PHMR: Status of the Reserve Report 2008
Nicola L. Foster, PhD. Senior Marine Biologist Marine & Coastal Research and Monitoring Program
Nicola L. Foster, PhD. Toledo Institute for Development & Environment P.O. Box 150 1 Mile San Antonio Road Punta Gorda Town Belize, C.A.
Tel: + 501 722 2274 Fax: + 501 722 2655 Mob: + 501 628 2145 Email:
[email protected] Website: www.tidebelize.org
Introduction The Toledo Institute for Development and Environment (TIDE) was founded in 1997 to meet the growing environmental and development needs of the Toledo District. TIDE's focus is to enable community‐ based forest, marine and coastal conservation in the Maya Mountain Marine Corridor, while developing viable economic alternatives for residents that do not rely on resource extraction. TIDE has grown from its inception in 1997 as a local, grassroots response to manatee poaching, to a leading non‐government organization in Belize with a budget of ~$1.7 Million US. In 2000, after six years of lobbying by TIDE and community members, the Port Honduras Marine Reserve was declared and TIDE was granted co‐ management authority, with the Fisheries Department, by the Government of Belize. The reserve was established to protect the physical and biological resources of Port Honduras and develop a sustainable fishery for the buffer communities of the reserve. The Port Honduras Marine Reserve covers an area of 160 square miles and encompasses 138 mangrove cayes. The borders of the reserve run from south of the Rio Grande River to North of Monkey River Town and East to the edge of the Snake Cayes (Figure 1). The reserve is divided into 3 zones; 95% is a general use zone where commercial, subsistence and recreational fishing activities are permitted; 4% is designated a conservation zone where “no‐take” recreational activities are permitted; and the remaining 1% is designated a preservation zone where no activities are permitted. In addition, the use of gill nets, long lines and beach traps is prohibited anywhere within the reserve.
Figure 1: Area covered by the three zones of the Port Honduras Marine Reserve, Belize. Nicola L. Foster, PhD.
Since 2003, reasonably consistent monitoring of the key habitats and species within Port Honduras Marine Reserve has taken place and large amounts of data have been collected. Up until recently, these data had not been thoroughly analysed or utilised. Here, we present an overview of the monitoring data collected over the past 5 years and discuss what these results mean in terms of the effectiveness of the reserve. Ultimately, these results will be used to develop the 2009 management plan for the Port Honduras Marine Reserve and update the protocols used to monitor the key habitats and species within the reserve.
Water Quality within PHMR The water quality parameters of temperature, salinity and dissolved oxygen are important components of the monitoring program. Variations in these parameters can greatly affect the health of the ecosystem and organisms within it. For example, an increase in temperature can initiate a bleaching response in hard and soft corals (Brown 1997, Fitt et al. 2001) and may affect the metabolism of many fish and invertebrates, especially during their early life history (Munday et al. 2008). Changes in salinity can affect reproduction and physiological responses in many organisms including fish and corals (Vermeij et al. 2006, Koenig et al. 2007), and the level of dissolved oxygen in the water column determines the numbers of organisms it can support (Dubinsky & Stambler 1996). Water quality has been monitored across the Port Honduras Marine Reserve since 1998, albeit some years were more consistent than others. Typically, eleven sites are surveyed once a month for temperature, salinity and dissolved oxygen content using a portable water quality meter. Unfortunately, a full 12 month survey has not been completed, however, the data collected do show some interesting trends.
Water Temperature Between 1998 and 2008, water temperature varied with season and among years (Figure 2). On average, the coldest months were observed in winter, from November through February. From March, water temperature typically rose to a peak in July or August, after which it began to decline again. All years show similar variations among months, however, 2000 was a particularly cold year compared to the remaining 9 years and 2003 was a particularly warm year (Figure 2). Although the change in water temperature between 2000 and 2003 was only approximately 2oC, such a small difference can have a dramatic effect on the habitats and organisms subject to the change. Interestingly, 1998, a year of extreme bleaching events worldwide, was not a notably warm year for the Port Honduras Marine Reserve (Figure 2).
Nicola L. Foster, PhD.
34.00
32.00
Temperature (oC)
1998
30.00
1999 2000 2001
28.00
2003 2004
26.00
2005 2006
24.00
2008
22.00 Jan Feb Mar Apr May Jun
Jul Aug Sept Oct Nov Dec
Month
Figure 2: Average monthly water temperature recorded within Port Honduras Marine Reserve from 1998 to 2008.
Salinity Salinity within PHMR also showed variation between seasons and years (Figure 3). The lowest salinity was frequently recorded at the height of the rainy season in July and August when increased freshwater from rivers enters the bay. At the peak of the dry season in March and April, salinity levels are typically at their highest (Figure 3). In some years, there was a difference of 10 ppt in salinity between March and July. If freshwater input through rainfall is expected to have the greatest influence on salinity within PHMR, then 2005 was one of the driest years since 1998, and 2006 was one of the wettest. Large fluctuations observed in salinity over any 12 month period demonstrate the substantial influence that the surrounding watershed has on the Port Honduras area and the habitats and organisms within it.
Nicola L. Foster, PhD.
40.00 38.00
Salinity (ppt)
36.00 34.00
1998
32.00
1999 2000
30.00
2001
28.00
2003 2004
26.00
2005
24.00
2006
22.00
2008
20.00 Jan Feb Mar Apr May Jun
Jul Aug Sept Oct Nov Dec
Month
Figure 3: Average salinity recorded within Port Honduras Marine Reserve from 1998 to 2008.
Dissolved Oxygen Dissolved oxygen levels within PHMR varied between years and between months (Figure 4). Typically, the highest levels of dissolved oxygen are observed between December and March and the lowest levels are observed from April to August. However, there are some notable exceptions to this pattern. In 2005, the lowest dissolved oxygen levels were recorded between February and March and the highest were recorded between September and November. 2005 was also one of the driest (Figure 3) and warmest (Figure 2) years of the monitoring period which may have had some influence on dissolved oxygen levels. Another exception to the general pattern is the year 2008, which has shown a steep decline in dissolved oxygen levels between August and November. These are the lowest dissolved oxygen levels recorded within PHMR in 10 years of data collection and require further investigation to elucidate what is occurring.
Nicola L. Foster, PhD.
10.00 9.00
Dissolved Oxygen (mg/l)
8.00 7.00
1998 1999
6.00
2000
5.00
2001
4.00
2003 2004
3.00
2005
2.00
2006
1.00
2008
0.00 Jan Feb Mar Apr May Jun
Jul Aug Sept Oct Nov Dec
Month
Figure 4: Average dissolved oxygen levels within Port Honduras Marine Reserve from 1998 to 2008.
Coral Reefs Coral reefs are an essential component of the Port Honduras Marine Reserve and the health of coral reef habitats has a significant influence on the vertebrate and invertebrate populations that inhabit them. Most importantly, healthy coral reefs, in conjunction with seagrass and mangrove habitats, support larger populations of species compared to unhealthy reefs. To determine reef health, a variety of aspects have been monitored since 2003, including benthic composition, coral diversity, coral mortality and coral disease. Coral reefs at eight sites within the Port Honduras Marine Reserve have been assessed annually, unfortunately, consistent data regarding coral disease and mortality is absent. Benthic cover is assessed using the AGGRA survey method of liner point intercept transects whereby the type of benthic cover is recorded every 25cm along six 30 metre transects at each site. The average benthic composition within PHMR varied between 2003 and 2008 (Figure 5). Live coral cover has increased from an average of 8% in 2003 to 17% in 2008. In contrast, the cover of turf algae has decreased from an average of 14% in 2003 to 8% in 2008. Macroalgal cover has fluctuated over the 5 year period from 22% in 2003 to 12% in 2008. Dead coral has been largely absent over the 5 years and coralline algal cover has remained relatively constant at approximately 3%.
Nicola L. Foster, PhD.
Percent cover of benthic component
100% 90%
Other
80%
Bare Substrate Sand
70%
Coralline Algae
60%
Turf Algae
50%
Macroalgae Sponge
40%
Zoanthid
30%
Gorgonian
20%
Dead Coral
10%
Live Coral
0% 2003
2004
2005
2006
Year
2008
Figure 5: Average benthic composition within Port Honduras Marine Reserve from 2003 to 2008. Looking specifically at live coral and macroalgal cover at each of the sites over the 5 year period shows a more detailed pattern (Figure 6). From 2003 to 2008 there is a gradual decrease in macroalgal cover and a simultaneous increase in coral cover across the majority of sites. Such changes in benthic cover can be an indication of increased reef health which may be associated with the protection provided through the marine reserve. However, Frenchman Caye (FMC) and Wilson Caye (WC) continue to be dominated by macroalgae into 2008. Frenchman Caye and Wilson Caye are closer inshore than the other sites and thus are more exposed to freshwater and sediment input from the watersheds surrounding Port Honduras. Increased sedimentation can limit recruitment of coral species, restrict growth rates of individual corals and increase coral mortality through smothering (Rogers 1990, Birrell et al. 2005). Furthermore, East Snake Caye (ESC), South Snake Caye (SSC), West Snake Caye (WSC) and Middle Snake Caye (MSC) are located within the conservation and preservation zones of the marine reserve. Commercial and recreational activities are restricted in these areas and as such a larger population of fishes may be present on these reefs compared to Frenchman Caye and Wilson Caye. Herbivorous fish species in particular help to control the growth of macroalgae through grazing and thus promote coral recruitment and survival (Mumby et al. 2006, Mumby et al. 2007). Nevertheless, while the decrease in macroalgal cover over the 5 year period is a good indication of increasing reef health, coral cover is still relatively low.
Nicola L. Foster, PhD.
60.00 Macroalgae
Live Coral
50.00
Cover (%)
40.00
30.00
20.00
10.00
ESC WSC SSC MSC FMC WC B2 B3 ESC WSC FMC B3 ESC WSC SSC MSC FMC WC ESC WSC SSC MSC FMC WC B2 ESC WSC SSC MSC FMC WC B2 B3
0.00
2003
2004
2005
Site and Year
2006
2008
Figure 6: Cover of coral and macroalgae at sites within Port Honduras Marine Reserve from 2003 to 2008. More detailed surveys conducted in 2008 show the coral diversity at each of the sites monitored within Port Honduras Marine Reserve (Figure 7). A total of 29 species were observed across the eight sites and the composition of coral species differs between sites. The two deeper sites, Bank 2 (B2) and Bank 3 (B3), are dominated by Agaricia tenuifolia (Lettuce coral), whereas the other sites have a higher proportion of the reef building corals, Montastraea spp. Interestingly, all sites have a high proportion of the fire coral, Millepora alcicornis. Wilson Caye is the least diverse of all the sites and has the lowest coral cover which, as mentioned previously, may be due to increased sedimentation at this site. Further investigation of sedimentation rates across PHMR in 2009 will help to determine which sites receive the most sedimentation and how this affects the habitats at those sites. Interestingly, total coral cover does not denote the number of coral species observed. For example, Bank 3 (B3) has the highest percent coral cover, yet only 11 coral species were observed along the transects. In contrast, Frenchman Caye (FMC) has one of the lowest percent covers, yet a total of 12 coral species were observed along the transects.
Nicola L. Foster, PhD.
25 11
16 15
20 11
Cover (%)
19 10
15
12 5 10
5
Ssid
Srad
Sint
Scub
Ppor
Past
Mmea
Mlam
Mfra
Mfav
Mdec
Mdan
Mcav
Mann
Mali
Malc
Isin
Efas
Dstr
Dsto
Dlab
Dcli
Cnat
Aten
Apal
Alam
Afra
Acer
Aaga
0 ESC
WSC
SSC
MSC
FMC
WC
B2
Site
B3
Figure 7: Coral species composition and diversity at each site surveyed within the Port Honduras Marine Reserve in 2008. Numbers above bars denote total number of species observed.
Reef Fish In conjunction with the coral surveys conducted within PHMR, reef fish surveys were also carried out between 2003 and 2008. At 6 of the sites used for the coral reef monitoring, a minimum of six 30 metre by 2 metre transects were surveyed and the size and number of all reef fish encountered were recorded. Figure 8 shows the density of reef fish at each of the sites over the 5 year period. Reef fish density was highest at all sites in 2003 and has decreased significantly since then; in some cases by more than 50%. In 2003, density varied between sites, however, in 2006 and 2008, density was similar across the 6 sites. These results demonstrate a significant decline in reef fish numbers, possibly through over fishing and / or loss of habitat within PHMR. Unfortunately data for 2004 and 2005 is largely absent and it is impossible to tell if the low densities observed at the few sites surveyed is due to incomplete data collection or a response to an incident within PHMR.
Nicola L. Foster, PhD.
140
Fish Density (Numbers/100 m2)
120 100 WSC
80
ESC MSC
60
SSC FMC
40
WC
20 0 2003
2004
2005
2006
2008
Year
Figure 8: Density of reef fish at 6 sites within the Port Honduras Marine Reserve between 2003 and 2008.
Conch Strombus gigas (Queen Conch) is one of the major commercial fisheries species harvested from within the general use zone of PHMR and populations have been monitored since 2004. One role of the no‐ take zones (conservation and preservation zones) within the reserve is to provide a refuge for species from fishing, including queen conch. These areas enable populations to reproduce and reach maturity without the threat of being caught. Eventually population numbers within no‐take zones become large enough that spill‐over into the surrounding general use zone is inevitable and fisheries are supplemented. Queen conch populations were monitored at 12 sites strategically placed throughout PHMR from 2004 to 2008. At each site, a minimum of four 50 metre transects were surveyed and all queen conch individuals encountered were recorded. Measurements of shell length and lip thickness were also taken. Numbers of queen conch encountered within PHMR has gradually declined from 2004 to 2008 despite the protection offered by the no‐take zones (Figure 9). Unexpectedly, between 2004 and 2006 numbers of queen conch recorded in the general use zone was greater compared to the no‐take zones. One explanation may be the inclusion of a site at Abalone Caye in the General Use Zone, the location of the Rangers Station. Fishing may be reduced at this site due to the constant presence and close proximity of the rangers. However, in 2008 numbers of queen conch recorded in the no‐take zones was greater than in the general use zone. These results suggest that the no‐take zones within PHMR need to be increased in order to be effective and patrols within these zones need to be increased to ensure harvesting of conch from no‐take zones does not occur. Nicola L. Foster, PhD.
80
Number of Individuals
70 60 50 40
GUZ
30
NTZ
20 10 0 2004
2005
2006
2008
Year
Figure 9: Numbers of Queen Conch recorded in the general use (GUZ) and no‐take (NTZ) zones of Port Honduras Marine Reserve between 2004 and 2008. 30
Average Shell Length (cm)
25
20 2004 15
2005 2006
10
2008
5
0 GUZ
NTZ Zone within PHMR
Figure 10: Average shell length of Queen Conch within general use (GUZ) and no‐take (NTZ) zones of Port Honduras Marine Reserve between 2004 and 2008. The red line indicates 17.8cm, the legal size for harvesting under Belize Fisheries Regulations. Nicola L. Foster, PhD.
Figure 10 shows the average shell length of queen conch individuals encountered within the general use and no‐take zones of PHMR between 2004 and 2008. For all years, average queen conch length is greater than the legal size limit for harvesting under Belize Fisheries Regulations. However, it would be expected that queen conch encountered within no‐take zones would be larger than those in the general use zone due to the protection provided against fishing. Shell length of queen conch was greater in the no‐take zones during 2005 and 2006, but not during 2008 suggesting that further protection, through enlargement of the no‐take zones, is required to enable queen conch to reach a larger size, thus ensuring reproduction occurs. Lip thickness of queen conch is used as a measure of maturity, with a thickness of 0.5cm and above being considered mature (Gascoigne & Lipcius 2004). It can take an average of three to four years for a queen conch to reach maturity, and thus reproduce. Harvesting queen conch while immature can have serious and irreversible consequences for the population, and will ultimately lead to the collapse of the fishery. The no‐take reserves within PHMR provide a refuge for queen conch to enable them to reach maturity and reproduce. Figure 11 shows average lip thickness of queen conch in the no‐take zones is always greater than 0.5cm, whereas in the general use zone the average lip thickness is frequently less than 0.5cm. These data indicate that mature queen conch have been harvested from the general use zone, leaving only immature individuals. Mature queen conch within the no‐take zones indicate that the area is effective in allowing individuals to reach maturity. 1.8
Average Lip Thickness (cm)
1.6 1.4 1.2 1
2004
0.8
2005 2006
0.6
2008
0.4 0.2 0 GUZ
NTZ Zone within PHMR
Figure 11: Average lip thickness of Queen Conch in the general use (GUZ) and no‐take (NTZ) zones of Port Honduras Marine Reserve from 2004 to 2008. The red line indicates 0.5cm, above which queen conch are considered to be mature.
Nicola L. Foster, PhD.
Lobster As with queen conch, Panulirus argus (spiny lobster) is also a major commercial fisheries species harvested from the general use zone of PHMR. To assess population numbers and determine the effectiveness of the no‐take zones on spiny lobster abundance, monitoring of populations began in 2003. However, due to inconsistent data prior to 2005, only data from 2005 to 2008 is presented here. Eleven sites across the reserve were surveyed using two 30 minute timed swims conducted simultaneously by two diver pairs. Surveys were conducted in February, prior to the closure of the fishery and in June, just prior to the fishery re‐opening. In 2008, an additional survey was conducted in October, four months after the fishery re‐opened. For each spiny lobster encountered, data regarding carapace length, sex, presence of tar spots and eggs were recorded. Overall, numbers of spiny lobster observed within PHMR have declined between 2005 and 2008 (Figure 11). Prior to 2006, lobster numbers were greater in the no‐take zones compared to the general use zone, suggesting that the no‐take areas were providing a safe refuge for spiny lobster. However in 2008, numbers observed in the general use zones were greater than in the no‐take zones (Figure 11). These data indicate a possible increase in the numbers of spiny lobster harvested from PHMR or a decrease in reproduction of lobsters. Further investigation is required to fully elucidate what is occurring within the spiny lobster populations. An increase in the size of the no‐take areas can only benefit population numbers (Cox & Hunt 2005). 20.0 18.0
Number of Individuals
16.0 14.0 12.0 10.0
GUZ
8.0
NTZ
6.0 4.0 2.0 0.0 Feb‐05
Jun‐05
Mar‐06
Jun‐06
Mar‐08
Jun‐08
Oct‐08
Year
Figure 12: Numbers of spiny lobster observed in the general use (GUZ) and no‐take (NTZ) zones of Port Honduras Marine Reserve between 2005 and 2008. Nicola L. Foster, PhD.
Despite the decline in spiny lobster numbers, the average size of lobsters (carapace length) has remained relatively constant over the 3 year period (Figure 13). In addition, no‐take zones are having a positive influence on lobster size, with the average carapace length being greater in no‐take zones compared to the general use zone (Figure 13). October 2008 is the exception to this and may be the result of increased fishing activity in the months following the opening of the fishery. Whether a reduction in size within the no‐take zones is due to movement of lobsters to available habitat within the general use zone or due to illegal fishing activity is unclear. Spiny lobster populations require further monitoring to fully understand their population dynamics within the zones of PHMR. 12.0
Average Carapace Length (cm)
10.0
8.0
6.0
GUZ NTZ
4.0
2.0
0.0 Feb‐05
Jun‐05
Mar‐06
Jun‐06
Mar‐08
Year
Jun‐08
Oct‐08
Figure 13: Average carapace length of spiny lobster in the general use (GUZ) and no‐take (NTZ) zones of Port Honduras Marine Reserve from 2005 to 2008.
Conclusions The aim of this report is to present the results of the monitoring program to date and evaluate the effectiveness of the Port Honduras Marine Reserve in conserving both habitat diversity and viable populations of commercial species. The results demonstrate that PHMR is effective in many ways, but more can be done to improve the protection provided for many key species. Water quality monitoring shows that regular freshwater input from rivers can affect even the most distant sites of PHMR through changes in salinity and sedimentation. Dissolved oxygen content is generally good, however, more recently this has begun to decline and warrants further investigation. Nicola L. Foster, PhD.
Coral cover is shown to be increasing and macroalgal cover decreasing at many sites, however fish density is declining. In particular, herbivorous fish, such as parrotfishes, provide a fundamental role in maintaining the balance between coral and algal cover on reefs (Mumby et al. 2006) and maintaining healthy fish stocks is a key component in preventing phase shifts to algal dominated reefs (Hughes et al. 2007). A considerable decline in population numbers can be sufficient to allow a rise in macroalgal cover and subsequent decline in coral cover and reduced coral recruitment (Aronson & Precht 2000, Lirman 2001, Jompa & McCook 2002). Fish populations within PHMR need to be evaluated further to determine which species are under most threat and how protection can be improved. The two major fisheries species of PHMR, queen conch and spiny lobster, have both shown large declines over the past 3 to 5 years, despite the existence of no‐take zones. In contrast, the size of both species has remained relatively constant and in the majority of cases the no‐take zones contain larger individuals of each species. However, both fisheries need considerable improvement to remain sustainable. For lobster, the closed season allows population numbers to increase, however upon opening the fishery, numbers are rapidly depleted. Such fluctuations in population numbers suggest an unstable population that cannot continue to sustain current levels of harvesting without further protection. Improvements need to be made in many areas of both the monitoring program and the management of Port Honduras Marine Reserve. While data has been collected on a variety of key habitats and species for a number of years, large inconsistencies and missing data make detailed analysis impossible. In order to improve the monitoring program and subsequent assessment of the reserve, specific protocols need to be adhered to for each habitat and species monitored. Surveys need to be conducted at regular intervals and over many years to allow any trends or patterns to become evident. When conducting each survey all sites need to be included and the minimum data collected at each site. Typically with previous data, sites were regularly missing from surveys and in many cases only half the data required was collected from sites. In addition, more key species and marine processes need to be incorporated into the monitoring program to ensure that a thorough evaluation of the reserves effectiveness can be made in the future. For example, it is recommended that data be collected for sea turtles, sea birds, manatees, commercial fisheries species and sedimentation rates. The management of the reserve also needs to be addressed. While this report has some positive aspects, many key species are in decline. It is evident that the reserve is not functioning as effectively as it could in preserving population numbers and benthic habitats. The area of no‐take zones within PHMR accounts for only 5% of the reserve area, which is 15% less than the area recommended by the Belize Fisheries Department. In addition, studies have shown that many species utilise seagrass beds, mangroves and coral reefs at various stages of their life history (Roberts et al. 2003, Mumby 2006). Thus, an increase in the no‐take area of PHMR would ensure inclusion of a larger area of each of these key habitats. It is recommended that the no‐take zones within PHMR be increased to 20%, either through the expansion of the existing conservation and preservation zones or through the creation of new conservation and preservation areas, or a combination of both. The results of this expansion in no‐take
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areas will not be evident immediately as it will take time for species to reproduce and increase population numbers. However, the long‐term benefits to the Port Honduras area will be substantial.
References Aronson RB, Precht WF (2000) Herbivory and algal dynamics on the coral reef at Discovery Bay, Jamaica. Limnol Oceanogr 45:251‐255 Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Marine Pollution Bulletin 51:408‐414 Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129‐S138 Cox C, Hunt JH (2005) Change in size and abundance of Caribbean spiny lobsters Panulirus argus in a marine reserve in the Florida Keys National Marine Sanctuary, USA. Mar Ecol Prog Ser 294:227‐ 239 Dubinsky Z, Stambler N (1996) Marine pollution and coral reefs. Global Change Biology 2:511‐526 Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51‐65 Gascoigne J, Lipcius RN (2004) Conserving populations at low abundance: delayed functional maturity and Allee effects in reproductive behaviour of the queen conch Strombus gigas. Mar Ecol Prog Ser 284:185‐194 Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh‐Guldberg O, McCook L, 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 Jompa J, McCook LJ (2002) Effects of competition and herbivory on interactions between a hard coral and a brown alga. J Exp Mar Biol Ecol 271:25‐39 Koenig CC, Coleman FC, Eklund AM, Schull J, Ueland J (2007) Mangroves as essential nursery habitat for goliath grouper (Epinephelus itajara). Bull Mar Sci 80:567‐585 Lirman D (2001) Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19:392‐399 Mumby PJ (2006) The impact of exploiting grazers (scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747‐769 Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98‐101
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Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natn Acad Sci USA 104:8362‐8367 Munday PL, Jones GP, Pratchett MS, Williams AJ (2008) Climate change and the future for coral reef fishes. Fish And Fisheries 9:261‐285 Roberts CM, Andelman S, Branch G, Bustamante RH, Castilla JC, Dugan J, Halpern BS, Lafferty KD, Leslie H, Lubchenco J, McArdle D, Possingham HP, Ruckelshaus M, Warner RR (2003) Ecological criteria for evaluating candidate sites for marine reserves. Ecol Appl 13:S199‐S214 Rogers CS (1990) Responses of Coral Reefs and Reef Organisms to Sedimentation. Mar Ecol Prog Ser 62:185‐202 Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119‐ 128
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