict the response of coral reefs to climate o C) that probably are key to their success in change using appropriately-parameterized DEB the lagoon. Data: Edmunds models.

43 Using microcosms regulated for temperature and light levels, our group has been exploring the effects of eight temperatures on the growth (calcification) of the corals Porites rus and Pocillopora meandrina from the lagoon. For temperatures ranging from 25 oC to 32 oC, the

70 analyses are revealing strong

60 curvilinear responses with surprisingly o 50 high thermal optima of ≈29 C (Fig. 63). These results suggest that corals 40 in the lagoon are well adapted to 30 tolerate high seawater temperatures, 20 and indeed the thermal optimum is 10 considerably higher than cited 0 0 10203040506070 frequently for coral calcification (ca. o % Reduction in Length 27.5 C). Monotonic rises in seawater Figure 64. Effects of elevated pCO2 on the growth of temperature to high values rarely are Acropora hyacinthus (right), specifically to test the ecologically relevant on coral reefs, hypothesis that mass deposition and morphology (here, and in the lagoon of Moorea, strong linear extension) are affected unequally by rising pCO2. Preliminary results (left), showing the percentage change in diurnal variation in temperature also linear extension and mass deposition for four colonies (i.e., has strong effects on coral genotypes). Importantly, in 3 out of 4 cases, linear extension performance (described in the Bio- is more severely affected than mass deposition by rising CO2. Physical Interactions and Coupling Data: Muehllehner section). We also have been exploring the effects of rising C02 on coral calcification, specifically asking whether mass deposition can be traded against changes in morphology to mitigate the negative effects of rising C02 on the deposition of limestone. We have Massive Porites P. irregularis 0 designed lab-based experiments in 1.4 Ambient 1

- High 1.2 which manipulations of seawater pH 2 - 1.0 are used indirectly to alter carbonate 0.8 Growth 0.6 chemistry, and although the results are 0.4 preliminary, for Acropora hyacinthus 0.2 the results suggest that linear extension 0 ATAL ATLLLTAL LTLL ATAL ATLLLTAL LTLL is affected more severely than mass Pre-Treatment deposition by rising C02 (Fig. 64). Figure 65. Results of a microcosm experiment with juvenile This result is important as it suggests colonies of Porites and the branching coral P. irregularis that was designed to test the hypothesis that acclimation to “winter- that morphology may be an additional like” conditions can modulate the response to “summer-like” axis along which the effects of rising upward thermal stress. Corals initially were acclimated for 15 C02 can be manifested, with potentially days to four combinations of light (AL – ambient light, or LL – important consequences for low light) and temperature (AT- ambient temperature, or LT – morphology, strength, and rates of low temperature) before being exposed to high (31oC) or low (28oC) temperature. The initial acclimation conditions altered linear reef accretion. coral biomass, and importantly, for massive Porites (but not P. irregularis) also affected the response to thermal stress. In One important thrust of our research brief, exposure to ATAL conditions appeared to mitigate the has been to investigate the causes and effects of thermal stress, whereas exposure LTLL conditions consequences of the storage of greatly accentuated the effects. Data: Edmunds resources in coral tissue. This theme strikes at one central aspect of DEB theory - the size and purpose of food

44 reserves - which for corals is germane 1.5 16 A) Growth/Colony B) Growth/Colony Log Linear 14 on account of the well-known seasonal 1.0 12 -1 -1 10 0.5 -1 -1 variation in biomass (which is high in

8 0 the winter and low in the summer), and 6 mg colony d Log(mg colony d ) 4 -0.5 evidence that it also varies with age in o Cool (25.7 C) 2 Warm (27.6 o C) -1.0 0 juvenile colonies. Our work recently 0.2 1.4 0 1.2 has started to explore these effects on -0.2 1.0 -1 -1 -2 -0.4 0.8

-2 several fronts, first to test for the

-0.6 0.6

mg cm d effects of tissue thickness on the Log(mg cm d ) -0.8 0.4

-1.0 0.2 response of corals to summertime C) Growth/Area D) Growth/Area Log Linear -1.2 0 0.9 1 1.1 1.2 1.3 1.4 1.5 1.6 0 5 10 15 20 25 30 35 40 thermal stress, and second to Log(Diameter, mm) Diameter (mm) Figure 66. Results of a manipulative experiment that tested the determine whether temperature can effects of two temperatures on the scaling of growth in juvenile modulate scaling in juvenile corals colonies of massive Porites. Corals were grown at 26 oC (cool) o through indirect effects on biomass. In or 28 C (ambient) for 15 days and the scaling of growth (both the case of the response to summer mass per colony, upper panels, and mass per area per colony (lower panels) recorded. The results are presented both on log- thermal stress, manipulative log plots (left) and linear-linear plots (right) in order to illustrate experiments with small colonies of power scaling as straight lines (i.e., allometry) as well as in a massive Porites have shown that pre- format that is more readily interpretable. The important exposure to cool and shaded conditions outcomes are that (a) scaling of colony-normalized rates were can indeed modulate biomass and the unaffected by temperature, yet (b) area-normalized rates were inversely related to size at high temperature, but not low response to high temperature (Fig. 65). temperature. It is hypothesized that this effect is mediated by In terms of scaling effects, similar tissue thickness that is greater in larger corals; at high manipulations have shown that temperature oxygen becomes limiting in the larger corals and temperature can alter the mode of this depressed growth rates. Data: Edmunds growth scaling in juvenile colonies of

70 massive Porites, specifically by causing negative 1000 Intake Cost growth allometry at high temperatures, but isometric 60 Total expenditure

growth at low temperatures (Fig. 66). Finally, we also 50 500 have started to explore the roles of environmental 40 energy Daily conditions (including stress) in mediating the fecundity Count 30 0 of tropical reef corals and the investment of energy in 0 0.5 1 1.5 2 Biomass reproduction. Traditionally, these questions have been 20 challenging to address for reef corals as there are no 10 0 visual indications of reproductive condition that could 0 20 40 60 80 100 120 140 allow corals to be scored for reproductive condition. Surface area (cm2) To avoid this problem, we are exploring the possibility Figure 67. Fungia concinna in Moorea; the of developing molecular markers (e.g., patterns of gene size-frequency distribution of corals on the outer reef and (inset) the scaling of metabolic expression) that can be used to score coral colonies for costs (dashed line) and inputs (from reproductive status through the sampling of a miniscule autotrophy, solid line) as a function of size piece of tissue. Once developed, such a tool would be (biomass) (Elahi and Edmunds in press). extremely valuable in addressing the effects of Importantly, (1) the scaling data demonstrate environmental conditions on coral reproduction, and that inputs continue to increase with size, and thus are unlikely to limit the development of moreover, could serve an important role in resource this coral, and (2) the most common corals are management to assess quickly and easily the potential small enough that they do incur an energy for coral populations to replace themselves through shortfall, which may be causative reason for reproduction. intense selective pressure for rapid growth in small sizes. Data: Elahi

45

Our group also has started to address the flow of energy in reef corals, for example, in one study asking for the large, solitary, and motile reef coral Fungia concinna, whether the maximum size of the coral is limited by energy. This is an intriguing question to ask for corals, for in closely related actiniarians (Anthopleura sp.), there is strong evidence that the maximum size is dictated by the flux of energy. F. concinna, like all reef building corals, differs from actiniarians in possessing a calcareous skeleton and symbiotic zooxanthellae that create the potential for autotrophy with respect to carbon. In the case of F. concinna, we have found that the maximum size is not dictated by

Figure 68. Growth of Acropora elseyi as function of energy per se (Fig. 67), rather it is likely zooplankton availability and protection from predators. a function of other agents such as space Interestingly, while growth was enhanced by the supply of in the community and weight of the plankton, this effect was modulated by the presence of coral skeleton. The results of this study may predators, and in fact disappeared without the use of cages underestimate the extent of surplus to exclude predators. Data: Lenihan and Brooks energy, a potentially important supply of resources to microbial consortia and the entire reef ecosystem, because this work did not extend to a consideration of zooplankton. Our group is studying zooplankton availability extensively, and our initial results have revealed the complexity of interactions between zooplankton availability and coral predators in determining the growth rates of small corals (Fig. 68). In brief, for Acropora elseyi, growth rates are greatly enhanced by the availability of zooplankton, but only when the corals are protected from coral predators.

Members of our group have started to explore the ways in which reef corals interact with the reef community through both biological and physical mechanisms. One elegant example is provided by our analyses of the potentially crucial way that symbiotic crabs affect the health and survival of corals on tropical reefs; this research has demonstrated the importance of an association between reef corals and trapeziid crabs, which reduces the adverse effects of high rates of sedimentation (Stewart et al. 2006) (Fig. 69). A field experiment in which crabs were removed from two species of branching corals on a fringing reef resulted in 50 to 80% of those corals dying in less than a month; by contrast, all corals with crabs survived. For surviving corals that lacked crabs, growth rate was slower, tissue bleaching was greater and sediment load was higher. Laboratory experiments revealed that corals with crabs not only shed substantially more of the sediments deposited on coral surfaces, but also that crabs were most effective at removing grain sizes that were most damaging to coral tissues. The nature of this common symbiotic relationship has not been recognized previously, and its role in maintaining coral health is likely to become even more critical as tropical reefs worldwide experience increasing levels of sedimentation. An important implication of this work is that many aspects of the functional

46 importance of biodiversity on reefs are still poorly understood. Associated organisms (including fishes and shrimp) can provide nutrients to and aerate corals with their swimming and increase growth rates and asexual reproduction of hosts.

Branching corals such as Pocillopora eydouxi are common in the lagoons of Moorea, and like other such corals, P. eydouxi provides structural habitat for a variety of reef fishes; in turn, these fishes may augment the overall nutrient supply to the coral when sheltering. Thus, the interactions between branching

Figure 69. Analysis of the effects of symbiotic crabs corals and fish populations provide a tractable (Tetralia spp. and Trapezia spp.) on sediment system to investigate the role of interactions shedding by two common genera of reef corals. The between the biotic realm of coral colonies and symbiosis between the coral and crab greatly the biotic component of the surrounding increased the ability of the corals to reject sediment, environment, with the potential for physical thereby increasing chances of survival during periods of heavy sedimentation, notably during the austral forcing through modulation of the putative summer when heavy rains result in heavy sediment mechanism (concentrations of an important loading in the lagoon. Stewart, Holbrook, Schmitt metabolite, ammonium) by water flow. To and Brooks 2006). explore these interactions, we have conducted a field experiment to estimate the degree to which the presence of refuging damselfishes might accelerate the growth rates of P. eydouxi. Two pre-weighed “nubbins” of coral were transplanted into each of 20 mature conspecific colonies, and ten of these colonies were caged to exclude resident fishes. All nubbins were returned to the lab and re- weighed after 30 days. This experiment revealed that P. eydouxi with resident fishes grew significantly faster than neighbors that lacked them (Fig. 70). Further, the observed Figure 70. Results of an experiment to test the effects increase in coral growth rates was of fish on their host corals. Nubbins outplanted into significantly and positively associated with the Pocillopora eydouxi colonies containing fishes grew total abundance of sheltering damselfishes. significantly faster than those outplanted into colonies without fishes (P = 0.02). Shown is the average increase in weight over 30 d (± 95% CL) for each treatment. The magnitude of the growth stimulation caused by the fishes was associated positively and linearly with the number of fishes within each colony (P = 0.04, results not shown). Our analyses suggest that this effect is mediated by ammonium excreted by the fishes. Data: Holbrook, Schmitt, Brooks, Stewart

47 Dynamic Energy Budget Modeling

MCR has a diverse range of projects that focus on the physiology and population dynamics of corals and organisms with which they interact, on ecosystem processes on and near coral reefs, and on the physical environment. One priority, detailed above, is to develop a unified body of theory and a suite of models that can support individual projects and (more importantly) contribute to synthesis. We decided to use an approach that describes the flows of both energy and elemental matter within organisms and between organisms and their environment. This approach is generally known as dynamic energy budget (DEB) theory, though for our applications, the flows of key elements (C,N, Ca) play a larger role than energy. DEB theory offers a single framework within which to describe all of these. In brief, assimilated energy is stored, and then utilized for growth, maintenance and reproduction. Flow of elemental matter is calculated from knowledge of the stoichiometry of the components. Some recent extensions of the theory open the possibility of a rigorous treatment of adaptation and of evolutionary processes. We are aware of no previous research that has applied DEB theory to organisms with colonial modular design, but we know of no other formalism that allows consideration of the multi-scale feedbacks that operate on coral reefs.

The transition to colony dynamics is achieved through individual-based models with each “individual” (for corals, a polyp) described by a DEB model. This computer-intensive approach is practical, but there are also some simplifications that lead directly to representations of interacting populations through a system of differential equations (as in our prototype model – see below). Our models differ from traditional individual-based population models through the focus on fluxes of elemental matter, and are thus particularly appropriate for the study of symbiosis (e.g., corals and zooxanthellae), and of interactions mediated by microbial processes (e.g., corals and mucus).

We have developed a prototype coral-symbiont-mucus model, outlined in Fig. 71. Our immediate priorities are to use this for the following modeling studies:

1. Functional significance of changing zooxanthellae types. 2. Damaging effects of high irradiance. 3. Relating properties of microbial consortium in mucus to strength of mutualism. 4. Characterizing the impact of fluxes in and out of corals on trophic relations outside corals. 5. Impact of the reef community on corals.

Item 1 is our highest priority, with the model development being conducted in cooperation with related work at NCEAS that uses phenomenological models to predict the effects of zooxanthellae adaptation on coral response to temperature change at decadal scales.

48 Figure 71. Schematic representation of the prototype DEB model. The model has 6 state variables: the ambient ammonium concentration, mucus matrix (units to be decided), host reserves density and structure, symbiont reserves density and structure. The differential equations are derived using principles proposed by Kooijman. For stoichiometric specificity, ammonia is taken as the only inorganic nitrogen source and the sole mineral nitrogen product. In the diagram we use the symbol NH3 to cover all N fluxes, but known stoichiometry is considered when parameterizing the model. Similarly CO2 refers to the sum of carbon dioxide, carbonic acid, bicarbonate and carbonate and other carbon compounds. Organisms are considered to have a fixed surface area to volume ratio. Polyps grow in two ways: somatic growth and via asexual reproduction. Somatic growth leads to an increase in the size of the polyp; with this mode of growth the surface area to volume ratio declines as the polyp grows larger. Asexual reproduction via budding or fission leads to an increase in the number of polyps, which stay metabolically connected. With this mode of growth, the surface to volume ratio is approximately constant. Zooxanthellae are endosymbionts, implying that they do not interact directly with the ambient. Therefore we assume that the host controls all fluxes from and to the ambient, with the exception of photons. Zooxanthellae are encapsulated by two membranes, one of the host and one of the symbiont. This implies that both partners may have control of interspecies fluxes. We assume that both species fully control their internal fluxes and that only compounds produced in excess are exchanged with the partner. The work on DEB theory has wide ecological implications beyond coral reefs, and opens new possibilities for cross-site collaborations. It may also contribute to fundamental ecological theory by providing a route to empirical verification of important concepts that underpin the so- called “metabolic theory of ecology” (MTE). MTE approaches multi-scale phenomena starting from evidence of an allometric relationship between metabolic rates and organism size. Metabolic scaling has implications for population dynamics and ecosystem processes that are being explored for other systems within the LTER framework (e.g., session on MTE and Stream

49 Ecosystems at the 2006 LTER ASM), and many workers regard this as an important unifying approach in ecology. Yet the “universal” mechanisms assumed in MTE are hard to interpret in the context of coral reef communities, and there are alternative approaches to synthesis based on DEB theory. A rigorous study in this context will thus almost certainly have wider implications.

Summary and Future Plans

Our progress towards developing DEB theory for corals has only just begun, although as a group we are on our way to developing research initiatives to better understand key aspects of the functional biology of corals. Clearly, we have substantial hurdles to overcome before we have developed an effective DEB model, and to this end we are submitting a proposal to the NSF Advancing Theory in Biology (ATB) program. The principal goal of this proposal will be to finalize the development of the model, ground truth its efficacy using empirical data, and identify the significant gaps in understanding the functional biology of corals. Ongoing efforts within the MCR LTER can be used to address many of these issues, and will likely include studies of the effects of CO2 and temperature on coral performance, as well as a broadening of the taxonomic base of coral model systems, and additional funding will be sought for more specific studies. We see the emerging DEB theory as a diverse and powerful tool that can be used to unify our understanding of the reefs of Moorea by forming a theoretical framework bridging the investigative domains of bio-physical coupling with population and community biology.

Box 9: MCR LTER scientists affiliated with the DEB/Coral Functional Biology working group and their principal interests († - faculty, * - postdocs, § - graduate students)

A Brooks† Ecology of coral-fish interactions C Carlson† Microbial consortia associated with corals and reef benthos P Edmunds† Ecophysiology of tropical reef corals R Elahi§ Energy allocation and scaling in reef corals J Fram* Water flow, boundary layer dynamics, flow-benthos coupling R Gates† Molecular biology of Symbiodinium and reef corals S Holbrook† Population biology/fish ecology H Lenihan† Effects of biological and physical processes on the success of coral recruits R Morris* Microbial consortia associated with corals and reef benthos R Nisbet† Dynamic energy budget modeling S MacIntyre† Net water transport, boundary layer dynamics, flow-benthos coupling N Muehllehner§ Effects of carbon dioxide on the growth and morphology of corals J Padilla-Gamino§ Environmental effects on coral reproduction and expression of “reproductive genes” R Schmitt† Population biology/fish ecology H Stewart* Ecology of coral-invertebrate interactions

50 Information Management

Objective

The primary objective of the MCR Information Management System (IMS) is to facilitate scientific research conducted by investigators located at multiple universities. The goal is to design and implement tools for highly automated processing of data over their lifecycle from acquisition to archiving, and subsequent data access, ensuring security, integrity and consistency throughout the whole cycle. The system focuses on:

• Participation in network efforts to optimize scientific data management • Collaboration with other research sites • Support of trends toward increasingly interdisciplinary studies • Preserving data quality by providing comprehensive metadata formatted in the network metadata standard Ecological Metadata Language (EML) • Modularity of the IMS to easily integrate future site projects • Development of software tools (including GUIs) for automated post-processing of data collected in the field • Implementation of security measures

MCR LTER is part of an evolving information management environment within the Marine Science Institute (MSI) at the University of California, Santa Barbara (UCSB). Several scientists affiliated with MCR LTER are also affiliated with SBC LTER and the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO), and so there is a trend toward use of common protocols and data formats. The close collaboration of these projects allows IM personnel to more optimally allocate software, hardware and personnel expertise within the very diverse domain of information management. Outside of MSI, the IM team also collaborates with the Coral Reef Environmental Observatory Network (CREON), the LTER Network Information System (NIS), the LTER Network Office (LNO), and the National Center for Ecological Analysis and Synthesis (NCEAS).

Data Acquisition and Processing

MCR’s core data are broadly partitioned into three groups according to data acquisition and processing methods, with each requiring specific treatment:

• Manually collected population or ‘census’ data (photo imaging or hand written observations) • Samples and probes that are analyzed in the lab, such as chemical or genetic data • Physical parameters measured either by permanently deployed instruments or measured discretely in space and time

Census data are either collected directly by recording numeric values to data sheets or by analysis of images. Customized web forms to input observations recorded on data sheets into the site database were developed in cooperation with scientists and their teams. The web forms

51 replaced Excel forms, which allow inconsistencies. Chemical and genetic data are small in data volume but labor intensive. These data are stored in common formats such as Excel spreadsheets or the GenBank sequence database. Archiving of physical parameters is very straightforward compared to the rest. Data are recorded on a data logger in a well known format and can be machine harvested to the site database or file system. Since the volume of MCR LTER data is growing quickly, the way data are queried is more important in designing the backend. Each research group follows its own protocols and quality control methods. However, not all protocols are formally available yet.

Approach

MCR’s website has two basic portions: public and internal areas. The public web page (http://mcr.lternet.edu/) emphasizes LTER network membership and provides the site’s research objectives and derived information and products. Metadata can be explored and data downloaded or requested by the public under MCR’s data use policy (http://mcr.lternet.edu/MCRDatausepolicy.html). The internal website (https://mcr.lternet.edu/) provides resources for researchers and their teams. It is secured through an SSL connection requiring a site user account. The resources consist of links to internal data, lists and administrative tools for research boats and equipment, and travel information.

Most of MCR’s time series datasets have metadata described in EML. The current progress is shown in Table 2 below. Once storage of metadata is fully supported in the site database, it should be editable by scientists and the EML document shall be regenerated automatically. Currently EML documents are created using XML Spy, the software generously provided by LNO. The EML documents are archived at the metadata catalog Metacat at the LNO.

Relative Sampling Relative Storage Documented EML frequency Volume Datasets Documentation Level Census Data Low High 100 % 5 Samples Low Low 80 % 2-5 Sensor Data High Low 80 % 2-5 Table 2. Percentage of MCR time series data described in EML

System Architecture

The system architecture is a three-tiered design (Fig. 72), which is hosted by PISCO and relies completely on open source software. It consists of data storage, middleware, and application layers. The storage layer consists of an online storage array (file server) and a geospatial relational database (PostgreSQL), and an LDAP directory server that allows administration of user access to the system resources. The middleware layer currently consists of a Samba File Server, an Apache Web Server, and custom web applications such as PHP scripts. The application layer currently provides read and write access to the file server via desktop file- sharing clients and to the database via both web applications and Java applications with graphical user interface. Code implemented by the IM team is documented and under version control.

52

Figure 72. MCR LTER System Architecture

The UCSB research network infrastructure consists of a 1 Gigabit switched Ethernet backbone that connects departments and laboratories on campus. The MSI network internally maintains 100 Megabit switched Ethernet networks for individual workstation connections. The system architecture, described above, lives on three servers. The servers are protected against power outages and surges. The shared storage space is 4 Terabytes in both internal and external enclosures of which MCR produces 20 GB annually. The SCSI disks are configured as a RAID 5 array, which includes a hot swap failover disk. The backup system consists of a LTO-3 tape drive. The backup schedule follows a daily (level 9) and weekly (level 5) incremental scheme, with a (level 0) entire system backup once each month. The servers are configured with firewall and intrusion detection software to safeguard against internet-based exploits. The servers support Macintosh, Windows, and Linux/Unix client connections over HTTP, SMB, AppleTalk, and SSH protocols.

In collaboration with SBC LTER, a major focus of the data management system design was directed toward the design of a database schema for managing data and metadata. Data and datasets are independent in the schema. While dataset definitions will be stored in the relational database, the data may be stored in the database or on the file system. In the interest of cross-site usability and likelihood of acquiring new types of data, the database was designed to be extensible and easily maintained.

Database Interfaces

Currently, data are input to the relational database using web forms, Java desktop applications and Java programs harvesting data, triggered by cron jobs. Data are queried via an URL using the EML document ID and entity index.

Population data: Since population data in their raw form cannot be electronically analyzed or easily shared, they were highly ranked in terms of the need for development of database

53 interfaces. Customized web forms using common methods for error reduction and expedited data entry were developed with design input from MCR researchers.

The census images can be archived to the database by using a customized Java desktop application (http://mcr.lternet.edu/data/im/coralImageRenaming.php) which features both renaming of the images using date and location of image acquisition, and batch upload. Once the images are uploaded, they can be viewed online at http://mcr.lternet.edu/data/census/coralImage.php. If the percent coverage of corals was analyzed the results will show to the right of the image. The interactive page allows the user to select a date and location to query the data. To view full resolution images, the user is required to log in; by default the user will see images in lower resolution. Currently the availability of low resolution images is delayed but the software will be updated so that it will insert a lower resolution image automatically with the original image.

Sensor data: Currently only a few sensor datasets are being stored in the database. Since the data logger software does not support database connectivity, a cron job runs a Java program at the frequency of data acquisition to insert the data from a text file into the database.

Metadata: These interfaces are used exclusively by information managers. Further implementations and an extensive testing phase are required before they will be accessible to site scientists. This will be conducted in a prioritized, but incremental way with input from the scientific community. We expect the first results from this effort in the next year.

Future directions

Dynamic EML creation: A major advance will be generation of EML metadata documents directly from the database. In order to achieve this goal, the database needs to contain all commonly occurring metadata tags. Second, scripts for generating EML need to be implemented. To speed the process, we anticipate collaborating with LTER sites that have this ability. New interfaces will allow site researchers to augment and update their metadata.

Increase EML richness: Not all datasets are integrated into the IM system at the same level, particularly chemical and genetic data. We are prioritizing the upgrading of non level 5 metadata and the design of tools for managing those data. One initiative in upgrading EML will be to establish a standardized protocol library among major collaborators.

Network participation: MCR LTER has not submitted data to ClimDB yet but will follow up as soon as a data processing protocol is defined. The MCR site has submitted a number of datasets to the LNO Trends project.

Apply sub-setting tools: For users interested in temporal or spatial subsets of a dataset or only particular parameters, graphical user interfaces for selecting the options shall be provided. SBC LTER already has developed such tools for common datasets and we will modify these for use with MCR LTER datasets.

54 Online analysis tools: In order to benefit from the near real time analysis of data, the MCR LTER IMS will be augmented with online analysis tools based on several available software packages (such as R, SAS or Kepler).

Security: Server scripts will be revisited continually to ensure web security and add more documentation. While our current website provides excellent functionality in terms of user access, information dissemination and outreach services, we plan to redesign the site to take better advantage of more contemporary web development techniques. This will permit us to add to and modify the website more efficiently in the future.

55 56 Site Management and Institutional Relations

Site Management

Management of the Moorea Coral Reef LTER project encompasses governance, project resource acquisition and allocation, agency, university and public relations, communication with MCR LTER personnel, and day-to-day operations. As lead investigator, Russ Schmitt serves as the project’s primary point of contact with NSF, the LTER Network, and campus administrative units. In close cooperation with the three Co-Principal Investigators (Robert Carpenter, Peter Edmunds and Sally Holbrook) Schmitt also oversees day-to-day operations of the project and implementation of all its components. A half-time Deputy Director (Andrew Brooks) assists with all aspects of the project, and he also serves as the liaison between the project’s investigators and the Information Management team (Sabine Grabner and Beth O’Connor), the Education and Outreach specialist (Michele Kissinger) and various University committees (Diving Safety and Small Boat Safety).

Research direction, strategic planning of major tasks, initiatives, and policies are determined by consensus of an Executive Committee consisting of the four Principal Investigators plus three of the Associate Investigators (currently Alice Alldredge, Sally MacIntyre and Susan Williams). The Associate Investigators serve on the committee on a rotating basis; and to date, one replacement (Williams for Gretchen Hofmann) has occurred. The Deputy Director (Brooks), Information Manager (Grabner) and Education Coordinator (Kissinger) participate in the Executive Committee on an ex officio basis. The committee meets once or twice a year; minutes are archived on the MCR LTER internal server. In addition, some business is handled by email. During the first three years of the project, the Executive Committee developed and implemented several important policies regarding: (1) data access and sharing, (2) use of MCR LTER vehicles, boats and instrumentation, and (3) collaborative activities with groups outside the MCR LTER. These policies are posted along with the Executive Committee meeting minutes on the server, as well as in the appropriate locations on the MCR LTER website.

During the first three years of the project, research and resource allocation at the MCR site have been structured around groups of two to six investigators who each year receive funding to carry out long term trends measurements as well as process studies. Groups submit short proposals and funding decisions are made by the Principal Investigators; allocations are annual and specific decisions on expenditures within each group are made internally. All participating investigators are required to provide a brief annual update of their activities.

Information transfer among researchers of the MCR LTER site is crucial because individuals are located at six different universities, and considerable effort goes into maintaining open channels of communication and maximizing the input of all participants. Each year we hold a 2-day MCR All-Investigator Meeting at UC Santa Barbara, which is attended by approximately 30-40 MCR investigators, postdocs, graduate and undergraduate students and staff. Highlights of these meetings include research presentations by MCR graduate students and postdocs, as well as working groups for research synthesis and planning. The annual workshops were so successful that in 2006, it led to the grass-roots establishment of three MCR LTER science working groups: (1) Coral Functional Biology, (2) Bio-physical Interactions and Coupling, and (3) Population and

57 Community Dynamics that consist of students, postdocs and investigators (most participate in more than one working group). The goal of these groups is to enhance communication among MCR investigators, synthesize findings, and develop and plan research initiatives. The working groups meet several times per year and also communicate extensively through the use of email listservers. Any MCR LTER affiliated individual may be a member of one or more of the working groups.

The MCR LTER website is another valuable tool for communication with both MCR personnel and other entities. The website and data server are important vehicles for sharing project-related information, data and documents. MCR LTER research occurs at a distant research station in Moorea, French Polynesia, and our website provides researchers with valuable information regarding travel and research station logistics, visas, requirements for SCUBA and boating certifications, etc. We also use our website for communication with the public. We post announcements regarding MCR LTER activities, and recently we initiated our Marine Life of Moorea educational website, as well as a real-time display of oceanographic and meteorological data comparable to those displayed on the website of Santa Barbara Coastal (SBC) LTER.

Institutional Relations

The MCR LTER is administered by the UC Santa Barbara’s Marine Science Institute (MSI). The Marine Science Institute is an organized research unit (ORU) under the auspices of UC Santa Barbara’s Office of Research, overseen by Professor Michael Witherell, Vice Chancellor of Research for UCSB. Administration of the MCR by the Marine Science Institute greatly facilitates coordination with the three other University of California campuses involved in the project (inter-UC campus financial dealings are seamless), as well as with California State University Northridge and the University of Hawaii. Because five UC campuses are involved in the MCR (investigators from 4; field operations from the research station of a fifth), the MCR has direct communication with the system-wide University of California Office of the President (UCOP). UCOP Vice Provost for Research Lawrence Coleman and Director of Science and Technology Research Cathie Magowan give input on issues related to the operations of multi- campus research entities, development of MOU’s and international collaborations.

Field operations of the MCR LTER center at the University of California’s Richard B. Gump South Pacific Research Station on Moorea (http://moorea.berkeley.edu/). The Gump Station supports active research on terrestrial, freshwater and marine biology, geology, geography and anthropology/archeology, and several university-level field courses are taught there annually. The MCR LTER is a major client of the Gump Station and we enjoy a close and cooperative working relationship with Director Dr. Neil Davies, as well as with his staff. The Gordon and Betty Moore Foundation has provided exceptional infrastructure support to the Gump Station;

58 award of the MCR LTER in 2004 stimulated a new $2.5 million award for infrastructure needed to service the LTER and other research users. At the research station, MCR has approximately 1,200 ft2 of dedicated laboratory and office space plus a large storage facility. MCR researchers also have access to all of the additional station facilities (approximately 4,000 ft2) of laboratory and library facilities. In addition to station-owned equipment, field vehicles and boats, the MCR has its own trucks, small to medium-sized boats (8 total) and an extensive array of equipment and instrumentation, purchased primarily with a $1.4 million grant from the Gordon and Betty Moore Foundation (Vol. II Appendix VII).

The Gump Station has been operated by the University of California for two decades. The research station has been funded and managed by the UC Berkeley Campus since the mid-1980s, but it is currently undergoing a transition to a broader governance and funding structure. The UC Berkeley Office of Research will manage the station, a system-wide Advisory Committee has been established, and base financial support will be shared by several UC campuses and the UC Office of the President. MCR LTER Principal Investigator Russ Schmitt is a member of the Advisory Committee.

During the past several years, a streamlined procedure for application for scientific research permits in French Polynesia has been initiated by the Territorial Government. At the present time, all MCR investigators apply annually for a research permit that is issued by the Delegation for Research at the High Commission of the Territorial Government in Papeete; the Gump Station handles all of the paperwork. Upon receipt of a research permit, Figure 73. Oscar Tamaru, President of investigators can obtain at their nearest French French Polynesia, welcomes MCR LTER Co- Consulate the appropriate visa (depending on length th PIs Sally Holbrook and Russ Schmitt to a 4 and frequency of research visits) to enter French of July ‘Texas’ barbeque hosted at the Presidential Palace on Tahiti in 2005 to Polynesia. Students and technicians obtain their visas celebrate the inaugural flight of Air Tahiti using their supervisor’s research permit. Nui from Papeete to New York City.

59 60 Education and Outreach

Education

The Education activities of the MCR LTER include the training of undergraduate and graduate students and postdoctoral fellows. During the first three years of the project, we have engaged 8 postdoctoral, 26 graduate and 27 undergraduate students. The focus at all three levels of training is to involve students directly in the research activities of the program. Most of these participants conduct field work at the Gump Research Station on Moorea; some others work mainly in the campus laboratories of their advisors. Students of all levels are encouraged to attend the annual MCR All-Investigator Meeting (usually held in late fall at UC Santa Barbara), as well as other site activities, such as research seminars and the project’s ongoing interdisciplinary working groups.

Graduate students are pursuing M.S. and/or Ph.D. degrees, and they receive advanced training in field and laboratory techniques, including use of instrumentation, that are essential for completion of their projects. In addition, efforts are made to provide each graduate student with exposure to additional aspects of the project to enhance their scientific experience and provide multidisciplinary training. Senior investigators work closely with graduate students both in their home laboratories and at the field site. MCR LTER graduate students are encouraged to mentor less advanced students as part of their overall graduate training; several UCSB graduate students have received Worster Awards that support summer research of teams (each consisting of an undergraduate mentored by a graduate student). Graduate students are also encouraged to seek extramural funding and are mentored on proposal development; to date, MCR students have received funding from a variety of sources ranging from the American Museum of Natural History, the International Society for Coral Reef Studies, to the PADI Foundation.

Undergraduate students are also involved in every phase of MCR LTER research as participants in the REU program, as research assistants on investigator projects (both in the field and in campus laboratories) and as recipients of mentoring by graduate students, postdocs and investigators. Some of our undergraduates have graduated and are now pursuing advanced degrees.

In addition to education and training of U.S. students, we have initiated student and researcher exchange programs with two international programs: the Kenting Coral Reef ILTER site in Taiwan and the University of French Polynesia. Planning sessions during 2005 with the Lead PI of the Kenting ILTER (Prof. K.T. Shao) resulted in successful proposals to the OISE, NSF and federal agencies in Taiwan. In February 2007, MCR had its first graduate student exchange with the Kenting ILTER site. Three MCR graduate students and one of the Principal Investigators visited the National Museum of Marine Biology and Aquarium (NMMBA) in the Kenting National Park. They conducted laboratory experiments examining the behavior and physiology of settling corals, and did surveys at field sites of the Kenting ILTER. One of the graduate students is returning to southern Taiwan during summer 2007 to participate in the East Asia and Pacific Summer Institutes (EAPSI) administered by NSF. Dr. Fan, one of our Taiwanese collaborators, will visit the United States in August 2007, and plans to visit both UCSB and CSUN, and will spend a week working with one of our co-PIs in the Caribbean where he is

61 completing time series analyses of coral reefs with the support of the NSF-LTREB program. During 2008, Dr. Fan and several of his graduate students will visit Moorea to conduct research, and another team of MCR investigators and graduate students will return to NMMBA in 2008. As another important step in this collaboration, we are discussing plans to integrate our international efforts with Taiwan through a formal MOU arrangement that will tie CSUN, UCSB and the NMMBA in Taiwan.

Figure 74. Dr. Pete Edmunds (MCR Co-PI; seventh from left) and MCR graduate students Gerick Bergmsa (top), Nichole Price (sixth from left) and Hollie Putnam (fourth from left) participated in a collaborative exchange with Taiwan’s Kenting Coral Reef ILTER at the National Museum of Marine Biology and Aquarium (NMMBA) (http://eng.nmmba.gov.tw/) in March 2007. Their host, Dr. Tung-Yung Fan, is eight from left. Hollie Putnam will be returning to southern Taiwan this summer as a participant in NSF’s East Asia and Pacific Summer Institutes program to work with Dr. Fan.

The MCR LTER has also initiated a relationship with Dr. Patrick Capolsini of the University of French Polynesia to provide master's level students at his institution with opportunities to develop practical applications for the management and conservation of marine resources. Mathieu Vimont, the first student from the University of French Polynesia to work under this cooperative relationship between the MCR LTER, the Gump Station and CRIOBE, will focus on the development of a GIS database to store spatially explicit data relating to the newly established Marine Protected Areas around Moorea.

The MCR LTER project has taken steps to integrate research activities with undergraduate and graduate instruction. One means to achieve this outcome has been the Three Seas Program of Northeastern University, which is a year-long program in marine biology offering a 10-week section in Moorea. This program creates opportunities for several MCR LTER faculty to become involved as instructors as well as for MCR LTER graduate students to obtain field support (in Moorea) in exchange for employment as teaching assistants.

In brief, the Three Seas Program hosts up to 20 students at the Gump Station from January- March, during which instruction in coral biology, fish ecology, tropical terrestrial ecology,

62 physical oceanography, and independent study is offered. The objective is to train the next generation of marine biologists through exposure to multiple ecosystems (tropical south Pacific, southern California coastal, and New England subtidal), formal coursework, and hands-on fieldwork. Our ongoing efforts to develop strong links with the Three Seas Program have multiple advantages:

• The Three Seas Program provides opportunities for MCR LTER faculty to describe their LTER research objectives in an instructional environment, thereby both disseminating the goals of the project and creating an environment encouraging the involvement in LTER projects by undergraduate students. • The Three Seas Program supports travel and lab fees for faculty teaching in the program, thereby effectively representing leveraged funds that complement those of the MCR LTER project. • The Three Seas Program provides access to 20 students/year that are highly motivated in marine sciences, experienced in a diversity of ecosystems including Moorea, and anxious to obtain additional field experience. Such a pool of candidates provides a strong resource from which graduate students can be recruited to the research labs of MCR LTER faculty, and student labor can be directed to time-intensive tasks within the MCR LTER project. • The Three Seas Program provides opportunities for graduate students affiliated with MCR LTER faculty, who also teach within the Three Seas Program, to spend lengthy periods (10 weeks) in Moorea while working as a teaching assistant and completing their own research. During this period, graduate students are support entirely by the Three Seas Program (travel, food, lab fees, boats, etc.) and can expect to have approximately seventy percent of their time available for their own research.

One of the MCR LTER PIs (Edmunds) is integrally associated with the Three Seas Program through a lengthy commitment to instruction (he has taught their coral biology program since 1990) and service as the Chair on the Three Seas Advisory Board. Several other MCR LTER investigators and graduate students are involved with the Three Seas Program:

• Gates has been teaching with the program since 2004 and offers an independent module on the molecular biology of reef corals; one of her graduate students (Jackie Padilla) was supported as a teaching assistant for the Three Seas Program in 2007. • Leichter has a strong history of teaching physical oceanography in the tropics and teaches an independent module on physical oceanography in tropical systems; one of his graduate students (Kate Hanson) was a teaching assistant for the Three Seas Program in 2007. • Brooks began teaching with the Three Seas Program in 2007. He co-teaches an independent module on ichthyology and the ecology of coral reef fishes with Dr. Mark Steele of the California State University, Northridge. • Carpenter often presents guest lectures in the program; most recently during January 2007. • Hoffman teaches for the Three Seas Program, although her involvement takes place during the California portion of the program.

Findings of the MCR LTER are also being regularly used in the course training of undergraduates and graduate students by MCR LTER investigators. For example, a number of

63 undergraduate courses within the UC Santa Barbara Department of Ecology, Evolution and Marine Biology (EEMB 120, EEMB 142A, EEMB 142B, EEMB 152) incorporate recent research findings from the MCR LTER in their curricula. Teaching in the Three Seas Program makes extensive use of MCR LTER findings. Additionally, two graduate level courses at the UC Santa Barbara Bren School of Environmental Science and Management (ESM 260 and ESM 217) are focused on problems associated with coral reef management and restoration.

Outreach

The MCR SLTER education program has four main objectives: (1) to develop novel educational materials that focus on MCR LTER research and to curate an online library of existing K-12 lesson plans, curricula, etc. relative to coral reef ecology, (2) to provide opportunities to K-12 teachers to engage in hands-on activities at the Moorea field site and translate those into learning materials through supported professional development, (3) to identify and plan partnership opportunities with existing education programs on Moorea, and (4) to support public education regarding marine ecosystems in general and coral reef systems in particular. Below we describe accomplishments to date on these initiatives.

Ali Whitmer functioned as our Education and Outreach Coordinator for the first two years of the MCR program, and stepped down when she accepted a new administrative position at Georgetown University. Michele Kissinger is a full-time employee of the UCSB Marine Science Institute and she serves as the Outreach Coordinator for the MCR LTER. To assist with her professional development, Michele has been accepted into our Master of Science program in the Department of Ecology, Evolution and Marine Biology (Co-advised by Sally Holbrook and Russ Schmitt).

Development of an online education resource: Funds were used to develop an online encyclopedia of the Moorea Coral Reef ecosystem for use in various program components including public outreach, teacher professional development, educational materials development, and undergraduate research programs. The website is modeled on the successful ‘Encyclopedia of the Sanctuaries’ resource developed by NOAA’s National Marine Sanctuary program. The resource, Coral Reefs of Moorea (http://mcr.lternet.edu/education/index.php), is organized into four sections: background information about Moorea, the Encyclopedia, information about research, and resources for teachers. The Encyclopedia consists of individual pages about organisms found in the coral reef system of Moorea. Each card provides natural history information, photos, and video clips. The pages are organized into sections that include corals, other invertebrates, fish, and turtles. These sections are organized by habitat - the reef, water column, and lagoon. Students, teachers, and the general public can easily access information on their favorite organism, learn about new organisms, or navigate through habitats to learn more about the creatures that live there. The research section of the website hosts video clips of MCR LTER researchers describing their research projects for a general audience. The narration is accompanied by video of the field station and lab and underwater footage highlighting the research organisms and sites. The teacher resource section has been designed to host K-12 teaching resources including those developed by MCR LTER teachers as well as published coral reef ecology lesson plans.

64

Our online resource has been developed by web designers who have built the site for expansion. Professional marine photographers and videographers visited the MCR site and developed an extensive image and video database for current and future use. To date, 34 pages of the Encyclopedia along with 26 video clips are published. We have also published our first video interview of Co-PI Peter Edmunds. We are currently working to publish additional pages for the Encyclopedia and translate the resource from English into French and Tahitian, as well as to add additional teacher resources (such as lesson plans) to the site.

RET, Educational Materials Development and Lesson Plan Library: The MCR has supported one teacher through an RET supplement to engage in research and develop associated lesson plans. Kira Withy-Allen, who teaches at the University of Hawaii’s Outreach School, a K-12 public charter school on Oahu, Hawaii, was selected to participate in a research project in Moorea. She explored the interaction between anthropogenic and natural factors that affect the health and survival of reef-building (stony) corals, and the role coral symbionts (zooxanthellae and coral crabs) play in maintaining coral populations. Ms. Withy-Allen incorporated research findings into her revision of existing units on consumer-producer relations in ecosystems and the development of new units on symbiosis and anthropogenic effects on coral reefs. Ms. Withy- Allen also developed a portfolio of research projects from Moorea for an inquiry-based activity, where groups of students form “research teams” and are asked to devise experiments to answer questions MCR researchers are addressing. Research teams then compare their methods to those actually being used by MCR investigators. Ms. Withy-Allen is working on a digital ‘slideshows’ for students to better visualize the scientific methodology. She aligned her curriculum to 7th grade Hawaii State Science Content Standards and the National Science Standards.

We have recruited another teacher, accomplished in developing GIS-based lesson plans for use in middle school classrooms, to prepare a lesson plan based on Moorea’s coral reefs. She previously developed a lesson plan focusing on kelp forests. The proposed module will compare and contrast coral reef ecosystems with kelp forest ecosystems. This approach will facilitate the use of both modules in classrooms to support science content standards that focus on ecology and ecosystems as well as science inquiry standards.

MCR LTER also is building a relationship with Milken Community High School, located in Los Angeles, California, to provide science training opportunities for High School students and teachers. To date, we have engaged a high school student to use underwater photographs from Moorea in her High School science project to determine the role of asexual reproduction as Figure 75. A photoquadrat (0.5 x 0.5 m) from the a mechanism driving population dynamics in fringing reef in Moorea. The coral is Porites rus, the reef coral Porites rus (Fig. 75). The images and the image is representative of the data set that is being analyzed by a High School student.

65 are part of the MCR LTER Long Term Trends dataset.

Partnerships with Moorea Community Education Programs: The MCR LTER has been in contact with and begun conversations with the Gump Station Executive Director, Neil Davies, and Hinano Murphy, the coordinator of education programs for the local association called Te Pu 'Atiti'a. The Gump Station and Te Pu 'Atiti'a pursue common educational and research programs focused on marine and terrestrial biodiversity, traditional knowledge, culture, and the relationship between human societies and natural ecosystems. The MCR LTER program will work with Davies and Murphy to consider partnerships that will bring together LTER researchers and educators with local scientists, educators and residents to develop community- based education programs.

General Public Outreach Efforts: The MCR LTER has sponsored two public outreach activities - a coral reef exhibit at the UCSB educational aquarium (The REEF) and the Annual Santa Barbara Ocean Film Festival. The REEF is an educational aquarium that hosts school and community groups with guided tours focusing on the marine environment. A coral reef exhibit highlights ongoing research at the MCR LTER; this will undergo expansion in the latter half of 2007 with newly-awarded SLTER funds. The Santa Barbara Ocean Film Festival is a competitive filmmaking event developed to bring the finest ocean films from around the world to Santa Barbara for screenings. Films are entered in one of three categories: Marine Conservation and Biodiversity, Ocean Travel, and Ocean Adventure. The most recent year's event received nearly 200 film entries from 7 countries. The showcase film was ‘Coral Reef Adventure’ (IMAX MacGillivray Freeman Film), an award winning film about understanding and preserving the world's coral reefs.

66 Network, Cross-Site and Collaborative Activities

LTER Network Activities

During its first three years MCR has participated in a variety of Network activities. These include service on various committees and participation in research activities such as workshops and meetings as well as network level information management.

As Principal Investigator, Russ Schmitt has been a member of the Coordinating Committee (now the Science Council). Other MCR investigators are on network committees. Libe Washburn is a member of NISAC, and Sally Holbrook has just joined the Executive Committee. Several MCR personnel have been engaged in the LTER Planning process: Russ Schmitt and Sally Holbrook attended the Meeting of 100, and Bob Carpenter serves as the MCR site representative for the planning process. Ali Whitmer, MCR’s Education and Outreach Coordinator until December 2006, is leading the Education and Outreach aspects of the planning process.

A group of 13 MCR investigators and students attended the 2006 LTER All-Scientists meeting in Estes Park. MCR Investigators also attended the Ecosystem Services Workshop and the Long term Trends Workshop held at the 2007 LTER Science Council meeting in Portland.

MCR is involved in information management at the network level. Sabine Grabner, our Information Manager, is currently co-editor of LTER DataBits. Our site has contributed a number of datasets to the LTER Trends Project.

LTER Cross-Site Interactions

UC Santa Barbara is the lead campus for both the SBC and MCR LTER sites, and this provides many opportunities for synergism. Sally Holbrook is a Co-Principal Investigator on both projects, and six MCR Investigators (Craig Carlson, Hunter Lenihan, Sally MacIntyre, Roger Nisbet, Russ Schmitt, Libe Washburn) are participants in both projects. In addition, MCR’s Information Manager (Sabine Grabner) interacts closely with her SBC counterpart, Margaret O’Brien. As a result, there is extensive cross-site communication and interaction at many different levels. Graduate students and postdocs working at each site are co-mingled in some of the investigator’s lab groups. The sites sometimes participate in each other’s annual meetings; the next such event is planned for June, 2007, when all MCR personnel have been invited to attend SBC’s annual meeting. Because of the marine orientation and close physical proximities, graduate students and key investigators from the California Current Ecosystem (CCE) and Santa Barbara Coastal (SBC) will join students and investigators from MCR this for a graduate student symposium to enhance cross-site interactions and for community building; we anticipate this becoming a regular event.

Several types of collaborative and cross-site research also have begun. For example, Roger Nisbet, working with both SBC and MCR graduate students, is developing a suite of models to explore the dynamics of phase shifts in temperate rocky reef and coral reef ecosystems. Sally MacIntyre and postdoc John Fram, working with both MCR and SBC investigators, are conducting comparative studies of turbulence and benthic metabolism studies in SBC kelp

67 forests and MCR coral reefs. In the 2007 LTER supplements, we received funding for a cross- site socioeconomic project led by Hunter Lenihan and David Carr (from SBC), and for simultaneous website display of SBC’s and MCR’s online streaming oceanographic data (led by Libe Washburn).

MCR LTER is collaborating with an international group of scientists, including those from other LTER and ILTER sites, to develop sensor networks for data sharing in lakes and coral reefs, and to promote scientific research motivated by network-level science questions. Environmental observing science is undergoing dramatic changes through revolutions in information technology, including development and deployments of sensors, sensor networks, cyber- infrastructure and service oriented architectures. Researchers increasingly can form collaborative teams to address questions at larger scales than possible before by sharing expertise, resources and data without the barrier of distance. A grass-roots effort for lakes (GLEON, http://www.gleon.org/) and for coral reefs (CREON, http://www.coralreefeon.org) has been underway for approximately two years. The GLEON and CREON groups have met together approximately twice per year since 2004 to exchange findings and develop solutions for common problems and include several LTER (NTL, FCE, MCR) and ILTER (Kenting Coral Reef, Taiwan) sites. Sally Holbrook is a member of the CREON Organizing Committee, Andrew Brooks, Russ Schmitt, Robert Carpenter, Libe Washburn, Sally MacIntyre and Peter Edmunds have participated in one or more GLEON/CREON workshops. As part of this effort, several MCR LTER faculty have been working with senior scientists from Taiwan (Dr. T-Y Fan) and Australia (Dr. S. Kininmonth) to develop, and implement, a ‘proof of concept” biological study that can explore the utility of such a sensor network through a biologically significant experiment. The first iteration of this experiment – designed to test for biogeographic constraints on coral performance with regards to their response to temperature in Taiwan, Moorea and Australia (GBR) – is not partially in place. The major international partners for CREON are the Kenting Coral Reef ILTER site in Kenting, Taiwan, and the Australian Institute of Marine Science in Townsville, Australia. The Gordon and Betty Moore Foundation has provided major funding for the GLEON/CREON effort.

Figure 76. MCR Investigators participated in joint international GLEON – CREON workshops in San Diego, Townsville, Australia (left) and Hsinchu, Taiwan (right) to develop common research, sensor and cyber- infrastructure platforms. MCR Co-PI Sally Holbrook is a member of the CREON organizing committee. The Gordon and Betty Moore Foundation has provided major support for GLEON and CREON activities.

68

Other National and International Collaborations (a full list of partners and website addresses is given at the end of the document)

MCR is developing a collaboration with researchers at UC San Diego, particularly in Calit2 (California Institute for Telecommunications and Information Technology), and the San Diego Supercomputer Center. The underlying concept of this effort is to create a Digital Moorea, a dynamic, three-dimensional, (near) real-time visualization of physical/chemical data (e.g., current field around the island) gathered continuously by an extensive network of embedded sensors; biological data would be spatially mapped onto this dynamic representation allowing investigators to explore the complex interactions between the physical environment and biological communities. Components of Digital Moorea include the sensors and the local networking backbone, instrument and data management and data storage, data visualization, and a computational element (including linking data to models). Digital Moorea would serve as a model system that informs us as to how to develop and use a living laboratory in a networked, technologically advanced context. Several working meetings with key personnel were held in 2006. In May 2007, funding was provided by the University of California Office of the President for a set of workshops to develop linkages and formulate research plans. The first workshop was held at UC San Diego in May 2007, and included four MCR LTER personnel (Andrew Brooks, Sally Holbrook, Jim Leichter, Russ Schmitt) and 20 participants from UC San Diego units including the San Diego Supercomputer Center, Calit2, and Scripps Institution of Oceanography, as well as University of Queensland, San Diego State University, and the University of California Irvine (by videoconference). Two initial collaborative projects were identified: (1) a geographic visualization of Moorea and surrounding lagoons using several types of digital imagery (aerial and satellite imagery, bathymetry, digital elevation maps, etc.) and (2) design and implementation of an islandwide wireless network for transmission of data from deployed physical oceanographic sensors to the Gump Research Station.

We have initiated three different collaborations with investigators from the UC Santa Barbara School of Engineering. The first project aims to develop and implement technology for underwater acoustic communication; this will enable us to build a network for data transmission from our deployed oceanographic instrumentation. This work has been funded by the W.M. Keck Foundation. A prototype “AquaModem” has been developed by Ryan Kastner, Hua Lee, and Ron Iltis and tested in the laboratory. During summer 2007, a 5-member research team from Kaster’s laboratory will conduct the first ocean testing in lagoons at Moorea. In a second project, MCR LTER investigators (Alice Alldredge, Andrew Brooks, Sally Holbrook, Russ Schmitt) have been working with engineers in California NanoSystems Institute and Solid State Lighting and Display Center of the School of Engineering to develop bio-engineering solutions to address pressing marine conservation problems. With funding from the W.M. Keck Foundation, we already have developed and tested a potentially practical conservation tool at the MCR LTER site: a larval light beacon for rapidly enhancing diversity and abundance of depleted stocks of reef fishes. The light lures are constructed of arrays of GaN LEDs, an energy efficient, powerful light source whose wavelengths can be tailored. The third project involves development of DEB (dynamic energy budget) models of coral growth, reproduction and survival. Further devices are under development. The third project addresses modeling efforts for coral reef ecosystems. MCR Investigator Roger Nisbet and Frank Doyle of the Chemical Engineering Department have formed a seminar/working group of faculty (including SBC LTER

69 investigator Dave Siegel), graduate students and postdocs in theoretical ecology and systems biology that meets weekly. Doyle together with MCR Investigators Nisbet and Pete Edmunds are preparing a grant submission for the July 2007 deadline for the new NSF program Advancing Theory in Biology.

CRIOBE, (Centre de Recherches Insulaires et Observatoire de l'Environnement) is the French research station on Moorea operated by the French agencies EPHE (l’Ecole Pratique des Hautes Etude) and CNRS (Centre National de la Recherche Scientifique) and the University of Perpignan, France. Approximately two years ago, a working committee consisting of representatives from MCR, CRIOBE and the Gump Research Station was formed to increase communications and scientific inateractions. This committee meets twice per year. Several MCR investigators have formed individual collaborations with French scientists affiliated with CRIOBE. These include, for example, studies of coral biology (Peter Edmunds, Hunter Lenihan). In 2006, MCR joined a research effort that uses stable isotope analysis to examine trophic structure of reef fish assemblages in French Polynesia, in collaboration with Michel Kulbicki of IRD (Institut de recherche pour le Développement, France). His agency provided ship time and research funding for MCR Investigator Brooks (together with Dr. Jeffrey T. Williams from the Department of Vertebrate Biology of the Smithsonian Institution) to participate in a 2-week cruise to Mururoa Atoll, where extensive collections of reef fishes and other organisms were made. MCR is performing the stable isotope analyses on the collections. MCR participants on this project include Andy Brooks, Sally Holbrook, Susan Williams and Russ Schmitt. MCR has also initiated a collaboration with scientists from CRIOBE, the University of Florida, and Victoria University in Wellington, NZ to perform sampling to assess impacts of the newly-formed Marine Protected Areas on Moorea. This sampling occurs twice each year for a ten-day period and includes MCR graduate students as member of the international team; the program is planned to continue until at least 2010. MCR Investigator Andy Brooks is a member of the Moorea MPA Monitoring Consortium Executive Committee, which oversees the scientific and technical aspects of the project. MCR has also committed to aid in the data management and website hosting of the MPA datasets.

With funding from NSF’s OISE, MCR scientists and graduate students have begun what we expect to be a long term series of exchanges and scientific interactions with investigators and students from the Kenting Coral Reef ILTER site in Taiwan. Our first event was a joint MCR- Kenting Research Symposium held in Taiwan in October 2006. This was held at the National Chung Hsing University (N.C.H.U.) in Taichung, Taiwan. The symposium was sponsored by the Environmental Restoration and Disaster Reduction Research Center and the Department of Life Sciences at N.C.H.U., the Research Center for Biodiversity, Academia Sinica and the National Museum of Marine Biology and Aquarium. In March 2007, Peter Edmunds and MCR graduate students Gerick Bergmsa, Nichole Price, and Hollie Putnam visited the National Museum of Marine Biology and Aquarium (NMMBA) in the Kenting National Park. Their host, Tung-Yung Fan, an Associate Research Fellow at NMMBA, timed their arrival with the monthly spawning of several species of cultivated, brooding corals so that the harvested larvae could be used in several preliminary experiments examining the behavior and physiology of settling corals. A short publication describing the results of this study shortly will be submitted to the Biological Bulletin (Putnam, Edmunds, and Fan “The effects of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata”). Hollie Putnam will be

70 returning to southern Taiwan this summer as a participant in the East Asia and Pacific Summer Institutes (EAPSI) administered by NSF to work with Dr. Fan. We expect that during 2008, Dr. Fan and several of his students will visit Moorea to conduct research, and another team of MCR investigators and graduate students will return to NMMBA.

MCR Investigators Andy Brooks, Sally Holbrook and Russell Schmitt are collaborating with scientists (Geoffrey Jones, Phil Munday, Maya Srinavasen) from James Cook University, Townsville, Australia in a study of functional consequences of variation in diversity of foundation species (coral). Funding for the project comes from the Gordon and Betty Moore Foundation and the Australian Research Council. Installation of the first set of experiments occurred in Papua New Guinea in April 2007; the Australian Figure 77. Joint MCR LTER – Kenting Coral Reef ILTER team will spend a month at the Symposium participants at the National Chung Hsing Gump Station in June-July 2007 to University in Taichung, Taiwan, October 2006 initiate the experiment in Moorea.

MCR LTER Investigators Libe Washburn, Hunter Lenihan, and Sally MacIntyre interact extensively with Stephen Monismith and his research group from Stanford University. Monismith recently received NSF funding for a large study of lagoon circulation on Moorea.

List and Brief Description of Collaborators and Organizational Partners

Domestic:

Gordon and Betty Moore Foundation (http://www.moore.org/) The Gordon and Betty Moore Foundation provided $1,391,000 to UCSB for the purchase of start-up instrumentation for the Moorea Coral Reef LTER. Equipment includes boats, vehicles, oceanographic instruments and laboratory instruments.

In addition, the Gordon and Betty Moore Foundation provided $2,500,000 to UC Berkeley for facilities improvements at the UCB Gump Research Station on Moorea, the site of the MCR LTER. Improvements include a new laboratory building and housing.

W.M. Keck Foundation (http://www.wmkeck.org/) The W.M. Keck Foundation, in a $1,255,000 award to MCR LTER PIs at UC Santa Barbara, has funded a collaborative effort by marine scientists and engineers to develop and implement technological solutions to conservation problems on coral reefs. Funds have also been used to support the research of graduate students associated with the MCR LTER.

71 Bodega Marine Laboratory (BML), UC, Davis (http://www.bml.ucdavis.edu/) Bodega Marine Laboratory, UCD, provides research and administrative support to MCR LTER Associate Investigator Williams.

The Donald Bren School of Environmental Science and Management, UC Santa Barbara (http://www.bren.ucsb.edu/) The Donald Bren School, UCSB, provides research and administrative support to MCR LTER Associate Investigator Lenihan.

California NanoSystems Institute, UC Santa Barbara / UCLA and Solid State Lighting and Display Center, UC Santa Barbara (http://www.cnsi.ucsb.edu/) MCR LTER investigators are working with engineers in CNSI and Solid State Lighting and Display Center to develop bio-engineering solutions to address pressing marine conservation problems. We already have successfully developed and tested two potentially practical conservation tools: a larval light beacon for rapidly enhancing diversity and abundance of depleted stocks of reef fishes, and a type of larval flypaper to speed recovery of degraded corals on tropical reefs.

CalIT2 and San Diego Super Computer Center, UC San Diego (http://www.calit2.net/) MCR LTER has initiated a collaborative effort with Drs. Larry Smarr, Peter Arzberger and Tony Fountain to use the MCR LTER site as a test bed for development of “Digital Moorea”. This will include a dynamic, three-dimensional, (near) real-time visualization of physical/chemical data (e.g., current field around the island) gathered continuously by an extensive network of embedded sensors; biological data would be spatially mapped onto this dynamic representation allowing investigators to explore the complex interactions between the physical environment and biological communities. Components of Digital Moorea include the sensors and the local networking backbone, instrument and data management and data storage, data visualization, and a computational element (including linking data to models). Digital Moorea would serve as a model system that informs us as to how to develop and use a living laboratory in a networked, technologically advanced context.

Coastal Research Center, UC Santa Barbara (http://www.coastalresearchcenter.ucsb.edu/) Provides administrative and logistical support to MCR LTER affiliated researchers, students and staff.

Hawai’i Institute of Marine Biology (HIMB), University of Hawaii (http://www.hawaii.edu/HIMB/) The Hawai’i Institute of Marine Biology, UH, provides research support and molecular facilities to MCR LTER Associate Investigator Gates.

Institute for Computational Earth System Science (ICESS), University of California, Santa Barbara (http://www.icess.ucsb.edu/) The Institute for Computational Earth System Science, UCSB, provides research and administrative support to MCR LTER Associate Investigator Maritorena.

72 Marine Science Institute (MSI), University of California, Santa Barbara (www.msi.ucsb.edu) The Marine Science Institute, UCSB, provides IT/IM facilities support as well as research and administrative support to MCR LTER Associate Investigators Brooks and Whitmer.

Milken Community High School, Los Angeles, CA (http://www.milkenschool.org/splash.aspx) Milken High School facilitates high school science projects for highly motivated students. In 2007, student Sarah Robin completed an independent project analyzing images that are part of the MCR LTER long term trends data set.

National Aeronautics and Space Administration, NASA (http://www.nasa.gov/) NASA provides SeaWiFS and MODIS-Aqua ocean color data sets.

National Oceanic and Atmospheric Administration, NOAA (http://www.noaa.gov/) NOAA provides the SST data set from the NOAA AVHRR sensor network.

Scripps Institution of Oceanography, UC San Diego (http://sio.ucsd.edu/) The Scripps Institution of Oceanography, UCSD, provides research and administrative support to MCR LTER Associate Investigator Leichter.

Stanford University (www.stanford.edu) Stanford University provides research and administrative support to Jim Hench, Postdoctoral fellow with MCR LTER Associate Investigator Leichter.

UC Berkeley Gump Research Station (http://moorea.berkeley.edu/) The Moorea Coral Reef LTER is based at the UC Berkeley Gump Research Station on Moorea, French Polynesia. The UCB Gump Research Station provides logistical, administrative and research support to the MCR LTER.

UC Santa Barbara Aquanode Project (http://aquanode.ece.ucsb.edu/) The aqaunode project represents a collaboration between MCR LTER affiliated researchers and faculty, postdocs and graduate students within the UC Santa Barbara College of Engineering to design modem architectures for wireless underwater transmission of data collected by sensors; a key component to the development of WETNet (a subtidal Wireless Eco-surveillance Technology Network) and a critical hardware component of Digital Moorea. The AquaNode modem under development employs wideband Walsh/m-sequence signaling for resistance to multipath and narrowband ocean ambient noise, major constraints to the use of current underwater modems for shallow coastal applications.

73 International:

Australian Institute of Marine Science (http://www.aims.gov.au/index.html) AIMS (Australian Institute of Marine Science) continues to promote scientific exchanges and collaborative research involving the development and deployment of marine sensor networks.

Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Australia (http://www.coralcoe.org.au/) Investigators affiliated with the ARC Centre of Excellence for Coral Reef Studies and MCR LTER investigators are initiating a large field experiment to explore responses of reef fish assemblages to variation in coral species composition and abundance across a biodiversity gradient.

Centre d’ecologie tropicale et mediterraneenne (http://cbetm.univ-perp.fr/) Serge Plane’s lab at the Centre d’ecologie tropicale et mediterraneenne, University of Perpignan, France, provided laboratory and technical support to MCR LTER affiliate graduate student Marina Ramon and postdoc Ricardo Beldade in conjunction with their work focusing on the parentage analyses of the orange clownfish, Amphiprion chrysopterus.

CREON (http://www.coralreefeon.org/) CREON (Coral Reef Environmental Observatory Network) is a collaborative association of scientists and engineers from around the world striving to design and build marine sensor networks. Primary partners include the MCR LTER site, Australian Institute of Marine Science, the Kenting ILTER site and the NOAA sponsored Integrated Coral Observing Network (ICON).

CRIOBE (http://webup.univ-perp.fr/ephe/criobe.htm) CRIOBE (Centre de Recherches Insulaires et Observatoire de l'Environnement) is the French research center on Moorea operated by the French agencies EPHE (l’Ecole Pratique des Hautes Etude) and CNRS (Centre National de la Recherche Scientifique) and the University of Perpignan, France. Scientists from the MCR LTER and CRIOBE collaborate on a variety of projects, and each uses the facilities available at UCB Gump and CRIOBE.

GLEON (http://www.gleon.org/) GLEON (Global Lake Environmental Observatory Network) works closely with the MCR LTER and other CREON partners in a grass roots effort to develop an international environmental sensor network in lakes and on coral reefs. Activities include joint meetings and workshops, scientific collaborations, technology exchange.

IRD (http://www.ird.fr/) IRD (Institut de recherche pour le Développement, France) provided ship time and research funding for MCR LTER Associate Investigator Brooks to participate in the Mururoa Isotope Mission.

74 ISPA (http://www.ispa.pt/ISPA/vPT/Publico/) ISPA (Instituto Superior de Psicologia Aplicada, Lisbon, Portugal) provided all funding for airfare, food, lodging and salary for Ricardo Beldade, Postdoctoral fellow with MCR LTER Associate Investigator Bernardi.

Moorea Marine Protected Areas Monitoring Consortium The MCR LTER became a full partner in the Moorea MPA Monitoring Consortium in early 2006. Other partners include the UC Berkeley Gump Research Station, CRIOBE, the University of Florida and Victoria University of Wellington (New Zealand). MCR LTER Associate Investigator Brooks is a member of the Moorea MPA Monitoring Consortium Executive Committee and MCR LTER affiliated graduate students (Adam, Price, Talmage) have assisted with the Consortium’s bi-annual, biotic monitoring surveys. MCR LTER personnel also will participate in the data management for this program.

Moorea Biocode Program The Moorea Biocode Program is a joint Franco-American effort to genetically barcode the complete tropical ecosystem of Moorea. The team is led by researchers at the University of California Berkeley, Berkeley Natural History Museums, and the CNRS France through their field stations (Gump Research Station and CRIOBE) on Moorea. MCR LTER Associate Investigator Alldredge provided zooplankton and larval invertebrate samples and Associate Investigator Brooks provided samples of reef fishes for bar coding. In addition, the MCR LTER Encyclopedia of Marine Life contains links to data on individual species within the Moorea Biocode Project to provide Outreach and Education opportunities.

National Museum of Marine Biology and Aquarium/National Dong Hwa University, Taiwan (http://eng.nmmba.gov.tw/) The National Museum of Marine Biology and Aquarium, Taiwan, has (and continues) to play a central role in the development of a collaborative research program between the MCR LTER and the Kenting ILTER (Taiwan). This includes an exchange of graduate students.

Taiwan Ecological Research Network (TERN) (http://lter.npust.edu.tw/tern/e_english/english_home.htm) TERN (Taiwan Ecological Research Network) and the Kenting Coral Reef ILTER site continue to promote scientific exchanges, collaborative research, and graduate student training and research opportunities with the MCR LTER.

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