UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
CENTRO DE BIOCIÊNCIAS
PROGRAMA DE PÓS GRADUAÇÃO EM ECOLOGIA
MONITORAMENTO DA SAÚDE DE CORAIS EM RECIFES COSTEIROS E OCEÂNICOS UTILIZANDO MODELOS 3-D
LOUIZE FREYRE DA COSTA CORREIA
ORIENTADOR: Prof. Dr. Guilherme Ortigara Longo
3 LOUIZE FREYRE DA COSTA CORREIA
MONITORAMENTO DA SAÚDE DE CORAIS EM RECIFES COSTEIROS E OCEÂNICOS UTILIZANDO MODELOS 3-D
Dissertação apresentada ao Programa de Pós-Graduação em Ecologia do Centro de Biociências da Universidade Federal do Rio Grande do Norte como requisito parcial para a obtenção do título de Mestre em Ecologia.
4 NATAL (RN)
FEVEREIRO - 2020
Banca examinadora de defesa
__________________________________________________________________ Prof. Dr. Guilherme Ortigara Longo - UFRN
(Presidente/Orientador)
__________________________________________________________________ Profª. Drª Bárbara Segal Ramos - UFSC
(Examinador Externo)
__________________________________________________________________ Profª. Drª. Juliana Deo Dias - UFRN
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GRADECIMENTOSAos meus pais minha eterna gratidão, por serem os principais incentivadores e apoiadores diários dos meus estudos. Obrigada pelo amor e por acreditarem em mim.
Agradeço ao meu amor Daniel Rovira, por compartilhar a vida ao meu lado. Pelos ouvidos, pela paciência e companheirismo de sempre. Gratidão!
Agradeço imensamente ao meu orientador Guilherme Longo, por me permitir fazer parte do Laboratório de Ecologia Marinha (LECOM), pelas oportunidades e conhecimentos compartilhados. Obrigada pela atenção, incalculáveis contribuições, momentos de incentivo e encorajamento. É impossível conversar com você e não sair pensando que a nossa pesquisa é a mais importante do mundo!
Agradeço a todo o pessoal do LECOM pelas vivências, trocas de conhecimentos, apoio e ajudas constantes, em campo e em laboratório.
Agradeço ao Instituto Serrapilheira pelo fianciamento em grande parte desta pesquisa. Agradeço ao IDEMA e ICMBio pelas licenças concedidas para coleta de dados na APARC/RN e PARNAMAR/Fernando de Noronha. Agradeço também a todas as equipes de apoio logístico que possibilitaram as saídas de campo.
Meu muito obrigada a todo o corpo docente do Programa de Pós Graduação em Ecologia da UFRN, por todos os ensinamentos e contribuições fornecidas ao longo destes dois anos. Agradeço também a Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), pela concessão da bolsa.
Agradeço a todos os amigos e amigas que estiveram ao meu lado durante esta caminhada, por me ouvirem e me apoiarem em todos os momentos.
6 Agradeço, por fim, a todos que de alguma forma contribuíram para o desenvolvimento deste trabalho. Muito obrigada!
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ISTA DE FIGURAS1. STUDY SITE AND 3D MODELS EXAMPLES ………... 18 2. REPRESENTATION OF ANALYZED HEALTH VARIABLES.……….... 20 3. TEMPORAL VARIATION OF TEMPERATURE……… 22 4. HEALTH VARIABLE ANALYZED FOR Siderastrea stellata……….………... 24 5. HEALTH VARIABLE ANALYZED FOR Montastraea cavernosa……..…...… 26 6. COLOR DIFFERENCE OF Siderastrea stellata PRESENT IN COASTAL AND
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ISTA DE TABELAS1. PERMANOVA TABLE OF RESULTS FOR Siderastrea stellata…………...…. 23 2. SIMPER TEST FOR MOST SIGNIFICANT DIFFERENCES BETWEEN
OCEANIC SITES FOR Siderastrea stellata……….…....…….. 25 3. PERMANOVA TABLE OF RESULTS FOR Montastraea cavernosa…....…….. 27 4. SIMPER TEST FOR HEALTH VARIABLES BETWEEN COASTAL AND OCEANIC AREAS FOR Montastraea cavernosa……...….... 27 5. SUPPLEMENTARY TABLE OF TYPES OF REEFS, SITES OF DATA COLLECTION, GEOGRAPHIC COORDINATES, MONTHS OF MONITORING
AND NUMBER OF MONITORED
COLONIES………. 45 6. SUPPLEMENTARY TABLE OF THE ANTHROPOGENIC IMPACTS IN
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ONTEÚDO 1. RESUMO ………...…..….….…….. 8 2. ABSTRACT ... 9 3. INTRODUÇÃO GERAL ………...…... 10 4. ABSTRACT ………....….…... 14 5. INTRODUCTION ………..…. 156. MATERIAL AND METHODS ………....….. 17
5.1.: Study Site ……….... 17
5.2.: Data Collection ...……… 19
5.3.: Image processing ……… 19
5.4.: Coral health variables ………. 20
5.5.: Data Analysis ……….. 21 6. RESULTS ... 21 7. DISCUSSION ………... 27 8. Acknowledgements ... 32 9. CONCLUSÃO GERAL ... 32 10. References ... 34 11. Supplementary material ... 45
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ESUMODevido à sua proximidade a áreas mais populosas, recifes costeiros podem estar potencialmente mais propensos aos efeitos de impactos antropogênicos em comparação aos recifes oceânicos. Em ambientes costeiros, os corais podem ser mais rapidamente afetados por esses impactos locais, apresentando alterações em suas condições de saúde, dependendo da espécie e de variáveis ambientais como profundidade, temperatura e exposição à luminosidade. Comparar a saúde dos corais em ambientes costeiros e oceânicos, dentro da mesma faixa latitudinal, pode fornecer informações sobre como os impactos antropogênicos e a dinâmica natural do ambiente contribuem para determinar a saúde dos corais. Monitoramos 53 colônias do coral Siderastrea stellata (~5m de profundidade) e 28 de Montastraea cavernosa (~30m de profundidade) em recifes costeiros (Rio Grande do Norte; ~ 5 ° S) e oceânicos (Fernando de Noronha; ~ 3 ° S) do nordeste brasileiro. Nesses locais, as espécies monitoradas estão entre os principais corais construtores dos recifes. Monitoramos essas colônias trimestralmente durante um ano (2018-2019), utilizando modelos tridimensionais gerados por fotogrametria, a partir dos quais avaliamos indicadores de saúde dos corais (branqueamento, mortalidade, doenças e sobrecrescimento de algas). Ambas as espécies monitoradas apresentaram bom estado de saúde nos recifes costeiros e oceânicos ao longo de todo o ano, sem registro de branqueamento intenso durante o período monitorado. Em um dos ambiente recifais oceânicos, observamos períodos de maior branqueamento relacionado à dinâmicas naturais deste ambiente levando ao soterramento das colônias. Colônias de S. stellata permaneceram, em geral, mais saudáveis em áreas costeiras do que oceânicas, o que pode estar relacionado à menor exposição à luz nas áreas costeiras, onde há maior turbidez da água, em comparação aos recifes oceânicos. O estado de saúde de M. cavernosa foi estável e, apesar de apresentarem diferenças entre áreas costeiras e oceânicas, os corais em todos os locais monitorados mantiveram em média, 80% de sua superfície em estado saudável. A temperatura superficial da água também foi semelhante e relativamente constante em recifes costeiros e oceânicos. A saúde dos corais foi mais afetada por variações do ecossistema local (e.g. soterramento natural) do que pela
10 proximidade com o impacto humano, indicando que a dinâmica temporal local precisa ser levada em consideração ao avaliar a resposta dos corais aos impactos humanos.
Palavras-chave: Ecossistemas recifais, Siderastrea stellata, Montastraea cavernosa, impactos antropogênicos, dinâmicas locais, branqueamento de corais, Fernando de Noronha.
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BSTRACTDue to their proximity to more populated areas, coastal reefs can be more prone to the effects of local anthropogenic impacts than oceanic reefs. The response of corals to these impacts will depend on the species but also on environmental variables such as depth, temperature and exposure to light, determined by the local dynamics of each ecosystem. Comparing coral health between coastal and oceanic environments, within the same latitudinal range, can inform how anthropogenic impacts and the ecosystem´s natural dynamics affect coral health. We monitored colonies of the corals Siderastrea stellata (~ 5m deep) and Montastraea cavernosa (~ 30m deep) on coastal (Rio Grande do Norte; ~ 5 ° S) and oceanic (Fernando de Noronha; ~ 3 ° S) reefs in northeastern Brazil, where these species are among the main reef builders. We monitored 53 colonies of S. stellata and 28 of M. cavernosa quarterly for one year (2018-2019), using three-dimensional models generated from photogametry. From the models, we quantified the percentage of coral surfaces presented bleaching, mortality, disease and algal overgrowth, as indicators of coral health. Both monitored species presented good health status in coastal and oceanic reefs, with no record of intense bleaching during the monitored period, except for one of the oceanic reef environments that experienced an expressive burial event due to the local dynamics. Colonies of S. stellata, remained generally healthier in coastal areas than in oceanic areas, which may be related to less exposure to light in coastal areas compared to oceanic reefs. The health status of M. cavernosa was stable and, despite differing between coastal and oceanic areas, the corals in all monitored sites had, on average, 80% of their surface in a healthy state indicating relatively stable health conditions. The water temperature was also similar and relatively constant in coastal and oceanic reefs. Coral health was more affected by variations in the local ecosystem (e.g. natural burial) than by proximity to human impact, indicating that natural local dynamics needs to be accounted when assessing the response of corals to human impacts.
Keywords: Reef ecosystems, Siderastrea, Montastraea, anthropogenic impacts, local dynamics, coral bleaching, Fernando de Noronha.
11 INTRODUÇÃO GERAL
Ambientes recifais possuem alta diversidade, riqueza e produtividade, e, portanto, desempenham funções e fornecem serviços ecossistêmicos que abrangem esferas sociais, econômicas e ambientais (Birrel et al. 2008; Burke et al. 2011). Ocupando aproximadamente 0,02% da área total dos oceanos, os recifes abrigam cerca de 25% de todas as espécies marinhas existentes (Spalding & Grenfell, 1997; Davidson, 1998). As principais espécies bioconstrutoras destes ambientes são os corais, organismos sensíveis a alterações climáticas e por isso, bons bioindicadores de mudanças ambientais, sejam elas de origem antrópica ou natural (West & Salm 2003; Leão et al. 2008). Os corais são importantes organismos estruturadores dos recifes, possuem alta relevância ecológica e conferem maior complexidade aos ambientes recifais (Wilson et al. 2007; Cinner et al. 2009; Graham et al. 2009; Graham & Nash, 2013)
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Devido à complexidade, os corais podem gerar maior disponibilidade de alimento, refúgio contra predação e abrigo para diversas espécies (Wilson et al. 2006; Pratchett el al., 2008; Pratchett et al. 2014).As formações recifais coralíneas abrangem 109 países ao redor do mundo e são predominantemente encontradas em ambientes tropicais de águas mais quentes e transparentes (Hoegh-Guldberg, 1999; Birkeland, 1997; Pandolfi et al. 2011). No Brasil os recifes coralíneos situam-se principalmente ao longo da região Nordeste, geralmente próximos a costa (Ferreira & Maida, 1997), onde há também maior concentração populacional, favorecendo atividades econômicas, turísticas, esportivas e de recreação (Soopa et al. 2007). Essas atividades antrópicas acabam por gerar diversos impactos locais nestes ambientes no Brasil e em outros países do mundo. Como resultado, cerca de 20% dos recifes do planeta já foram degradados e aproximadamente 35% encontram-se ameaçados (Wilkinson et al. 2008).
Como consequência dos crescentes impactos, os seres que habitam esses ambientes são afetados. No caso dos corais, o principal sintoma é o branqueamento, caracterizado pela interrupção da simbiose entre corais e dinoflagelados conhecidos como zooxantelas, podendo ocorrer em porções ou em toda a superfície coralínea (Hoegh-Guldberg et al. 2007). O branqueamento pode ser desencadeado de diversas formas, como por exemplo, com o aumento da temperatura, variações de salinidade, aporte de nutrientes, poluição e infecções virais (Birkeland, 1997; Stone et al. 1999; Hughes et al. 2007 Vermeij & Sandin, 2008).
12 Outros efeitos podem se desenvolver a partir do branqueamento como palidez, adoecimento, sobrecrescimento de algas e até morte (Raymundo et al. 2005; Kaczmarsky, 2006). A diminuição na condição de saúde e consequente morte dos corais pode ocasionar a degradação do ecossistema e resultar em perda de complexidade e diversidade (Alvarez-Filip et al. 2009).
Por consequência dos ambientes recifais localizarem-se em maioria próximos a áreas costeiras e, portanto, mais populosas, os recifes dessa região podem ser também os mais propensos a sofrerem os efeitos diretos e indiretos dos impactos antropogênicos (Gorgulla & Connell, 2004; Fabricius et al. 2007; Bellwood et al. 2011; Mora et al. 2011) em comparação aos recifes oceânicos com menor população humana (Pandolfi et al. 2003; Sandin et al. 2008). Em ambientes costeiros, os corais podem ser mais rapidamente afetados por esses impactos que tendem a ser mais frequentes, apresentando alterações em suas condições de saúde (Guldberg & Wilkinson, 2004). Os efeitos das mudanças globais combinadas às mudanças locais, abióticas ou antropogênicas, podem influenciar fortemente os recifes, à medida que estão mais próximos da superfície e das atividades humanas do entorno, fazendo com que os impactos sejam sentidos de forma muito mais intensa (Brown e Howard, 1985; Hoeksema e Matthews, 2011).
Os ambientes naturais estão sob constante processo de mudanças como resultado das diversas variações em condições ambientais. Avaliar o ambiente ao longo do tempo nos permite medir como uma perturbação que ocorre no período atual pode influenciar a resposta futura desse ambiente em um período subsequente (Kelmo & Attrill, 2013). Também é importante analisar séries temporais considerando identificar dinâmicas naturais e diferenciá-las de impactos locais e globais. Em ambientes recifais, sensíveis a distúrbios, os estudos temporais podem ajudar a prever como esses ecossistemas responderão às mudanças ambientais, quão resilientes são e o processo pelo qual o ambiente está passando (Hughes et al. 2016).
Existem diversas formas de avaliar a saúde dos corais, dentre elas se destaca o monitoramento através de censos visuais e fotografias (Gutierrez-Heredia et al. 2016). Realizar o acompanhamento de formações coralíneas possui grande importância para que seja possível mensurar como estes organismos respondem aos impactos e dinâmicas locais, e também para fazer previsões sobre como os corais poderão reagir a cenários futuros de mudanças ambientais (Todd et al. 2001). Mais recentemente, a modelagem tridimensional a partir da fotogrametria passou a ser utilizada com mais frequência em estudos de ambientes
13 recifais, particularmente com foco na avaliação da complexidade estrutural (Dustan et al. 2013). Esta técnica, apresenta grande potencial para monitorar de forma mais precisa e acurada variáveis de saúde dos corais. Modelos tridimensionais reduzem a perda de informações que ocorre em imagens bidimensionais devido ao achatamento (Vieira et al. in prep.), permite identificar mudanças bruscas e não naturais na estrutura dos corais, e reduz o tempo em campo, viabilizando a elaboração de um banco de dados temporais que podem ser sempre revisitados e utilizados em estudos futuros (Shortis et al. 1998; McKinnon et al. 2011).
Neste trabalho, monitoramos os corais Siderastrea stellata (Verril, 1868) e Montastraea cavernosa (Linnaeus, 1767) em recifes costeiros (Rio Grande do Norte) e oceânicos (Fernando de Noronha) do nordeste brasileiro, a fim de compreender se os diferentes níveis de impacto antrópico local poderiam influenciar a saúde desses corais. Essas espécies apresentam grande relevância ecológica, estão entre os principais corais bioconstrutores dos ambientes recifais brasileiros e apresentam alta tolerância às constantes variações ambientais. Monitoramos colônias trimestralmente ao longo do período de um ano em quatro ambientes recifais situados na zona costeira do Rio Grande do Norte, sendo dois rasos (até 5 metros de profundidade) e dois mais profundos (até 30 metros de profundidade) e três ambientes recifais oceânicos, localizados no Arquipélago de Fernando de Noronha, sendo dois rasos e um mais profundo, seguindo as mesmas profundidades dos recifes costeiros. Esperávamos encontrar que os níveis de saúde dos corais em recifes oceânicos fossem melhores do que os encontrados em recifes costeiros, devido a menor influência antrópica e que essas diferenças fossem menores em recifes mais profundos devido à um menor impacto local direto. Sendo assim, esta dissertação está estruturada em um capítulo único intitulado “3-D MONITORING OF CORAL HEALTH: COMPARISONS BETWEEN COASTAL AND OCEANIC REEFS”, apresentado em formato de artigo científico.
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CAPÍTULO ÚNICO
3-D MONITORING OF CORAL HEALTH: COMPARISONS BETWEEN COASTAL AND OCEANIC REEFS
15 3-D MONITORING OF CORAL HEALTH:
COMPARISONS BETWEEN COASTAL AND OCEANIC REEFS Louize F. C. Correia1, Jessica Bleuel1, Edson A. Vieira1, Guilherme O. Longo1 ¹ Laboratório de Ecologia Marinha, Departamento de Oceanografia e Limnologia, Universidade Federal do Rio Grande do Norte. Av. Via Costeira/Senador Dinarte Mariz s/n – 59014-002 Natal, RN, Brasil.
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BSTRACTDue to their proximity to more populated areas, coastal reefs can be more prone to the effects of local anthropogenic impacts than oceanic reefs. The response of corals to these impacts will depend on the species but also on environmental variables such as depth, temperature and exposure to light, determined by the local dynamics of each ecosystem. Comparing coral health between coastal and oceanic environments, within the same latitudinal range, can inform how anthropogenic impacts and the ecosystem´s natural dynamics affect coral health. We monitored colonies of the corals Siderastrea stellata (~ 5m deep) and Montastraea cavernosa (~ 30m deep) on coastal (Rio Grande do Norte; ~ 5 ° S) and oceanic (Fernando de Noronha; ~ 3 ° S) reefs in northeastern Brazil, where these species are among the main reef builders. We monitored 53 colonies of S. stellata and 28 of M. cavernosa quarterly for one year (2018-2019), using three-dimensional models generated from photogametry. From the models, we quantified the percentage of coral surfaces presented bleaching, mortality, disease and algal overgrowth, as indicators of coral health. Both monitored species presented good health status in coastal and oceanic reefs, with no record of intense bleaching during the monitored period, except for one of the oceanic reef environments that experienced an expressive burial event due to the local dynamics. Colonies of S. stellata, remained generally healthier in coastal areas than in oceanic areas, which may be related to less exposure to light in coastal areas compared to oceanic reefs. The health status of M. cavernosa was stable and, despite differing between coastal and oceanic areas, the corals in all monitored sites had, on average, 80% of their surface in a healthy state indicating relatively stable health conditions. The water temperature was also similar and relatively constant in coastal and oceanic reefs. Coral health was more affected by variations in the local ecosystem (e.g. natural burial) than by proximity to human impact, indicating that natural local dynamics needs to be accounted when assessing the response of corals to human impacts.
Keywords: Reef ecosystems, Siderastrea, Montastraea, anthropogenic impacts, local dynamics, coral bleaching, Fernando de Noronha.
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NTRODUCTIONReef environments harbor great biodiversity and ecological importance (Connell, 1978), providing many ecosystem goods and services to human societies (Birrel et al. 2008; Burke et al. 2011). Coralline organisms are often the main reef bioconstructors, adding complexity to the environment, which generates shelter, refuge and food for several species (Wilson et al. 2007; Cinner et al. 2009; Graham et al. 2009; Graham & Nash, 2013). However, reefs are constantly under the influence of increasing anthropogenic impacts resulting from multiple sources, including global climate change, pollutant dispersion, river nutrient input, solid waste deposition and overfishing (Wooldridge et al. 2005). Simultaneously, reef ecosystems also experience the local dynamics of abiotic factors that may also affect the health status of these organisms and their ability to cope with anthropogenic impacts. Given the scenario of reef degradation, it is fundamental to understand the relative role of local ecosystem dynamics and anthropogenic impacts in determining coral health.
Coral health can vary with environmental conditions and human impacts, which can cause bleaching, paleness, disease and algal overgrowth (Bellwood et al 2004; Wilkinson, 2008). Coral bleaching is an interruption of the symbiosis between corals and dinoflagellates of the family Symbiodiniaceae, which provide nutrients and often pigmentation to corals (Douglas, 2003; Hoegh-Guldberg et al. 2007; La Jeunesse et al. 2018). Bleaching represents the partial or total loss of symbiotic algae or photosynthetic pigments (Lough & van Oppen, 2009) and, once it occurs, the coral often become more prone to develop secondary effects such as diseases, algal overgrowth and even death (Raymundo et al. 2005; Kaczmarsky, 2006). Increasing water temperature is one of the main factors responsible for coral bleaching in several reefs in the world (Stone et al. 1999). Less rainy months associated with high solar irradiation on the water column, may cause coral bleaching (Brown et al. 2000; Dunne & Brown, 2001; Lesser & Farrell, 2004). Also, sedimentation, or levels of turbidity, can vary between coastal and oceanic reefs, due to their own local dynamics, and, burial, which is the mostly responsible of abrasion events, this factors can be critical determinants of coral health (Rogers, 1990; Lirman & Manzello, 2010; Segal & Castro, 2011). Therefore, the survival of corals depend not only on the anthropogenic factors themselves, but also on the influence of other abiotic factors such as solar radiation intensity, sedimentation, nutrient intake and pH. (Birkeland, 1997; Fitt et al. 2001; Hughes et al. 2007; Vermeij & Sandin, 2008; Albright et al. 2008; Castro et al. 2012).
17 Natural environments are constantly changing, as a response to seasonal changes, rainfall, exposure to waves, among others. A time-scale environmental assessment allows us to measure how a disturbance occurring in the current period may influence the future response of such environment in a subsequent period (Kelmo & Attrill, 2013). It is also important to analyze time series to identify and differentiate natural dynamics from local and global anthropogenic impacts. In reef environments, which are sensitive to disturbances, temporal studies can help to predict how these ecosystems will respond to environmental changes, how resilient they are, and the process that the environment is undergoing (Hughes et al. 2016).
There are several techniques commonly used to perform coral monitoring in natural environments, including visual censuses, transects, photographs, videos, among others (Gutierrez-Heredia et al. 2016). Coral monitoring can be an important tool to identify anthropogenic and environmental changes in a short period, as well as assessing the ability of these organisms to resist and recover from drastic changes along time (Todd et al. 2001). With the growing development of technologies, using 3D models to monitor corals is now possible and can be an effective approach to perceive subtle changes (Dustan et al. 2013). Tridimensional models can reduce the information loss that occurs in photographs, reduces fieldwork effort which is often expensive, enable accurate measurements through software and allows researcher to develop a temporal database that can always be revisited and even be used for future studies (Shortis et al. 1998; McKinnon et al. 2011).
Most coral monitoring studies are conducted in tropical reefs in the Pacific and in the Caribbean (Bakker et al. 2017; Hedge et al. 2017; Steneck et al. 2019), while the temporal dynamics of corals in marginal reefs are less explored. The Brazilian coast harbor most reefs in South Western and are characterized by dominance of macroalgae and low occurrence of corals (Aued et al. 2018). Although in relatively low density in most areas, corals are the main bioconstructors organisms in Brazilian reef environments (Ferreira & Maida, 1997; Aued et al. 2018). Monitoring coral health in marginal reefs may provide information on their role as potential refugia in future climate change scenarios (Cacciapaglia & Woesik, 2015), elucidating how coral health can be affected by both local environmental dynamics and anthropogenic impacts in these areas. A promising approach to understand the relative contribution of the local dynamics and anthropogenic impacts on coral health is to monitor the same coral species in coastal reefs (closer to higher human density and likely under higher human impact) and oceanic reefs (with less direct human influence and likely less
18 direct human impact) within the same latitudinal range. This minimize variations in abiotic factors such as temperature and solar radiation, ensuring the similarity among locations to some extent.
We monitored colonies of Siderastrea stellata (~2m deep) and Montastraea cavernosa (~25m deep) in coastal (5°S) and oceanic (3 °S) reefs in northeastern Brazil using 3D models derived from structure from motion photogametry. These species, S. stellata and M. cavernosa are the most common reef bioconstructors organisms in the shallow (S. stellata) and deeper (M. cavernosa) reefs of northeastern Brazil(Ferreira & Maida, 1997; Leão et al. 2003). Assuming that coastal reefs are potentially under higher local human impact than oceanic reefs, we hypothesized that coral health in these areas would be worse in comparison to corals in oceanic reefs, which are potentially less impacted by local human impacts. Such differences in coral health would be more intense in shallower areas, which are more prone to both human impact and variation in abiotic variables, in comparison to more stable deeper areas.
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ATERIAL ANDM
ETHODS STUDY SITESThis work was conducted in Northeastern Brazil, at coastal reefs along the state of Rio Grande do Norte (05 ° 33 '32 "S; 35 ° 04 '21 "W), with four sampling sites, two shallow reefs in Rio do Fogo, ‘Garças’ and ‘Rastro’ (~ 2m deep) and two deeper reefs in Natal, ‘Batente das Agulhas’ and ‘Travessa’ (~ 25m deep); and at the oceanic Archipelago of Fernando de Noronha, that lies about 345km from the mainland (03 ° 50 '25 "S, 32 ° 24' 41" W), with two shallow reefs, ‘Atalaia’ and ‘Sueste’ (~ 2m deep), and one deeper reef ‘Laje Dois Irmãos’ (~ 25m deep), (Figure 1; Table S1). The shallow reef of Rio do Fogo (05 ° 16 '22 "S; 35 ° 22 '59 "W) is within Coral Reef Environmental Protection Area (APARC; Amaral et al. 2005) directed and enforced by the State government of Rio Grande do Norte. The deeper reefs are located about 20 km from the coast in front of the city of Natal (05 ° 33 '32 "S; 35°04 '21"W) and are not within marine protected areas. Fernando de Noronha Archipelago comprises two marine protected areas: a National Marine Park and an Environmental Protection Area, both allowing different levels of sustainable use (low use and high use, respectively), managed by Chico Mendes Institute for Conservation of Biodiversity (ICMBio) directed by Brazilian federal government.
19 Fig. 1 Coastal sites are represented by Rio do Fogo (05 ° 16 '22 "S; 35 ° 22 '59 "W) and Natal (05 ° 33 '32 "S; 35 ° 04 '21 "W) reefs, colored in light green. Oceanic sites are represented by Fernando de Noronha archipelago (03 ° 50 '25 "S, 32 ° 24' 41" W), colored in dark green. In shallow reefs (up to 5 meters) the species sampled was Siderastrea stellata and in deeper reefs (up to 30 meters) Montastraea cavernosa, at both coastal (on the left) and oceanic (on the right) areas. the numbers represent the data collection locations, 1: Laje Dois Irmãos; 2: Sueste; 3: Atalaia; 4: Garças; 5:
20 Rastro; 6: Batente das Agulhas; 7: Travessa. Below, schematic representation of three-dimensional models generated by AgiSoft PhotoScan 3D modeling software, of the same individuals of Siderastrea stellata (on the left) and Montastraea cavernosa (on the right) along the four monitoring periods represented by T1, T2, T3 and T4.
DATA COLLECTION
We marked 24 colonies of S. stellata in two different areas of a coastal reef (Rio do Fogo: Garças and Rastro reefs), with individuals tagged in each area (depth 0-3m during low tide). Similarly, in Fernando de Noronha, 29 corals were marked in two distinct reef environments, the Sueste Bay and Atalaia pool, in both places the depths interval is 0 - 2 meters during low tide. For M. cavernosa, we marked 14 colonies in two deeper reefs (18- 30 m) near the coast of Rio Grande do Norte (Travessa and Batente das Agulhas) (Table S1). In Fernando de Noronha, 14 colonies were marked at a single deeper site, Laje Dois Irmãos, due to logistical constrains. We deployed rebars and PVC tags in the reef matrix on the vicinity of the monitored coral without damaging any organism. The same colonies were visited four times, April 2018 (T1), July 2018 (T2), October 2018 (T3) and January 2019 (T4) (Table S1), respectively fall, winter, spring and summer in the south hemisphere. In this study, reefs between depths of 18-30 meters, where we monitored M. cavernosa, will be addressed as deep reefs, despite being within the euphotic zone, and reefs up to 5 meters, where we monitored S. stellata will be addressed as shallow reefs. Within these sites, we also monitored sea surface temperature (SST) throughout Aqua Moderate Resolution Imaging Spectroradiometer (Aqua Modis) satellites. We also collected information on human populations and characterization of anthropogenic impacts in our coastal and oceanic reefs using data from the Brazilian Institute of Geography and Statistics (IBGE). We indicate the estimated population of each location, demographic density, number of tourists, fishermen and watercrafts (Table S2).
IMAGE PROCESSING
Underwater imaging was performed using a GoPro Hero 6 and colonies were carefully recorded (360°), from a mean distance of 30 centimeters, making sure that the entire organism was framed. From the videos, we obtained a 100 frames, uploaded them in AgiSoft PhotoScan software (standard version 64 bit), in which we: aligned the photos, built dense clouds, mesh and texture, finally obtaining the 3D models (Figure 2). We then exported 3D models and performed the measurements using the MeshLab version 2016.12,
21 from the models, we quantify the surface area of each colony and from this, we quantify the percentage area bleached, overgrown with algae, sick and pale, for each colony. In total we generated 367 three-dimensional models, 202 of Siderastrea stellata and 165 of Montastraea cavernosa.
CORAL HEALTH VARIABLES
We analyzed the surface of each colony in order to characterize its health status, classified within four health variables as indicators: bleaching, paleness, algae overgrowth and disease. Therefore, we describe coral health as the percentage of coral surface within each category. Coral bleaching was considered the total loss of natural pigmentation provided by zooxanthellae, resulting in a portion of the colony all white (Figure 3a). Paleness was recognized by the intermediate state between the healthy and the bleached color of the colony, characterized by a faint color different from the natural hue (Figure 3b). Paleness does not necessarily mean that the colony will bleach and may return to healthy color without going through the full bleaching process. Algal overgrowth was characterized by initially small patches of algae growing over the surface of the coral. This process can be progressive and irreversible, since the colony has covered points, hardly returns to its initial state (Figure 3c). For the diseases category, the presence of particular attributes was observed, such as pink spots scattered across the surface of the coral, usually appearing around spots overgrown by algae and may result in bleaching (Aeby, 1993; Benzoni et al. 2010; Raymundo et al. 2008; Thinesh et al. 2013) facilitating algal colonization or returning to a healthy state if conditions become favorable (Figure 3d).
Fig. 2 Health variables analyzed in this study: A) Bleaching; B) Paleness; C) Algae overgrowth; D) Diseases. Photos are of Siderastrea stellata. The same health categories were considered for Montastraea cavernosa but due to little variation in this specie, it was not possible to illustrate.
22 DATA ANALYSIS
To assess whether coral health status was influenced by location relative to the coastal and oceanic areas, we used multivariate analysis considering all the health parameters. For both species, similarity matrices were constructed using the health parameters (square root transformed) and the Bray-Curtis distance. Health comparisons of the two coral species were made separately for each species using PERMANOVAS with 999 permutations (Anderson, 2001). Health status of Siderastrea stellata was compared between areas (fixed factor, 2 levels: coastal and oceanic), considering two sites in each area (nested random factor, 2 levels: Garças and Rastro in the coastal area; Atalaia and Sueste in the oceanic) over one year (random factor, 4 levels: T1, T2, T3, T4, corresponding to each of the four visits). Because it was not possible to sample two sites in the oceanic area, comparisons on the health status of Montastraea cavernosa followed the same model of S. stellata, but in this case, with only area and time. For significant effects or interactions, pairwise comparisons were conducted and the most important health parameters for such differences were obtained using SIMPER test (Clarke, 1993).
R
ESULTSThe sea surface temperature was similar between coastal and oceanic sites throughout the monitoring period (Fig. 3), with temperature peaking between the months of January and April 2019. While the average temperature for coastal reefs was 27.9ºC and the maximum of 29.9°C, the average and maximum at oceanic reefs were 27.7°C and 29.8°C, respectively.
23 Fig. 3 Abiotic data of sea surface temperature (SST), collected from satellite database for coastal sites (blue line) and oceanic sites (orange line). (Aqua Modis satellites data). Monitoring periods are indicated by the dashed arrows.
Along the entire monitoring period, Siderastrea stellata in coastal reefs were generally healthier than those in oceanic reefs (Table 1, Fig. 4). Colonies of S. stellata in coastal areas presented higher healthy (26% of contribution to differences between areas - Simper results), paleness levels (20% of contribution - Simper results) and disease (14% of contribution), while colonies in the oceanic reefs showed a higher bleaching (20% of contribution) and algae overgrowth (20% of contribution) values (Fig. 4). Bleaching was higher in oceanic times, especially on T2, when bleaching reached ~25% after a burial event.
24 Coral disease, characterized by pink spots, generally maintained a percentage around 30% of all colonies for the localities where it was present and was stable over time. Algal overgrowth was more frequent in the shallow oceanic reefs, where 42% of the colonies where overgrown by algae after the burial event. The colonies in this site presented up to 50% of their surface area covered by seaweed on T4.
Table 1: Summary results of PERMANOVA test comparing the health status between coastal and oceanic areas along time for Siderastrea stellata, considering two sites in each area (Garças and Rastro at the coastal area; Atalaia and Sueste at the oceanic area). Values in bold indicate significant effects.
PERMANOVA table of results for Siderastrea stellata
Source df SS MS Pseudo-F P(perm)
Area 1 13338 13338 3.55 0.046
Time 3 3878 1292 1.09 0.402
Site(Area) 2 5278 2639 2.23 0.110 AreaxTime 3 4372 1457 1.23 0.384 Site(Area)xTime 6 7102 1183 2.92 0.003
26 There was also an interaction between sites and time, indicating that shallow oceanic sites varied through time. While sites in the coastal area were not different in any of the sampling times, Atalaia and Sueste, in oceanic shallow reefs, showed differences on T1 (post-hoc comparison; p-value = 0.003) and T2 (post-hoc comparison; p-value = 0.015) (see Table 1 for the main test). In T1, Atalaia showed a higher algal overgrowth, disease and paleness, while colonies in Sueste showed higher levels of healthy and bleaching. While in T2, colonies in Sueste showed higher levels of healthy and disease while in Atalaia a burial event resulted in a higher bleaching and algae overgrowth. These indicators contributed to the differences responsible for the interaction between sites and time (Table 2).
Table 2: SIMPER result showing the relative contribution (%) of the health variables that most
contributed to significant differences in health status between the oceanic shallow reefs, Atalaia (A) and Sueste (S) at sampling times T1 and T2 for Siderastrea stellata. Abbreviations in front of each variable stand in which location the health variable was higher.
T1
T2
Health variables (%) Health variables (%) Algae overgrowth (A) 31.22 Healthy (S) 36.45 Disease (A) 25.19 Bleaching (A) 34.28
Pale (A) 18.38 Disease (S) 11.56
Healthy (S) 12.63 Algae overgrowth (A) 11.44
Bleaching (S) 12.59
In general, Montastraea cavernosa presented a stable health status, between 70% and 100% healthy (Fig. 5). Paleness levels for this species reached up to approximately 40% at both coastal and oceanic areas, but showed rapid recovery in the oceanic area, on T3 and T4 (Fig. 5-h). In general, colonies of M. cavernosa, showed differences in health status between coastal and oceanic reefs during the sampling period, but depending on time, since on T2 both areas showed a similar health status (Table 3, Fig. 5).
28 The differences between coastal and oceanic reefs observed for M. cavernosa were majorly due to healthier colonies in oceanic reefs when compared to colonies in coastal reefs that showed higher levels of paleness (Table 5, Fig. 5). Additionally, disease was also important for differences between areas on T4, being higher in coastal area (Table 5). Table 3: Summary results of PERMANOVA test comparing the health status between coastal and oceanic areas along time for Montastraea cavernosa. Values in bold indicate significant effects.
PERMANOVA table of results for Montastraea cavernosa
Source df SS MS Pseudo-F P(perm)
Area 1 3460 3460 1.70 0.318
Time 3 6168 2056 8.04 0.001
AreaxTime 3 6176 2058 8.05 0.001
Table 4: SIMPER result showing the relative contribution (%) of the health variables that most
contributed to significant differences in health status between coastal (C) and oceanic (O) reefs at sampling times T1, T2 and T4 for Montastraea cavernosa. Abbreviations in front of each variable stand in which location the health variable was higher.
T1 T2 T4 Health variables (%) (%) (%) Pale (C) 74.29 68.24 64.12 Healthy (O) 22.68 23.93 25.24 Disease (C) - - 5.72
D
ISCUSSIONOverall, both Siderastrea stellata and Montastraea cavernosa showed high healthy percentages over the monitoring period. We found that potential proximity to anthropogenic pressures and coastal influence did not explain coral health status in shallow (<5m) and deeper (18-30m) reef environments, but that intrinsic conditions at each location strongly determined coral health. Our results indicate that S. stellata and M. cavernosa were able to cope with the environmental variations along the monitored year. While M. cavernosa may have been healthier and more stable than S. stellata due to the greater depth, S. stellata is known for its high resistance and resilience to environmental disturbance events, as well as variations of temperature, salinity, water turbidity (Leão et al. 2003) and burial (Lirman &
29 Manzello, 2009). M. cavernosa is broadly tolerant to temperature variations (Fitt and Warner, 1995), is efficient under low light conditions (Lesser et al. 2010) and have phenotypic plasticity to better adapt to the environment where they are (Davies, 1980). Our hypotheses predicted that there would be a difference in health status between coral colonies from coastal and oceanic environments, and that the greatest damage to health status would be in coastal environments due to the proximity of anthropic influence. We observed differences between coastal and oceanic areas for both species, however the healthiest reefs were the oceanic, not the coastal reefs. This could indicate that environments under chronic stress may favor increasingly resistant populations (Weis, 2010; McClanaham, 2017; Safaie et al. 2018) or that the human impact do not vary significantly between the locations we compared. We also predicted that such impacts would be stronger in shallow than in deeper reefs, as the depth increases, the external influence is attenuated. Indeed, there was greater stability in the health of M. cavernosa, indicating that this may be related to the deeper reefs suffering less from external influence (Bongaerts et al. 2010; Frade et al. 2018). Despite these common outcomes, S. stellata, presented particular dynamic among the studied sites.
For Siderastrea stellata colonies, the indicator with the greatest influence on their health status was paleness, reaching approximately 15% in coastal reefs. This variation could be explained according to the light intensity received (Brown & Dunne, 2008). The density of zooxanthellae in the coralline polyps is directly related to the need of the coral to achieve its photosynthetic efficiency (Hoegh-Guldberg & Smith, 1989; Deschaseaux et al. 2014). As the luminosity intensifies in an environment, there may be a greater outflow of these microalgae and thus avoid photoinhibition of these organisms (Lesser & Shick, 1989; Nakamura et al. 2005). The effects of global change combined with local changes, abiotic or anthropogenic, directly influence shallow reef environments as they are closer to the surface and surrounding human activities, so, impacts are felt much more intensely (Brown and Howard, 1985; Hoeksema and Matthews, 2011). As observed in the coral health status, variations in shallow environments, especially in the oceanic reefs, were felt with more evident fluctuations for bleaching and algae overgrowth. The low depth favors that a greater amount of light penetrating and heating the water, affecting the coral health status.
Interestingly, we observed differences in the color tone of Siderastrea stellata, with coastal colonies being darker than and oceanic colonies. Such variation in tones does not necessarily mean that the corals are not healthy, but that this difference may be related to how the abiotic variables of temperature and mainly luminosity are influencing the type and
30 density of endosymbionts in the colonies (Stimson, 1997; Brown et al. 1999; Costa et al. 2004). Colonies of Siderastrea stellata in the oceanic sites presented a more faded shade of yellow in detriment to the corals of the same species that inhabit the coastal reefs. High radiation can cause photoinhibition of zooxanthellae microalgae and, consequently, dissociate them with corals, explaining why the lighter shade in corals. On the other hand, suspended sediment, that affects water transparency, can preserve corals for bleaching effects, contributing to the photoprotective effect and making turbid water areas less vulnerable to bleaching than clearer waters (Phongsuwan, 1998; Piniak and Storlazzi, 2008; Erftemeijer et al. 2012).
Fig. 6 Variations in the color tone of Siderastrea stellata between shallow coastal reefs represented by (A) and (B) and oceanic reefs represented by (C) and (D).
In oceanic reefs, because the bleaching event occurred shortly after a mass burial, this would be the main indicator that influenced the health status of the colonies, burial can cause abrasion in the coral tissues, resulting in loss of mucosa and pigments, causing bleaching and susceptibility to diseases. Although the burial was not measured, it was observed in the field, where we noticed that almost 50% of the colonies at Atalaia site were completely covered. After this event, the buried colonies had 100% bleaching on their
31 surface, indicating the consequences of the abrasion. Over the following monitoring periods, it was possible to notice the color recovery also associated with the appearance of diseases (about 7%) and mainly the overgrowth of algae (approximately 20%). Algae overgrowth in corals may be related to coral fragility after bleaching events, where coral is more susceptible to overgrowth of organisms on its surface (Smith et al. 2008; Barott et al. 2012). The high oligotrophy of these environments allows a lot of light radiation to penetrate the water column and reach the surface of the coral (Braga et al. 2018). Further favoring the overgrowth of algae that photosynthetically benefits from light (Singh & Singh, 2015). Burial in corals can cause several damages, such as temporary reduction of photosynthetic capacity, reduction of colony growth rate, tissue death, bleaching and thus colony death (Segal et al. 2008; Lirman & Manzello 2009). Burial may also be considered catastrophic for some coralline environments (Pastorok and Bilyard, 1985), whether covered with a few centimeters (Rogers, 1990). On the other hand, reefs can be largely resistant to burial events, even if the colonies are covered for several days and weeks, without suffering many negative effects (Erftemeijer et al. 2012). Algae shading and competition for space between these benthic organisms and algae, can also result in damage to the surface of the colonies, such as disease and bleaching (Barott et al. 2014).
Oceanic reefs tend to be more susceptible to natural events such as strong waves and winds (Nieuwaal, 2001; Barros et al 2014). To exemplify how resilient and resistent corals can be, as soon as they were dug up, a rapid and progressive recovery process began, 3 months later, the bleaching rate had already decreased ~20% and 6 months later reached less than 10%. Lirman and Manzello (2009) tested the photosynthetic capacity and respiration of Siderastrea radians colonies and observed that after 24h of burial, there was a significant decline in photosynthesis and after 48h, the respiration rate exceeded photosynthesis. One week after the burial event, the S. radians colonies were fully recovered. In shallow coastal reef environments, we observed no large variations over time, only a predominance of the pale variable in the colonies. This could be because the environmental conditions experienced by these shallow coastal reefs are more moderate than oceanic reefs.
For the same degree of disturbance, shallow and deep reef environments may respond in different ways, with shallow reefs being the most impacted (Frade et al. 2018). The coral Montastraea cavernosa in the deeper reefs of the euphotic zone (~25 m), were also influenced by abiotic factors, although in smaller proportions. Temperature oscilations can affect the tonality of the colonies and cause pallor on their surface, as we can observe for
32 time T3 of the oceanic reefs, which had an increase in temperature reaching almost 30ºC (Fig. 3), fading occurred and was followed by almost 100% recovery three months after the event. For deeper reefs, the environmental conditions are generally more stable and do not vary dramatically over time (Frade et al. 2018). Some of the mentioned impacts also occur on deeper reefs, but not to the same magnitude or frequency. Corals in deeper zones may show little variation in their health status, because these zones suffer less variation of abiotic factors, remaining relatively stable throughout the year (Frade et al. 2018).
The stability of abiotic conditions in deeper environments, could attenuate the consequences of increasing temperatures because environmental changes can be more gradual, resulting in less coral bleaching (Teixeira et al. 2019). This process may be happening to M. cavernosa, which occurs in deeper zones, presenting lower temporal variation and higher health percentage for all sampled periods in both coastal and oceanic areas. Although coastal reef waters show higher levels of suspended sediment (Gorgulla & Connell, 2004; Aued et al. 2018), it is possible that this difference is not as significant between the deeper coastal and oceanic reefs, therefore does not cause significant changes to the health of the colonies in both sites. While deeper environments can act as refuge for drastic climate variations, they can only moderate impacts temporarily, as changes become more frequent and pronounced, the effects on corals can be just as harmful as in shallow environments (Erftemeijer et al. 2012).
The local dynamics in each studied location was more important to determine the health status of coral colonies than the proximity to anthropic impacts and coastal influence. For example, extreme events of burial that occurred in one of the shallow oceanic reefs, can strongly affect the healthy state of the corals. So, the effect of sedimentation and, consequently abrasion in shallow reefs can command the dynamic of these locals and possibly determine bleaching, and, that shallower reefs can be more instable and vary more over time, than deeper reefs with natural dynamics more stable. Therefore, the anthropogenic impacts on these environments may not be intense enough to cause severe damage to corals, or both areas are under similar levels of anthropogenic impacts. Alternatively, the stress regime suffered by these environments is happening at such a fast and constant pace that it is favoring the selection of increasingly resistant populations (Weis, 2010; McClanaham, 2017; Safaie et al. 2018). The intrinsic characteristics of each species studied and the location in which they live, allowed us to understand that Siderastrea stellata and Montastraea cavernosa are important reef-building organisms, able to withstand adverse conditions and
33 tolerate drastic changes without losing the resilient potential. Our results indicate that in order to understand the health dynamics of corals over time and how they will respond to global changes, it is necessary to account for the local dynamics (e.g., tidal conditions, wave action, wind, burial). Therefore, long-term monitoring can provide more accurate and reliable assessments of how ecosystems will respond to current and future impacts at the local and global levels.
A
CKNOWLEGDEMENTSWe would like to thank the Chico Mendes Institute for Conservation of Biodiversity (ICMBio), particularly Thayná Mello and volunteers and the staff of the diving company Sea Paradise in Fernando de Noronha; Dido and all the LECOM staff for technical and logistical support; as well as MM Teschima, NC Roos, JD Dias and B Segal for reading earlier drafts. This work was funded by Serrapilheira Institute (grant number Serra-1708-15364) awarded to GOL; by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 through a masters scholarship to LFCC and a postdoctoral scholarship to EAV; by the National Council for Scientific and Technological Development (CNPq) through a grant awarded to GOL (435201/2018-2) that funded a scholarship to JB and through the Long-Term Ecological Monitoring Program (PELD-ILOC ; 441241/ 5152016-6; C. E. L. Ferreira PI). GOL is grateful to a research productivity scholarship provided by the Brazilian National Council for Scientific and Technological Development (CNPq; 310517/2019-2).
C
ONCLUSÃO GERALDe forma geral, as espécies de corais Siderastrea stellata e Montastraea cavernosa apresentaram elevados níveis de saúde ao longo de todo o período de monitoramento. Ambas as espécies estudadas possuem características que as conferem mecanismos de resistência e resiliência. S. stellata é conhecida por sua alta resistência e resiliência a eventos de perturbação ambiental, além de variações de temperatura, salinidade, turbidez (Leão et al. 2003) e soterramento (Lirman & Manzello, 2009). Enquanto que M. cavernosa é tolerante à oscilações de temperatura (Fitt e Warner 1995), usa de forma eficiente a baixa luminosidade recebida (Lesser et al. 2010) e possui plasticidade fenotípica para melhor se adaptar a diversos ambientes ( Davies, 1980).
34 Houveram diferenças nas condições de saúde das colônias de Siderastrea stellata entre ambientes recifais costeiros e oceânicos, sendo que contrário às nossas predições, as taxas mais elevadas de saúde encontradas foram nos recifes costeiros. Houve maior ocorrência de branqueamento para S. stellata, particularmente em um dos sítios recifais rasos oceânicos, em decorrência de um evento de soterramento, onde 50% das colônias marcadas ficaram completamente cobertas. As colônias soterradas branquearam em 100%, mas recuperaram-se gradativamente nos períodos seguintes. Este evento tem relação com dinâmicas naturais deste local, o Atalaia em Fernando de Noronha, que passa por eventos periódicos de soterramento, causando recobrimento e abrasão das colônias que causam branqueamento. Em relação ao fato de que os corais costeiros apresentaram saúde elevada, é possível inferir que: esses ambientes que se encontram sob constantes estresses, possam favorecer populações cada vez mais resistentes a perturbações (Weis, 2010; McClanaham, 2017; Safaie et al. 2018); a pressão antrópica nesses ambientes não é suficiente para causar mudanças significativas sobre os corais; ou que o impacto antrópico entre os ambientes costeiros e oceânicos varia pouco. Ainda, a sedimentação mais intensa em recifes costeiros pode conferir foto proteção às colônias, reduzindo as chances de branqueamento.
Nossa hipótese inicial era de que os impactos sofridos em formações recifais seriam sentidos de forma mais forte e intensa nos recifes rasos do que em recifes mais profundos, pois à medida que a profundidade aumenta, a influência externa é atenuada. De fato, para Montastraea cavernosa habitando recifes mais profundos (18-30m) vimos altos níveis de saúde. Houve um certo equilíbrio nas condições de saúde de M. cavernosa entre os recifes costeiros e oceânicos, o que pode estar relacionado ao fato de que recifes mais profundos sofrem menos com influências externas (Bongaerts et al. 2010; Frade et al. 2018). Concluímos que a dinâmica local particular de cada ambiente se mostrou mais importante do que os impactos antropogênicos, na determinação do estado de saúde dos corais. É preciso ressaltar ainda a importância de se realizar monitoramentos em longo prazo, a fim de que seja possível conhecer todos os aspectos do ecossistema em questão, separando efeitos da dinâmica natural de perturbações de origem antrópica.
35
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EFERENCESAeby, G. S. (2003). Corals in the genus Porites are susceptible to infection by a larval trematode. Coral Reefs, 22(3), 216. https://doi.org/10.1007/s00338-003-0310-9.
Albright, R., Mason, B., & Langdon, C. (2008). Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs, 27(3), 485– 490. https://doi.org/10.1007/s00338-008-0392-5.
Alvarez-Filip, L., Dulvy, N. K., Gill, J. A., Coˆté, I. M., & Watkinson, A. R. (2009). Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings of the Royal Society B: Biological Sciences, 276(1669), 3019-3025.
Amaral, R. F. et al. Diagnóstico Ambiental da Área de Uso Turístico Intensivo (AUTI) no Parracho de Maracajaú. IDEMA-RN. Relatório Interno. 128 p., 2005.
Anderson, M. J., & Walsh, D. C. I. (2013). PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs, 83(4), 557–574. https://doi.org/10.1890/12-2010.1.
Aued, A. W., Smith, F., Quimbayo, J. P., Cândido, D. V, Longo, G. O., Ferreira, C. E. L., Segal, B. (2018). Large-scale patterns of benthic marine communities in the Brazilian Province. PLOS ONE, 13(6), 1–15. https://doi.org/10.1371/journal.pone.0198452.
Barott, K. L., Williams, G. J., Vermeij, M. J. A., Harris, J., Smith, J. E., Rohwer, F. L., & Sandin, S. A. (2012). Natural history of coral-algae competition across a gradient of human activity in the Line Islands. Marine Ecology Progress Series, 460, 1–12. https://doi.org/10.3354/meps09874.
Barros, K. V. de S., & Rocha-Barreira, C. D. A. (2014). Influence of environmental factors on a Halodule wrightii Ascherson meadow in northeastern Brazil. Brazilian Journal of Aquatic Science and Technology, 18(2), 31. https://doi.org/10.14210/bjast.v18n2.p31-41. Bellwood, D. R., Hoey, A. S., & Hughes, T. P. (2012). Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proceedings of the Royal Society B: Biological Sciences, 279(1733), 1621-1629.
Bellwood, D. R., Hughes, T. P., Folke, C., & Nyström, M. (2004). Confronting the coral reef crisis. Nature, 429(6994), 827–833. https://doi.org/10.1038/nature02691.
36 Benzoni, F., Galli, P., & Pichon, M. (2010). Pink spots on Porites: Not always a coral disease. Coral Reefs, 29(1), 153–153. https://doi.org/10.1007/s00338-009-0571-z.
Birkeland, C. (1997). Life and Death of Coral Reefs. Ecology, 78(8), 2639. https://doi.org/10.2307/2265925.
Birrell, C. L., Mccook, L. J., Willis, B. L., & Diaz-Pulido, G. A. (2008). Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanography and Marine Biology: An Annual Review, Vol 46, 46, 25--+. https://doi.org/doi:10.1201/9781420065756.ch2.
Bongaerts, P., Ridgway, T., Sampayo, E. M., & Hoegh-Guldberg, O. (2010). Assessing the ‘deep reef refugia’hypothesis: focus on Caribbean reefs. Coral reefs, 29(2), 309-327. Braga, E. D. S., Chiozzini, V. G., & Berbel, G. B. B. (2018). Oligotrophic water conditions associated with organic matter regeneration support life and indicate pollution on the western side of Fernando de Noronha Island-NE, Brazil (3° S). Brazilian Journal of Oceanography, 66(1), 73-90.
Brown, B. E., & Dunne, R. P. (2008). Solar radiation modulates bleaching and damage protection in a shallow water coral. Marine Ecology Progress Series, 362, 99-107
Brown, B. E., & Howard, L. S. (1985). Assessing the Effects of “Stress” on Reef Corals. In J. H. S. Blaxter, F. S. Russell, & M. B. T.-A. in M. B. Yonge (Eds.), Advances in Marine Biology (Vol. 22, pp. 1–63). Academic Press. https://doi.org/10.1016/S0065-2881(08)60049-8.
Brown, B. E., Dunne, R. P., Ambarsari, I., Le Tissier, M. D. A., & Satapoomin, U. (1999). Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Marine Ecology Progress Series, 191, 53–69. https://doi.org/10.3354/meps191053.
Brown, B. E., Dunne, R. P., Goodson, M. S., & Douglas, A. E. (2000). Bleaching patterns in reef corals. Nature, 404(6774), 142-143.
Burke, L., Reytar, K., Spalding, M., & Perry, A. (2011). Reefs at Risk: Revisted. In World Resources Institute. https://doi.org/10.1016/0022-0981(79)90136-9.
Cacciapaglia, C., & van Woesik, R. (2015). Reef‐coral refugia in a rapidly changing ocean. Global Change Biology, 21(6), 2272-2282. https://doi.org/10.1111/gcb.12851
37 Cinner, J. E., McClanahan, T. R., Daw, T. M., Graham, N. A., Maina, J., Wilson, S. K., & Hughes, T. P. (2009). Linking social and ecological systems to sustain coral reef fisheries. Current Biology, 19(3), 206-212.
Clarke, K. R. (1993). Non‐parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18(1), 117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x.
Connell, J. H. (1978). Diversity in tropical rain forests and coral reefs. Science, 199(4335), 1302-1310.
Costa, C. F., Sassi, R., & Amaral, F. D. (2004). Population density and photosynthetic pigment content in symbiotic dinoflagellates in the Brazilian scleractinian coral Montastrea cavernosa (Linnaeus, 1767). Brazilian Journal of Oceanography, 52(2), 93–99. https://doi.org/10.1590/s1679-87592004000200001.
D. McKinnon, H. He, B. Upcroft and R. N. Smith. (2011). Towards automated and in-situ, near-real time 3-D reconstruction of coral reef environments. OCEANS'11 MTS/IEEE KONA, Waikoloa, HI, pp. 1-10. doi: 10.23919/OCEANS.2011.6106982
Davidson, O. G. (1998). The enchanted braid: Coming to terms with nature on the coral reef. New York: Wiley.
Davies, P. S. (1980). Respiration in some Atlantic reef corals in relation to vertical distribution and growth form. The Biological Bulletin, 158(2), 187–194. https://doi.org/10.2307/1540930.
Davis, D., & Tisdell, C. (1995). Recreational scuba-diving and carrying capacity in marine protected areas. Ocean and Coastal Management, 26(1), 19–40. https://doi.org/10.1016/0964-5691(95)00004-L.
De Bakker, D. M., Van Duyl, F. C., Bak, R. P., Nugues, M. M., Nieuwland, G., & Meesters, E. H. (2017). 40 Years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs, 36(2), 355-367.
Deschaseaux, E. S. M., Beltran, V. H., Jones, G. B., Deseo, M. A., Swan, H. B., Harrison, P. L., & Eyre, B. D. (2014). Comparative response of DMS and DMSP concentrations in Symbiodinium clades C1 and D1 under thermal stress. Journal of experimental marine biology and ecology, 459, 181-189. https://doi.org/10.1016/j.jembe.2014.05.018.
38 Douglas, A. E. (2003). Coral bleaching - How and why? Marine Pollution Bulletin, 46(4), 385–392. https://doi.org/10.1016/S0025-326X(03)00037-7.
Dunne, R., & Brown, B. (2001). The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs, 20(3), 201-210.
Dustan, P., Doherty, O., & Pardede, S. (2013). Digital reef rugosity estimates coral reef habitat complexity. PloS one, 8(2). doi: 10.1371/journal.pone.0057386 PMID: 23437380 Dutra, L. X. C., Kikuchi, R. K. P., & Leão, Z. M. A. N. (2000). Thirteen months monitoring coral bleaching on Bahia’s north coast, Brazil. In Proc. Int. Coral Reefs Symp (Vol. 9, p. 373).
Erftemeijer, P. L. A., Riegl, B., Hoeksema, B. W., & Todd, P. A. (2012). Environmental impacts of dredging and other sediment disturbances on corals: A review. Marine Pollution Bulletin, 64(9), 1737–1765. https://doi.org/10.1016/j.marpolbul.2012.05.008.
Fabricius, K. E., Golbuu, Y., & Victor, S. (2007). Selective mortality in coastal reef organisms from an acute sedimentation event. Coral Reefs, 26(1), 69-69.
Ferreira, B. P. & Maida, M. (2006). Monitoramento dos Recifes de Coral do Brasil: situação e perspectivas. Monitoramento dos recifes de coral do Brasil. doi:M744
Fitt, W. K., & Warner, M. E. (1995). Bleaching patterns of four species of Caribbean reef corals. Biological Bulletin, 189(3), 298–307. https://doi.org/10.2307/1542147.
Fitt, W. K., Brown, B. E., Warner, M. E., & Dunne, R. P. (2001). Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral reefs, 20(1), 51-65. https://doi.org/10.1007/s003380100146.
Frade, P. R., Bongaerts, P., Englebert, N., Rogers, A., Gonzalez-Rivero, M., & Hoegh-Guldberg, O. (2018). Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching. Nature Communications, 9(1). https://doi.org/10.1038/s41467-018-05741-0.
Giglio, V. J., Luiz, O. J., & Schiavetti, A. (2016). Recreational Diver Behavior and Contacts with Benthic Organisms in the Abrolhos National Marine Park, Brazil. Environmental Management, 57(3), 637–648. https://doi.org/10.1007/s00267-015-0628-4.
39 Goldberg, J., & Wilkinson, C. (2004). Global Threats to Coral Reefs: Coral Bleaching, Global Climate Change, Disease, Predator Plagues, and Invasive Species. Status of Coral Reefs of the World: 2004 Volume I. https://researchonline.jcu.edu.au/24190/.
Gorgula, S. K., & Connell, S. D. (2004). Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Marine Biology, 145(3), 613-619. https://doi.org/10.1007/s00227-004-1335-5
Graham, N. A. J., & Nash, K. L. (2013). The importance of structural complexity in coral reef ecosystems. Coral Reefs, 32(2), 315-326.
Graham, N. A. J., Wilson, S. K., Pratchett, M. S., Polunin, N. V., & Spalding, M. D. (2009). Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodiversity and Conservation, 18(12), 3325-3336.
Gutierrez-Heredia, L., Benzoni, F., Murphy, E., & Reynaud, E. G. (2016). End to end digitisation and analysis of three-dimensional coral models, from communities to corallites. PloS one, 11(2).
Hedge, P., Molloy, F., Sweatman, H., Hayes, K. R., Dambacher, J. M., Chandler, J., ... & Elliot, B. (2017). An integrated monitoring framework for the great barrier reef world heritage area. Marine Policy, 77, 90-96.
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world’s coral reefs. Marine and Freshwater Research 50, 839–866
Hoegh-Guldberg, O., & Smith, G. J. (1989). The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. Journal of Experimental Marine Biology and Ecology, 129(3), 279-303.
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., … Hatziolos, M. E. (2007). Coral reefs under rapid climate change and ocean acidification. Science (New York, N.Y.), Vol. 318, pp. 1737–1742. https://doi.org/10.1126/science.1152509.
Hoeksema, B. W., & Matthews, J. L. (2011). Contrasting bleaching patterns in mushroom coral assemblages at Koh Tao, Gulf of Thailand. Coral Reefs, 30(1), 95. https://doi.org/10.1007/s00338-010-0675-5.
40 Hughes, T. P., Anderson, K. D., Connolly, S. R., Heron, S. F., Kerry, J. T., Lough, J. M., … Wilson, S. K. (2018). Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science, 359(6371), 80–83. https://doi.org/10.1126/science.aan8048.
Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J., & Steneck, R. S. (2010). Rising to the challenge of sustaining coral reef resilience. Trends in Ecology and Evolution, Vol. 25, pp. 633–642. https://doi.org/10.1016/j.tree.2010.07.011.
Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., Willis, B. (2007). Phase Shifts, Herbivory, and the Resilience of Coral Reefs
to Climate Change. Current Biology, 17(4), 360–365.
https://doi.org/10.1016/j.cub.2006.12.049.
Kaczmarsky, L. T. (2006). Coral disease dynamics in the central Philippines. Diseases of Aquatic Organisms, 69(1), 9–21. https://doi.org/10.3354/dao069009.
Kelmo, F., & Attrill, M. J. (2013). Severe Impact and Subsequent Recovery of a Coral Assemblage following the 1997-8 El Niño Event: A 17-Year Study from Bahia, Brazil. PLoS ONE, 8(5), e65073. https://doi.org/10.1371/journal.pone.0065073.
Knowlton, N., & Jackson, J. B. (2008). Shifting baselines, local impacts, and global change on coral reefs. PLoS biology, 6(2). https://doi.org/10.1371/journal.pbio.0060054.
LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R., & Santos, S. R. (2018). Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Current Biology, 28(16), 2570-2580.e6. https://doi.org/10.1016/j.cub.2018.07.008.
Leão, Z. M. A. N., De Kikuchi, R. K. P. & De Oliveira, M. D. D. M. (2008). Branqueamento de corais nos recifes da Bahia e sua relação com eventos de anomalias térmicas nas águas superficiais do oceano. Biota Neotrop. 8, 69–82
Leão, Z. M. A. N., Kikuchi, R. K. P., & Testa, V. (2003). Corals and coral reefs of Brazil. In Latin American Coral Reefs (pp. 9–52). https://doi.org/10.1016/B978-044451388-5/50003-5.
Lesser, M. P., & Farrell, J. H. (2004). Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral reefs, 23(3), 367-377.
