Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
Project 6. Population dynamics of coral populations
under environmental change
2
Eran Brokovich, Omri Bronstein, Jessica Gilner, Yossi Loya, Juan Carlos Ortiz, Rob van Woesik, and
Assaf Zvuloni.
Location: Mesoamerican CoE, Australasian CoE, East African Coe, and Philippines CoE
Key results
This project examined the population dynamics of coral populations at a scale which is highly novel relative
to previous studies. In addition to establishing the monitoring of coral reefs at the four Centres of Excellence
across the CRTR Program, this project delivered a number of important research outcomes and conclusions.
Outcomes included corrections developed to eliminate biases that occur because of boundary effects
when measuring the size of benthic organisms, as well as a series of relationships between 2-dimensional
and 3-dimensional estimates of coral growth. Several important ecological phenomena were also identified,
including two modes of partial mortality affecting coral species in the Caribbean; with some species rapidly
losing colony integration while others maintained integration and sacrificed marginal tissue. Research
within this group also identified the critical observation that mild thermal stress events showed different
responses than extreme events: during extreme events, small colonies do better than larger colonies, while
during mild events, colony size did not influence bleaching. In both cases massive corals were found to be
more sensitive than branching corals. The research within this project also identified the important influence
of substrate reflection, for example from sand, increasing available light and exacerbating the risk of coral
bleaching. Indeed, corals growing on and near sand showed more intense bleaching than those growing
on or near substrate with lower reflectivity. The group also made some interesting long-term observations,
such as sea urchin densities on the western reefs of Zanzibar increasing 6 to 10-fold since 1996; with fish on
the same reefs increasing considerably in the last three years.
Background
The overall objective in this project was to assess coral-population dynamics within the context of coral
bleaching and subsequent effects. Given the importance of comparing between regions, in terms of the
ability to generalise about the ecological behaviour of coral reefs, the team decided to focus work around
3 CoEs in the initial stages: Puerto Morelos (Mexico), Heron Island (Australia), and Zanzibar (Tanzania). This
project also undertook activities in the Philippines and Palau. This CoE-centered approach allowed for a
focus on coral dynamics which were easily accessible, and where the research activity could evoke
collaboration among the other working groups with the Coral Reef Targeted Research Program.
We focused on quantifying both state (i.e., coral cover, macroalgal cover, size-frequency distributions) and
process (or vital-population rates) variables (including coral recruitment rates, individual growth rates,
partial mortality rates, and survival). We were also interested in the macro-processes, such as predation,
herbivory, and oceanography that influenced the corals' vital-population rates. Our approach allowed us to
determine which vital rates were responsible for the state of the reef, and allowed us to derive novel yet
pragmatic models that would predict population changes and the future state of the reefs.
Objectives
One of our primary goals was to understand: Which coral species were physiologically more tolerant to
thermal stresses than others, and why? Which interacting variables and processes are driving coral
population structure? Which processes are primarily responsible for coral population change?
Does differential coral population response to, and recovery from, thermal stress vary among regions and
habitats? What role do remnants play in recovery processes? Is annual recruitment vital in all habitats?
Which habitats recover more rapidly than others? Which coral species will adjust to global climate change?
Can differential and local management practices influence thermal-stress response and recovery?
53
Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
Our primary task was to assess the dynamics of coral
populations and associated coral reef organisms by
2
defining the key ecological processes that regulate the
populations (Figure 15). Understanding these processes,
assessing their spatial variation and their relationship with
state variables, including size-frequency distributions,
leads to predictive models of population trajectories,
relative population size distributions, and community
change
under
different
climate
change
scenarios.
We predicted that size-frequency distributions coupled
with partial mortality information could provide a reliable
indicator of coral stress and provide insight into the future
of coral reefs.
Specifically we examined:
1. Spatial patterns in coral population size-frequency
distributions and temporal changes of the populations
at three CoEs;
2. Scale dependence of key process variables, including
rates of recruitment, partial mortality, and mortality;
3. Relationships between processes and state variables
and whether size-frequency distributions reflected
population performance;
4. Effect
of
macro-processes,
including
herbivory
(i.e., density and composition of urchins and fishes), on
coral population vital rates and diseases.
Figure 15. Total mortality of a coral colony over a year
period. Photo: R. van Woesik
Methods
The sampling strategy captured state and process variables at a spatial scale of 10s of kilometers (herein
called a Location). Sampling aimed at establishing 6-7 sites per location. Sites were spaced approximately
2 km apart, representing a 103 m spatial scale, with random stations nested within sites. Sites were
systematically selected based on the targeted depth
regime where sampling efforts were focused on one depth
zone (2-5 m), rather than stratifying the design by depth
and reducing the spatial area to be sampled. Stations were
randomly selected and nested within sites, representing a
104 m spatial scale and were 75 x 25 m. However, these
dimensions remain plastic depending on the reef
morphology, while maintaining a total area of 1875 m2.
Stations were the effective sampling units. Within each
station we ran at least 5, 50 m transects that were re-
randomized each sampling period, and used to estimate
state variables (i.e. size frequency distributions, benthic
composition). Three randomly selected 16 m2 quadrats
were placed in each station, and marked for relocation
purposes (Figure 16), and used to assess processes (i.e.
recruitment, growth, partial mortality, mortality etc.) across
time (repeated measures design). Both quadrats and belt-
Figure 16. Permanent quadrat in Puerto Morelos,
transects are effectively sub-samples from which we
Mexico (~ 50, 1 m2 photos were overlapped to
derived estimates of means for each station at each
generate a 16 m2 mosaic using Matlab® software).
sampling event (because the station was the effective
Photo: Nuno Garcia
sampling unit).
54
Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
Results and discussion
2
a. Advancements in coral reef sampling
Throughout this project various techniques for monitoring populations have been used and tested. Zvuloni
et al. (2008) elucidated the biases that can arise in the application of popular and traditional sampling
methods (e.g. quadrat, belt-transect, and line-intercept). Simple mathematical corrections were developed
that provide unbiased estimations for previously collected data acquired by these widely used methods.
In addition, alternative sampling methods were identified that do not suffer from these shortcomings.
Eliminating these types of sampling errors provide better assessments of the status of a given coral reef,
and provide precise comparisons among coral reefs in different regions. This work is equally relevant in
other ecological contexts, not just corals.
Limitations with photographic analyses have also been recognized as a 3-dimensional (3-D) reef is turned
into a 2-dimensional (2-D) photo. For some growth morphologies such as branching corals, this significantly
affects growth measurements. Holmes et al. (2008) found a significant difference in growth when comparing
2-D and 3-D measurements for two branching species. These findings suggest that growth measurements
are only reliable when measured in 3-D, and 2-D measurements can be corrected to provide reliable coral
estimations.
b. Population dynamics
Key process variables (i.e. partial mortality, whole colony
mortality, recruitment, and growth) have been identified
and investigated to some degree in each region. In the
Caribbean, partial mortality appears to be a primary
mechanism of coral-cover degradation (Figure 17).
Two modes of partial mortality were identified: (1)
peripheral-partial mortality, occurring between live tissue
and substrate, and (2) centralised-partial mortality,
occurring within the colony, completely surrounded by live
tissue.
All
species
investigated
(Diploria
strigosa,
Siderastrea siderea, Porites astreoides, Agaricia agaricites
and Montastraea cavernosa) were affected by peripheral
mortality, while P. astreoides and S. siderea were more
likely to also exhibit centralized mortality.
Figure 17. Partial mortality of Montastraea one year to
the next in Puerto Morelos, Mexico. Photo: J. Gilner
c. Response and recovery from bleaching events
These same process variables were investigated on Heron Island in response to a mild thermal stress event.
Mortality, recruitment, and growth were examined for four targeted coral taxa (Pocillopora damicornis,
Stylophora pistillata, Favites/Goniastrea, and Favia spp.) to determine sensitivity to a mild thermal-stress
event (in January-May 2006 on Heron Island in the Great Barrier Reef). The mild thermal stress event
showed a different response than major thermal stress events. The mild stress showed that coral-colony
size did not influence bleaching response, and massive corals were more affected by bleaching than
branching corals. Because massive corals were primarily surrounded by sand, it was hypothesized that
light reflectance from sand increased incoming irradiance and hence elevated stress. During extreme
thermal-stress events small-coral colonies were least effected, as were massive and encrusting colonies.
Therefore, various thermal stress anomalies show different bleaching responses.
d. Thermal stress, bleaching, and diseases
The prevalence of black-band disease (BBD) was strongly associated with high-water temperature.
BBD infected coral colonies exhibited aggregated distributions on small spatial scales (up to 1.9 m).
Newly-infected corals appeared in proximity to existing infected corals. Previously infected corals were
more susceptible the following summer season. Therefore, water-borne infection is likely to be a significant
transmission mechanism of BBD.
55
Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
e. Coral-community structure
The patterns of coral community composition and diversity
2
were examined around Zanzibar at three spatial scales
ranging from transects ( 20 m), stations (< 100 m), to sites
(< 1000 m). Two sites of the four, Chumbe and Mnemba,
are located within marine protected areas (MPAs) and the
other two sites, Bawe and Changuu, are not protected.
Additive partitioning was used to examine diversity within
and between the three spatial scales, where individual-
based rarefaction was used as a null model. We show that
each of the sites is different in species composition, except
Bawe vs. Changuu. Chumbe and Mnemba, the most
diverse sites, exhibited (local) and (turnover)-diversity
as expected by random, whereas Bawe and Changuu were
Figure 18. Permanent quadrat to assess coral-
different than expected. In general, given the regional
community structure and herbivory by sea urchins in
Zanzibar. Photo: A. Zvuloni
species pool, diversity among sites was significantly higher
than expected. These results suggest that nonrandom
processes interact on an among-sites scale (i.e., ca. kilometers), and in Bawe and Changuu they also interact
on a within - and between-transects scale. The nonrandom outcome helps identify appropriate boundaries
for studying mechanisms that generate and maintain biodiversity within this region. In considering coral
diversity in Bawe, the number of rare species and singleton species (only found in one locality) suggests
that Bawe should be declared a Marine Protected Area (MPA).
f. Macro-processes
i. Herbivory by sea urchins
We assessed the impact of sea urchin populations on coral
communities around the island of Zanzibar. Twice a year,
between 2007 and 2008, surveys of urchin populations
(species, densities and size-frequency distributions) were
performed at the same six locations used for coral and fish
monitoring. Urchin bioerosion experiments were conducted
separately for each of the study sites. Dominance of two
urchin species was evident: Diadema setosum and
Echinometra sp., in five out of six stations, with D. setosum
dominating the western side of Zanzibar and Echinometra
sp. dominating the eastern side (Figure 19). Average
densities of D. setosom and Echinometra sp. ranged from
0-30 and 0-88 individuals m-2, respectively. Eastern sites
Figure 19. Dominant sea urchins in Zanzibar.
showed 2-4 times more sea urchins than the western sites.
A Echinothrix diadema, B Echinometra sp, C Diadema
savignyi and D. setosum. Photos: O. Bronstein
Urchin species assemblage did not change significantly
throughout the duration of the study, nor did it change in
comparison to 1996 (McClanahan et al. 1999), whereas sea urchin densities at Changu and Chumbe
increased 6-10 fold since 1996. Mnemba showed the lowest sea urchin densities (1.2 urchins m-2) and the
highest abundance of urchin-preying fish. Molecular and morphological studies conducted on Echinometra
sp. from 8 locations around the island of Zanzibar and 3 locations in the northern Red Sea suggest that
urchins from the genus Echinometra are a suite of new species.
56
Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
ii. Fish communities
Zanzibar's economy relies heavily on fishes, which are used
2
both for food and as an attracting component in the coral
reef tourism industry. We studied the coral reef fish
community structure around Zanzibar to establish a base-
line for future monitoring of fish interactions with corals
and sea urchins (herbivory, predation). In April 2009 we
compared four sites around the island. Two sites are marine
reserves (Chumbe in the west side of the island and
Mnemba in the east) and another two (Changu and Bawe,
located on the west side) are not protected and are heavily
fished. We visually sampled fish in replicated 25 by 2 m
transects, identifying fishes to the species level and
estimating their abundance and length (Figure 20). We
Figure 20. The grunt fish Blackspotted rubberlip
used point sampling along transects to estimate habitat
(Plectorhinchus gaterinus) is a component of the reef
parameters. We sampled 7046 individuals from 153 species
fisheries in Zanzibar. Photo: E. Brokovich
belonging to 30 fish families. Using a null model we found
that alpha diversity was lower than expected by chance but also that the sites were highly heterogeneous.
The fish community structure differed remarkably between the sites with the two non- managed sites being
the most similar. The fish-community structure was influenced by the amount of living coral cover, particularly
branching coral colonies and substrate structural complexity. Regardless of low coral cover, the number of
fish species was highest at Mnemba (a protected site). The amount of large exploitable fish (> 20 cm) was
highest in the protected sites (16% of all fish in Chumbe and 6% in Mnemba as oppose to ca. 3% in the non
protected sites). Mnemba had the highest number of sea urchin predators and the fewest sea urchins.
Comparing this study with previously reported data from the same area which was affected by the 1998
bleaching event, we show that fish density increased dramatically in the last three years.
57
Bleaching and Related Ecological Factors:
CRTR Working Group Findings 2004-2009
Theme 2: Organismal mechanisms to ecological outcomes
Key literature generated with Full/partial project support:
1.
Brokovich E, Zvuloni A, Bronstein O, Loya Y (in prep) Changes in fish assemblages around Zanzibar Island (Tanzania) with respect to habitat complexity and management
practices.
2.
Bronstein O, Loya Y (in prep) A new sea urchin species of the genus Echinometra from the Red Sea and western Indian Ocean.
2
3.
Bronstein O, van Woesik R, Loya Y (in prep-a) Population shifts of sea urchins on the coral reefs of Zanzibar.
4.
Bronstein O, van Woesik R, Loya Y (in prep-b) Spatial patterns of sea urchin bioerosion on the coral reefs of Zanzibar.
5.
Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef:
climate change, algal overgrowth and coral recovery. PLoS ONE 4:e5239
6.
Fabricius KE, Wild C, Wolanski E, Abele D (2003) Effect of transparent exopolymer particles and muddy terrigenous sediments on the survival of hard coral recruits. Est Coast
Shelf Sci 57:613-621
7.
Field SN, Glassom D, Bythell JC (2007) Effects of artificial settlement plate materials and methods of deployment on the sessile epibenthic community development in a
tropical environment. Coral Reefs 26:279-289
8.
Fleitmann D, Dunbar RB, McCulloch M, Mudelsee M, Vuille M, McClanahan TR, Cole JE, Eggins S (2007) East African soil erosion recorded in a 300 year old coral colony
from Kenya. Geophysical Research Letters 34:L04401
9.
Gilner JE, Van Woesik R (in prep) Partial mortality of Caribbean corals: modes, trends and consequences. Marine Biology
10. Gleason DF, Edmunds PJ, Gates RD (2006) Ultraviolet radiation effects on the behavior and recruitment of larvae from the reef coral Porites astreoides. Marine Biology
148:503-512
11. Golbuu Y, Victor S, Penland L, Idip D, Emaurois C, Okaji K, Yukihira H, Iwase A, van Woesik R (2007) Palau's coral reefs show differential habitat recovery following the
1998-bleaching event. Coral Reefs 26:319-332.
12. Holem L, Koksal S, van Woesik R (in prep) Vital rates influencing population dynamics of Indo-Pacific reef corals. Oecologia
13. Holmes G (2008) Estimating three-dimensional surface areas on coral reefs. Journal of Experimental Marine Biology and Ecology 365:67-73
14. Holmes G, Ortiz JC, Kaniewska P, Johnstone R (2008) Using three-dimensional surface area to compare the growth of two Pocilloporid coral species. Marine Biology 155:421-427
15. Houk P, Bograd S, van Woesik R (2007) The Transition Zone Chlorophyll Front acts as a trigger for Acanthaster planci outbreaks in the Pacific Ocean: a historical confirmation.
Journal of Oceanography 63:149-154
16. Houk P, van Woesik R (2008) Dynamics of shallow-water assemblages in the Saipan Lagoon. Marine Ecology Progress Series 356:39-50
17. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook LJ, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory,
and the resilience of coral reefs to climate change. Current Biology 17:360-365
18. Jupiter S, Roff G, Marion G, Henderson M, Schrameyer V, McCulloch M, Hoegh-Guldberg O (2008) Linkages between coral assemblages and coral proxies of terrestrial
exposure along a cross-shelf gradient on the southern Great Barrier Reef. Coral Reefs 27:887-903
19. Kleypas, JA, and O. Hoegh-Guldberg (2007) Coral reefs and global climate change, Chapter 3 in Wilkinson, C. (ed.) Status of Caribbean Coral Reefs after Bleaching and
Hurricanes in 2005. GCRMN, Townsville.
20. Ledlie MH, Graham NAJ, Bythell JC, Wilson SK, Jennings S, Polunin NVC, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral
Reefs 26:641-653
21. Obura DO (in press) Bleaching as a life history trait in coral-zooxanthellae holobionts - relevance to acclimatization and adaptation 11th International Coral Reef Symposium,
Ft. Lauderdale, USA
22. Ortiz JC, Gomez-Cabrera MD, Hoegh Guldberg O (submitted) Effect of colony size and surrounding substrate on corals experiencing a mild bleaching event on Heron Island
reef flat (southern Great Barrier Reef, Australia). Coral Reefs
23. Ortiz JC, Holmes G, Gomez-Cabrera MD, Hoegh Guldberg O, van Woesik R (in prep-a) Using population's demographic dynamics as early indicator of communities'
response to subtle stress: A coral reef case study. Ecological applications
24. Ortiz JC, van Woesik R, Hoegh-Guldberg O (in prep-b) Interpreting coral reefs evenness dynamics in a changing environment.
25. Ortiz JC, van Woesik R, Marshall D, Hoegh-Guldberg O (in prep-c) `The balance between how much we should do and How much we can do: Maximizing the power and
accuracy of a monitoring program dataset'.
26. Ridgway T, Gates RD (2006) Why are there so few genetic markers available for coral population analyses? Symbiosis 41:1-7
27. Ridgway T, Riginos C, Davis J, Hoegh-Guldberg O (2008) Genetic connectivity patterns of Pocillopora verrucosa in southern African Marine Protected Areas. Marine Ecology
Progress Series 354:161-168
28. Rongo T, Bush M, van Woesik R (2009) Voyages of discovery or necessity: harmful algal blooms cause ciguatera poisoning in fishes and contribute to the contemporary and
late Holocene Polynesian migrations. Journal of Biogeography doi:10.1111/j.1365-2699.2009.02139.x
29. Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin H, Loya Y (in press) Role of microorganisms in coral bleaching. Environmental Microbiology
30. Rosenfeld M, Shemesh A, Yam R, Sakai K, Loya Y (2006) Impact of the 1998 bleaching event on Ð18O records of Okinawa corals. Marine Ecology Progress Series 314:127-133
31. Rusch A, Huettel M, Wild C, Reimers CE (2006) Benthic oxygen consumption and organic matter turnover in organic-poor, permeable shelf sands. Aqu Geochem
32. van Woesik R, Ganase A, Sakai K, Loya Y (in prep) Coral bleaching: the winners and the losers, ten years on. Ecology Letters
33. van Woesik R, Koksal S (2006) A coral population response (CPR) model for thermal stress. In: Phinney J.T. et al (ed) Coral reefs and climate change: science and management.
American Geophysical Union, Washington DC, p 129-144
34. van Woesik R, Lacharmoise F, Koksal S (2006) Annual cycles of solar insolation predict spawning times of Caribbean corals. Ecology Letters 9:390-398
35. Wagner D, Mielbrecht E, van Woesik R, (2008) Application of landscape ecology to spatio-temporal variance of water-quality parameters along the Florida Keys reef tract.
Bulletion of Marine Science 83:553-569
36. Weeks SJ, Anthony KRN, Bakun A, Feldman GC, Hoegh-Guldberg O (2008) Improved predictions of coral bleaching using seasonal baselines and higher spatial resolution.
Limnology and Oceanography 53:1369-1375
37. Wehrmann LM, J. KN, Pirlet H, Unnithan V, Wild C, Ferdelman TG (2009) Carbon mineralization and carbonate preservation in modern cold-water coral reef sediments on
the Norwegian shelf. Biogeosciences 6:663-680
38. Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh-Guldberg O (2007) Increased prevalence of ubiquitous ascomycetes in an acropoid coral (Acropora formosa)
exhibiting symptoms of brown band syndrome and skeletal eroding band disease. Applied and Environmetal Microbiology 73:2755-2757
39. Zvuloni A, Armoza-Zvuloni R, Loya Y (2008a) Structural deformation of branching corals associated with the vermetid gastropod Dendropoma maxima. Marine Ecology
Progress Series 363:103­108
40. Zvuloni A, Artzy-Randrup Y, Stone L, Kramarsky-Winter E, Barkan. R, Loya Y (2009) Spatio-temporal transmission patterns of black-band disease (BBD) in a coral community.
PLoS ONE 4 e4993
41. Zvuloni A, Artzy-Randrup Y, Stone L, Loya Y (in prep-a) Spatio-temporal relations between two coral diseases: black-band and white plague-like.
42. Zvuloni A, Artzy-Randrup Y, Stone L, van Woesik R, Loya Y (2008b) Ecological size-frequency distributions: how to prevent and correct biases in spatial sampling. Limnology
and Oceanography: Methods:144-153
43. Zvuloni A, Brokovich E, Hosgin I, van Woesik R, Loya Y (in prep-b) Porites micro-atolls are diversity hot spots.
44. Zvuloni A, Mokady O, Al-Zibdah M, Bernardi G, Gaines SD, Abelson A (2008c) Local scale genetic structure in coral populations: A signature of selection. Marine Pollution
Bulletin 56:430-438
45. Zvuloni A, Stone L, Loya Y (in prep-c) Obtaining ecological count-based measures of sessile organism distributions from line-intercept data.
46. Zvuloni A, van Woesik R (in prep) Spatial patterns of coral diversity around Zanzibar Island.
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