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Can Porites spp. corals be used as a bio-indicator for sediment stress on coral reefs?
Ecological Indicators 106 (2019) 105538
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Letter to the Editor Can Porites spp. corals be used as a bio-indicator for sediment stress on coral reefs?
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ARTICLE INFO
ABSTRACT
Keywords: Coral reefs Bio-indicator Impact assessment Dredging Sediment Porites Mucus
Bessell-Browne et al. (2017) published a paper where they proposed using mounding Porites spp. corals from Western Australia as a bio-indicator of sediment stress on coral reefs. They based their interpretations on results obtained during the monitoring of a capital dredging program coupled with laboratory sediment dousing experiments. They stated that because these Porites species generate mucous sheets in response to sediment loading, they could be used as an early warning indicator of sediment stress adjacent to sensitive coral resources. While their results are compelling, there are several confounding issues that arise questioning the wide-scale application and use of Porites spp. corals as bio-indicators. Using examples of Porites species from both the IndoPacific and Caribbean, I detail a number of contrary results that reveal that mucous sheet development is most likely attributed to mucus production and subsequent mucus sloughing that are cued to an endogenous lunar cycle (approximately 28 days in duration) and not necessarily as a direct strategy to protect the coral tissue from harm due to sediment stress. While the mucous sheet becomes fouled with sediment during the cycle, the amount of sediment observed may not be a response to the level of sediment stress, but where in the 28-day cycle the mucous sheet is observed. Thus, depending on when you observe the colony (early, middle or late in the 28-day cycle) the level of purported sediment impact would be highly variable. This variability leads to an unacceptably high rate of both Type-I and Type-II statistical errors. Because of the cyclical, endogenous nature of mucus production in many Porites spp., extreme caution should be employed before using these species to infer the level of sediment impact associated with dredging projects or their use as a predictive tool of sediment stress on coral reefs.
1. Introduction In biological impact studies, the amount of ecological data collected is often overwhelming. To reduce the information overload, scientists often attempt to isolate key aspects of the environmental condition by focusing on specific biological indicators that act as surrogates for the entire ecosystem. Bio-indicators possess a strong appeal for field biologists, conservationists, managers, and regulators as they provide a cost- and time-efficient means to assess the impacts of environmental disturbances on an ecosystem by focusing on a single organism, species, or genus (Caro, 2010). In a recent manuscript, Bessell-Browne et al. (2017) provide convincing, yet equivocal evidence for the use of Porites spp. corals as a reliable bio-indicator for sediment stress on coral reefs. Specifically, they looked at the response of two mounding species, Porites lobata and Porites lutea, to variations in sedimentation related to a dredging project in Western Australia. As a response to elevated concentrations of suspended sediments and deposition of fine silt, they found that the two Porites species developed mucous sheets which became progressively fouled with sediments over time. These mucous sheets were periodically sloughed off resulting in a sediment-free surface that became re-fouled with the addition of new sediment. Results of laboratory experiments performed on these two species were similar to their in-situ field observations. In their study, mucous-sheet prevalence in Porites spp. was examined before and during a large-scale dredging program which resulted in an increase in the intensity, duration, and frequency of turbidity events compared to pre-project, base-line levels (Evans et al., https://doi.org/10.1016/j.ecolind.2019.105538 Received 28 June 2019; Accepted 1 July 2019 Available online 09 July 2019 1470-160X/ © 2019 Elsevier Ltd. All rights reserved.
2012; Fisher et al., 2015; Jones et al., 2015). At sites close to the dredging activities, mucous sheet prevalence reached as high as 50%, and over the duration of the dredging program ~75% of colonies were observed with a mucous sheet at some point-in-time (at least once over a 530-day period from 19 May 2010 to 31 October 2011). In contrast, at their far-field reference sites (> 20 km away), mucous-sheet prevalence was negligible (~0.2%) during the dredging program. These compelling results led Bessell-Browne et al. (2017) to posit a strong association between mucous-sheet coverage and prevalence suggesting this process is a viable, sub-lethal bio-indicator of sediment stress for coral reefs. Significantly, if Bessell-Browne et al. (2017) are correct in their assessment that mucous-sheet production is solely an emergency environmental response to an increase in sediment load, it should therefore be plausible to use Porites as a tool for monitoring and assessing sediment stress associated with dredging programs on coral reefs not just in Western Australia, but in all reef regions where these Porites species are present. Thus, a single, accurate coral proxy, in this case Porites spp., could potentially eliminate the need for additional indicators of sediment stress, ultimately simplifying and streamlining the monitoring process. In fact, their conclusion, while based on data limited to a few reefs in Western Australia, implies the broad application of using massive Porites spp. in this manner. Their take home message is “… mucous sheet prevalence appears to be a useful sub-lethal indicator of sediment related stress for coral communities and should be considered as a monitoring tool during future dredging projects or exposure to elevated sediment loads.” Unfortunately, it is not that simple; the adequate assessment of a
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Letter to the Editor
the surfaces of living corals can ultimately cause tissue necrosis and death because of the combined effects of smothering (Bak and Elgershuizen, 1976; Rogers, 1983, 1990; Erftemeijer et al., 2012; Duckworth et al., 2017) and microbial action (Hodgson, 1990). To that end, numerous researchers have been trying to understand the varying responses of corals to sediment stress and burial under both field and laboratory conditions (Lasker, 1980; Peters and Pilson, 1985; Rice and Hunter, 1992; Stafford-Smith, 1993; Telesnicki and Goldberg, 1995; Wesseling et al., 1999). One of the goals over the last two decades has been to find a single biological indicator for determining the response of corals to sediment stress (i.e. Wesseling et al., 2001; Nugues and Roberts, 2003; Vargas-Ángel et al., 2006; Rotmann and Thomas, 2012). To date, however, that search has been elusive. Corals use a number of methods to reject sediment from their colonies. These include both passive and active methods. Passive methods of sediment rejection include the influences of wave and current action as well as coral colony size, orientation, and morphology (Rogers, 1983; Stafford-Smith and Ormond, 1992; Sanders and Baron-Szabo, 2005). Active methods include tentacle manipulation, polyp expansion, pulsed polyp contraction, ciliary currents, tissue expansion, and mucus entanglement (Stafford-Smith and Ormond, 1992). Most reef-building corals use one or more of these mechanisms in tandem to assist in preventing sediment from accumulating and damaging coral tissues. It is because of the wide inter- and intraspecific variability in these processes that no two coral species on the reef respond to increases in sedimentation the same manner making it difficult, if not impossible, to use a specific coral as a proxy for the level of sedimentation or “stress” on the reef at any given snapshot in time (Lasker, 1980; Rogers, 1983; Brown and Howard, 1985; Gleason, 1998; Lui et al., 2012). Pichon (2011) noted “several species in the genus Porites produce abundant sheets of mucus, which covers and protects the living tissue, and on which the fine sediment particles get trapped. After some time, generally up to a few weeks, the sheet of mucus is eliminated, thus removing the sedimented particles, and the process may start again.” Bessell-Browne et al. (2017) attributed the development of these mucous sheets to high levels of suspended sediment in the water column as well as direct sediment contact with the colony surface. Stafford-Smith and Ormond (1992) proffered that the reason massive Porites colonies use mucus entanglement is because the coral calices are so small (< 2.5 mm) in diameter, that they are essentially incapable of actively rejecting sediment. However, Stafford-Smith and Ormond (1992) were unable to generate mucous sheet production in either laboratory or field experiments, even when exposing colonies to a steady input of fine, silt-sized particles. Rogers (1990) noted, “we might expect smaller-polyped 'autotrophic' corals which depend more on light to succumb more quickly to turbid conditions than large-polyped corals …” This, however, is contrary to field observations that show some small-polyped corals such as Porites, to be relatively tolerant of high levels of turbidity and sedimentation (Potts et al., 1985; Veron, 2000; Brown, 2007; Morgan et al., 2016). The coral surface mucus layer provides a vital interface between the surfaces of the coral polyp and the seawater environment and mucus can act in defense against a wide range of environmental stresses including sediment removal (Ducklow and Mitchell, 1979; Kato, 1987; Veron, 2000; Brown and Bythell, 2005; Huettel et al., 2006; Banaszak, 2007; Johnston and Rohwer, 2007; Jatkar, 2009; Wooldridge, 2009; Jatkar et al., 2010; Bythell and Wild, 2011; Glasl et al., 2016). The production of mucous sheets on corals has led some workers to propose that mucus production is solely a response to stressful conditions (Bak and Elgershuizen, 1976; Thompson, 1980; Krupp, 1984; Kato, 1987; Bessell-Browne et al., 2017).
Table 1 Criteria for the selection of indicator species (modified from Carignan and Villard, 2002; Goodsell et al., 2009, and Adams, 2003). (1) Biological Plausibility – There is a credible or reasonable biological and/or toxicological basis for the proposed mechanism linking the cause and effect. (2) The species must provide an early warning of the organism’s responses to the environmental stress. (3) Specificity of Association – Directly indicates the cause of the response to the stressor in question and eliminates other confounding stressors. (4) Biological Gradient – Provides a continuous assessment over a wide range and intensity of stress. (5) Strength of Association - Provides a measurable response to the stress. (6) Chosen species is sensitive to the stress but does not experience stress-related mortality. (7) Chosen species are locally abundant within the area of study including at both the impacted and control sites. (8) Chosen species are relatively stable despite environmental variability. (9) The ecology and physiology of the chosen species are well understood. (10) Chosen species are simple and cost-effective to monitor. (11) Chosen species can be accurately assessed by all personnel involved in the monitoring program. (12) Consistency of Association – The results need to be repeatable in time and space.
biological indicator depends on many factors and for Porites spp. to be considered useful as a bio-indicator it needs to possess, at a minimum, 12 significant characteristics or criteria (see Table 1). The most important of which is point 12; the results need to be repeatable both in time and space. In addition to meeting these 12 criteria, another critical aspect for bio-indicators to be useful in providing an early warning of sediment effects on reef corals is the rate of Type-I statistical errors encountered (that is an effect is indicated by statistical analysis when in fact one is not present). Thus, in order for the bio-indicator approach to be effective, the number of false positives (i.e. making a Type-I error) needs to be small, while false negatives, indicating no effect when there is in fact one present (a Type-II error), must be kept to an absolute minimum. In environmental terms, making Type-II errors are far more serious (Aronson and Precht, 2006). Thus, the effectiveness of a bio-indicator, as an early warning signal for environmental impacts, decreases with the number of false negatives as well as false positives. A ‘‘sensitive’’ bio-indicator would be expected to produce more false positives. However, the indicator should be sensitive enough to react in a detectable way when a system is affected by an outside stress, and they should also remain reasonably predictable in their undisturbed state (Mapstone, 1996). Thus, an ideal bio-indicator for environmental impact monitoring programs should have ‘‘optimal’’ rather than ‘‘maximum’’ sensitivity. While the Porites spp. used in the Bessell-Browne et al. (2017) manuscript meet many of the 12-point criteria listed above, a critical analysis using all these criteria should be analyzed for evaluating the efficacy of the chosen bio-indicator species. In addition, explicit attention to rates of Type-I and Type-II errors should become standard practice in all impact assessment studies (Anderson, 1998). This is especially important when using a single bio-indicator as a proxy for the impact because actions based on either type of error can be costly. Using examples of mucous-sheet development in Porites spp. colonies, I detail numerous conflicting and confounding issues that may make the use of Porites spp. as a broad-scale bio-indicator for coral reef sediment monitoring programs more illusory than real (see Zettler et al., 2013 for a similar critique in a different context). 2. Background It has long been known that sediments settling onto reef surfaces have been shown to exert control on the distributions and abundances of coral species through both lethal and sublethal effects (Rogers, 1983, 1990; Stafford-Smith and Ormond, 1992, Stafford-Smith, 1993, Erftemeijer et al., 2012; Flores et al., 2012; Duckworth et al. 2017). In worst case scenarios, the settlement of inorganic particles directly onto
3. Confounding problems 3.1. Caribbean examples of Porites mucous-sheet development Porites astreoides is one of the most common Caribbean reef corals 2
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increase in mucous sheet production in P. astreoides related to increased sedimentation, however, she did note there may be some modulation in mucus production associated with extremes in these parameters (Coffroth, 1991, see also Gleason, 1998; Wooldridge, 2009). Porites astreoides also exhibits variation in colony color that consists of brown, tan, green, and yellow individuals or morphs. Green and yellow morphs of this species appear to be better adapted than their tan and brown counterparts to inhabit shallow water areas where high intensities of ultraviolet radiation persist (Gleason, 1993). While these color morphs exhibit no other obvious differences in colony or polyp morphology (Potts et al., 1993), closer examination of morph-specific distributions at several sites suggest that at deeper depths or in areas exposed to greater sediment stress the brown morphs may be favored (Gleason, 1998). Gleason (1998) specifically noted that the brown morphs were better at shedding sediments than their lighter colored conspecifics even though their small-scale morphologies were very similar. Gleason attributed this to large amounts of fluid mucus (Coffroth, 1990) that, in tandem with water motion, appears to be important in clearing the colony of sediment. Gleason (1998) also noted that under both in situ and laboratory conditions surfaces of the brown morphs tended to be slimier to the touch than the green morphs suggesting that they produce greater quantities of fluid mucus. While not quantified, Gleason found that the brown morphs in sediment shedding experiments appeared to produce more mucus than the green morphs (i.e., cohesive mucoid coverings derived from fluid mucus), that assisted in shedding sediments and protecting the underlying tissues from damage. These mucous sheets may also include protection from increased temperature, ultra-violet radiation, and even pathogenic bacteria (Koh, 1997; Teai et al., 1998; Shnit-Orland and Kushmaro, 2009). It has also been shown that P. astreoides uses these mucus layers for feeding and nutrient cycling (Lewis and Price, 1975; Coffroth, 1990; Mills and Sebens, 2004). For instance, Mills and Sebens, (2004) noted that there was a decrease in percent nitrogen of the sediments egested by P. astreoides suggesting that these corals are removing nitrogen from sediments that settle on their surfaces. They also noted that the sediments sloughed by P. astreoides were also lower in percent nitrogen, indicating that this species may be selectively ingesting particles with higher nitrogen content, or stripping the sediment of organic nitrogen during the sloughing process (see also Lirman et al., 2008). Similar, observations of repeated, cyclical mucous sheet development and sloughing have been made by the author on encrusting, plating, and mounding Porites spp. throughout the Caribbean. Observations of mucous sheet development include areas of exceedingly low turbidity and sedimentation such as the reefs off Grand Cayman (Fig. 3A) as well as with those of highly turbid, lagoonal reef complexes in Bocas del Toro, Panama (Fig. 3B–D). These observations
occurring at depths from < 1 to > 20 m (Kissling, 1977; Gleason, 1992; Green et al., 2008; Aronson et al., 2008). Growth forms include massive, encrusting, and plating morphologies. Gleason (1992) noted that gradual reduction in colony convexity with increasing depth is an ecophenotypic response to an overall reduction in light intensity. Since coral scientists have been studying the effects of sedimentation on corals, P. astreoides has proved to be somewhat of a paradox. For instance, Rogers (1990) in her classic paper on sedimentation on coral reefs noted that “(F)ield observations are sometimes contradictory and at times appear to differ from laboratory results. For example, laboratory experiments (Hubbard and Pocock, 1972; Bak and Elgershuizen, 1976) indicated that Porites astreoides would be inefficient or only moderately good at rejecting sediments, relative to other species, but Morelock et al. (1983) and Cortés and Risk (1985) found it one of the most abundant species in heavily sedimented areas.“ Ultimately, this conundrum has led a number of researchers to try tease out the impacts of both turbidity and sedimentation on this common reef-building species (Coffroth, 1985, 1988a,b; Gleason, 1998). P. astreoides is an example of a coral that uses mucus entanglement as its major mode of sediment rejection (Lewis, 1973; Coffroth 1985, 1988a,b; Gleason, 1998). On P. astreoides, the mucous sheet is a translucent film that adheres tightly to the colony. With time, it becomes fouled with sediment and other debris developing a dirty, mat-like appearance (Fig. 1A). Eventually, the mucous sheet detaches from the coral and is wafted (sloughed) off by wave action and water currents (Fig. 1B and C; Coffroth, 1991). It is well established that Porites spp. have high production rates of mucus that cover coral colonies in the form of mucous sheets that exhibit a distinct aging cycle (Fig. 2) making it an ideal model system to study dynamics of the mucus-associated microbiota (Hadaidi et al., 2017). Coffroth (1991) specifically showed that the periodicity in these mucous sheet cycles are endogenous rhythms that are most likely caused by a lunar zeitgeber and/or the expression of a direct response to external stimuli that follow a lunar periodicity (approximately 28 days in duration). This circa-lunar rhythm may represent a powerful clock that is retained for synchronizing events such as monthly reproductive cycles (Olive and Garwood, 1983). This endogenous reproductive rhythm is commonly observed in brooding Porites spp. (Chornesky and Peters, 1987; McGuire, 1998). Glasl et al. (2016) showed convincing evidence that the surface mucus layer in P. astreoides contributes to coral health and vitality and that cyclical mucus shedding has a key role in the overall dynamics and regulation of the coral microbiome. Surprisingly enough, these cycles do not appear to be a response of the colony to environmental parameters such as temperature, salinity or sedimentation (Coffroth 1988a,b, 1991). Specifically, Coffroth (1985) found no significant
Fig. 1. (A) Porites astreoides from southeast Florida showing colony completely fouled by a sediment-laden mucous sheet. (B) Same colony showing progressive sloughing of mucous sheet; note how clear the colony is in the area where the mucous sheet has been sloughed. (C) Same colony after complete sloughing of mucous sheet. 3
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Fig. 2. Tagged P. astreoides colony from monitoring program associated with the Port Miami dredging project. This tagged coral was from one of the far-field control sites. Photo sequence shows the progressive fouling and clearing of a sediment-laden mucous sheet during a month of monitoring in June 2014. (A) Mucus-free colony in early portion of 28-day cycle. (B) Colony showing initial coating of mucus three days later. (C) Mucous sheet fully formed and coated with fine sediment. (D–F) Colony with progressive addition of sediment and debris on mucous sheet. (G) Maximum fouling of mucous sheet; note that without careful inspection. The colony is hardly discernable as a living coral. (H) Colony totally devoid of mucous sheet only four days after peak mucous sheet development.
immediately adjacent to one another are in opposite phases of a lunar cycle argues against sediment loading or some other local stress as being the proximal driver of mucous sheet development (Fig. 5).
confirm the limitations of using mucous sheet production as an early warning indicator of sediment stress. The author has also observed mucous sheets developed on branching Porites spp. (see Marcus and Thorhaug, 1981; Coffroth, 1983; Edmunds and Davies, 1986)
4. Discussion
3.2. Example project – dredging of Port Miami
There are a number of important questions raised by the BessellBrowne et al. (2017) manuscript. These include whether the Porites spp. used in their case study in Western Australia are an appropriate proxy to be used to detect sediment stress associated with dredging programs? While their data does show the potential for use on a case-by-case basis, questions remain whether their results have broad application within and between coral species in the Porites complex. Implicit in this analysis is a sound understanding of the biology of the organism used in the study, and whether its use as bio-indicator is narrowly constrained or is ubiquitous in its application. This is an especially daunting task as even experienced field personnel have trouble distinguishing between the massive Porites species in the wild (see Smith et al., 2007; Forsman et al., 2009; Tisthammer and Richmond, 2018, see also Abecia et al., 2016). This can be a significant issue throughout the Indo-Pacific where these Porites species form important components of the reef community (Veron, 2000; Pichon, 2011). Another important question is what is the ability to extrapolate the results from individual corals to the entire species population on a specific reef or area? For instance, their may be intraspecific (genotypic) variation of corals response to sediment stress on the same reef (Lui et al., 2012). This is an especially important question as BessellBrowne et al. (2017) noted that at sites close to the dredging activities, the prevalence of the colonies that developed a mucous sheet was < 50%. What about the other 50% of the colonies? Why did these corals not develop mucous sheets in response to the same level of sediment and turbidity stress? Bessell-Browne et al (2017) also note that in a sediment dousing laboratory experiment, < 30% of the fragments exposed to repeated sediment deposition events produced mucous sheets over the 28-day exposure period. Wouldn’t one expect a much higher
As part of compliance monitoring program associated with the Port Miami Phase III Deepening project, some 612 coral colonies from 23 different scleractinian species were followed through time for the duration of the project (Precht et al., 2019). This included 336 corals at sites that were adjacent to dredging and 276 at far-field controls. Most tagged corals were small, ranging from < 10 to 40 cm in diameter. Between 13 October 2013 and 15 July 2015 each Port Miami tagged coral monitoring location was surveyed approximately 40 times. Of these 612 tagged colonies, 105 were Porites astreoides. At the channelside sites immediately adjacent to the dredge activities, 54 out of 60 (90%) P. astreoides colonies developed mucous sheets during the project while at the far-field control sites, 48 out of 55 (87.3%) developed mucous sheets. These results show that the impact to the channel-side corals in terms of mucous sheet development was essentially invariant from their project controls. Therefore, the use of these tagged corals as an indicator of dredge-related stress would have resulted in an excessively high Type-I error rate with the project controls showing no difference than the impact site corals. Thus, at Port Miami the ability to use sediment covered mucous sheets on Porites spp. as an indicator of dredge-related stress would have led down a false trail. In addition, the development of mucous sheets at Port Miami generally followed a 28day cycle and thus, was likely controlled by endogenous rhythms and not local stressors (Figs. 3 and 4). It is important to note, however, that some P. astreoides colonies started their mucus cycle on the phase of the new moon while others on the full moon. It is presently unknown if there is a biological advantage for some of these corals being “out of phase” with each other within this 28-day lunar cycle. However, the fact that P. astreoides colonies 4
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Fig. 3. Paired sequential photographs using a framer with fixed focal distance showing the same Porites colonies with and without mucous sheets taken about a week apart. (A) Plating variety of P. astreoides from −17 m depth (57 ft.) in the West Bay Coral Reef Replenishment Zone off Seven-Mile Beach, Grand Cayman. Note the light fouling of the mucous sheet by sediment and debris in left panel. (B) Plating colony of P. astreoides from −12 m depth (39 ft.) at HS Reef in Bocas del Toro, Panama showing moderate fouling by sediment and debris in left panel. (C) Colony of P. colonensis from −10 m depth at HS Reef showing excessive sediment coating that rapidly cleared (sloughed off) within a week. (D) Massive form of P. astreoides from −3 m depth (10 ft.) on HS reef showing identical sequence as the plating forms; note sponge in upper right corner of photograph in left panel is absent in photo taken a week later.
mucous sheet response to experimental dousing experiments if the mucus production was initiated by the coral as a direct response to the amount of sediment exposure? We also need to know if other mounding or plating Porties spp. from other areas, such as Porites astreoides in the Caribbean can be used as a bio-indicator for sediment stress? Because mucous sheet development
in Caribbean Porites spp. are driven by an endogenous cycle (Coffroth, 1991), its usefulness as a sediment stress indicator is greatly diminished. For instance, the Florida Department of Environmental Protection (FDEP) developed a sediment scoring method for determining the level of sediment stress on a coral by visually assigning a rank score (FDEP, 2014). Categories of sediment cover would be reported on a 5
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Fig. 4. (A) Colony of P. astreoides at start of 28-day mucous sheet cycle (June 3, 2014). (B) Initial development of mucus coating three-days later June 7, 2014. (C–D) Progressive sediment fouling of mucous sheet over the next few weeks. (E) Sloughing of mucous sheet showing some sediment-covered mucus remaining on a portion of the colony on July 3, 2014. (F) Mucus-free colony approximately one-month after start of cycle.
Fig. 5. (A) Colony of P. astreoides without mucus coating. However, note smaller colony to right (highlighted with orange arrow) is covered in a sediment-fouled mucous sheet. (B) Same two colonies 21-days later showing exact opposite trend.
scale from 0 to 5; this scale represents a range of sediment cover from no cover (0), dusting of sediment (1), light accumulation of sediment (2), moderate accumulation of sediment (3), severe accumulation of sediment (4), and complete burial (5). However, based on the cyclical nature of mucous-sheet development and sloughing on encrusting, mounding, and plating Porites (see Figs. 1–4), the score would vary not based on the actual level of sediment stress at a given point-in-time but on where in the 28-day cycle the coral is observed (see Fig. 5). This assignment would result in a significant number of both Type-I and Type-II errors. For instance, early in the cycle, little mucus or sediment might be observed even during periods of excessive sedimentation (Type-II error), while late in the cycle, the coral may be fouled by a thick, opaque coating of sediment-laden mucus irrespective of
sedimentation level (Type-I error). 5. Conclusions Using the results from Bessell-Browne et al. (2017) combined with analysis from data collected for P. astreoides from throughout the Caribbean, and specifically at the Port Miami dredge project, it appears that Porites spp. corals do not always provide a consistent early warning of the deleterious effects of sediments on these corals. Specifically, difficulties in using Porites spp. as bio-indicators include their endogenous production of mucous sheets on a lunar cycle. Because of this, there is a danger of an excessive rate of both Type-I and Type-II statistical errors and accordingly, the perceived agent causing the 6
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Fig. 6. Massive Porites spp. colony photographed on low-energy patch reef within Cook’s Bay, Moorea, French Polynesia. (A) Colony covered with sediment-laden mucous sheet that tightly adheres to the coral surface. (B) Same colony four-days later showing initial stages of mucus sloughing.
validating these species to infer the level of sediment impact associated with dredging projects. Based on the present state of the science, it is apparent that a composite analysis of the representative corals present at a specific site should be performed for the most accurate assessment of sediment stress on a reef with the observations of sediment-fouled mucous sheets on encrusting, massive, and plating Porties species being an integral part of that equation.
development of mucous sheets may be wrongly attributed. Thus, the resulting management solution to the purported impact may therefore be inappropriate and/or ineffective (Anderson, 1998). Identifying causative agents and constructing the links that are necessary to establish cause-and-effect relationships are vitally important for use in coral reef resource management, protection, and even post-project litigation. While the two Porites species used in Bessell-Browne et al. (2017) show great promise as a bio-indicator, its application may be restricted to those specific Western Australian reefs that historically have very low natural background sediment levels. As Bessell-Browne et al. (2017) note “mucous sheet formation in clear-water environments such as Barrow Island is typically low (< 0.5% prevalence) and can increase 10-fold in response to elevated sediment loads.” While this result is important, its use as a broad bio-indicator for dredging projects in other regions throughout the Indo-Pacific is presently unknown. For instance, Bessell-Browne et al. (2017) did not observe cyclic (lunar) rhythms in the formation of mucous sheets but state that they are a direct, emergency response of the coral to excessive sediment stress. I fully agree with their assessment based on the extensive data set they used. However, on P. lobata colonies from the Arabian Seas, Hadaidi et al. (2017) found that mucous-sheet development was cyclical in nature. I have also observed cyclic development and shedding of sediment-laden mucous sheets on massive Porites lobata colonies in Moorea, French Polynesia (Fig. 6). These cycles mimic the lunar periodicity observed by Coffroth (1985, 1991) and Glasl et al. (2016) for P. astreoides. Thus, our collective enthusiasm for the potential use of Porites spp. as bio-indicators need to be tempered under further tests from other regions confirm the extremely compelling results presented in the BessellBrowne et al. (2017) manuscript. Based on all the reasons detailed above, sound inference derived from the most complete scientific evidence should be used when trying to find a species to employ as a proxy bio-indicator for assessing the level of sediment stress on coral reefs. This is why the 12-point analysis developed in Table 1 above is critical in determining, at a minimum, the efficacy and usefulness of a species proposed for use as a bio-indicator in environmental assessments. Unfortunately, at this time no such bioindicator has definitively been found for use as a viable, stand-alone tool in coral reef sediment impact assessments. Even if we agree that the Porites spp. documented in Bessell-Browne et al. (2017) could be used as a cost-effective tool for ecological monitoring programs associated with dredging programs, it is important to note that single-species surrogates are not as good at predicting overall sediment stress and impacts as multi-species surrogates. Because of the cyclical, endogenous nature of mucus production in some Porites species, we need to proceed with extreme caution before
Declaration of Competing Interest This work was supported in-part to the author by salary from the marine and environmental sciences firm Dial Cordy and Associates, Inc. (DCA). DCA received funding under contracts to Great Lakes Dredge and Dock Company, LLC sponsored by the USACE, Jacksonville District and PortMiami, Miami-Dade County for environmental compliance and analysis under FDEP Permit No. 0305721-001-BI. These contracts provided support to undertake monitoring of coral populations in the vicinity of PortMiami in Miami-Dade County, Florida. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. Research described in Moorea, F.P. and Bocas del Toro, Panama was performed by the author in association with Northeastern University’s Three-Seas Marine Biology Program where he teaches a course in coral reef ecology annually. This manuscript was written on the personal time of the author and the views, statements, findings, conclusions and recommendations expressed herein are his own and do not necessarily reflect the views of DCA, the USACE, PortMiami, Northeastern University, or Miami-Dade County. Based on the above, the author declares that no competing interests exist. References Abecia, J.E.D., Guest, J.R., Villanueva, R.D., 2016. Geographical variation in reproductive biology is obscured by the species problem: a new record of brooding in Porites cylindrica, or misidentification? Invert. Biol. 135, 58–67. Adams, S.M., 2003. Establishing causality between environmental stressors and effects on aquatic ecosystems. Human Ecol. Risk Assess. Int J. 9, 17–35. Anderson, J.L., 1998. Errors of inference. Chapter 6. Statistical Methods for Adaptive Management Studies. Res. Br., Victoria, BC, Land Manage. Handb. No. 42. Aronson, R., Bruckner, A., Moore, J., Precht, B., Weil, E., 2008. Porites astreoides. The IUCN Red List of Threatened Species 2008. e.T133680A3861919. Aronson, R.B., Precht, W.F., 2006. Conservation, precaution, and Caribbean reefs. Coral Reefs. 25, 441–450. Bak, R., Elgershuizen, J., 1976. Patterns of oil-sediment rejection in corals. Mar. Biol. 37, 105–113. Banaszak, A.T., 2007. Photoprotective physiological and biochemical responses of aquatic organisms. Royal Soc. Chem. UV Effects Aquat. Organ. Ecosyst. 1, 329–356. Bessell-Browne, P., Fisher, R., Duckworth, A., Jones, R., 2017. Mucous sheet production in Porites: an effective bioindicator of sediment related pressures. Ecol. Ind. 77, 276–285. Brown, B.E., 2007. Coral reefs of the Andaman Sea—an integrated perspective. Ocean.
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Phenotypic plasticity for skeletal growth, density and calcification of Porites lobata in response to habitat type. Coral Reefs 26, 559–567. Stafford-Smith, M.G., 1993. Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Mar. Biol. 115, 229–243. Stafford-Smith, M., Ormond, R., 1992. Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Mar. Freshwat. Res. 43, 683–705. Teai, T., Drollet, J.H., Bianchini, J.P., Cambon, A., Martin, P.M., 1998. Occurrence of ultraviolet radiation-absorbing mycosporine-like amino acids in coral mucus and whole corals of French Polynesia. Mar. Freshwat. Res. 49, 127–132. Telesnicki, G.J., Goldberg, W.M., 1995. Effects of turbidity on the photosynthesis and respiration of two South Florida reef coral species. Bull. Mar. Sci. 57, 527–539. Thompson, J.H., 1980. Responses of Selected Scleractinian Corals to Drilling Fluids Used in the Marine Environment. PhD Dissertation. 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Letter to the Editor histopathological rating scale of sedimentation stress in the Caribbean coral Montastraea cavernosa. In: Proc. 10th Int Coral Reef Symp, pp. 1168–1173. Veron, J., 2000. Corals of the World, vol.1–3, 1–3. Wesseling, I., Uychiaoco, A.J., Aliño, P.M., Aurin, T., Vermaat, J.E., 1999. Damage and recovery of four Philippine corals from short-term sediment burial. Mar. Ecol. Prog. Ser. 176, 11–15. Wesseling, I., Uychiaoco, A.J., Aliño, P.M., Vermaat, J.E., 2001. Partial mortality in Porites corals: variation among Philippine reefs. Int. Rev. Hydrobiol. 86, 77–85. Wooldridge, S.A., 2009. A new conceptual model for the enhanced release of mucus in symbiotic reef corals during ‘bleaching’conditions. Mar. Ecol. Prog. Ser. 396, 145–152.
Zettler, M.L., Proffitt, C.E., Darr, A., Degraer, S., Devriese, L., Greathead, C., Kotta, J., Magni, P., Martin, G., Reiss, H., Speybroeck, J., 2013. On the myths of indicator species: issues and further consideration in the use of static concepts for ecological applications. PLoS One 8, e78219.
William F. Precht Dial Cordy and Associates Inc., Coastal and Marine Programs, 1011 Ives Dairy Road, Suite 210, Miami, FL 33179, USA E-mail address: [email protected].
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Letter to the Editor Can Porites spp. corals be used as a bio-indicator for sediment stress on coral reefs?
T
ARTICLE INFO
ABSTRACT
Keywords: Coral reefs Bio-indicator Impact assessment Dredging Sediment Porites Mucus
Bessell-Browne et al. (2017) published a paper where they proposed using mounding Porites spp. corals from Western Australia as a bio-indicator of sediment stress on coral reefs. They based their interpretations on results obtained during the monitoring of a capital dredging program coupled with laboratory sediment dousing experiments. They stated that because these Porites species generate mucous sheets in response to sediment loading, they could be used as an early warning indicator of sediment stress adjacent to sensitive coral resources. While their results are compelling, there are several confounding issues that arise questioning the wide-scale application and use of Porites spp. corals as bio-indicators. Using examples of Porites species from both the IndoPacific and Caribbean, I detail a number of contrary results that reveal that mucous sheet development is most likely attributed to mucus production and subsequent mucus sloughing that are cued to an endogenous lunar cycle (approximately 28 days in duration) and not necessarily as a direct strategy to protect the coral tissue from harm due to sediment stress. While the mucous sheet becomes fouled with sediment during the cycle, the amount of sediment observed may not be a response to the level of sediment stress, but where in the 28-day cycle the mucous sheet is observed. Thus, depending on when you observe the colony (early, middle or late in the 28-day cycle) the level of purported sediment impact would be highly variable. This variability leads to an unacceptably high rate of both Type-I and Type-II statistical errors. Because of the cyclical, endogenous nature of mucus production in many Porites spp., extreme caution should be employed before using these species to infer the level of sediment impact associated with dredging projects or their use as a predictive tool of sediment stress on coral reefs.
1. Introduction In biological impact studies, the amount of ecological data collected is often overwhelming. To reduce the information overload, scientists often attempt to isolate key aspects of the environmental condition by focusing on specific biological indicators that act as surrogates for the entire ecosystem. Bio-indicators possess a strong appeal for field biologists, conservationists, managers, and regulators as they provide a cost- and time-efficient means to assess the impacts of environmental disturbances on an ecosystem by focusing on a single organism, species, or genus (Caro, 2010). In a recent manuscript, Bessell-Browne et al. (2017) provide convincing, yet equivocal evidence for the use of Porites spp. corals as a reliable bio-indicator for sediment stress on coral reefs. Specifically, they looked at the response of two mounding species, Porites lobata and Porites lutea, to variations in sedimentation related to a dredging project in Western Australia. As a response to elevated concentrations of suspended sediments and deposition of fine silt, they found that the two Porites species developed mucous sheets which became progressively fouled with sediments over time. These mucous sheets were periodically sloughed off resulting in a sediment-free surface that became re-fouled with the addition of new sediment. Results of laboratory experiments performed on these two species were similar to their in-situ field observations. In their study, mucous-sheet prevalence in Porites spp. was examined before and during a large-scale dredging program which resulted in an increase in the intensity, duration, and frequency of turbidity events compared to pre-project, base-line levels (Evans et al., https://doi.org/10.1016/j.ecolind.2019.105538 Received 28 June 2019; Accepted 1 July 2019 Available online 09 July 2019 1470-160X/ © 2019 Elsevier Ltd. All rights reserved.
2012; Fisher et al., 2015; Jones et al., 2015). At sites close to the dredging activities, mucous sheet prevalence reached as high as 50%, and over the duration of the dredging program ~75% of colonies were observed with a mucous sheet at some point-in-time (at least once over a 530-day period from 19 May 2010 to 31 October 2011). In contrast, at their far-field reference sites (> 20 km away), mucous-sheet prevalence was negligible (~0.2%) during the dredging program. These compelling results led Bessell-Browne et al. (2017) to posit a strong association between mucous-sheet coverage and prevalence suggesting this process is a viable, sub-lethal bio-indicator of sediment stress for coral reefs. Significantly, if Bessell-Browne et al. (2017) are correct in their assessment that mucous-sheet production is solely an emergency environmental response to an increase in sediment load, it should therefore be plausible to use Porites as a tool for monitoring and assessing sediment stress associated with dredging programs on coral reefs not just in Western Australia, but in all reef regions where these Porites species are present. Thus, a single, accurate coral proxy, in this case Porites spp., could potentially eliminate the need for additional indicators of sediment stress, ultimately simplifying and streamlining the monitoring process. In fact, their conclusion, while based on data limited to a few reefs in Western Australia, implies the broad application of using massive Porites spp. in this manner. Their take home message is “… mucous sheet prevalence appears to be a useful sub-lethal indicator of sediment related stress for coral communities and should be considered as a monitoring tool during future dredging projects or exposure to elevated sediment loads.” Unfortunately, it is not that simple; the adequate assessment of a
Ecological Indicators 106 (2019) 105538
Letter to the Editor
the surfaces of living corals can ultimately cause tissue necrosis and death because of the combined effects of smothering (Bak and Elgershuizen, 1976; Rogers, 1983, 1990; Erftemeijer et al., 2012; Duckworth et al., 2017) and microbial action (Hodgson, 1990). To that end, numerous researchers have been trying to understand the varying responses of corals to sediment stress and burial under both field and laboratory conditions (Lasker, 1980; Peters and Pilson, 1985; Rice and Hunter, 1992; Stafford-Smith, 1993; Telesnicki and Goldberg, 1995; Wesseling et al., 1999). One of the goals over the last two decades has been to find a single biological indicator for determining the response of corals to sediment stress (i.e. Wesseling et al., 2001; Nugues and Roberts, 2003; Vargas-Ángel et al., 2006; Rotmann and Thomas, 2012). To date, however, that search has been elusive. Corals use a number of methods to reject sediment from their colonies. These include both passive and active methods. Passive methods of sediment rejection include the influences of wave and current action as well as coral colony size, orientation, and morphology (Rogers, 1983; Stafford-Smith and Ormond, 1992; Sanders and Baron-Szabo, 2005). Active methods include tentacle manipulation, polyp expansion, pulsed polyp contraction, ciliary currents, tissue expansion, and mucus entanglement (Stafford-Smith and Ormond, 1992). Most reef-building corals use one or more of these mechanisms in tandem to assist in preventing sediment from accumulating and damaging coral tissues. It is because of the wide inter- and intraspecific variability in these processes that no two coral species on the reef respond to increases in sedimentation the same manner making it difficult, if not impossible, to use a specific coral as a proxy for the level of sedimentation or “stress” on the reef at any given snapshot in time (Lasker, 1980; Rogers, 1983; Brown and Howard, 1985; Gleason, 1998; Lui et al., 2012). Pichon (2011) noted “several species in the genus Porites produce abundant sheets of mucus, which covers and protects the living tissue, and on which the fine sediment particles get trapped. After some time, generally up to a few weeks, the sheet of mucus is eliminated, thus removing the sedimented particles, and the process may start again.” Bessell-Browne et al. (2017) attributed the development of these mucous sheets to high levels of suspended sediment in the water column as well as direct sediment contact with the colony surface. Stafford-Smith and Ormond (1992) proffered that the reason massive Porites colonies use mucus entanglement is because the coral calices are so small (< 2.5 mm) in diameter, that they are essentially incapable of actively rejecting sediment. However, Stafford-Smith and Ormond (1992) were unable to generate mucous sheet production in either laboratory or field experiments, even when exposing colonies to a steady input of fine, silt-sized particles. Rogers (1990) noted, “we might expect smaller-polyped 'autotrophic' corals which depend more on light to succumb more quickly to turbid conditions than large-polyped corals …” This, however, is contrary to field observations that show some small-polyped corals such as Porites, to be relatively tolerant of high levels of turbidity and sedimentation (Potts et al., 1985; Veron, 2000; Brown, 2007; Morgan et al., 2016). The coral surface mucus layer provides a vital interface between the surfaces of the coral polyp and the seawater environment and mucus can act in defense against a wide range of environmental stresses including sediment removal (Ducklow and Mitchell, 1979; Kato, 1987; Veron, 2000; Brown and Bythell, 2005; Huettel et al., 2006; Banaszak, 2007; Johnston and Rohwer, 2007; Jatkar, 2009; Wooldridge, 2009; Jatkar et al., 2010; Bythell and Wild, 2011; Glasl et al., 2016). The production of mucous sheets on corals has led some workers to propose that mucus production is solely a response to stressful conditions (Bak and Elgershuizen, 1976; Thompson, 1980; Krupp, 1984; Kato, 1987; Bessell-Browne et al., 2017).
Table 1 Criteria for the selection of indicator species (modified from Carignan and Villard, 2002; Goodsell et al., 2009, and Adams, 2003). (1) Biological Plausibility – There is a credible or reasonable biological and/or toxicological basis for the proposed mechanism linking the cause and effect. (2) The species must provide an early warning of the organism’s responses to the environmental stress. (3) Specificity of Association – Directly indicates the cause of the response to the stressor in question and eliminates other confounding stressors. (4) Biological Gradient – Provides a continuous assessment over a wide range and intensity of stress. (5) Strength of Association - Provides a measurable response to the stress. (6) Chosen species is sensitive to the stress but does not experience stress-related mortality. (7) Chosen species are locally abundant within the area of study including at both the impacted and control sites. (8) Chosen species are relatively stable despite environmental variability. (9) The ecology and physiology of the chosen species are well understood. (10) Chosen species are simple and cost-effective to monitor. (11) Chosen species can be accurately assessed by all personnel involved in the monitoring program. (12) Consistency of Association – The results need to be repeatable in time and space.
biological indicator depends on many factors and for Porites spp. to be considered useful as a bio-indicator it needs to possess, at a minimum, 12 significant characteristics or criteria (see Table 1). The most important of which is point 12; the results need to be repeatable both in time and space. In addition to meeting these 12 criteria, another critical aspect for bio-indicators to be useful in providing an early warning of sediment effects on reef corals is the rate of Type-I statistical errors encountered (that is an effect is indicated by statistical analysis when in fact one is not present). Thus, in order for the bio-indicator approach to be effective, the number of false positives (i.e. making a Type-I error) needs to be small, while false negatives, indicating no effect when there is in fact one present (a Type-II error), must be kept to an absolute minimum. In environmental terms, making Type-II errors are far more serious (Aronson and Precht, 2006). Thus, the effectiveness of a bio-indicator, as an early warning signal for environmental impacts, decreases with the number of false negatives as well as false positives. A ‘‘sensitive’’ bio-indicator would be expected to produce more false positives. However, the indicator should be sensitive enough to react in a detectable way when a system is affected by an outside stress, and they should also remain reasonably predictable in their undisturbed state (Mapstone, 1996). Thus, an ideal bio-indicator for environmental impact monitoring programs should have ‘‘optimal’’ rather than ‘‘maximum’’ sensitivity. While the Porites spp. used in the Bessell-Browne et al. (2017) manuscript meet many of the 12-point criteria listed above, a critical analysis using all these criteria should be analyzed for evaluating the efficacy of the chosen bio-indicator species. In addition, explicit attention to rates of Type-I and Type-II errors should become standard practice in all impact assessment studies (Anderson, 1998). This is especially important when using a single bio-indicator as a proxy for the impact because actions based on either type of error can be costly. Using examples of mucous-sheet development in Porites spp. colonies, I detail numerous conflicting and confounding issues that may make the use of Porites spp. as a broad-scale bio-indicator for coral reef sediment monitoring programs more illusory than real (see Zettler et al., 2013 for a similar critique in a different context). 2. Background It has long been known that sediments settling onto reef surfaces have been shown to exert control on the distributions and abundances of coral species through both lethal and sublethal effects (Rogers, 1983, 1990; Stafford-Smith and Ormond, 1992, Stafford-Smith, 1993, Erftemeijer et al., 2012; Flores et al., 2012; Duckworth et al. 2017). In worst case scenarios, the settlement of inorganic particles directly onto
3. Confounding problems 3.1. Caribbean examples of Porites mucous-sheet development Porites astreoides is one of the most common Caribbean reef corals 2
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increase in mucous sheet production in P. astreoides related to increased sedimentation, however, she did note there may be some modulation in mucus production associated with extremes in these parameters (Coffroth, 1991, see also Gleason, 1998; Wooldridge, 2009). Porites astreoides also exhibits variation in colony color that consists of brown, tan, green, and yellow individuals or morphs. Green and yellow morphs of this species appear to be better adapted than their tan and brown counterparts to inhabit shallow water areas where high intensities of ultraviolet radiation persist (Gleason, 1993). While these color morphs exhibit no other obvious differences in colony or polyp morphology (Potts et al., 1993), closer examination of morph-specific distributions at several sites suggest that at deeper depths or in areas exposed to greater sediment stress the brown morphs may be favored (Gleason, 1998). Gleason (1998) specifically noted that the brown morphs were better at shedding sediments than their lighter colored conspecifics even though their small-scale morphologies were very similar. Gleason attributed this to large amounts of fluid mucus (Coffroth, 1990) that, in tandem with water motion, appears to be important in clearing the colony of sediment. Gleason (1998) also noted that under both in situ and laboratory conditions surfaces of the brown morphs tended to be slimier to the touch than the green morphs suggesting that they produce greater quantities of fluid mucus. While not quantified, Gleason found that the brown morphs in sediment shedding experiments appeared to produce more mucus than the green morphs (i.e., cohesive mucoid coverings derived from fluid mucus), that assisted in shedding sediments and protecting the underlying tissues from damage. These mucous sheets may also include protection from increased temperature, ultra-violet radiation, and even pathogenic bacteria (Koh, 1997; Teai et al., 1998; Shnit-Orland and Kushmaro, 2009). It has also been shown that P. astreoides uses these mucus layers for feeding and nutrient cycling (Lewis and Price, 1975; Coffroth, 1990; Mills and Sebens, 2004). For instance, Mills and Sebens, (2004) noted that there was a decrease in percent nitrogen of the sediments egested by P. astreoides suggesting that these corals are removing nitrogen from sediments that settle on their surfaces. They also noted that the sediments sloughed by P. astreoides were also lower in percent nitrogen, indicating that this species may be selectively ingesting particles with higher nitrogen content, or stripping the sediment of organic nitrogen during the sloughing process (see also Lirman et al., 2008). Similar, observations of repeated, cyclical mucous sheet development and sloughing have been made by the author on encrusting, plating, and mounding Porites spp. throughout the Caribbean. Observations of mucous sheet development include areas of exceedingly low turbidity and sedimentation such as the reefs off Grand Cayman (Fig. 3A) as well as with those of highly turbid, lagoonal reef complexes in Bocas del Toro, Panama (Fig. 3B–D). These observations
occurring at depths from < 1 to > 20 m (Kissling, 1977; Gleason, 1992; Green et al., 2008; Aronson et al., 2008). Growth forms include massive, encrusting, and plating morphologies. Gleason (1992) noted that gradual reduction in colony convexity with increasing depth is an ecophenotypic response to an overall reduction in light intensity. Since coral scientists have been studying the effects of sedimentation on corals, P. astreoides has proved to be somewhat of a paradox. For instance, Rogers (1990) in her classic paper on sedimentation on coral reefs noted that “(F)ield observations are sometimes contradictory and at times appear to differ from laboratory results. For example, laboratory experiments (Hubbard and Pocock, 1972; Bak and Elgershuizen, 1976) indicated that Porites astreoides would be inefficient or only moderately good at rejecting sediments, relative to other species, but Morelock et al. (1983) and Cortés and Risk (1985) found it one of the most abundant species in heavily sedimented areas.“ Ultimately, this conundrum has led a number of researchers to try tease out the impacts of both turbidity and sedimentation on this common reef-building species (Coffroth, 1985, 1988a,b; Gleason, 1998). P. astreoides is an example of a coral that uses mucus entanglement as its major mode of sediment rejection (Lewis, 1973; Coffroth 1985, 1988a,b; Gleason, 1998). On P. astreoides, the mucous sheet is a translucent film that adheres tightly to the colony. With time, it becomes fouled with sediment and other debris developing a dirty, mat-like appearance (Fig. 1A). Eventually, the mucous sheet detaches from the coral and is wafted (sloughed) off by wave action and water currents (Fig. 1B and C; Coffroth, 1991). It is well established that Porites spp. have high production rates of mucus that cover coral colonies in the form of mucous sheets that exhibit a distinct aging cycle (Fig. 2) making it an ideal model system to study dynamics of the mucus-associated microbiota (Hadaidi et al., 2017). Coffroth (1991) specifically showed that the periodicity in these mucous sheet cycles are endogenous rhythms that are most likely caused by a lunar zeitgeber and/or the expression of a direct response to external stimuli that follow a lunar periodicity (approximately 28 days in duration). This circa-lunar rhythm may represent a powerful clock that is retained for synchronizing events such as monthly reproductive cycles (Olive and Garwood, 1983). This endogenous reproductive rhythm is commonly observed in brooding Porites spp. (Chornesky and Peters, 1987; McGuire, 1998). Glasl et al. (2016) showed convincing evidence that the surface mucus layer in P. astreoides contributes to coral health and vitality and that cyclical mucus shedding has a key role in the overall dynamics and regulation of the coral microbiome. Surprisingly enough, these cycles do not appear to be a response of the colony to environmental parameters such as temperature, salinity or sedimentation (Coffroth 1988a,b, 1991). Specifically, Coffroth (1985) found no significant
Fig. 1. (A) Porites astreoides from southeast Florida showing colony completely fouled by a sediment-laden mucous sheet. (B) Same colony showing progressive sloughing of mucous sheet; note how clear the colony is in the area where the mucous sheet has been sloughed. (C) Same colony after complete sloughing of mucous sheet. 3
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Fig. 2. Tagged P. astreoides colony from monitoring program associated with the Port Miami dredging project. This tagged coral was from one of the far-field control sites. Photo sequence shows the progressive fouling and clearing of a sediment-laden mucous sheet during a month of monitoring in June 2014. (A) Mucus-free colony in early portion of 28-day cycle. (B) Colony showing initial coating of mucus three days later. (C) Mucous sheet fully formed and coated with fine sediment. (D–F) Colony with progressive addition of sediment and debris on mucous sheet. (G) Maximum fouling of mucous sheet; note that without careful inspection. The colony is hardly discernable as a living coral. (H) Colony totally devoid of mucous sheet only four days after peak mucous sheet development.
immediately adjacent to one another are in opposite phases of a lunar cycle argues against sediment loading or some other local stress as being the proximal driver of mucous sheet development (Fig. 5).
confirm the limitations of using mucous sheet production as an early warning indicator of sediment stress. The author has also observed mucous sheets developed on branching Porites spp. (see Marcus and Thorhaug, 1981; Coffroth, 1983; Edmunds and Davies, 1986)
4. Discussion
3.2. Example project – dredging of Port Miami
There are a number of important questions raised by the BessellBrowne et al. (2017) manuscript. These include whether the Porites spp. used in their case study in Western Australia are an appropriate proxy to be used to detect sediment stress associated with dredging programs? While their data does show the potential for use on a case-by-case basis, questions remain whether their results have broad application within and between coral species in the Porites complex. Implicit in this analysis is a sound understanding of the biology of the organism used in the study, and whether its use as bio-indicator is narrowly constrained or is ubiquitous in its application. This is an especially daunting task as even experienced field personnel have trouble distinguishing between the massive Porites species in the wild (see Smith et al., 2007; Forsman et al., 2009; Tisthammer and Richmond, 2018, see also Abecia et al., 2016). This can be a significant issue throughout the Indo-Pacific where these Porites species form important components of the reef community (Veron, 2000; Pichon, 2011). Another important question is what is the ability to extrapolate the results from individual corals to the entire species population on a specific reef or area? For instance, their may be intraspecific (genotypic) variation of corals response to sediment stress on the same reef (Lui et al., 2012). This is an especially important question as BessellBrowne et al. (2017) noted that at sites close to the dredging activities, the prevalence of the colonies that developed a mucous sheet was < 50%. What about the other 50% of the colonies? Why did these corals not develop mucous sheets in response to the same level of sediment and turbidity stress? Bessell-Browne et al (2017) also note that in a sediment dousing laboratory experiment, < 30% of the fragments exposed to repeated sediment deposition events produced mucous sheets over the 28-day exposure period. Wouldn’t one expect a much higher
As part of compliance monitoring program associated with the Port Miami Phase III Deepening project, some 612 coral colonies from 23 different scleractinian species were followed through time for the duration of the project (Precht et al., 2019). This included 336 corals at sites that were adjacent to dredging and 276 at far-field controls. Most tagged corals were small, ranging from < 10 to 40 cm in diameter. Between 13 October 2013 and 15 July 2015 each Port Miami tagged coral monitoring location was surveyed approximately 40 times. Of these 612 tagged colonies, 105 were Porites astreoides. At the channelside sites immediately adjacent to the dredge activities, 54 out of 60 (90%) P. astreoides colonies developed mucous sheets during the project while at the far-field control sites, 48 out of 55 (87.3%) developed mucous sheets. These results show that the impact to the channel-side corals in terms of mucous sheet development was essentially invariant from their project controls. Therefore, the use of these tagged corals as an indicator of dredge-related stress would have resulted in an excessively high Type-I error rate with the project controls showing no difference than the impact site corals. Thus, at Port Miami the ability to use sediment covered mucous sheets on Porites spp. as an indicator of dredge-related stress would have led down a false trail. In addition, the development of mucous sheets at Port Miami generally followed a 28day cycle and thus, was likely controlled by endogenous rhythms and not local stressors (Figs. 3 and 4). It is important to note, however, that some P. astreoides colonies started their mucus cycle on the phase of the new moon while others on the full moon. It is presently unknown if there is a biological advantage for some of these corals being “out of phase” with each other within this 28-day lunar cycle. However, the fact that P. astreoides colonies 4
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Fig. 3. Paired sequential photographs using a framer with fixed focal distance showing the same Porites colonies with and without mucous sheets taken about a week apart. (A) Plating variety of P. astreoides from −17 m depth (57 ft.) in the West Bay Coral Reef Replenishment Zone off Seven-Mile Beach, Grand Cayman. Note the light fouling of the mucous sheet by sediment and debris in left panel. (B) Plating colony of P. astreoides from −12 m depth (39 ft.) at HS Reef in Bocas del Toro, Panama showing moderate fouling by sediment and debris in left panel. (C) Colony of P. colonensis from −10 m depth at HS Reef showing excessive sediment coating that rapidly cleared (sloughed off) within a week. (D) Massive form of P. astreoides from −3 m depth (10 ft.) on HS reef showing identical sequence as the plating forms; note sponge in upper right corner of photograph in left panel is absent in photo taken a week later.
mucous sheet response to experimental dousing experiments if the mucus production was initiated by the coral as a direct response to the amount of sediment exposure? We also need to know if other mounding or plating Porties spp. from other areas, such as Porites astreoides in the Caribbean can be used as a bio-indicator for sediment stress? Because mucous sheet development
in Caribbean Porites spp. are driven by an endogenous cycle (Coffroth, 1991), its usefulness as a sediment stress indicator is greatly diminished. For instance, the Florida Department of Environmental Protection (FDEP) developed a sediment scoring method for determining the level of sediment stress on a coral by visually assigning a rank score (FDEP, 2014). Categories of sediment cover would be reported on a 5
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Fig. 4. (A) Colony of P. astreoides at start of 28-day mucous sheet cycle (June 3, 2014). (B) Initial development of mucus coating three-days later June 7, 2014. (C–D) Progressive sediment fouling of mucous sheet over the next few weeks. (E) Sloughing of mucous sheet showing some sediment-covered mucus remaining on a portion of the colony on July 3, 2014. (F) Mucus-free colony approximately one-month after start of cycle.
Fig. 5. (A) Colony of P. astreoides without mucus coating. However, note smaller colony to right (highlighted with orange arrow) is covered in a sediment-fouled mucous sheet. (B) Same two colonies 21-days later showing exact opposite trend.
scale from 0 to 5; this scale represents a range of sediment cover from no cover (0), dusting of sediment (1), light accumulation of sediment (2), moderate accumulation of sediment (3), severe accumulation of sediment (4), and complete burial (5). However, based on the cyclical nature of mucous-sheet development and sloughing on encrusting, mounding, and plating Porites (see Figs. 1–4), the score would vary not based on the actual level of sediment stress at a given point-in-time but on where in the 28-day cycle the coral is observed (see Fig. 5). This assignment would result in a significant number of both Type-I and Type-II errors. For instance, early in the cycle, little mucus or sediment might be observed even during periods of excessive sedimentation (Type-II error), while late in the cycle, the coral may be fouled by a thick, opaque coating of sediment-laden mucus irrespective of
sedimentation level (Type-I error). 5. Conclusions Using the results from Bessell-Browne et al. (2017) combined with analysis from data collected for P. astreoides from throughout the Caribbean, and specifically at the Port Miami dredge project, it appears that Porites spp. corals do not always provide a consistent early warning of the deleterious effects of sediments on these corals. Specifically, difficulties in using Porites spp. as bio-indicators include their endogenous production of mucous sheets on a lunar cycle. Because of this, there is a danger of an excessive rate of both Type-I and Type-II statistical errors and accordingly, the perceived agent causing the 6
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Fig. 6. Massive Porites spp. colony photographed on low-energy patch reef within Cook’s Bay, Moorea, French Polynesia. (A) Colony covered with sediment-laden mucous sheet that tightly adheres to the coral surface. (B) Same colony four-days later showing initial stages of mucus sloughing.
validating these species to infer the level of sediment impact associated with dredging projects. Based on the present state of the science, it is apparent that a composite analysis of the representative corals present at a specific site should be performed for the most accurate assessment of sediment stress on a reef with the observations of sediment-fouled mucous sheets on encrusting, massive, and plating Porties species being an integral part of that equation.
development of mucous sheets may be wrongly attributed. Thus, the resulting management solution to the purported impact may therefore be inappropriate and/or ineffective (Anderson, 1998). Identifying causative agents and constructing the links that are necessary to establish cause-and-effect relationships are vitally important for use in coral reef resource management, protection, and even post-project litigation. While the two Porites species used in Bessell-Browne et al. (2017) show great promise as a bio-indicator, its application may be restricted to those specific Western Australian reefs that historically have very low natural background sediment levels. As Bessell-Browne et al. (2017) note “mucous sheet formation in clear-water environments such as Barrow Island is typically low (< 0.5% prevalence) and can increase 10-fold in response to elevated sediment loads.” While this result is important, its use as a broad bio-indicator for dredging projects in other regions throughout the Indo-Pacific is presently unknown. For instance, Bessell-Browne et al. (2017) did not observe cyclic (lunar) rhythms in the formation of mucous sheets but state that they are a direct, emergency response of the coral to excessive sediment stress. I fully agree with their assessment based on the extensive data set they used. However, on P. lobata colonies from the Arabian Seas, Hadaidi et al. (2017) found that mucous-sheet development was cyclical in nature. I have also observed cyclic development and shedding of sediment-laden mucous sheets on massive Porites lobata colonies in Moorea, French Polynesia (Fig. 6). These cycles mimic the lunar periodicity observed by Coffroth (1985, 1991) and Glasl et al. (2016) for P. astreoides. Thus, our collective enthusiasm for the potential use of Porites spp. as bio-indicators need to be tempered under further tests from other regions confirm the extremely compelling results presented in the BessellBrowne et al. (2017) manuscript. Based on all the reasons detailed above, sound inference derived from the most complete scientific evidence should be used when trying to find a species to employ as a proxy bio-indicator for assessing the level of sediment stress on coral reefs. This is why the 12-point analysis developed in Table 1 above is critical in determining, at a minimum, the efficacy and usefulness of a species proposed for use as a bio-indicator in environmental assessments. Unfortunately, at this time no such bioindicator has definitively been found for use as a viable, stand-alone tool in coral reef sediment impact assessments. Even if we agree that the Porites spp. documented in Bessell-Browne et al. (2017) could be used as a cost-effective tool for ecological monitoring programs associated with dredging programs, it is important to note that single-species surrogates are not as good at predicting overall sediment stress and impacts as multi-species surrogates. Because of the cyclical, endogenous nature of mucus production in some Porites species, we need to proceed with extreme caution before
Declaration of Competing Interest This work was supported in-part to the author by salary from the marine and environmental sciences firm Dial Cordy and Associates, Inc. (DCA). DCA received funding under contracts to Great Lakes Dredge and Dock Company, LLC sponsored by the USACE, Jacksonville District and PortMiami, Miami-Dade County for environmental compliance and analysis under FDEP Permit No. 0305721-001-BI. These contracts provided support to undertake monitoring of coral populations in the vicinity of PortMiami in Miami-Dade County, Florida. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. Research described in Moorea, F.P. and Bocas del Toro, Panama was performed by the author in association with Northeastern University’s Three-Seas Marine Biology Program where he teaches a course in coral reef ecology annually. This manuscript was written on the personal time of the author and the views, statements, findings, conclusions and recommendations expressed herein are his own and do not necessarily reflect the views of DCA, the USACE, PortMiami, Northeastern University, or Miami-Dade County. Based on the above, the author declares that no competing interests exist. References Abecia, J.E.D., Guest, J.R., Villanueva, R.D., 2016. Geographical variation in reproductive biology is obscured by the species problem: a new record of brooding in Porites cylindrica, or misidentification? Invert. Biol. 135, 58–67. Adams, S.M., 2003. Establishing causality between environmental stressors and effects on aquatic ecosystems. Human Ecol. Risk Assess. Int J. 9, 17–35. Anderson, J.L., 1998. Errors of inference. Chapter 6. Statistical Methods for Adaptive Management Studies. Res. Br., Victoria, BC, Land Manage. Handb. No. 42. Aronson, R., Bruckner, A., Moore, J., Precht, B., Weil, E., 2008. Porites astreoides. The IUCN Red List of Threatened Species 2008. e.T133680A3861919. Aronson, R.B., Precht, W.F., 2006. Conservation, precaution, and Caribbean reefs. Coral Reefs. 25, 441–450. Bak, R., Elgershuizen, J., 1976. Patterns of oil-sediment rejection in corals. Mar. Biol. 37, 105–113. Banaszak, A.T., 2007. Photoprotective physiological and biochemical responses of aquatic organisms. Royal Soc. Chem. UV Effects Aquat. Organ. Ecosyst. 1, 329–356. Bessell-Browne, P., Fisher, R., Duckworth, A., Jones, R., 2017. Mucous sheet production in Porites: an effective bioindicator of sediment related pressures. Ecol. Ind. 77, 276–285. Brown, B.E., 2007. Coral reefs of the Andaman Sea—an integrated perspective. Ocean.
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William F. Precht Dial Cordy and Associates Inc., Coastal and Marine Programs, 1011 Ives Dairy Road, Suite 210, Miami, FL 33179, USA E-mail address: [email protected].
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