Simulations of Long-Term Community Dynamics in Coral Reefs - How Perturbations Shape Trajectories
[['Tropical coral reefs are highly productive but also fragile ecosystems that provide habitats for the coastal fauna and multiple services to local human communities [1] .', 'Due to their high biodiversity , they exhibit a complex pattern of interactions between organisms and their environment with feedback loops within and between trophic as well as different hierarchical levels [2] , and thereby facilitate a framework of non-linear dynamics which complicates a holistic analysis .', 'Although extensive knowledge of corals , their responses to environmental change [3] and interaction with other organisms [4] , and reef resilience [5] has been gained in the last few decades , the understanding of coral reef functioning is still far from being complete [6] .', 'Reefs are increasingly under threat and many coral species are in danger of becoming extinct [7] , due primarily to anthropogenic influence .', 'Globally , coral reef systems are subject to rising sea surface temperatures which increase their susceptibility to bleaching , and to ocean acidification which erodes CaCO2 structures .', 'Both stressors are chronically increasing and can be attributed to climate change [3] , [5] .', 'Additionally it is predicted that extreme weather events ( e . g . el Niño or hurricanes ) will strike with increasing frequency [8] , [9] .', 'Directly imposed human pressure upon coral reefs can have physical – e . g . by the use of destructive fishing techniques [10] , [11] , sedimentation [12] , or anchorage [13]–[15] – or chemical – e . g . nutrients , sewage , pollution [11] , [16] consequences .', 'The overall tendency of coral reef systems to react to changes in environmental conditions and anthropogenic influences can be described by the term resilience .', 'It “… determines the persistence of relationships within a system […] and is a measure of the ability of these systems to absorb change […] and still persist . ” [17] .', 'In a coral reef it may be determined by species diversity , functional redundancy , life history of reef organisms , species functioning at different spatial and temporal scales , and connectivity to other reefs or habitat types [18] , [19] .', 'Reduced resilience can impose catastrophic regime shifts [20] , [21] and in a reef often lead to a phase shift from coral dominated systems to alternative states; i . e . dominance of macroalgae [16] , [22] , [23] or of other benthic organisms [24] , but see [25] .', 'During the last two decades a series of ecological models have been applied to coral reef ecosystems .', 'Among these we can find applications on various spatial and temporal scales .', 'While Kleypas et al . [26] sought to approximate the possible geographic range for coral reefs to exist globally , other applications focus on conservation [27] or sustainable fishing regimes [28] , [29] .', 'There are yet other models at the regional , local and/or small scale [30]–[34] with the purpose to explore the influence of environmental conditions on spatial processes and interactions of coral reef community dynamics , and some of these models , like [35] are designed to aid management decisions .', 'Individual-based models ( IBM ) have proven to be an exceptional tool to tackle ecological questions with adequate detail [36]–[38] because properties of investigated ecological systems can be described very close to reality .', 'By including , for example , heterogeneously varying individual interactions and spatial heterogeneity , IBMs considerably extend the range of ecological modelling [39] .', 'In this study we focus on individual benthic organisms and their interaction with the environment because these processes and the spatial configuration of a community are the basis for environmental responses to perturbations in reality .', 'There is a lot of knowledge on properties of individual coral colonies of various species; e . g . which symbionts they possess , how they grow , and how they react to thermal stress [40] , [41] , upon changing environmental settings in general , or if faced with other benthic organisms within their local neighborhood [42]–[45] .', 'All of these factors are relevant for the understanding of coral reef functioning and should be included in an analysis of local reef dynamics .', 'To date , the application of individual-based models in the context of coral reefs has been somewhat limited , but interesting models have been developed for some investigations .', 'Yniguez et al . [46] described the three-dimensional growth pattern of Halimeda tuna , a common macroalga in Florida Key reefs .', 'Sleeman et al . [47] utilize an individual-based model to analyze different spatial arrangements of coral transplants in order to improve reef restoration measures .', 'Koehl et al . [48] simulated larval transport in turbulent waters , and Brandt and McManus [49] investigated the spread of the white plague disease in various coral populations .', 'Tam and Ang [50] present a strictly theoretical 3-dimensional model in which they describe disturbance-induced changes in a coral community with three different hypothetical coral growth patterns .', 'Here , we present a generic multi-species individual-based coral reef model in which scleractinian coral species and algae compete for space .', 'This tool enables the analysis of key functions for coral reef resilience and the identification of major causes of phase shifts for local situations .', 'In our example we apply a basic system with a standard parameterization for a typical Western Indian Ocean reef system .', 'In order to improve the understanding of how climate change and different modes of human interference affect the benthic composition of specific reef sites and their resilience we examine community responses under various environmental settings .', 'Hence , we apply ( 1 ) different frequencies of temperature-induced bleaching , ( 2 ) two levels of mechanical disturbance regimes: a smaller one , which represents , for example , direct anchor damage or a smaller boat hitting the coral reef at low tide and a larger one representing , for example , damage by abrasion due to anchor chains , boat crashes or from fishing nets , and ( 3 ) both perturbations acting together to test the influences on the benthic community .'], ['At standard settings , the massive P . lutea dominated , followed by the branching A . muricata .', 'The other two species both leveled at around 5% coverage .', 'A . muricata exhibited the highest fluctuations in relative cover and P . lobata the lowest .', 'Surveyed exclusively , both perturbation modes triggered similar responses in the benthic community; not only changes in overall benthic coverage but also alterations in community composition .', 'For low frequencies of rare events , massive growth forms clearly dominated the system with high total benthic cover .', 'Macroalgal cover is negligibly low .', 'If perturbations occurred at intermediate frequencies , overall cover decreased and space was nearly evenly distributed between the two different growth morphologies .', 'At the highest perturbation levels , the total benthic cover was very low , the relative fraction of algae increased strongly and massive species were displaced by branching ones .', 'Nevertheless , single effect testing of major bleaching events and mechanical disturbances revealed that both perturbation types triggered differential responses of the benthic community .', 'These are discussed further below .', 'Without the influence of mechanical disturbances , there was nearly no visible change in the total benthic cover ( which was always ≥99% ) , if major bleaching events occurred in intervals of 16 years or higher .', 'The community was dominated by P . lutea with a relative coverage of ∼80% or larger ( Fig . 4 ) , followed by P . lobata ( ∼18% ) .', 'When extreme temperatures occurred every 10 to 15 years , major changes in relative cover arose mainly for P . lutea which decreased from 76 . 1 to 28 . 1% coverage , and P . lobata which decreased from 17 . 0 to 6 . 0% coverage .', 'For the dominance of P . lutea we identified a threshold of 8–9 years between major bleaching events ( Fig . 4 ) .', 'At very high bleaching frequencies the total coral cover did not exceed 2% coverage and macroalgae dominated the benthic community .', 'Branching corals dominated if bleaching events occurred every 8 years or more often .', 'Within this range the cover of P . damicornis increased gradually and A . muricata only dominated if extreme temperature events happened between 7 and 9 year intervals .', 'Without the influence of extreme temperature events both applied disturbance intensities triggered nearly the same community responses , although the frequency of the smaller size events had to be far higher for a similar effect ( Fig . 5 ) .', 'Increasing disturbance frequencies abetted dominance shifts from massive to branching growth forms , resembling the pattern of the single effect of bleaching .', 'The interface from the dominance of P . lutea to A . muricata , where the community featured the highest evenness , was restricted to a small range of configurations .', 'At standard frequencies ( i . e . for smaller intensities every 12 , and for larger ones every 60 months ) the total benthic cover was 117% ( see section ‘Environmental settings and scenario conditions’ ) where P . lutea clearly dominated , followed by P . lobata , the two branching coral species covered together ∼3% , and macroalgae covered 0 . 5% .', 'Under highest applied frequencies of mechanical disturbance events the total benthic cover amounted to 16 . 2% , and massive corals nearly disappeared altogether ( <0 . 1% cover ) with only the faster growing branching corals still present in the system .', 'Under the regime of both applied perturbations , where different frequencies of bleaching events were tested under standard mechanical disturbance levels the effect of bleaching was amplified ( Fig . 6 ) .', 'Similar to the single effect scenario the total coral cover was low and macroalgae dominated at very high frequencies of bleaching events .', "At 20 year intervals , the total benthic cover did not exceed 63% , and as in the assessment of the sole bleaching effect , P . lutea dominated the community , while all other species' coverage stayed below 10% .", 'P . lobata did not exceed 10% cover within any tested frequency .', 'Also contrasting is the behavior of A . muricata .', 'It dominated the community at extreme temperature intervals between 8 and 14 years but its cover decreased tremendously at higher frequencies .', 'P . damicornis again increased its relative cover gradually at high frequencies , but then stayed more or less constant at levels around 5% coverage if major bleaching occurred every 9 years or more seldom .', 'The ratio of massive and branching corals was nearly 4∶5 at 15 year intervals for major bleaching , and the dominance threshold for P . lutea was shifted from 8–9 year intervals up to 14–15 year intervals in the combined perturbations scenarios .'], ['The model outcome reflects findings of empirical studies in many regards and provides interesting insights on the influence of multiple perturbations on coral reef communities .', 'Massive corals are generally slow growing but exhibit a strong physical structure .', 'Provided their tissue is healthy and the defense intact , they are quite resistant to overgrowth by other organisms , like branching coral species or macroalgae which competitively mainly rely on their faster growth rates [63] .', 'In addition , both of the observed massive species feature low susceptibilities to bleaching among the tested corals , and a low bleaching-induced mortality .', 'The combination of slow growth and high endurance implies small fluctuations in relative coverage .', 'As yet another consequence of the above mentioned properties , massive species outcompete their benthic opponents gradually if perturbation levels are low , where P . lutea overrules P . lobata and dominates the community due to its higher growth rate ( see Fig . 4 and Fig . 5 at low perturbation levels ) .', 'This effect is also pronounced by the applied stock-recruitment relationship which leads to a self-enhancing process; i . e . individual colonies grow fast , reach maturity earlier , and produce many propagules again resulting in a higher recruitment rate and new colonies .', 'The branching species A . muricata exhibits the highest fluctuations in population size and relative coverage .', 'It has the fastest growth rate of all simulated species and , given there is enough space , can dominate the benthic community within a few years due to the self-accelerating process produced by the stock-recruitment relationship described above .', 'On the other hand , its bleaching vulnerability to thermal stress is the highest within the tested community , which leads to considerable losses due to extreme temperature events .', 'Acropora and Pocillopora are genera with many species which feature high susceptibility to bleaching [64] .', 'Accordingly , A . muricata is the only species in our model which shows bleaching responses in years when temperatures did not rise as high as in 1998 .', 'For P . damicornis the situation is different .', 'In our model , this species is the least susceptible of all tested species in terms of bleaching , but when a colony bleaches it nearly always dies .', 'Therefore , extreme weather events have nearly analogous effects on the mortality for both branching species .', 'The long term survival of a species is hence strongly dependent on larval input from the outside and thence influenced by asynchronies on the regional and trans-regional scale .', 'The results show that different types and levels of perturbations can lead to very diverse community responses and thereby reef fate .', 'In a mechanical disturbance event , the only reason for an individual to be affected is if it is located at the wrong spot at the wrong time .', 'At higher frequencies of these events the growth rate and recolonization speed of an organism decides winners and losers .', 'Extreme temperature events feature a more selective pattern .', 'Populations of higher susceptibility to thermally induced bleaching suffer the highest losses .', 'Their lower abundance evokes a reduced reproductive output for the next spawning event which , in the long run , might constitute a disadvantage over less susceptible species .', 'Generally , mechanical disturbances occur locally and do not affect the regional coral populations , so that neighboring reefs can serve as a source for new recruits and the local population can recover comparatively fast .', 'An increase of the sea surface temperature is affecting populations at a larger spatial extent and evokes a regional effect .', 'Conspecifics of a sensitive species are affected similarly region-wide if they are not protected from the high temperatures in some way .', 'In such a scenario the larval support between reefs can be hampered tremendously and the risk of extinction increases [65] .', 'Structural complexity of a coral reef is a very sensitive emergent property and high coral cover does not thoroughly imply high ecosystem function ( e . g . 3-dimensional framework ) [66] .', 'Perturbations at too high or too low frequencies cause a loss of biodiversity and thereby structural complexity .', 'Very low frequencies and/or intensities of mechanical disturbance events mostly lead to dominance of species with high competitiveness or endurance and it is just a matter of time until individuals of these species overgrow and displace inferior organisms .', 'In our example , massive corals dominate under very low disturbance regimes .', 'They do not provide as much structure as branching corals and so structural complexity is lost which might cause unfavorable conditions for other reef associated organisms which are deprived of hiding places .', 'One example is Changuu reef , close to the city of Zanzibar , a very exploited site by the means of fishing and under strong influence of waste water , and hence pollutants and nutrients from the town [67]–[69] .', 'Muhando et al . [70] found that corallimorpharians covered 14% of the reef , mainly on the reef crest and flat .', 'Here a large part of the ( still persisting ) coral cover is made up by Galaxea astreata and Porites rus [71] , both of which seem to be quite resistant to environmental change and possess strong competitive traits over other taxa ( e . g . corallimorpharians ) but which facilitate scarce structure .', 'Therefore this site exhibits low biodiversity of fish and other associated organisms .', 'Under very high physical disturbance levels the overall coral cover is generally very low .', 'These conditions are detrimental for massive corals and thus provide free settling ground for branching species .', 'On the other hand branching corals are affected as well , because without shelter from surge or strong currents , they might break off .', 'Nevertheless , due to their high growth rates they play a crucial role in post-disturbance recolonization [72] and reef building event though recovery periods may be too short for slower growing massive coral species .', 'Although branching coral species are displaced by massive species in Indo-Pacific reef sites [73] , this trend cannot only be attributed to the two perturbation types , addressed in this study , but is also owed to the fact that massive species are more resistant to other threats , like pollution [74] or more selective mechanical disturbances like hurricanes , which invoke strong surge and currents [72] .', 'In the given context and despite the limited number of represented species , the principles of the intermediate disturbance hypothesis [75] are well resembled by our model results and in line with previous studies [30] , [50] .', 'At high and low disturbance regimes one species dominates , whereas the evenness is highest at intermediate disturbance levels .', 'In order to investigate the sole effects of perturbations on long term dynamics of a reef without the effect of extinctions , we made two major assumptions .', 'First , we kept the grazing intensity on algae more or less constant , assuming that the herbivore community is completely independent of the structural complexity that the reef is providing .', 'The general view is that the abundance of herbivorous fish and other associated reef organisms is directly influenced by the availability of sheltering places provided by the reef structure [19] , [76] , [77] , and especially by the abundance of branching corals [66] .', "A loss of a reef's structural complexity therefore reduces herbivore abundance , macroalgae are not grazed efficiently and their populations can proliferate freely .", 'Resulting stands of macroalgae decrease coral recruitment success [78] , [79] which can then produce a feedback in which macroalgae may take over a once coral dominated system .', 'Secondly , we assume a constant larval supply from the outside , on top of the applied stock-recruitment relationship .', 'According to McClanahan et al . [80] the extinction risk of all species tested here as a response to bleaching seems to be very low in the Western Indian Ocean region , with Pocillopora and Acropora showing a probability of 12 and 11% , respectively , and the massive Porites of 7% .', 'In contrast to the observations that McClanahan et al . [81] made in Kenya , where they observed that Pocillopora was completely depleted at protected sites and close to gone from unprotected ones , P . damicornis survives in our simulations .', 'This is due to our second assumption that nearby source reefs were not as much affected by high temperature influences as the focal reef , either because they are located in deeper waters where the heating effect is alleviated or by mixing of water masses .', 'These two assumptions implicate limitations for model extrapolations .', 'To transfer the model to other sites , specific adaptations to the local conditions and to local species parameters have to be made .', 'This also applies to the other explicit and implicit assumptions , underlying the model development , such as the 2-dimensional spatial configuration , the choice of reef components , and their rules of interaction and competition .', 'Additionally , the applied parameter specifications , most of all the relative rates of growth , the reaction to bleaching and larval recruitment , are important for the model outcome .', 'Although there are many types of perturbations , in this article we concentrated on two of the main ones , which concern coral reefs and most probably will have increasing impact in the future; bleaching as a result of global climate change and anchor and boat damage due to an increased demand for food and in consequence more fishing on reefs .', 'The framework of our model allows for the addition of other substantial threats , like ocean acidification , nutrient input ( which hampers coral fitness but may have a positive effect on algae ) , coral diseases , and sedimentation , all of which will affect resource allocation in virtual corals and thereby decrease growth rates and/or competitive strength .', 'Intensive fisheries constitute a fundamental problem for future coral reefs which should be treated with special attention .', 'Enhanced fishing pressure depletes stocks , which most probably results in either higher effort ( i . e . more fishing trips ) and/or the utilization of more efficient fishing gear that often has destructive capacities .', 'Both practices increase the risk of reef degradation ( i . e . by more frequent anchorage and boat damage , or directly through fishing gear ) .', 'In the longer run this might evoke a downward spiral .', 'While we are still far away from the point in which we can represent all features of these highly complex biota , our study extends model capabilities from former coral reef models .', 'This extension improves the accuracy of involved processes as well as on the spatial scale and resolution of the simulated reef system .', 'The model reflects important coral reef dynamics and allows us to test different scenarios relevant for resilience research .', 'Its generic and modular structure and the potential to parameterize different reef components and different coral species , as well as environmental influences provides the possibility for adapting it to represent many reef sites worldwide .', 'The model clearly shows that even when perturbation regimes are kept constant the system never reaches a stable state and stochasticity produces a continuously adapting and fluctuating community response .', "Pulse events can have a strong influence on ecosystem functioning , especially if they amplify each other's effects or stress the ecosystem in addition to a prevailing chronic disturbance [21] such as increasing nutrient loads or sedimentation .", 'This may cause a shift of general system properties , and lead to , for example , a coral-algae phase shift [82] .', 'Several studies that have quantified resilience with a small number of key parameters have already provided interesting insights [83]–[85] .', 'Nevertheless , measuring resilience in such complex systems as coral reefs is hard to accomplish because the high number of site specific relations and components complicates generalization and extrapolation of specific findings considerably .', 'However , management has a high interest in , and demand for , tools which aid in tracing and identifying distinct drivers for the decline of specific coral reefs .', 'Only a clear recognition of drivers , mechanisms and causes makes it possible to establish or introduce adequate protection measures .', 'Generic frameworks , like the model presented here , allow a fairly easy integration of site specific features and may serve as an appropriate basis for management support tools .']]
['Introduction', 'Results', 'Discussion']
['Tropical coral reefs feature extraordinary biodiversity and high productivity rates in oligotrophic waters .', 'Due to increasing frequencies of perturbations – anthropogenic and natural – many reefs are under threat .', "Such perturbations often have devastating effects on these unique ecosystems and especially if they occur simultaneously and amplify each other's impact , they might trigger a phase shift and create irreversible conditions .", 'We developed a generic , spatially explicit , individual-based model in which competition drives the dynamics of a virtual benthic reef community – comprised of scleractinian corals and algae – under different environmental settings .', 'Higher system properties , like population dynamics or community composition arise through self-organization as emergent properties .', 'The model was parameterized for a typical coral reef site at Zanzibar , Tanzania and features coral bleaching and physical disturbance regimes as major sources of perturbations .', 'Our results show that various types and modes ( intensities and frequencies ) of perturbations create diverse outcomes and that the switch from high diversity to single species dominance can be evoked by small changes in a key parameter .', 'Here we extend the understanding of coral reef resilience and the identification of key processes , drivers and respective thresholds , responsible for changes in local situations .', 'One future goal is to provide a tool which may aid decision making processes in management of coral reefs .']
['The degradation of coral reefs is a major threat for tropical coastal environments , worldwide .', 'For this reason we developed a spatially explicit model which simulates competition in a benthic reef community under the influence of various environmental factors .', 'Here we highlight the impact of two major perturbation types ( mechanical disturbance events and temperature-induced bleaching events ) on the long-term dynamics of a standard coral reef off Zanzibar Island , Tanzania .', 'While mechanical disturbances are more non-specific and affect all organisms of the reef similarly , temperature-induced bleaching causes selective impact among coral species within the benthic community .', 'Our results show clearly that complex systems which are organized of a multitude of diverse entities and hence feature complex emergent properties need to be analyzed on different integration levels rather than seen as a black box .', 'Our tool may help to disentangle the combined effects of different perturbations and to analyze their respective impact on the benthic community of a coral reef .', 'Hence , it will help to direct future research foci and to coordinate management measures for distinct site specific contexts .']
['simulation languages', 'community structure', 'computerized simulations', 'marine biology', 'corals', 'coral reefs', 'marine and aquatic sciences', 'biology', 'community ecology', 'computer science', 'programming languages', 'ecology', 'marine ecology', 'species interactions']