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Marine Pollution Bulletin xxx (2015) xxx-xxx
Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul Si MABIWE POIXOTTBON BDUXEUM
Review
Effects of sediments on the reproductive cycle of corals
R. Jones a'b'd'*, G.F. Ricardo a'b'c, A.P. Negri a'b
a Australian Institute of Marine Science (AIMS), Perth, Australia b Western Australian Marine Science Institution (WAMSI), Perth, Australia
c Centre of Microscopy, Charaterisation and Analysis, The University of Western Australia, Perth, Australia d Oceans Institute, University of Western Australia, Perth, Australia
ABSTRACT
Dredging, river plumes and natural resuspension events can release sediments into the water column where they exert a range of effects on underlying communities. In this review we examine possible cause-effect pathways whereby light reduction, elevated suspended sediments and sediment deposition could affect the reproductive cycle and early life histories of corals. The majority of reported or likely effects (30 + ) were negative, including a suite of previously unrecognized effects on gametes. The length of each phase of the life-cycle was also examined together with analysis of water quality conditions that can occur during a dredging project over equivalent durations, providing a range of environmentally relevant exposure scenarios for future testing. The review emphasizes the need to: (a) accurately quantify exposure conditions, (b) identify the mechanism of any effects in future studies, and (c) recognize the close interlinking of proximate factors which could confound interpretation of studies.
© 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).
Contents
1. Introduction ............................................................................................................................0
2. Example of water quality conditions during a large dredging program ....................................................................0
3. Gametogenesis and reproductive synchrony................................................................................................0
3.1. Effects of sediment on gametogenesis and reproductive synchrony ....................................................................0
4. Spawning synchrony and egg-sperm bundle release ........................................................................................0
4.1. Effects of sediment on spawning synchrony and egg-sperm bundle release ............................................................0
5. Fertilization..............................................................................................................................0
5.1. Effects of sediment on fertilization ..................................................................................................0
6. Embryogenesis and larval development....................................................................................................0
6.1. Effects of sediment on embryogenesis and larval development ........................................................................0
7. Settlement and metamorphosis............................................................................................................0
7.1. Effects of sediment on settlement ..................................................................................................0
8. New recruits ............................................................................................................................0
8.1. Effects of sediment on metamorphosis and new recruits ..............................................................................0
9. Conceptual models and cause-effect pathways..............................................................................................0
10. Discussion and conclusions ..............................................................................................................0
Funding sources ..............................................................................................................................0
Author contributions..........................................................................................................................0
Competing interests ..........................................................................................................................0
References....................................................................................................................................0
* Corresponding author.
E-mail addresses: r.jones@aims.gov.au (R. Jones), g.ricardo@aims.gov.au (G.F. Ricardo), a.negri@aims.gov.au (A.P. Negri).
http://dx.doi.org/mi 016/j.marpolbul.2015.08.021
0025-326X/© 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
ARTICLE INFO
Article history:
Received 29 May 2015
Received in revised form 29 July 2015
Accepted 2 August 2015
Available online xxxx
Keywords:
Sediment
Dredging
Coral spawning
Reproduction
Fertilization
Settlement
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1. Introduction
Natural resuspension events, terrestrial run-off and dredging-related activities can temporarily increase suspended sediment concentrations (SSCs) in the water column. The effects of suspended sediments on adult corals are well known (Erftemeijer et al., 2012a; Rogers, 1990) but nevertheless constitute only part of the demographic equation (Hughes et al., 2000, 2011). The sensitivity of the early life-history stages of corals has also been recognized for over a century (Stephenson, 1931; Wood-Jones, 1910), but even before fertilization, embryogenesis and the establishment of the sessile, and benthic juvenile form, sediments could exert a range of effects on the reproductive cycle including gametogenesis, spawning synchrony and on gametes in the water column.
This review examines the effects of turbidity on all aspects of the coral life cycle of corals from gamete development to the early post-settlement stage. The focus is on the effects of sediments on broadcast spawning species which usually dominate the tropical coral reef environment. Their life cycle is complex involving gametogenesis, reproductive synchronization, fertilization at the surface and larval development in the water column, leading finally to settlement and metamorphosis into a sessile polyp. Their life-cycle is stylized in Fig. 1 and based on Acropora spp.
Natural resuspension events regularly occur in the shallow, tropical marine environment (Anthony et al., 2004) and although resuspension and transport of suspended material may be strongly influenced by unidirectional currents, wind-driven waves are the primary mechanism of turbidity generation in the shallow reef environment (Jing and Ridd, 1996; Larcombe et al., 1995, 2001; Lawrence et al., 2004; Ogston et al.,
2004; Verspecht and Pattiaratchi, 2010). In the shallow inshore turbid zone of the Great Barrier Reef, resuspension of bottom sediment by waves affects coral communities on an estimated 110 days year-1 (Orpin et al., 1999). During predicted coral spawning periods wind speeds have averaged 8-10 m s-1 (or 15-20 knots) on six out of eleven years from 2000-2010 (AIMS, 2011). At these wind speeds natural resuspension and wind-wave induced turbidity would occur in the inshore turbid zones (Larcombe et al., 1995; Orpin et al., 2004; Orpin and Ridd, 2012) with possible implications for spawning and recruitment success of local corals.
In addition to natural events, anthropogenic activities can also release sediment into the water column, and dredging and disposal of dredged material (spoil) are the most well-known sources and are also the most amenable to management. In recognition of the sensitivity of the early life-cycle stages of corals, and since reproduction and recruitment processes underpin the maintenance and resilience of communities to disturbance, policy makers have attempted to protect coral spawning periods from sediments generated by dredging-related activities. Since 1993 dredging projects in Western Australia that are close to reefs are required to temporarily stop when corals are spawning (Baird et al., 2011; EPA, 2011). This regulatory condition is currently set as 5 days before spawning to 7 days afterwards. This is referred to as the coral spawning environmental window (EW) and is associated with the well-known synchronous, multi-specific release of gametes by broadcasting spawning coral species that can occur in WA in single epidemic events of relatively short duration (EPA, 2011; Simpson, 1985; Styan and Rosser, 2012). Unfavorable conditions during a spawning period could result in loss of the entire reproductive output for the year (Harrison et al., 1984). This management approach has also been adopted
Fig. 1. A stylized depiction of the reproductive cycle of the broadcast spawning Acropora species with indicative timings based on the studies of Hayashibara et al. (1997), Okubo and Motokawa (2007), Okubo et al. (2008) and Ball et al. (2002). The cycle begins and ends with gametogenesis in the adult colonies on the reef, but in between there are a complex sequence of phases which are spatially and temporally separated. Spawning occurs through the release of positively buoyant membrane-less, mucous bound egg and sperm bundles which dissociate at the surface and upper water column releasing the eggs and sperm. Fertilization occurs at the surface and upper water column where the initial stages of embryogenesis occur. Cleavage takes place by progressive furrow formation and the embryos of most Acropora species undergo an relatively unordered, irregular division cycle after the 8-cell stage eventually and after the morula stage becomes a convex-concave cellular bi-layer stage (the prawn-chip stage sensu Hayashibara et al., 1997) then bowl stage. The embryos then fatten to become a roughly spherical shape and by 36 h develop cilia over the epidermis, which beat synchronously imparting mobility to the planulae larvae. The larvae then become progressively elongated and begin searching substrata and eventually settle and undergo metamorphosis into juvenile polyps.
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in some dredging projects on the Great Barrier Reef (Koskela et al., 2002) and the possibility of introducing this practice to other locations such as Singapore has been suggested (Erftemeijer et al., 2012b).
This management approach is highly contentious internationally as it can significantly inflate costs for project sponsors (Suedel et al., 2008). One of the most contested issues is the length of the window and also whether dredging-related turbidity-generating activities need to cease entirely or whether dredging can continue but must adhere to more conservative water quality guidelines. Addressing these issues associated with a coral spawning environmental window is technically challenging as it requires an understanding of how all possible proximate stressors (causal agents) associated with turbidity generation can directly or indirectly influence all stages in the coral reproductive cycle. Over the last 20 years there have been several studies examining the effects of sediments on the early life-cycle stages, but perhaps more importantly there is now a much greater understanding of the reproductive biology of corals. It is now possible to more fully examine the mechanisms where sediments could affect the reproductive cycle (i.e. cause-effect pathways) and also to identify biologically plausible mechanisms. In epidemiology, biologically plausible mechanisms are those where there is a credible or reasonable biological and/or toxicological basis linking the proposed cause and effect (Adams, 2005; Hill, 1965; Suter, 2006).
This review focuses on the biology of the reproductive cycle that could be susceptible to effects of sediments (including high SSCs, sediment deposition, and changes in light quality and quantity) and other dredging-associated pressures (including sound and sediment contamination). For orientation purposes within this review, we first describe each stage of the life-cycle from gametogenesis to post-settlement survival, describe past studies, and then use this information to generate the conceptual model of known and plausible cause-effect pathways. Testing the cause-effect pathways requires a knowledge of where the processes occur (benthos, water surface, water column), and the length of each of the stages, so information is included on the duration of these phases where available. For experimental testing of each of the stages it is also necessary to know what the environmentally realistic or relevant exposure conditions (SSCs, light reduction, etc.) are over the relevant time frames for each stage. There is surprisingly little published information on water quality conditions that can occur during dredging programs on a coral reef to frame such an analysis. For contextual purposes, the review therefore starts with a brief description of water quality conditions from a recent large scale dredging project in the Pilbara region of Western Australia.
2. Example of water quality conditions during a large dredging program
The Barrow Island dredging project in NW Australia is one of the largest and well-studied dredging projects undertaken in a clear-water, coral reef environment, and involved the removal of ~8 Mm3 of sediment to create an access channel for a liquefied natural gas (LNG) gas plant (Evans et al., 2012; Hanley, 2011). Spatial and temporal scales of SSC dynamics in dredging programs are highly dependent on distance from the dredge, the dredging method, mode of operation(s), type of sediment dredged and the local hydro-meteorological (metocean) conditions (Black and Parry, 1999; Collins, 1995; Havis, 1988; Herbich and Brahme, 1991; Spearman et al., 2007). Data from the Barrow Island project (Fig. 2) show that natural background SSC levels are typically low < 5 mg L-1, with episodic increase associated with storms and wind-wave re-suspension events (Fig. 2A). During dredging, and a few hundred meters away from a working trailing suction hopper dredge (TSHD), SSC levels can increase by 1 -2 orders of magnitude with instantaneous values regularly exceeding 100 mg L-1 and maximum instantaneous readings exceeding 200 mg L-1. As the time averaging period increases to 30 d, the maximum average SSCs decrease to <20 mg L-1 (Fig. 2A).
Daily Light Integrals (DLIs) during the baseline period ranged seasonally from typically 1-10 mol m-2 with occasional very low light periods occurring during the austral winter time (Fig. 2B). During the dredging period DLIs regularly fell below 1 mol quanta m-2 and corals were occasionally exposed to extended periods of semi-dark, caliginous, twilight periods. In one of the worst periods the irradiance levels did not exceed 0.3 mol m-2 over a 21 day period which is equivalent to an average daytime instantaneous flux of < 10 |amol quanta m-2 s-1 (Fig. 2B).
3. Gametogenesis and reproductive synchrony
Scleractinian corals vary in their breeding systems, having either separate sexes (gonochorism) or combined sexes i.e. simultaneous hermaphroditism. Corals also vary in their mode of development and are either broadcast spawning species (spawners) which release gametes for external fertilization and with subsequent embryo and larval development in the planktonic phase, or breeding/brooding species, which have internal fertilization, brood embryos and develop planula larvae within their polyps (Fadlallah, 1983; Harrison and Wallace, 1990; Richmond and Hunter, 1990). These combinations (gonochorism versus hermaphroditism and spawners versus brooders) result in four basic patterns of sexual reproduction, and of the nearly four hundred species of corals examined to date approximately ~ 63% are hermaphroditic spawners (Baird et al., 2009; Harrison, 2011; Harrison and Wallace, 1990; Richmond and Hunter, 1990).
The timing of gametogenesis leading up to reproductive synchrony is depicted on the left of Fig. 3 with gonad production in the benthic, polyp phase typically occurring over a period of < 12 months culminating in the annual coral spawning event. In most hermaphroditic species, oogenesis occurs over a period of months while spermatogenesis occurs more rapidly just prior to spawning and can be completed in a few weeks (Harriott, 1983; Harrison et al., 1984; Harrison and Wallace, 1990; Kojis and Quinn, 1982; Richmond and Hunter, 1990; Wallace, 1985b). Many broadcast spawning species synchronize their gameto-genic cycles to potentially reduce predation (predator satiation) by planktivorous fish or filter feeders including other corals (Babcock et al., 1986; Baird et al., 2009; Harrison, 2011; Harrison et al., 1984; Harrison and Wallace, 1990; Hughes et al., 2000; Oliver et al., 1988; Pratchett et al., 2001). Spawning can also be synchronous between many different species and families of corals. This is the basis of the well-known multispecific, synchronous, coral spawning events, first identified in the early 1980s on the Great Barrier Reef (GBR) and involving at least 133 species of coral from ten scleractinian families (Harrison et al., 1984; Babcock et al., 1986; Willis et al., 1985; Harrison and Wallace, 1990). Change in sea surface temperature (Hayashibara et al., 1993), and solar insolation (Penland et al., 2004; Van Woesik et al., 2006), may constitute the proximate environmental cue(s) that instigates oogenesis, and temperatures over subsequent months may also affect the duration of oocyte development (Nozawa, 2012). Since its discovery, multispecific spawning events have increasingly been recorded in the Indo-Pacific and many other regions i.e. Caribbean, Japan, Gulf of Mexico (Baird and Guest, 2009; Baird et al., 2009; Harrison, 2011; Hayashibara et al., 1993).
3.1. Effects of sediment on gametogenesis and reproductive synchrony
No studies have directly manipulated SSC and sedimentation levels to examine the effects on gametogenesis, however several studies have correlated reproductive output with turbidity or sedimentation (Kojis and Quinn, 1984; Tomascik and Sander, 1987). Inferences were based on correlation (which does not prove causality) and using a similar approach Padilla-Gamino et al. (2014) did not find any differences in gamete production in Montipora capitata in Hawaii in areas with different sediment trap accumulation rates.
The proposed mechanisms for decreased reproductive output were: (i) increased energy expenditure for self-cleaning, and (ii) that a
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Month Time interval (days)
Fig. 2. (A) Nephelometric turbidity units (NTUs) collected every 10 min and (B) Daily Light Integral (DLI, mol m2) calculated from instantaneous fluxes collected from sensor platforms mounted 0.4 m above the seabed at 6-9 m depth at 3 locations <500 m away for a dredge during the Barrow Island (Pilbara, Western Australia) dredging project in the baseline (pre-dredging period) period or during the 1.5 year dredging program. Figures on the right hand side show the 95th and 100th (maximum) percentiles of the NTUs for different running mean periods (from 1 h-30 days) before (dashed lines) and during (solid lines) the dredging program or the 5th and 1st percentiles of DLI (mol photon m-2). Nephelometer turbidity units (NTUs) can be converted to SSCs using a conversion factor of 1.3 to 1.6 determined from regressions of SSC (assessed gravimetrically) versus NTU (nephelometer) readings. The Barrow Island project involved the excavation of-7.6 Mm3 of sediment dredged over 530 days from 19 May 2010 to 31 October 2011. The dredging occurred on a 7 days x 24 h basis, using a combination of trailer suction and cutter suction dredges and back hoes. Dredging stopped only for maintenance and bunkering requirements, the passage of cyclones and storms and over the coral spawning window (CSW) which was from 20-31 March 2011 (see arrows in Fig. 2A). The Ministerial approval statement for this dredging project (MS800) is searchable on the WA EPA website (http://www.epa.wa.gov.au).
reduction in light reduced translocation of photosynthate from the algal symbionts to the host (Kojis and Quinn, 1984; Rinkevich, 1989; Tomascik and Sander, 1987). Since many corals species rely on their algal symbionts for a large proportion of energy required for growth and reproduction (Muscatine, 1990; Rinkevich, 1989), it is plausible that long-term shading by increased SSDs may impact upon gametogenesis. While no direct experiment have tested this directly, Shimoike et al. (1992) suggested reduced light and hence energy translocation could have accounted for the observed differences in spawning times of Acropora spp. in Okinawa which varied depending on whether parts of colonies were shaded by other acroporids. Similarly, Cantin et al. (2007) showed that chronic exposure of two broadcast spawning species (Acropora tenuis and Acropora valida) and a brooding species Pocillopora damicornis to photosystem II herbicide (diuron) that blocks photosynthesis caused reduced lipid levels (indicating less energy production). Polyp fecundity was subsequently reduced by 6-fold in A. valida, and both A. valida and P. damicornis were unable to spawn or planulate following long-term exposures.
These studies provide experimental evidence of links between reduced energy acquisition due to shading, inhibition of algal symbiont photosynthesis or by bleaching. Cause-effect pathways and modes of action could therefore include interference with algal photosynthesis in adults, larvae with symbionts and recruits (autotrophy reduction) and heterotrophic suspension feeding (heterotrophy reduction, see Houlbreque and Ferrier-Pages, 2009) which would reduce energy for gametogenesis (Fig. 4). Other effects of high sediment deposition rates
include reduced energy from increased self-cleaning. A reduction in light and changes in light cues associated with elevated turbidity could disrupt synchronization of oogenesis or spermatogenesis (game-togenic asynchrony, Fig. 4).
4. Spawning synchrony and egg-sperm bundle release
Synchronization of gametogenesis occurs progressively in a population as development proceeds, culminating in the co-ordinated spawning of mature gametes. Overall spawning synchrony and gamete release is likely to be co-ordinated by a cascade of environmental variables such as temperature, seasonal solar insolation, wind speeds, monthly lunar or tidal cycles, and diel light cycles which are operating on increasingly finer time scales and acting alone or in combination to harmonize reproduction (Babcock et al., 1986; Harrison and Wallace, 1990; Oliver et al., 1988; Rosser, 2013; Van Woesik, 2010; Van Woesik et al., 2006). The final sequence of events are complex, starting with the egg and sperm being packaged together in a mucous-layer to form an egg-sperm bundle (Okubo and Motokawa, 2007; Padilla-Gamino etal., 2011). Just prior to spawning the bundles are moved into the oral disc area where they become visible in the pharynx, this is referred to as 'setting' (Babcock et al., 1986; Wallace, 1985b). The release of bundles varies between species, but typically occurs within minutes to hours of setting (Babcock et al., 1986; Fukami et al., 2003; Levitan et al., 2004; Toh et al., 2012; Van Veghel, 1994). Spawning usually occurs through the extrusion or forcible ejection of the bundles from the mouth (Babcock et al., 1986) although
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Fig. 3. Durations of each of the life-cycle phases depicted in Fig. 1, from broadcast spawning species listed in Table 1. Maturity, oogenesis and spermatogenesis estimates are from (Harrison and Wallace, 1990) and (Wallace, 1985b) and bundle rise rates are estimated from 1-15 m depth based on a vertical rise rates of 8.3 mms-1 (Levitan etal., 2004). Most studies describing cleavage were conducted ex-situ and insemination was controlled and therefore cleavage is given as the time from insemination, not spawning. Movement is defined as any observable motion of the larvae associated with ciliation, and swimming is active movement in a given direction although detailed time-courses have not always been well-defined. Settlement is estimated from those studies where appropriate settlement cues have been used and associated with binding of the larvae to a substrate and not necessarily metamorphosis. Studies where references to timing were too vague, or studies where settlement cues were either not provided or not specified, were not included in the analyses. Extended larval durations are based on (Figueiredo et al., 2013; Harii et al., 2007; Harrison, 2006; Miller and Mundy, 2003; Nishikawa et al., 2003; Nozawa and Harrison, 2002; Nozawa and Harrison, 2005, 2008; Suzuki et al., 2011; Toh et al., 2012). The present coral spawning environmental window in Western Australia is from 5 days before to 7 days after the predicted start of coral spawning (i.e. for 12 days).
extrusion through temporary openings in the tentacles has been seen with some brooding (Duerden, 1902), and broadcast spawning species (Vermeij et al., 2010b).
Babcock et al. (1986) described the spawning of 17 species of corals within an hour of each other on the same day. Although the release of the egg-sperm bundles can be highly synchronous, different species can spawn between one and eight days after the full moon with peak spawning on the third to sixth night. Similarly, mass spawning in Acropora in Okinawa, Japan occurs from three days before up to seven days after the full moon (Hayashibara et al., 1993) and some species can spawn on multiple nights. Importantly, different species also have different release times from 10 min after sunset (i.e. A. tenuis) to -3.5 h after sunset (i.e. Platygyra sinensis). The release times for these species may be within 15 min of each other between years (Babcock et al., 1986). Subtle differences in the timing of the arrival of eggsperm bundles at the surface could be a mechanism for reproductive isolation i.e. a prezygotic isolating barrier to prevent or reduce hybridization between closely-related species (Fukami et al., 2003; Knowlton et al., 1997; Levitan et al., 2004; van Oppen et al., 2002; Willis et al., 2006).
Jokiel et al. (1985) showed lunar periodicity in the brooding species P. damicornis is entrained by cyclic variation in night-time irradiance, while Gorbunov and Falkowski (2002) demonstrated expansion and contraction behavior of polyps from several coral species in response to moonlight and that the response was not related to photosynthetic activity of the algal symbionts. Subsequently, Levy et al. (2007) reported the presence of cryptochromes (CRYs), blue-light sensing photoreceptors in the ectoderm of both larval and adult Acropora millepora and coral rhodopsin-like genes have been described from A. millepora larvae (Anctil et al., 2007). Entrainment of corals by the lunar cycle results in the synchronisation of spawning to within a few nights for most coral species, but the ultimate trigger for gamete release seems to be related to light (period after sunset) (Babcock et al., 1986; Harrison et al., 1984).
In the natural environment, egg-sperm bundle release is relatively consistent for each species at a given location; however, spawning can be accelerated or delayed. Delays can be induced by keeping corals in extended light periods (Harrison et al., 1984; Hayashibara et al., 2004). Conversely, corals can be induced to spawn early by placing corals in darkness during the day or by shortening the photoperiod (Babcock, 1984; Hunter, 1988; Knowlton et al., 1997). Brady et al. (2009) suggested the early shift was directly controlled by the solar cycle and not an entrained clock as Montastraea ( = Orbicella) franl<si spawned early following a single photoperiod manipulation. While these studies clearly suggest light is one of the proximal factors controlling the timing of spawning, they cannot explain the very tightly coupled spawning behavior within a single day i.e. to very discrete, 20-30 min periods when spawning occurs for each species. Possible cues include falling light intensities and the length of a period of darkness (Babcock, 1984; Hunter, 1988; Knowlton et al., 1997), and detection of the blue region of moonlight (Gorbunov and Falkowski, 2002). Tying these observations together Boch et al. (2011) and Sweeney et al. (2011) suggest that the presence, phase and position of the moon modulates the intensity and color (i.e. a blue shift) of downwelling irradi-ance during twilight, and that this is the final discrete, proximate trigger for the synchronous spawning of corals.
Buoyancy of invertebrate eggs and larvae is determined by lipid (i.e. wax esters, triglycerides and phospholipid) content (Chia et al., 1984) and coral eggs are very lipid-rich (Arai et al., 1993; Figueiredo et al., 2012; Harii et al., 2007, 2010; Padilla-Gamino et al., 2013; Richmond, 1987; Wellington and Fitt, 2003). Consequently once released the egg-sperm bundles usually rise through the water column to the surface and form a slick (Fig. 1). Newly fertilized eggs of Montastraea ( = Orbicella) faveolata have a vertical rise rate of 1.8 mm s-1 (Szmant and Meadows, 2006) and Levitan et al. (2004) recorded an average ascent rate of 8.3 mm s-1 for Montastrea ( = Orbicella) fran<<si bundles. Although clearly dependent on depth, typically the time taken for the
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Fig. 4. Conceptual model of the effects of dredging activity on the early life-history stages of corals including sources of sediments, dredging and dredging-related turbidity-generating activities (see text), as well as proximal stressors, interacting stressors are depicted along with modes of action and likely physiological and ecological responses (see text for explanation). G = gametes, L = larvae, R = recruits and A = adults.
egg-sperm bundles to rise through the water column to form the coral-spawn surface slick would be typically less than an hour (Oliver and Babcock, 1992; Van Veghel, 1994).
4.1. Effects of sediment on spawning synchrony and egg-sperm bundle release
No studies have directly examined the effects of sediments on spawning but a range of plausible cause-effect pathways exist involving masking of synchronization cues by changes in light quantity and quality which could affect the timing of egg-sperm bundle setting and release processes (spawning asynchrony, Fig. 4). Such asynchronisation has been demonstrated by shading colonies, showing the mechanism is probable (Brady et al., 2009; Levitan et al., 2004). This asynchronization could result in the un-coordinated arrival of the egg-sperm bundles on the surface. Sediment deposition and temporary smothering of corals could also interfere with egg-sperm bundle release (bundle release blocking, Fig. 4). Kojis and Quinn (1981a) described the stickiness of egg-sperm bundles of Goniastrea australensis and recent studies
(Ricardo unpublished data) have shown that sediments can directly bind to egg-sperm bundles ofAcropora nasuta (Fig. 5A) and under conditions of high SSCs and could cause sinking of bundles or reduce the ascent rate following spawning (bundle ascent lag, Fig. 4). High rates of sedimentation could have a similar effect. As with asynchronous spawning, bundle ascent lag could also affect the co-ordinated arrival of egg-sperm bundles at the sea surface.
5. Fertilization
At the surface the bundle dissociates releasing the eggs and sperm (Fig. 1). Reported times taken for the bundles to dissociate ranges from less than 5 min to more than 4 h, but the process is typically complete within an hour (Heyward and Collins, 1985; Padilla-Gamino et al., 2011; Richmond, 1997; Wolstenholme, 2004) (Fig. 3, Table 2). Wolstenholme (2004) noted that in Acropora sp. the time for bundle dissociation is consistently different for each of species (and morphs) and this could also be part of a mechanism for reproductive isolation.
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Fig. 5. (A) Silt and clay sized sediment attached to the mucous-layer of an intact and a partially dissociated egg-sperm bundle of Acropora nasuta. Attachment of the negatively buoyant sediment to the bundles could reduce their buoyancy reducing ascent rate and at high concentrations even preventing them reaching the surface (Image: Gerard Ricardo). (B) Sperm from Acropora tenuis intertwined with silt and clay sized sediment particles. Sediments could act as a barrier and impediment to sperm movement and sediments with attached sperm could settle out of suspension potentially stripping them from the upper water column hence reducing egg-sperm contact time (Image: Gerard Ricardo). (C, D, E) Recently settled coral larvae (Pocillopora actua) 3 days h after exposure to single sediment deposition event of 1 mg cm2,10 mg cm2 and 100 mg cm2 of fine sediments (median grain size of ~50 |jm), showing the successful clearance of sediments from the polyp's surface under 1 mg cm2, but a progressive smothering of the polyps at higher concentrations (Image: Gerard Ricardo).
Since eggs are positively buoyant they remain on the surface, while the negatively buoyant sperm sink in the water column and became diluted at depth (Padilla-Gamino et al., 2011). Scleractinian eggs range in size from 400-800 |jm in Acroporidae and Mussidae, 300-500 |am in Faviidae and Pectiniidae and 100-250 |am in Agariciidae, Fungiidae and Pocilloporidae (Harrison and Wallace, 1990). Mature anthozoa sperm are typically ~50 |am long with a head diameter of 1-3 |am (Hagedorn et al., 2006; Harrison, 1985; Steiner, 1991; Steiner and Cortés, 1996) as compared with silt sized sediments which range from 4-62.5 |am based on the Udden-Wentworth (Wentworth, 1922) US standard classification scale of sediment (see Fig. 5B).
Fertilization in broadcast coral species occurs when the eggs and sperm dissociate from the bundle and become viable. This usually takes place at the surface or in the upper water column (Fig. 1). Heyward and Babcock (1986) noted for many corals (including several faviids) final maturation, division of the oocytes and the release of polar bodies occurred 15-30 min after spawning (see also Okubo and Motokawa (2007)). Consequently, it seems unlikely that the eggs are fertile until sometime after release from the bundles. For the sperm, Oliver and Babcock (1992) suggest they are also inactive when highly concentrated within the egg-sperm bundles at the time of spawning and become capable of full activity during the early stages of fragmentation of the bundles.
Morita et al. (2006) showed that sperm of Acropora digitifera, Acropora gemmifera and A. tenuis become activated when in close (<300 |jm) proximity to conspecific eggs but not eggs of different species. Coll et al. (1994) described substances extracted from eggs of Montipora digitata that activated and attracted sperm, while, Morita
et al. (2006) also described how sperm flagellar motility decreased when they came close to eggs where many sperm had already attached to the egg surface. These observations suggest the presence of sperm activation, attraction, chemotaxis (orientation with respect to a chemical concentration gradient) and suppressor(s), and a mechanism to prevent polyspermy given that eggs of corals do not have fertilization membranes (Babcock and Heyward, 1986; Oliver and Babcock, 1992).
First cleavage in laboratory studies generally occurs from < 1 h-6 h following fertilization (Fig. 3, Table 2) and the capacity for fertilization decreases with time, falling rapidly > 1.5 h after spawning in M. digitata (Oliver and Babcock, 1992), 2 h after spawning in Montastrea annularis species complex (Levitan et al., 2004), >3 h in Platygyra sinensis (Oliver and Babcock, 1992), >5-6 h after spawning in M. digitata, A. tenuis, Goniastrea aspera and Goniastrea favulus (Heyward and Babcock, 1986), and A. millepora (Wallace and Willis, 1994; Willis et al., 1997). However, the majority of these fertilization studies were conducted in the laboratory (in vitro) (Table 1), without the natural dilution factors such as diffusion, advection and sinking of the sperm. Dilution of sperm in the field is likely to significantly impact on the length of the fertilization window and Omori et al. (2001) suggests that the in situ fertilization is unlikely as little as 1 h after spawning.
5.1. Effects of sediment on fertilization
The earliest study of the effects of sediment on fertilization was conducted with A. digitifera exposed to high sediment concentrations (1280 mg L-1) at a low (28.5 ppt) salinity (Richmond, 1996; Richmond, 1993). Fertilization was much lower in the experimental
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Table 1
Studies of the effects of sediments on aspects of the reproductive life-cycle of corals.
Species
Particle size (Mm)
Contaminant screening
Dose-response relationship
Gametogenesis and reproductive synchrony Tomascik and Sander Porites porites (1987)
Kojis and Quinn (1984) Acropora palifera Montipora capitata
Not quantified Nutrients only
Padilla-Gamino et al. (2014)
Fertilization Gilmour (1999)
Not quantified Not quantified
Acropora digitifera 50-200 Mm Humphrey et al. (2008) Acropora millepora Pectinia lactuca
Erftemeijer et al. (2012b)
Embryogenesis and larval development Gilmour 1999 Acropora digitifera
Humphrey et al. (2008) Acropora millepora
Settlement and metamorphosis Hodgson (1990) Pocillopora
damicornis
Babcock and Davies Acropora millepora (1991)
50-200 |im <63 |im (Measured)
Sand 12% Silt 67% Clay 21% Fine sand and silt
Babcock and Smith (2002)
Te (1992)
Gilmour (1999) Perez et al. (2014)
New recruits Babcock and Smith (2002)
Pocillopora damicornis
Acropora digitifera
Pocillopora damicornis
50-200 Mm <63 m
None None
Metals
<63 Mm (Measured) Not quantified
Metals and nutrients Not quantified
Metals Metals and nutrients
Acropora millepora 90% <63 Mm None
Unspecified None
Metals None
Acropora millepora 90% <63 Mm None
Mean number of larvae per cm2 of coral planulating Acropora palifera in Papua New Guinea, in shallow, turbid water sites was consistently half the value than at the clear water sites
Reduction in reproductive activity in Porites porites in Barbados along an increasing eutrophication gradient
No differences in gamete production in Montipora capitata in Hawaii between areas with different sediment trap accumulation rates.
Effects of sediments collected from a terrestrial dredge spoil ground measured at 50 mg L-1 and 100 mg L-1 (measured concentrations)
Dose-response relationships established for % fertilization versus SSC over a range from 4-1024 mg L-1 and an LOEC established at 100 mg L-1 for a range of sediment types Reduction at 43 mgL-1 and but significant reduction at169mgL-1 (nominal concentrations) tested against a reference sample of 6 mg L-1
No effects at concentrations of 100-150 mg L-1 No effects at concentrations up to 200 mg L- 1
Planulae settlement was markedly reduced where there was a layer of sediment <1 mm thickness
Reduced settlement at sediment traps accumulation rates of-3 (LOEC), 6-7 and 110-325 mg cm-2 day-1 measured using sediment traps as compared with controls at 0.5 mg cm-2 day-1 (NOEC)
Settlement lower in sediment treated areas (1.9-11.7 mg cm-2 day-1) scrubber pad accumulation rates as opposed to control sites where sedimentation rates were 0.8-1.3
mg cm- 2 day- 1
0,10,100, and 1000 mg L-1 (NOEC) concentrations with no significant difference in settlement between control and highest concentrations tested but polyp bailout in 100 and 1000 mg L-1 concentrations
50 mg L-1 and 100 mg L-1 (measured concentrations) tested against a reference of >1 mgL-1
No settlement on surfaces >0.9 mg cm-2
Settlement lower in sediment treated areas (1.9-11.7 mg cm-2 day-1) scrubber pad accumulation rates as opposed to control sites where sedimentation rates were 0.8-1.3 mg cm-2 day-1
treatment than controls (0.45 im filtered seawater at 34 ppt and no sediment); however those results could be partially due to osmotic effects since later experiments showed similarly low fertilization rates at low salinity without sediments (see also Humphrey et al., 2008).
Several studies have examined the effects of suspended sediment on fertilization in A. digitifera (Gilmour, 1999), A. millepora (Humphrey et al., 2008), and Pectinia lactuca (Erftemeijer et al., 2012b), using sediments collected from terrestrial dredge spoil grounds and surficial sub-tidal sediments collected from a range of locations including pristine and contaminated sites (Table 1).
The effects of suspended sediments on coral fertilization varied considerably in these studies. Some of the differences may be due to uncertainty in the amount of sediments suspended over the duration of the exposures. In the most sensitive study, Gilmour (1999) placed hundreds of grams of sediment in a container and used aeration from aquarium pumps channeled through a pipette to re-suspend the fine-grained sediment from the container floor to the desired levels in the water column. Recent attempts to create uniform suspensions of sediments using the same techniques have not been successful and new techniques are currently being developed (Ricardo unpublished).
Fertilization is known to be one of the most vulnerable life-history stages to toxicants, and some of the variation between studies could be associated with contaminants and genotoxic effects. Other possible
cause-effect pathways lie with the binding of nutrients and microorganisms, potentially forming 'sticky' particles that may attract and capture coral sperm. It is notable that the clean aragonite sediments used by Humphrey et al. (2008) did not cause any measureable effect on fertilization at 1000 mg L-1 as compared to the potentially contaminated sediments collected from beside a nearshore, operational dock where affects were observed at 100 mg L-1. Similarly, sediments in the study of Erftemeijer et al. (2012b) were collected from Singapore waters which are likely to be contaminated by a range of pollutants, including potentially toxic persistent organic pollutants (Wurl and Obbard, 2005).
Another source of the variability between the studies could be methodological differences especially in sperm concentrations. So far studies have used only a single sperm concentration but if suspended sediments limit the available sperm for fertilization, then the fertilization rate can be highly dependent on the sperm concentration used, masking effects at very high in vivo sperm concentrations and exacerbating effects at low sperm concentrations (Marshall, 2006). The experiments so far have typically used a single sperm concentration and while the use of a single concentration is quick and convenient, future studies need to consider a range of sperm concentrations since fertilization success is proportional to sperm-egg contact and increases with increasing sperm concentration (Iguchi et al., 2009; Marshall, 2006; Oliver and
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Babcock, 1992). Different techniques and metrics have been proposed to address this and other issues, including use of a number of sperm concentrations, the use of a standard sperm-egg contact times, optimizing sperm and egg concentrations for each species to maximize the sensitivity of an assay (Oliver and Babcock, 1992; Omori et al., 2001), and using sperm of multiple corals (Marshall, 2006).
The mechanism whereby sediments effect fertilization is unknown and could include physical effects on egg/sperm interactions through affecting sperm activation, effects on motility, and entry and attraction. As with processes leading to asynchrony, these may serve to reduce eggsperm interactions and will ultimately affect recruitment. Humphrey et al. (2008) and Erftemeijer et al. (2012b) speculated that sediments may block sperm entry to the egg via the micropyle, and while these structures are found in fish, insects and cephalopods, they have not been described yet for coral eggs. Gilmour (1999) observed unusual clustering or aggregation of A. digitifera eggs on the water surface in sediment-treated samples. These observations are similar to those made with Pacific herring where sediments attach and aggregate eggs and embryos in the early post-fertilization period, remaining there for the duration of embryonic development (Griffin et al., 2009).
Other possible pathways include attachment of sediment to the mucus-layer of the egg-sperm bundles preventing or delaying break up (bundle cloaking in Fig. 4). Silt sized sediments (4-62 |am) could also interfere with sperm movement decreasing sperm-egg interactions (sperm motility in Fig. 4) and possibly by masking activation and attraction cues from the eggs (egg chemotaxis in Fig. 4). As with the effects on egg-sperm bundles, attachment of sediments to sperm could cause them to sink (sperm drop-out in Fig. 4, Fig. 5B, C) and high sedimentation rates could accelerate this process.
6. Embryogenesis and larval development
The term embryo is used here to describe the early development phase of fertilized eggs up until the stage where the epidermis begins to differentiate and cilia form, at which stage the developing propagule is termed as larvae (Ball et al., 2002; Harrison and Wallace, 1990). Babcock and Heyward (1986) described embryogenesis in 19 species of corals from initial cleavage to 10 days afterwards including settlement and metamorphosis. Detailed time-courses in embryogensis in gamete spawning Acropora, including the appearance of polar bodies, development of the zygote from cleavage, morular and blastula stage and gastrulation have been given in Hayashibara et al. (1997), Okubo and Motokawa (2007), Okubo et al. (2008, 2013) and Ball et al. (2002) and used to develop the stylized life-cycle in Fig. 1.
Fertilization and the initial stages of embryogenesis occur at the sea surface and upper water column (Fig. 1). The positive buoyancy in eggs and recently fertilized embryos during the first few days would enhance passive dispersal by currents, but an important feature of embryogenesis is a general decrease in buoyancy (Babcock, 1984; Figueiredo et al., 2012; Harrison et al., 1983; Wilson, 1888). Motility is typically first observed by 1-2 days after fertilization and active swimming after 23 days, although more rapid development have been recorded in some species such as P. lactuca (Fig. 3, Table 2). These observations on movement and swimming in the laboratory are supported by studies of coral slicks at sea (Babcock and Heyward, 1986) and the downward movement of larvae could be assisted by swimming (Harii et al., 2007; Tay et al., 2011). Willis and Oliver (1988) observed larval numbers increasing under the surface after 24 h and after five days the larvae were distributed evenly through the water column. The decrease in buoyancy and onset of motility results in a breakup of the coral surface spawn slicks, consistent with aerial observations that the slicks were visible for 1-2 days (Oliver and Willis, 1987).
Once motile, the planulae change from a barrel to a pear/elongate/ spindle/tear drop shape (Hayashibara et al. (1997)) and are active swimmers, spiraling along their principal axis exhibiting a range of geo-tactic and negative and positive phototactic responses which contribute
to their ultimate settlement and attachment location (Lewis, 1974). Hodgson (1985) suggested evidence of vertical migration, with coral larvae residing near the surface at night and moving to several meters depth during the day. When swimming in the water column the downward navigation of the planulae in two brooding coral species (Agaricia tenuifolia and Porites astreoides) can be cued by seawater collected from the reef i.e. involves water-borne signals (Gleason et al., 2009). Vermeij et al. (2010a) also showed that planktonic phase larvae of Montastraea faveolata respond to underwater reef sounds such as fish calls and grunts and the snapping of shrimps by swimming to the substratum.
Non-symbiotic coral larvae are lecitotrophic and acquire energy endogenously from the parent generation and the rich lipid content is a plausible, primary energy source (Arai et al., 1993; Harii et al., 2007; Richmond, 1987; Wellington and Fitt, 2003). This is consistent with the slow decrease in the lipid content in P. damicornis (Richmond, 1987,1997), A. tenuis (Harii et al., 2007), P. damicornis and M. digitata (Harii et al., 2010) during the planktonic phase, linked to loss of buoyancy. However also associated with the energy status of the larvae, and one of the most critically important events in the early life history stages, is the acquisition of photosynthetic, symbiotic dinoflagellate microalgal symbionts (Symbiodinium spp. = zooxanthellae) (discussed further below under metamorphosis). Species of the genus Acropora were believed to only uptake algae after metamorphosis (Babcock and Heyward, 1986; Babcock, 1988; Harrison and Wallace, 1990) but many recent studies have now shown that Acropora larvae can form symbioses at the larval stage (van Oppen, 2001; Baird et al., 2006; Adams et al., 2009; Harii et al., 2009; Baird et al., 2010; Cumbo et al., 2013). Richmond (1981) showed that between 13 and 27% of carbon fixed by Symbiodinium in P. damicornis larvae is translocated to the host, depending on light quality and temperature. This horizontal acquisition of symbiotic dinoflagellates at the larval stage or maternal inheritance in eggs has implications for the nutrition of the larvae, potentially increasing the length of the settlement-competency period and hence for dispersal.
6.1. Effects of sediment on embryogenesis and larval development
Gilmour (1999) and Humphrey et al. (2008) examined effects of sediments on early embryonic development in A. digitifera and A. millepora and showed no effect at the highest concentrations tested (100-150 and 200 mg L-1, respectively) (Table 1). Studies on the effects of sediments on the subsequent development in larvae is limited to the work of Gilmour (1999) where, in contrast to the lack of effects on embryogenesis, significant effects were noted from 1.5-6.5 days after spawning at concentrations as low as 50 mg L-1. To undertake this study, larvae were incubated in rearing jars containing several hundred grams of sediment and tethered in situ to mooring buoys. The ends of the jars were covered with a 60 |im plankton mesh to allow water exchange and retain the sediments which were kept in suspension by natural agitation of the buoy and containers by wave motion. These types of experiments are uncontrolled in that sediment particles less than the mesh size are likely to be lost and water flow inside the container was likely to be minimal because of clogging of the mesh by sediment. Gilmour (1999) described these limitations and how the containers were regularly squeezed to facilitate water exchange, but how this did not remove all solid materials caught inside the mesh which resulted in the build-up of tissue debris and organic material. Build-up of dead material could also have been exacerbated by the comparatively high larval densities of -15 mL-1 which may increase mortality within the meshed containers (Negri unpublished results). Despite these considerable methodological limitations, the impact on survival of 50 mg L-1 has been widely cited, including in several recent reviews (Erftemeijer et al., 2012a; Fabricius, 2005; Gleason and Hofmann, 2011) but should be validated under more reliable conditions.
There are a number of potential cause-effect pathways whereby dredging could negatively or positively affect the larvae while in the
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Timing information for egg-sperm bundle dissociation, first cleavage, movement, swimming and attachment/settlement, symbiosis formation and budding. Only studies that described the minimum time of a given developmental stage were included and only studies on broadcast spawners that meet the criteria discussed in the text.
Study Species Timing
Bundle break-up/dissociation
Kojis andQuinn (1982) Favites abdita, Leptoria phrygia A few minutes to 1 h after reaching the surface
Babcock (1984) Goniastrea aspera 30 min after reaching the surface
Hunter (1988) Montipora verrucosa, M. dilitata 45-90 min
Shlesinger and Loya (1991) Favia favus, Platygyra lamellina 10-20 min after spawning
Richmond (1997) Acropora digitifera 10-40min
Hayashibara et al. (1997) Acropora hyacinthus, A. nasuta, A. florida Immediately
Wolstenholme (2004) Acropora gemmifera, A. samoensis 5-30 min
Acropora humilis 1-4 h
Acropora monticulosa 30-60 min
Acropora digitifera 5-15 min
Szmant and Miller (2006) Montastraea faveolata, Acropora palmata 40 min, >60 min
Toh et al. (2012) Acropora hyacinthus, Pectinia lactuca 20-30 min
First cleavage
Babcock and Heyward (1986) Goniastrea favulus, G. aspera, Montipora digitata, Platygyra sinensis 2 h and ~100% fertilization at 5-7 h
Shlesinger and Loya (1991) Favia favus, Platygyra lamellina ~3 h after spawning
Hayashibara et al. (1997) Acropora hyacinthus, A. nasuta, A. florida 2-6 h after fertilization
Okubo and Motokawa (2007) Acropora digitifera, A. intermedia, A. hyacinthus, A. solitaryensis, A. tenuis Within 2 h after fertilization
Okubo et al. (2008)
Gilmour (1999) Acropora digitifera 1.5-3 h after fertilization
Hirose et al. (2008) Acropora microphthalma, A. nobilis 2 h after spawning more than 90% began cleavage
Okubo et al. (2008) Acropora intermedia 2 h after spawning
Erftemeijer et al. (2012a,b) Pectinia lactuca ~1 h after fertilization
Movement
Kojis andQuinn (1981a) Goniastrea australensis Ciliated in <2 days
Babcock (1984) Goniastrea aspera Some movement 24-36 h after spawning
Harrison et al. (1984) Acropora hyacinthus, A. muricata, A. tenuis, A. millepora, A. tenuis, Goniastrea aspera, 1.5 day
G. favulus
Babcock and Heyward (1986) Favia pallida, Goniastrea aspera, G. favulus, Montipora digitata, Platygyra sinensis 24 h
Acropora muricata, A. millepora, Galaxea fascicularis, Goniopora lobata, Lobophyllia Mobile when first observed at 36 h
corymbosa, Montipora tuberculosa, Mycedium elephantotus, Paraclavarina triangularis,
Pectinia alcicornis, P. paeonia
Favites complanata Mobile when first observed at 48 h
Hayashibara et al. (1997) Acropora hyacinthus 36 h
Schwarz et al. (1999) Lobactis scutaria 12 h after fertilization
Gilmour (1999) Acropora digitifera Most by 36 h
Hayashibara et al. (2000) Acropora nasuta Second day after fertilization
Miller and Mundy (2003) Platygyra daedalea 42 h
Goniastrea favulus 48 h
Nozawa and Harrison (2005) Favites chinensis, Goniastrea aspera Mobile <24 h after spawning
Nozawa and Harrison (2006) Acropora muricata, A. valida Mobile when first observed at 3 days
Harrison (2006) Acropora longicyathus, A. hyacinthus 2 days after spawning
Nozawa et al. (2006) Acropora solitaryensis, Cyphastrea serailia, Favia favus 48-72 h after spawning
Okubo and Motokawa (2007) Acropora digitifera, A. hyacinthus, A. intermedia, A. solitaryensis, A. tenuis 36 h
Okubo et al. (2008)
Toh et al. (2012) Acropora hyacinthus Within 48 h
Pectinia lactuca 18 h
Erftemeijer et al. (2012b) Pectinia lactuca 12-18 h after fertilization
Figueiredo et al. (2013) Palauastrea ramosa 8 h
Danafungia horrida, Leptastrea purpurea 12 h
Goniastrea aspera 16 h
Goniastrea retiformis, Pachyseris speciosa, Platygyra daedalea, Porites australiensis 18 h
Echinopora lamellosa, Merulina ampliata, Montipora digitata 24 h
Anacropora puertogalerae 26 h
Physogyra lichtensteini, Plerogyra sinuosa 30 h
Acropora gemmifera 32 h
Acropora humilis, A. millepora, A. pulchra, A. valida 36 h
Okubo etal. (2013) Pavona decussata 12 h after spawning
Oulastrea crispata 13 h after spawning
Favites pentagona, Echinophyllia aspera 15 h after first cleavage
Galaxea fascicularis, Goniastrea favulus 18 h after spawning
Platygyra contorta, Phymastrea valenciennesi 19 h after spawning
Favites abdita 22 h after first cleavage
Dipsastraea speciosa 24 h
Montipora digitata, M. hispida 33 h after spawning
Swimming
Babcock (1984) Goniastrea aspera 48 h
Babcock and Heyward (1986) Acropora millepora, Favia pallida, Goniastrea aspera, G. favulus, Montipora digitata, 48 h
Platygyra sinensis
Echinopora gemmacea 36 h
Galaxea fascicularis, Goniopora lobata, Goniastrea retiformis, Lobophyllia hemprichii 72 h
Hayashibara et al. (1997) Acropora florida, A. hyacinthus, A. nasuta, A. secale 72 h
Schwarz et al. (1999) Lobactis scutaria Within 24 h of fertilization
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Table 2 (continued)
Species
Timing
Swimming Harii et al. (2007) Hirose et al. (2008) Erftemeijer et al. (2012b)
Settlement
Babcock (1985)
Babcock and Heyward (1986)
Harrison (1997)
Hayashibara et al. (1997) Heyward and Negri (1999) Schwarzet al. (1999)
Hayashibara et al. (2000) Nozawa and Harrison (2002)
Fabricius et al. (2003)
Miller and Mundy (2003) Nishikawa et al. (2003)
Nozawa and Harrison (2005)
Harrison (2006) Harii et al. (2007) Hirose et al. (2008) Nozawa and Harrison (2008) Okubo et al. (2008) Heyward and Negri (2010)
Suzuki etal. (2011)
Tayet al. (2011)
Tohet al (2012)
Figueiredo et al. (2013) Graham et al. (2013) Okubo et al. (2013)
Dixson et al. (2014)
Symbiosis Babcock (1985) Babcock and Heyward (1986) Hayashibara et al. (1997) Hayashibara et al. (1997) Schwarzet al. (1999)
Harii et al (2009) Graham et al. (2013)
Budding
Shlesinger and Loya (1991) Hayashibara et al. (1997) Graham et al. (2013)
Acropora tenuis
Acropora microphthalma, A. nobilis Pectinia lactuca
Goniastrea aspera, A. millepora, Platygyra sinensis Favia pallida, Platygyra sinensis, Goniastrea aspera, Galaxea fascicularis Goniastrea aspera, G. favulus, G. retiformis, Montipora digitata Acropora longicyathus
Acropora secale Acropora millepora Lobactis scutaria
Acropora nasuta Platygyra daedalea
Acropora willisae
Goniastrea favulus, Platygyra daedalea Acropora tenuis
Favites chinensis Goniastrea aspera
Acropora longicyathus, A. hyacinthus Acropora tenuis
Acropora microphthalma, A. nobilis Acropora muricata, A. valida Acropora intermedia
Acropora millepora, Fungia repanda, Symphyllia recta A. spathulata Acropora spp.
Pectinia lactuca, Platygyra sinensis
Acropora hyacinthus Pectinia lactuca
Acropora gemmifera, A. humilis, A. millepora, A. valida, Goniastrea retiformis, Platygyra daedalea Acropora tenuis
Favites pentagona
Favites abdita
Pseudosiderastrea tayamai
Acropora millepora, A. nasuta, and A. tenuis
Acropora millepora, Goniastrea aspera, Platygyra sinensis Acropora millepora, Goniastrea favulus, Platygyra sinensis Acropora microphthalma, A. nobilis Acropora florida, A. hyacinthus, A. nasuta Lobactis scutaria
Acropora digitifera, A. tenuis Acropora tenuis
Favia favus Acropora secale
2 days after fertilization
By 18 h most larvae were rapidly motile
After 4.5 days and the majority after 8-10 days 4.5 days 5 days
Settlement 2-4 days and metamorphosis 3-4 days after spawning 17-24 days 5 days
Larvae began to settle and metamorphose 5-14 days after fertilization
3-4 days after fertilization peaking after 7 days Settlement 3-4 days and metamorphosis 4-6 days after spawning
Settled and metamorphosized 3-5 days after spawning
Settlement started at between 2.5 and 2.75 days 4 days after spawning peaking 7 days after spawning
1 -2 days after spawning 3-4 days after spawning 2-3 days after spawning
3 days
2-16 days after fertilization
First observed at 5-6, peaked at 7-8 days 7 days after spawning
4 days after spawning
3-4 days after spawning
Commencing 2-5 days after spawning but 80% settled by 5-8 days
Peak settlement 3 and 6 days day after spawning respectively
>50% settled by 1.7 days after fertilization Starting at 3 days and > 50% by 4 days after fertilization
-Metamorphosis 3-6 days from spawning
A few were competent to settle as early as 4 days after spawning
Started swimming at about 15 h Started swimming at about 15 h 3 days after spawning
6-7 days after spawning
Between 5 and 10 days after settlement Sometime within 13 days after settlement 16 and 30 days after settlement Established symbiosis after 30 days Symbionts phagocytosed as early as 3 days after fertilization
5-6 days after fertilization 15 days after settlement
7-9 months after spawning
2 months after fertilization -22 days after settlement
planktonic phase. Sound from dredging operations, high SSCs or reduced light levels associated with the high turbidity, could affect the macro-scale habitat selection, the orientation of the larvae in the water column and the downward movement towards the reef (i.e. sound masking, reef chemotaxis, phototaxis, in Fig. 4). High SSCs could also interfere with the algal acquisition process which is mediated by a feeding. The energetics of larvae may also be taxed by excessive particle removal (self-cleaning; Fig. 4) or avoidance and reductions in light quantity and quality would most likely negatively affect
photosynthesis in larvae that have acquired symbionts (autotrophy reduction in Fig. 4).
There are, however, a number of possible benefits of turbidity generating activities while embryos and larvae are in the water column. Resuspended sediments may include free-living algal symbionts increasing the chances of forming a stable symbiosis (see below). Light reduction could also reduce UV damage in embryos and oxidative stress in larvae that recently acquired symbionts in the planktonic phase and reduce losses to visual predators.
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7. Settlement and metamorphosis
The pelagic larval phase ends with a gradual descent of the planulae from the surface and water column (i.e. planktonic stage) to a temporary demersal stage (Fig. 1). Subsequently there is a final, benthic stage, involving settlement and eventually permanent attachment (Fig. 1). Gleason and Hofmann (2011) have recently reviewed the '... dizzying array of abiotic and biotic factors, both positive and negative, that can determine whether a coral larva ultimately ends up on the reef as anew recruit.'.
Once near the seabed planulae exhibit thigmotaxic 'searching' behavior, touching the substrate, temporarily 'resting', 'creeping' and 'crawling' over the surface before eventually attaching and settling (Fig. 1). Many studies have described similar processes with larvae of several brooding species and introduced the colloquial terms for the stages (Atoda, 1947a,b,1951a,b; Duerden, 1902; Krupp, 1983; Wilson, 1888). Coral larvae lack the apical tufts found in some cnidarians but appear to have sensory cells in their aboral epidermis for substratum detection i.e. tasting surfaces for suitable cues. Vandermeulen (1974) described these sensory cells for larvae of P. damicornis as bearing a single flagellum and surrounded by a collar of microvilli. The nature of these cells and the location of chemoreception has recently been examined byTran and Hadfield (2013) who showed that larvae M. capitata would not undergo metamorphosis if the first quarter of the aboral pole was removed. While suggesting sensory cells used in detecting cues are likely to be located there, much larger larvae of P. damicornis lacking the aboral pole were also able to settle and metamorphose. This indicated the cue-detecting cells could also be located along the sides of the body and there are differences between species in cue-detection.
Planulae of A. nasuta have 2 types of cnidae, a microbasic b-mastigophore nematocyst and a spirocyst (Hayashibara et al., 2000) that may aid attachment to surfaces. Spirocysts are known to be adhesive organelles in cnidaria and the discharged threads can link together in a fine web or meshwork (Mariscal et al., 1977). In A. nasuta the appearance of cnidae 3-4 days after fertilization coincides with the swimming phase and first attachment (Fig. 3), and a continued increase in numbers until 8 days after fertilization coincides with maximum settlement (Hayashibara et al., 2000). Okubo and Motokawa (2007) also observed an increase in numbers of spirocysts in a concave structure of the aboral region of developing A. millepora larvae. Hayashibara et al. (2000) suggested that the spirocysts were associated with attachment and Okubo and Motokawa (2007) proposed that the brim of the concave structure may sense the environmental signals for metamorphosis.
The settlement of mature planulae requires the presence of an appropriate substratum as well as chemical and/or biological cues and in some instances the presence of compatriots i.e. gregarious settling behavior (Birkeland et al., 1981; Duerden, 1902; Edmondson, 1929; Kojis and Quinn, 1981a; Puill-Stephan et al., 2012; Tran and Hadfield, 2011; Wilson, 1888). Baird etal. (2003) showed that settlement of larvae is much higher on artificial surfaces which had been conditioned (left in situ for 8 weeks) in the parental habitat suggesting species-and habitat-specific substratum cues (see also Suzuki and Hayashibara (2011)). Marine bacteria and biofilms are a potential source of the cues on some conditioned surfaces (Negri et al., 2001; Webster et al., 2004), however the settlement of some coral larvae is most powerfully initiated by the presence of various species of crustose coralline algae (CCA) (Golbuu and Richmond, 2007; Harrington et al., 2004; Morse et al., 1988). While chemical inducers from CCA are far more potent than all other factors affecting the settlement of Acropora spp. (Tebben et al., 2015), larvae often prefer to attach immediately adjacent to the CCA (Heyward and Negri, 1999; Szmant and Miller, 2006) which has an array of defenses including sloughing of surface cells and natural an-tifouling compounds protecting it from colonization (Harrington et al., 2004).
Following the searching/exploring stage the larvae settle, undergoing attachment by the aboral end, followed by contraction at the oral-aboral axis forming a flattened disc that eventually becomes subdivided radially by mesenteries (Ball et al., 2002) (Figs. 1, 5C). Metamorphosis involves a dramatic reorganisation and tissue remodeling creating the sessile primary polyp (Grasso et al., 2011; Hirose et al., 2008; Vandermeulen, 1974,1975; Vandermeulen and Watabe, 1973). In particular the aboral ectoderm is transformed into the calicoblastic ectoderm, which is responsible for secretion of the coral skeleton, and the oral ectoderm is stabilized (Grasso et al., 2011). While metamorphosis in most invertebrate larvae is usually an irreversible process, at least one species, P. damicornis, can undergo reversible metamorphosis back into the planktonic form under conditions of environmental stress or energy constraint (Miller and Mundy, 2003; Richmond, 1985).
Many studies of recruitment patterns suggest that larvae can exhibit adaptive behavior and actively settle at sites where the light quality and quantity regime is optimum (Duerden, 1902; Edmondson, 1929; Lewis, 1974; Miller and Mundy, 2003; Mundy and Babcock, 1998). In shallow environments juvenile corals tend to be found on vertical sides and cryptically, on the undersides of surfaces of dead corals or artificially provided settlement media such as settlement plates (Babcock and Mundy, 1996; Bak and Engel, 1979; Birkeland, 1977; Duerden, 1902; Harriott and Fisk, 1987; Wallace, 1985a). On the underside of plates settlement is often in an aggregated distribution near the edge (Maida et al., 1994) and recruits eventually extend out from these cryptic habitats as they grow. These settlement patterns have been suggested to be due to avoidance of predation or herbivorous grazing, or avoidance of sediment deposition and algal biomass (Birkeland, 1977; Maida et al., 1994) or an interaction whereby filamentous algae traps more sediment. However, it has also been pointed out that the majority of the settlement studies have used settlement plates with smooth upper surfaces which lack sufficient surface rugosity to provide refuge for small corals (see Penin et al. (2010), Nozawa et al. (2011), Edmunds et al. (2014), Nozawa et al. (2011) and Penin et al. (2010).
The cryptic recruitment pattern on settlement plates reverses with depth, and on a proportional basis more juvenile corals tend to be found settled on horizontal than vertical surfaces in deeper water (Birkeland, 1977; Birkeland et al., 1981; Rogers et al., 1984; Sammarco and Carleton, 1981; Wallace, 1985a). This pattern has been suggested to be due to reduced light intensities at depth (Bak and Engel, 1979) and can occur either through settlement behavior or post settlement mortality. Mundy and Babcock (1998) found that some deeper water corals preferred low intensity blue light, indicating that spectral light quality is also an important cue for the settlement response in deep-water corals. The cryptic settlement pattern could also be related to ultraviolet radiation (UVR, 280-400 nm), which can penetrate to considerable depths (>24 m) in tropical waters (Banaszak and Lesser, 2009). Larvae appear particularly sensitive to UVBR (280-329 nm) radiation and exposure reduces survivorship in the brooding (Gleason and Wellington, 1995) and broadcasting species (Wellington and Fitt, 2003). While Baker (1995), Kuffner (2001) and Gleason et al. (2006) recorded reduced settlement of larvae from some brooding species in response to UVR there were no impacts on larval survival. Cryptic settlement appears to represent a relatively straightforward mechanism of reducing UVR damage and maximizing survival during the very early stages of recruit establishment. Overall, settlement of coral larvae probably represents a balance between opposing selective pressures of access to adequate light for photosynthesis versus avoidance of UV damage and competition with algae, sediment, and grazers (Gleason and Hofmann, 2011).
The minimum competency periods for coral larvae varies considerably (Fig. 3, Table 2). Part of the variation could be due to differences in the experimental systems used to quantify the onset of competency—see Heyward and Negri (2010) for a reliable technique for some species. If critical factors which influence settlement were not optimized in laboratory-based experiments then this may have led to some of the
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extended minimum settlement times reported in the early literature—for example 36 days in Acropora hyacinthus (Harrison et al., 1984) as opposed to 7 days (Okubo and Motokawa, 2007), and 16-22 days in Acropora formosa (= Acropora muricata) (Harrison et al., 1984) as opposed to 56 days (Nozawa et al., 2006). Furthermore, the length of the competency period is likely to be underestimated as Acropora spp. kept in low densities and in the absence of cues to induce settlement are still competent to settle at least 60 days post-spawning (Negri unpublished data; Graham et al., 2008).
Of those studies where appropriate settlement cues were used to examine attachment, the settlement starts to occur from a few days to two weeks after spawning (Connolly and Baird (2010), Table 2). Most studies have described initial settlement but several more recent studies have followed the time course over several weeks (Harrison, 2006; Nozawa and Harrison, 2005, 2008; Suzuki et al., 2011; Tay et al., 2011; Toh et al., 2012) including a recent in situ study (Suzuki et al., 2011). Larval settlement generally peaks between 4 and 10 days after spawning but extended settlement times have been shown lasting several months, having implications for long-distance dispersal and increased genetic connectivity between distant reefs (Nishikawa et al., 2003; Nozawa and Harrison, 2005).
Several studies with A. hyacinthus, A. muricata, Acropora longicyathus, A. valida, Platygyra daedalea, Favites chinensis and broadcast spawned G. aspera on the southern Great Barrier Reef and in Japan, have shown the ability of larvae to rapidly settle and attach, occurring a few days after spawning and a few days before they achieve competence and undergo metamorphosis (Harrison, 1997, 2006; Miller and Mundy, 2003; Nozawa and Harrison, 2002; Nozawa and Harrison, 2005, 2008). This precocious settlement behavior, occurring prior to developing full competence, could provide a mechanism for some larvae of broadcast spawning corals to remain on or near their natal reef, allowing some degree of self-seeding of local populations.
7.1. Effects of sediment on settlement
There have been many more studies of the effects of sediments on settlement of broadcast and brooding species than at any other stage (Table 1). These studies have substantiated the observation by Johannes (1970) that coral larvae are reluctant to settle in the presence of sediment (Table 1). In laboratory-based experiments several different techniques have been used and sediment loads causing effects qualitatively and quantitatively described. Qualitative descriptions include '... a conspicuous layer of sediment.' (Babcock and Davies, 1991) or '... layer of sediment.' (Gilmour, 1999). More quantitative assessments have included the use of sediment traps to assess sedimentation rates (i.e. Babcock and Davies, 1991) which are unreliable for this purpose (see Storlazzi etal., 2011). The most recent work of Perez et al. (2014) has quantified the effect more thoroughly, showing that P. damicornis larvae would not settle on surface covered with a fine (< 63 |im) terrigenous sediment of as little as > 0.9 mg cm-2 or - < 80 |im thickness.
There are few field based studies examining the effects of sediment on settlement and of these Babcock and Smith (2002) showed the broadcast-spawning species A. millepora would not settle in silty environments. Manipulative field experiments are difficult, and in that particular experiment sediment was delivered using fine (90% <63 !m) terrestrial sediment consolidated into bricks placed beside settlement tiles. The bricks crumbled on submersion, distributing sediment in their immediate vicinity and onto nearby coral settlement plates. Sediment supply was continued by occasionally placing more bricks nearby over the next few months when possible. In this study sedimentation rates were estimated by attaching household scrubbing pads to the reef and the amount of sediment accumulating in these pads was weighed and expressed in terms of mg cm-2 day-1. The study confirmed the laboratory-based experiments, where corals will not settle in silty environment, however, this type of experiment is highly uncontrolled due to the application of sedimentation rates determined by a
method that cannot provide reliable quantitative information on the downward flux of sediments (Thomas and Ridd, 2004, 2005; Storlazzi et al., 2011; Risk and Edinger, 2011).
Birrell et al. (2005) examined settlement of A. millepora larvae on dead coral substrata with or without sediments and algal turf. Sediments were manipulated by placing 50 cm3 of very fine sediments (< 15 !m) collected by filtering reefal water in 9 L containers and allowing the sediment to settle over the experimental substrata. Maximum settlement occurred where sediments and algae were absent but the sedimentation rates or sediment thickness of suspended sediment concentrations were not quantified.
The most likely cause-effect pathways related to settlement are associated with sediment deposition and changes in light. These studies demonstrate that larvae prefer not to settle in the presence of sediment films. Unconsolidated sediment could mask or cover settlement cues like CCA or may simply represent a negative tactile response (settlement cue masking in Fig. 4). The ultimate effect is a reduction of suitable (bare) horizontally oriented substratum for settlement. Coral larvae have a tendency to settle in small cracks and crevices and Te (1992) and Babcock and Davies (1991) showed that they would settle in confined experimental containers under sedimentation regimes if presented with sediment-free refuges. In the field however, these are also areas where sediments would naturally accumulate.
A reduction in light or change in spectral quality could reduce the available substratum for settlement by reducing the photic zone (settlement site loss, Fig. 4). Gleason et al. (2006) suggested that under reduced light, larvae could mistakenly settle in areas (i.e. shallower depths) where the average light conditions do not favor long term survival once water clarity returns to normal. Larvae would then have to adapt rapidly to potentially high PAR or UV conditions or undergo reverse metamorphosis or polyp bail out to survive. Turbidity-dredging events could also result in such 'settlement mistakes' (Fig. 4).
8. New recruits
Immediately after settlement and metamorphosis, the corals are typically < 1 mm and visible only with a stereo microscope (Fig. 5D). Several recent studies have shown that despite their small size, hetero-trophic feeding (zooplanktivory) occurs quite quickly after settlement, with 2-day old recruits of A. hyacinthus and P. damicornis capable of capturing and consuming live brine shrimp (Artemia salina) nauplii (Toh et al., 2013). P. damicornis recruits fed with brine shrimp grew faster and had much higher survival rates when transferred to the field than unfed recruits (Toh et al., 2014). Acroporid and pocilloporid recruits can grow at a rate of-0.2 mm diameter a week (Schmidt-Roach et al., 2008), reaching 1 cm by about 1 year (Fig. 3) (Babcock, 1985).
The small size of the new recruits makes them particularly vulnerable to a range of factors including sediment smothering (see below) and overgrowth by algae, competition from conspecifics or other benthic organisms, and direct grazing by coral-feeding fish or incidental mortality from scraping herbivorous fish (Penin et al., 2010,2011). High mortality rates (>90%) are well known in most free-spawning marine invertebrates (Gosselin and Qian, 1997) and similarly high rates are also common in corals. Babcock (1985) reported mortality rates of -90% in juvenile A. millepora and -70% in G. aspera and P. sinensis which had attached on slabs of coral skeleton and returned to the field. Using similar techniques Nozawa et al. (2006) reported post-settlement mortality rates of 88-100% over a 3-month period in five species of scleractinian corals initially settled onto slate plates for a few months then transferred to the field. Nozawa (2010) reported post-settlement mortality rates of 40-60% per month and a yearly rate of 85% in Acropora solitaryensis which had been settled onto plain surfaces of fiber cement boards then transferred to the field. Similarly high rates of post-settlement mortality have also been observed in many other studies (see Nozawa, 2010; Nozawa and Okubo, 2011; Ritson-Williams et al.,
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2010; Suzuki et al., 2013; Szmant and Miller, 2006; Trapon et al., 2013a, b; Vermeij and Sandin, 2008).
In juvenile and adult corals their symbiotic algae provide photosyn-thetically fixed carbon to the host providing additional energy for respiration and growth (Lesser, 2004). The initial establishment of symbiosis in Acropora recruits involves an attraction step (of Symbiodinium to the recruits) and a subsequent selective uptake step, suggesting the operation of recognition sytems by 2 weeks (Yamashita et al., 2014). Symbiodinium are usually acquired by the hosts in feeding, and ultimately phagocytosed into the endodermal cells (Colley and Trench, 1983; Fitt and Trench, 1983a, b). The majority (~80%) of broadcast spawning species acquire the Symbiodinium horizontally (Douglas, 1994) i.e. from a free-living reservoir (Baird et al., 2009). Notable exception are Porites spp. and Montipora spp. where zooxanthellae are maternally inherited i.e. vertical transmission, through follicle cells into the unfertilized eggs shortly (weeks to days) prior to maturation (Babcock et al., 1986; Heyward and Collins, 1985; Kojis and Quinn, 1981b). In contrast, only about 15% of brooders acquire zooxanthellae from the environment (Baird et al., 2009). Symbiodinium ultimately reside in the endodermal tissues (Muscatine, 1990) of juveniles and adults at densities of typically one but up to six algae per host cell (Muscatine et al., 1998).
Forming the symbiosis enhances deposition of the skeleton in the well-known phenomenon of light-enhanced (DCMU-sensitive) calcification (Chalker and Taylor, 1975; Kawaguti and Sakumoto, 1948). Juvenile A. digitifera that have acquired algal partners calcify much faster than algal-free aposymbionts (Inoue et al., 2012; Tanaka et al., 2013) and the onset of the symbiosis is crucial for the energetic process of budding in newly settled A. tenuis recruits (Graham et al., 2013; Little et al., 2004).
Coffroth et al. (2006) successfully inoculated asymbiotic octocoral polyps (Briareum sp.) establishing an important step that some of the free-living Symbiodinium were capable of forming a symbiosis. Adams et al. (2009) subsequently established this for hard corals, showing aposymbiotic coral larvae acquired sediment-associated Symbiodinium spp. quicker and in greater abundance than when present in the water column. Collectively these observations suggest horizontal transmission of the symbionts comes primarily from a benthic free-living stage in the sediments (Adams et al., 2009; Coffroth et al., 2006). Under normal, ambient conditions Symbiodinium spp. are lost from corals at rates of 0.1-1% per day (Bhagooli and Hidaka, 2004; Hoegh-Guldberg and Smith, 1989; Jones, 1997; Jones and Yellowlees, 1997; Stimson and Kinzie, 1991) and these could be the ultimate source of symbionts for horizontal transmission.
The next stage is the process of budding i.e. formation of daughter, secondary polyps and Hayashibara et al. (1997) reported this occurs in Acroporasecale after 2 months (Figs. 1 and 3, Table 2) similarto rates reported for A. millepora and A. tenuis (Graham et al., 2013; Little et al., 2004). Acquisition of algal symbionts and also the type (clade) of symbionts is important for post-settlement survival (Suzuki et al., 2013) bud formation and budding rate (Graham et al., 2013; Little et al., 2004). Gamete-spawning species typically become reproductive at 4-5 years or older (Harrison and Wallace, 1990; Wallace, 1985b) although reproduction is related more to size than age, and for Acropora spp., newly formed areas in actively growing regions are typically initially sterile, especially when polyps were budded after the time of onset of gametogenesis (Wallace, 1985b) (Fig. 1).
8.1. Effects of sediment on metamorphosis and new recruits
Several studies have measured decreased recruitment rates in the field along quantified eutrophication gradients including spatial (Dikou and van Woesik, 2006; Hunte and Wittenberg, 1992) and temporal gradients (Thompson et al., 2014). Manipulative studies are more common and Sato (1985) conducted one of the first manipulative experiments to examine grazing on post-settlement survival in P. damicornis. Larvae were settled in the laboratory on plastic, pre-conditioned petri dishes
and then fixed back on the reef-flat oriented facing upwards, downwards or sideways. Some petri dishes were covered with a 1 cm mesh to protect from grazing. All larvae in the upwards facing dishes (either protected or unprotected) became rapidly smothered in sediment and died, while higher survival was noted in the downward facing petri dishes. Sato (1985) discussed the significance of algae trapping and thereby exacerbating the effects of sediments on larval survival but sediment deposition rates were not quantified.
Babcock and Smith (2002) extended their in situ study with rammed earth bricks and household scrubbing pads (see above) to several months, by episodically adding sediment bricks to ensure a continued sediment supply. After 8 months, the number of settled larvae in the sediment treated sites was only ~ 40% of the levels in the reference sites suggesting further mortality had occurred from the first census immediately following settlement of the larvae.
Cause-effect pathways associated with the effects of sediment on new recruits are likely to be similar to those of the adult corals and include covering by sediment and loss of autotrophic and heterotrophic feeding and reduced gas/metabolite exchange (metabolite exchange in Fig. 4). The smaller size of recruits however may make them more susceptible to smothering and/or low light stress from elevated sediment concentrations (see Fig. 5C, D, E).
9. Conceptual models and cause-effect pathways
Fig. 4 shows the conceptual model of the effects of sediments from dredging on the early life-history stage of corals based on the previous discussion. The framework used to connect the many possible cause-effect pathways and the interrelationship between the stressors is the US Environmental Protection Agency (USEPA) Causal/Diagnosis Decision Information System (CADDIS) (Norton et al., 2009; USEPA, 2004). The process allows the generation of a graphical display, of all known cause-effect linkages, steps along causal pathways and possible interacting stressors. The framework allows the inclusion of biologically plausible but as yet untested cause-effect pathways and, if parameterized, could ultimately form the basis of numerical process model to examine the risks of dredging during coral spawning.
Dredging activities can have both direct and indirect effects on benthic habitats with direct effects including the loss of organisms and habitat by removal of hard and soft substrate within the dredge footprint. Indirect and associated with either (1) sound or (2) 'turbidity-generation' or 'plume creation' from various dredging methodologies. Sound originates from propellers, pumps, drag and cutting heads, and engine and mechanical noise from dredges and support vessels. There has been much progress in recent years in characterizing of dredging sound and this has mostly been within the context of understanding the effects on marine mammals and fish (WODA, 2013). Sound can 'mask' biologically relevant signals and could result in reduced coral settlement success as noted above. A potentially beneficial effect of sound could be avoidance of dredging areas by planktivorous fish which may reduce predation on gametes and larvae. It is too early to evaluate the significance of these mechanisms as compared to the more well-known effects of increased water column suspended sediment concentrations.
The most likely cause-effect pathways associated with the effects of dredging is associated with turbidity-generating i.e. the release of sediment into the water column through a range of different processes (see Foster et al. (2010) and VBKO (2003)). Proximate stressors (or causal agents) can be grouped into physical effects and chemical effects (Fig. 4). Chemical effects are associated with legacy contaminants (pollution) and nutrient release from pore-water or sorption/desorption processes in the water column, and oxygen depletion. Nutrient release has the potential for direct metabolic effects and adverse effects through phytoplankton and microbial blooms and subsequent changes via oxygen concentrations. Contaminants have the potential for acute and chronic toxicological, cellular and physiological effects, including
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genotoxic (mutagenic, teratogenic and carcinogenic) effects (Fig. 4), as well as bioaccumulative effects through uptake and ingestion of contaminants (see for example Hedge et al., 2009). Prior to dredging sediments are normally examined for contaminant concentrations and if levels exceed screening guidelines (see for example DEWHA (2009)) are landfilled. Many capital dredging projects in the tropics are also green-field sites without historical pollution, and sediment contamination is a more significant issue for the marine environment of industrialized and typically temperate countries than for tropical benthic coral reef environments (with a few notable exceptions—see Jones (2011)). For these reasons the chemical effects are not considered further here.
The model graphically highlights some of the complexities associated with understanding the effect of sediments on the early life-history stages of corals. While some proximal stressors such as the effects of sound are isolated and distinct, most of the proximate stressors are associated with the release of sediment into the water column and once turbidity has been generated, the proximal stressors then become highly interlinked. Individual stressors become part of a causal pathway to other stressors (the inner triangle of Fig. 4).
This model highlights the multifaceted interactions of sediments with coral reproductive processes and early life history stages. Part of this complexity is due to multiple ways in which corals are affected (e.g. light reduction, physical interactions in the water column and smothering). The model also highlights that dredging and natural resuspension may affect more than one step in the reproductive sequence of corals. When the impacts on each step are documented then this should be accounted for in risk assessment modeling. Although this model reveals multiple stressor pathways, many of which have not been documented previously, it has not considered that other simultaneous stressors such as high sea surface temperature can increase the sensitivity of coral reproduction in an additive or synergistic way (Negri and Hoogenboom, 2011).
10. Discussion and conclusions
Turbidity and sedimentation are two of the most widely recognized threats to coral reefs (Johannes, 1970; Risk and Edinger, 2011; Rogers, 1990). There have been many studies of the effects of typically very high SSCs and sedimentation rates on adult corals, but the effects on coral communities may equally manifest themselves over longer periods and associated with changes at the population level via effects on reproduction and recruitment. This review was partly motivated by a recent resources boom in tropical Australia, the need for dredging for coastal infrastructure and shipping channels to export mineral and petroleum products, and current environmental regulations around protecting coral spawning events during dredging campaigns. However, the findings are equally as applicable to natural events in turbid-zone communities driven by wind-wave induced resuspension (Anthony et al., 2004; Jing and Ridd, 1996; Larcombe et al., 1995, 2001; Lawrence et al., 2004; Ogston et al., 2004; Verspecht and Pattiaratchi, 2010).
When the regulations were introduced in Western Australia, shortly after the discovery of co-ordinated spawning of corals comparatively little was known about the effects of sediments, hence the approach was precautionary (Kriebel et al., 2001). Since then an improved understanding of the biology of the early life-history stages of corals and also their response to sediments, coupled with a growing understanding of the water quality conditions that can occur during dredging programs, has allowed a more thorough analysis of the potential risks associated with turbidity generation on the early stages of the coral reproductive cycle.
The conceptual model (Fig. 4) highlights known and also biologically plausible cause-effect pathways including some potentially beneficial effects of turbidity. Benefits include a reduction in UV light penetration potentially reducing damage to gametes and embryos at the surface, a reduction in oxidative stress in symbiotic larvae and recruits (Abrego
et al., 2012; Yakovleva et al., 2009), a reduction in predation rates by reduced visibility and increased encounter rates of aposymbiotic larvae with sediment-associated free-living Symbiodinium released into the water column. Suspended and deposited sediments can act as an energy source for adult corals if it contains organic material (Anthony, 1999; Mills et al., 2004), and possibly recently settled corals—although this has yet to be examined. However, there are overwhelmingly more (30 + ) possible causal pathways whereby turbidity-generating activities can negatively affect reproduction.
Most studies of the effects of sediments have been associated with fertilization and subsequent larval development and settlement, but there is a suite of biologically plausible cause-effect pathways associated with turbidity-generation prior to these stages. The predictability of broadcast spawning corals in some species (to within a few minutes from year-to-year, Vize et al. (2005) and Babcock and Heyward (1986)) and subtle differences when gametes are released by different species, and even factors such as egg-sperm bundle dissociation rates (Wolstenholme, 2004), highlight the significance of timing and the synchronization process for successful fertilization. The time-window for fertilization could perhaps be less than an hour in vivo where sperm dilution and advection occurs (Omori et al., 2001). The available evidence also suggests that it is only very subtle changes in light quantity and quality (i.e. falling light intensities, the length of a period of darkness and the intensity and color of downwelling irradiance during twilight) (Babcock, 1984; Boch et al., 2011; Hunter, 1988; Knowlton et al., 1997; Sweeney et al., 2011) that are amongst the final discrete, proximate triggers for the spawning. This needs to be contrasted with the profound effects of high SSCs on light including producing extended darkness and semi-dark, caliginous, twilight periods. Altering the final cues could result in asynchronous spawning. The extended twilight periods could also affect gametogenic synchrony in the weeks and months leading up to spawning. Such a loss synchrony could ultimately affect the arrival of the gametes at the surface, blurring the temporal separation for each species which is believed to be an important pre-zygotic isolating barrier that prevents or reduces hybridization between closely-related species spawning at slightly different times (Fukami et al., 2003; Knowlton et al., 1997; Levitan et al., 2004; van Oppen et al., 2002; Willis et al., 2006; Wolstenholme, 2004).
A second suite of cause-effect pathways occurring before fertilization include the binding of sediments to egg-sperm bundles reducing ascent rates from the seabed and even cause ascent failure at very high SSCs (Ricardo et al., submitted). Even if not bound to the bundles, settling of silt-sized sediments could affect bundle rise rates, especially for deeper corals, also impacting the timely appearance at the surface. Sedimenting silt-sized particles, which are about the same size as coral sperm, could increase the sinking rates of the already negatively buoyant sperm from the upper-surface where fertilization occurs. As with the effects of light quality and quantity, collectively these mechanisms could also affect the temporal separation resulting in asynchrony and reducing the chances of egg-sperm encounter (Ricardo unpublished data).
Several studies have examined the effects of sediment on fertilization but with wide ranging effects, and it is clear that there is a need for greater standardization of approaches and consideration of experimental conditions such as egg and sperm concentrations and sperm contact times. Attention to these factors may also optimize the sensitivity of the assays for further use in risk models. As a generalization, embryogenesis appears to be relatively less sensitive to the suspended sediment concentration but more studies are needed on the effects on embryogenesis and early larval development to better understand the impacts on the planktonic phase. Early embryos are known to be very sensitive to turbulence, resulting in disintegration of embryos of A. millepora at the 2-16 cell stage creating irregular groups of cells or individual blastomeres (Heyward and Negri, 2012). To assess the effects in the water column alternative experimental approaches may be needed to keep the delicate embryos and larvae in suspension together with
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uniform sediment concentrations as well as allowing for water exchanges. Future studies will also need to address suitable end-points and how to account for disintegration and disappearance of the larvae which will also deteriorate water quality and affect the remaining larvae (Gilmour, 1999; Nozawa and Okubo, 2011).
The available laboratory and field studies suggests that one of the most sensitive stages is the effects of sediment on settlement and subsequent metamorphosis. High SSCs will affect light quality and quantity reducing the size of potential settlement areas by reducing available light and depth of the photic zone. However, in addition to light related changes, Johannes (1970) specifically linked the effects of sediment on settlement within the context of environmental damage '...no new corals can establish themselves where the soft, shifting sediments have covered the once hard calcareous substrate.'. These observations have been substantiated in the exposure conditions has been elusive, except perhaps with the recent work of Perez et al. (2014).
Much like the cascade of environmental variables operating alone or in combination at increasingly finer time scales to co-ordinate reproduction and spawning, Gleason and Hofmann (2011) describe a hierarchy of cues related to settlement, operating at sequentially finer scales and ultimately leading to the choice of a settlement site that is optimal for adult fitness (see also Suzuki et al. (2012)). The presence of sediment seems to be one of the more important final (negative) cues in this cascade, but how sediment is detected by the planulae is unknown. Possible mechanisms include masking of settlement cues and the failure of cnidae to attach in the presence of unconsolidated sediment. The sensing of sediments could occur by receptors on the brim of the concave structure of the aboral pole (Okubo and Motokawa, 2007), and better understanding of the detection mechanism is needed to establish causal relationships.
One of the least studied and potentially most sensitive life-history stages is the early post-metamorphosis survival where the sub-millimeter sized polyps often gain symbionts, start heterotrophic feeding (zooplanktivory) and develop secondary polyps. High post-settlement mortality rates (>90%) are well known in most free-spawning marine invertebrates (Gosselin and Qian, 1997) but the small size of the new recruits makes them difficult to study, and also vulnerable to a range of factors including sediment smothering. This is arguably one of the most important information needs with respect to the effects of sediment from dredging-related and natural turbidity events. Understanding the mechanism whereby sediments can affect the early life-history stages is essential for deriving dose-response relationships and ultimately for providing information that can be useful for management.
The conceptual model (Fig. 4) highlights some of the difficulties associated with establishing dose-response relationships and in particular the conflation of proximal stressors which could potentially confound establishing causal links. While some of the stressors are isolated and distinct, such as effects of sound, other proximal stressors are highly interlinked. Thus, suspended sediments can cause biological effects directly (i.e. by interfering with feeding), but high SSCs are also a step in the causal pathway to another proximal stressor, changes in light quantity (and quality). Similarly elevated SSCs are a necessary precursor to sediment deposition, which by veneering the corals' surface with a fine layer of sediment also reduces light availability and thus the mode-of-action of would also include those associated with light attenuation.
This close interlinking of proximate factors (the inner triangle in Fig. 4) makes it difficult to distinguish which factor or factors are responsible for observed effects in the laboratory or field and to establish quantitative relationships. This needs to be carefully considered in interpreting the results of past laboratory or field manipulations (Table 1) and for designing future studies. For example, Te (1992) found no effects of a 1000 mg L-1 sediment concentration on settlement of P. damicornis planulae in shallow, shaded bowls; however, at that concentration all light would be attenuated in situ within a meter (Te, 1997). Settlement and survival of planulae under those conditions
seems improbable. The pooling of results from past studies, as is common in review articles, can be very misleading unless the wider context of the treatment on other causal pathways is known: only then can the results be used in any kind of environmental context.
The causal/diagnosis decision information system (CADDIS) framework laid out in Fig. 4 has proved useful for identifying areas of uncertainty, knowledge gaps and guiding future laboratory or field studies. If used in combination, with the analysis of the timing of the various life-history stages, and the water quality characteristics during a dredging program over similar time periods, experiments can be designed with more environmentally relevant exposure conditions (Harris et al., 2014). Approximately 200 m from a trailer suction dredge SSCs can exceed hundreds of mg L-1 for short periods (hours) encompassing the duration of some of the stages in the life-cycle such as the fertilization window. Over longer time frames (i.e. days to weeks), which encompass embryogenesis and the pre-competent and competent stages through to settlement, average SSCs are lower in the tens of mg L- 1 range. Close to a dredge light levels can be reduced to zero for several days to a week. The 95th percentile of the data over the different time frames probably represents close to a worst case scenario but the intensity and duration of the disturbances will decrease with increasing distance from the turbidity-generating activity. While it is clear that water quality conditions (SSCs, sedimentation and light attenuation) during dredging have the potential to harm various early life stages of corals, much work needs to be done to improve experimental stress protocols before the risk to coral reproduction can be assessed. This needs to be considered in interpreting the results of past laboratory or field manipulations (Table 1).
Establishing relationships in situ is difficult because of operational exclusion zones frequently found around dredges and the associated flotilla of hopper barges, bunkering, crew transfer and support vessels. If studies are conducted in the laboratory they will need to overcome the often difficult problems associated with manipulating and keeping sediments in suspension. To derive accurate dose-response relationships for gametes, embryos and larvae it is essential that SSCs are quantified gravimetrically as opposed to being expressed nominally (Harris et al., 2014). Future studies will need to use suitably sized sediment particles, and undertake analyses of particle size distributions. Future studies will also need to undertake a full suite of organic and inorganic chemical analyses as part of normal ecotoxicological procedures (Klimisch et al., 1997) to discount effects of legacy contaminants. These can be significant even in non-industrialized reefal environments. Chemical analyses should be conducted of the typically fine clay and silt fractions used in the assays and not the coarser, bulk surficial sediments from the collection point. The use of clean aragonite or calcium carbonate sediments with similar particle size distributions is recommended as a positive control (Harris et al., 2014; Klimisch et al., 1997) and surrogates for sediments such as carborundum or kaolin clay should not be used. Attention to these details will assist in interpreting the results, verifying the conditions of the assay are optimized and working properly (Harris et al., 2014), and controlling for the effects of contaminants. Future studies need to identify cause-effect pathways, and recognize the effects of treatments on other potential cause-effect pathways and consider the dose-response relationships. Where appropriate statistical metrics such as ECi0 and EC50 values need to be derived rather than statistical testing of a few point concentrations (Chapman et al., 1996, 2001; Harris et al., 2014; Landis and Chapman, 2011).
The successful use of a coral spawning environmental window as a management tool depends upon a shutdown period which encompasses the entire period that turbidity-generating activities could have an effect on spawning and ultimately the successful recruitment of juveniles into the next generation. The window needs to contain sensitive stages such as settlement and early post-settlement survival (Trapon et al., 2013a; Vermeij and Sandin, 2008). From an operational perspective the success is also reliant upon the bracketing of an easily identifiable, discrete and highly co-ordinated spawning period. In Western
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Australia there is a well-known main autumn spawning period (Simpson, 1985), but more recently a significant spring spawning period has been identified (Rosser and Gilmour, 2008). The presently applied 12 days coral spawning shutdown period is too short to fully encompass the full settlement period, and all potential demographic bottlenecks associated with recruitment, especially settlement and early post-settlement survival (see Figs. 2 and 3). Extending the window for a few months before and after the predicted spawning date seems an obvious next step to also accommodate effects on gametogen-ic and spawning synchrony and to fully cover the settlement period. The window would also need to accommodate both the major (autumn) and minor (spring) spawning period as well split spawning events which occur every 2-3 years. This would significantly limit time that turbidity-generating activities could occur near coral reefs in any given year. Although the approach seems logical, the question is whether this approach is reasonably practicable and whether the resulting intermittent and protracted dredging operation would result in a better net environmental benefit than a shorter campaign. Conducting maintenance dredging activities away from coral spawning periods and settlement periods, and starting capital dredging programs at appropriate times to avoid spawning periods would constitute a best management practice.
Funding sources
This project was funded by the Western Australian Marine Science Institution as part of the WAMSI Dredging Science Node, and made possible through investment from Chevron Australia, Woodside Energy Limited, BHP Billiton as environmental offsets, and by co-investment from the WAMSI Joint Venture partners. This research was also enabled by data and information provided by Chevron Australia. The commercial investors and data providers had no role in the data analysis, data interpretation, the decision to publish or in the preparation of the manuscript.
Author contributions
RJ, GR, and AN wrote the review.
Competing interests
The authors have declared no competing interests exist.
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