Thought’s about the recent Venter PNAS publication, reproducible science, ethical competition, and post-publication peer review

I thought the recent story of the Venter PNAS publication (Lippert et al., 2017), the extremely quick critisicm from bioarxiv (Erlich 2017), and the piece by Nature that summarize the criticisms (for those that want the quick-and-dirty) would be of general interest to my twitter followers.

One of the things I found most interesting was how quickly a paper was published (1 day!?). I probably do not need to remind anyone that writing/publishing an article takes a lot of time so what were the reasons for this. Well it turns out that Lieppert et al., first submitted to Science and Dr. Yaniv Elrich (Associate Professor at Columbia University) was actually a reviewer – he told the editor that paper was “Arsenic-life” weak, which explains how he got the jump-start.

Two other things I thought were surprising was that Venter chose all 3 reviewers at PNAS which stinks of unethical competition. Secondly, the code was not made available upon publication, meaning Dr. Erlich had to engage in some forensic bioinformatics (although he probably built this model after reviewing it for science). What I found funny was Venter employed “close to ~30 authors and [used] a range of complex algorithms” and Dr. Erlich got better results with his own model (using just sex+age+ancestry. That’s right, using no genetic features which was the main claim of the paper) “after on hour of work” (quote excerpts from the bioarxiv paper).

Take home thoughts:

Something that annoys many bioinformaticians is reproducible science (e.g. data availability, source code, versions, and command line options, etc.). When I look at a paper, I want to be able to do exactly what you did (and preferably do so using raw data deposited alongside your publication, rather than digging around in databases and piecing together what you did after the fact). I think most of us can now agree that sharing data is a must (see backlash against NEJMs  criticism of “research parasites”), yet it still happens (e.g. newly published genomes are often embargoed for a year so the lab that produced the data has more time to mine it). FWIW probably won’t think highly of your paper if you don’t include code and data (I’ll think you have something to hide), besides sharing data also gets you more citations. So please use a github repos (with a DOI in the manuscript) and data repository (e.g. figshare) at the very least; if your pipeline uses many different software packages combine with a docker container (to run all the software).

This also got me thinking about the importance of being able to sniff out bad science. Just because something has published in a journal with a high-impact factor (it’s in Nature/Cell/Science/PNAS/NEJM it must be brilliant), or presume that anything from Dr. Famous’ lab must be right, does not mean its “good” science. Let us all try to be cynical about everything we read (and believe).

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Laboratory research will never be a substitute for fieldwork

A recent opinion piece published in Science (Minteer et al., 2014) titled “Avoiding (Re)extinction” has re-sparked an argument on the collection of specimens to confirm a species’ existence (see press release here). The authors argued that in lieu of killing and collecting the animal, photography, audio recording, and nonlethal sampling methods could be applied without increasing the extinction risk of endangered animals or newly discovered species. Social media discussions on Twitter and Ecolog-L listserve alerted me to two rebuttals which argue that this piece will only fuel anti-collecting sentiments espoused by a subset of people who don’t understand how research, scientific collecting and taxonomy work.

For an extensive view of the many problems with the authors’ argument you can read here and here. For the purpose of brevity suffice it to say that museum collections have a unique value and that the suggested nonlethal sampling methods are rarely possible and/or effective to document and understand species with reasonable confidence and therefore implement successful conservation plans.

If established scientists can make such asinine statements in such a popular journal I wondered if such ignorance and scientific-illiteracy could lends itself to the fieldwork I’m doing. Certainly one of the major impediments to research today is technophilia and a reduction in funding (Bury et al., 2006). I liked Bill Nye’s decision to engage in public debate with the creationist Ken Ham (not because I’m disillusioned that he will change his mind – he won’t) because I also believe it’s more important than ever to have an environmentally literate society.

So, is it really necessary to study animals in their natural environment? Could you not breed animals and study them in the laboratory rather than collecting threatened or endangered individuals from the wild? Certainly the advances in technology have enabled more work to be done in the laboratory than ever before. Sitting at a laboratory bench oblivious to nature outside you could devote an entire career to coral polyps alone and still make great contributions to science. However, this only scratches the surface. The genus sclearactinia is the product of many episodes of microevolution and interactions with other organism in the natural environment and very little at the molecular and cellular level makes sense until it has been placed inside this broader framework.

Certain scientists, like Jeremy Fox, vehemently champion artificial natural systems, like microcosms, because they can reduce the complexity enough to make it easier to solve ecological riddles in a controllable, replicable and cost-effective manner. However, these systems deal with protists which are very, very tiny and can be done in a glass mason jar. To scale this type of experiment up for corals would be very expensive; indeed, field studies are often the cheapest option for PhD students because there is no infrastructure or maintenance costs involved. The corals I study are broadcast spawners and only spawn once a year. That’s not much data, and certainly not enough for a thesis. So I do use a surrogate system in the laboratory (the sea anemone Aiptasia pallida), a somewhat well know species because it can be induced to spawn monthly giving me more data to analyze. However, these organisms are more distantly related systematically and ecologically. So to answer questions about coral definitively the work needs to be on corals and it needs to be geographically representative (McCallum and McCallum, 2006).

It’s important that we study these intriguing animals now because environmental stressors frequently influence life history characteristics early in the stress response (Newman and Unger 2002). It’s important we undertake these studies now in a “healthy” environment to potentially save them before they disappear from the biosphere.

“It seems to me that the natural world is the greatest source of excitement; the greatest source of visual beauty; the greatest source of intellectual interest. It is the greatest source of so much in life that makes life worth living.” – David Attenborough

References:

Bury, R.B. (2006) Natural history, field ecology, conservation biology and wildlife management: time to connect the dots. Herptological Conservation and Biology 1(1):56-61.

McCallum, M.L. and McCallum, J.L. (2006) Publication trends of Natural History and Field Studies in Herpetology. Herptological Conservation and Biology 1(1):62-67.

Minteer, B.A., Collins, J.P., Love, K.E., Puschendorf, R. (2014) Avoiding (Re)extinction. Science 344:260-261.

Newman, M.C. and Unger, M.A. (2002) Fundamental of Ecotoxicology, 2nd edition. CRC/Lewis Publishers, Boca Raton, Florida, USA.

Climate Change and Corals: Laying Siege to the Adaptation Mythos

This is my rebuttal to the recent blog by Jacob Jerome a Graduate Student and Intern at the University of Miami in the RJ Dunlap Marine Conservation Program titled “Climate Change and Corals: is it too late?”

Dear Mr. Jerome,

While I’m envious of your glass half-full outlook on the fate of corals to global warming, I feel that your only helping to propagate a persistent mirage; namely that *all* coral individuals or communities will adaptively respond in time to thermal stress. As will be argued here, this removes the onus of implementing a global strategy that can reduce both local and global stresses and implies that we have more time with respect to the pressures on coral reefs and related ecosystems.

Climate change is a major threat with rising sea surface temperatures and ocean acidification acting as chronic stresses which operate over long timescale. Implications include many adverse effects, bleaching, reduced growth and reproductive outputs, death and loss of biodiversity (Loya et al., 2001; Fabricius, 2005; De’ath et al., 2012). Thermal stress could potentially also increase viral load and corals susceptibility to disease. If we stopped emissions today, much of the warming would persist for centuries after greenhouse gas emissions stopped. If the current rate of emissions holds (business-as-usual), or increases, the ability of corals to respond evolutionarily to the rapid pace of change is doubtful (Dove et al., 2013).

Although evolutionary history is complicated by cyclical climate changes over geologic time (Vernon, 2000), coral reef system have changed as a result of climate change with few contemporary reefs existing in a “pristine” state. Most long-term studies show declines of around 50% since the early 1980’s. During this period coral composition has changed with the dominance of species being altered as well. By comparing recent events of decline to those of the past indicate that current rates of changes are orders of magnitude higher than they have been for tens of millions of years. You mentioned in your article that according to the Status of Coral Reefs of the World: 2008, 15 percent are seriously threatened. However, more recent studies looking across the world’s coral reefs, 75% are threatened (Burke et al., 2011). I’m not of the “coral reefs are doomed” prophecy point of view but I do believe that the situation is dire and that returning reefs to a pristine condition is not a realistic goal. Although I’m not suggesting we abandon all hope and toss in the towel (after all I’m not entirely a curmudgeon because then why would I even bother with the work I do?), I just think we need to be careful, and to tread lightly, when communicating as major funding agencies are often evaluating whether or not to continue funding coral reef management and management-related research.

Studies documenting recovery have yielded mixed conclusions. Some authors have proposed that individuals, or indeed communities, can adaptively respond to thermal stress (Logan et al., 2014). However; the broader scientific community has concerns as to whether Scleractinian (reef building species) will survive global warming and ocean acidification (Baker et al., 2008; Vernon et al., 2009; Hoegh-Guldberg, 2014). I think this is especially important for blog posts which are aimed at the broader public. We need to be clear about internal disagreement within the ivory towers for such contentious, and politically sensitive topics such as climate change. This has played out vividly in the past in such instances as “climategate”. As scientists we should leave ample room in our communications to highlight the dissent and nuances to complex topics in a way that the general public will recognize and think critically about.

I felt that you spun a one-sided story, in that you only included the exceptions to the rule rather than covering the wider accepted literature on reef resilience and adaptability. Most studies incorrectly extend the evidence which is necessary but not sufficient to support the conclusions that coral reefs will survive due to their ability to acclimatise, adapt and/or migrate to the current rapid environmental changes (Hoegh-Guldberg, 2014).

A couple of points I would like to address critically are as followed:

  • You mentioned the study by Raina and colleagues (2013) and suggested that this was evidence that this is a “fight” against temperature shifts? I fail to see how you can jump to such conclusions when juvenile corals were only exposed to elevated temperatures for 12 days. Moreover, adult colonies of A. millepora exposed to 32°C for 10 days had an 84% reduction in their Symbiodinium. To me, there findings only suggest a stress response which likely plays some role as an anti-oxidant in cellular processes. The loss of biodiversity in coral and symbiodinium following bleaching, added to increased probability of consecutive bleaching would suggest a loss in reef cover and diversity if current trends continue (Stat et al., 2006). The authors posit that release of DMS, as a result of bacterial conversion of DMSP, could be a major source of cloud condensation nuclei. However, I feel that your readiness to extrapolate and say that it would offer some sort of adaptive advantage is a far-reach by any estimate. Especially since the authors acknowledge that the declining trend in coral cover due to anthropogenic stressors can further destabilize local climate regulation.
  • Second, you mention the Cayman island recovery in 7 years as investigated by Manfrino et al. (2013). While I appreciate seeing findings which are contrary to common assumptions I think we need to take them with a large grain of salt. I would be the first to point out that in Samoa corals can thrive in 35°C water for a few hours each day, a “fact that they’re there means they’ve adapted to survive says Steve Palumbi. However, I believe this is an isolated case, and therefore not representative of the coral reefs by-and-large. Similar statistics have engendered debates about the value of marine protected areas (Huntington et al., 2011). We need to be honest by not omitting inconvenient truths, this is what it means to be a scientist, instead of say a lobbyist or philosopher. Johnson and Saunders (2014) suggest that demographic and economic factors influence the psychology of human decision to such a degree that it has a major impact on local ecology. The work they did in Curacao and Bonaire showed that socio-cultural-economic backgrounds influence marine resource management approaches which likely has an effect on the local ecosystems resilience and recovery. Curacao’s economy primarily relies on fishing (making money by exploiting resources), whereas Bonaire’s economy relies more heavily on revenue from tourism (making money by preserving resources). The Cayman Islands are therefore not representative of the vast majority of countries which harbor coral reefs (and rely on a subsistence economy) and it is unlikely that this study is representative of the broader global coral reef ecosystem.
  • Thirdly, you believe that “new scientific research indicates that not all corals are quite ready to give up”. I agree with you to the extent that this is true as in the case of Samoan corals or Dubai in the Arabian Gulf. Nonetheless, at what cost to the ecosystem if only a few corals, or communities, can survive? Massive plating and encrusting morphologies have been shown to be less susceptible than branching morphologies in a broad range of habitats, biogeographic regions and sea warming events (Loya et al., 2001). It has been shown that the rugosity of the substratum is positively correlated with observed fish species richness in most reports (Gratwicke & Speight, 2005) so a loss of substrate complexity could be bad news in a warming world.

One more thing to consider is symbiodinium clade changes, as algal symbionts are thought to play a key role in coral resistance and resilience. At the risk of not keeping my rebuttal germane (I know you never mentioned this, likely for the obvious reasons I’m about to bring up) I should mention another contentious issue as it relates to adaptation. Its alluring to think that hosts may switch/shuffle symbionts (Buddemeier & Fautin, 1993) for ones that may be more tolerant to the changing environmental conditions; this would overcome the slow pace of coral host evolution (a consequence of long generation times and low population diversity due to asexual reproduction). However, Lewis and Coffroth (2004) have shown that the octocoral Briareum only takes up symbionts that are found in normal conditions which does not represent the uptake of completely new symbionts to that host species. This suggest that the adaptive potential of corals may be limited to the existing types of symbionts present in the host. A number of authors have presented convincing data which suggests that few hosts have more than one type of symbiont (Baird et al., 2007), generalist corals such as Acropora and Pocillopora have a high flexibility, while specifist corals such as Porites have a low flexibility to symbionts diversity. Moreover, corals which harbor clade D are more thermo-tolerant, but the coral fitness may suffer energetic costs such as a reduction of growth and reproduction (Jones & Berkelmans, 2011). I think the paucity of evidence of propitious effects such as coevolution in the literature requires further investigation.

Due to the large policy implications I feel that your post should set a higher standard of demonstrating results beyond a reasonable doubt, or at the very least recognizing that scientists are split over this issue. I’m worried that certain subsets of the public will cherry pick results and trumpet “scientists prove reef extinction is not occurring”. After all there are those with a vested interest who will pervert fact and take things out of context. Others, such are media reporting may just skim right over this and not do background research on the actual papers referenced. In my own humble opinion the belief that somehow corals will magically evolve into a resilience state and alter the current trajectory of coral reef ecosystems under rapid anthropogenic climate change is a dangerous pipe-dream indeed.

References:

Baird, A.H., Cumbo, V.R., Leggat, W., Rodriguez-Lanetty, M. (2007) Fidelity and flexibility in coral symbioses. Marine Ecology Progress Series 347:307-309

Baker, A.C., Glynn, P.W., Riegl, B. (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science 80(4):435-471.

Buddemeier, R.W. & Faustin, D.G. (1993) Coral bleaching as an adaptive mechanism: a testable hypothesis. Bioscience 43:320-326.

Burke, L., Reytar, K., Spalding, M., Perry, A. (2011) Reefs at Risk Revisited. Washington, DC: World Resources Institute.

De’ath, G., Fabricius, K.E., Sweatman, H., Puotinen, M. (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences of the United States of America 109(44): 17995-17999.

Dove, S.G., Kline, D.I., Pantos, O., Angly, F.E., Tyson, G.W., Hoegh-Guldberg, O. (2013) Future reef decalicification under a business-as-usual C02 emission scenario. PNAS 110(38):15342-15347.

Fabricius, K. E. (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50(2):125-146.

Gratwicke, B., Speight, M.R. (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. Journal of Fish Biology 66:650-667.

Hoegh-Guldberg, O., 2004. Coral reefs in a century of rapid environmental change. Symbiosis 37:1–31.

Hoegh-Guldberg, O. (2014) Coral reef sustainability through adaptation: glimmer of hope or persistent mirage? Current opinion in Environmental Sustainability. 7:127-133.

Huntington BE, Karnauskas M, Lirman D (2011) Corals fail to recover at a Caribbean marine reserve despite ten years of reserve designation. Coral Reefs 30:1077–1085.

Johnson, A.E. and Saunder, D.K. (2014) Time preferences and the management of coral reef fisheries. Ecological Economics 100:130-139.

Jones, A.M., and Berkelmans, R. (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. Journal of Marine Biology 2011:1-12.

Lewis, C.L., Coffroth, M.A. (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304:1490–1492.

Logan, C.A., Dunne, J.P., Eakin, C.M., Donner, S.D. (2014) Incorporating adaptive responses into future projections of coral bleaching. Global Change Biology 20:125-139.

Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., Van Woesik, R. (2001) Coral bleaching: the winners and the losers. Ecology Letters 4(2): 122-131.

Manfrino, C., Jacoby, C.A., Camp, E., Frazer, T.K. (2013) A Positive Trajectory for Corals at Little Cayman Island. PLoS ONE 8(10):e75432.

Raina, J.B., Tapiolas, D.M., Forêt, S., Lutz, A., Abrego, D., Ceh, J., Seneca, F.O., Clode, P.L., Bourne, D.G. Willis, B.L., Motti, C.L. (2013) DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature Letters, 502: 677-680.

Stat, M., Carter, D., Hoegh-Guldberg, O. (2006). The evolutionary history of Symbiodinium and scleractinian hosts – Symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology, Evolution and Systematics 8:23-43.

Vernon, J. (2000) Corals of the World. Australian Institute of Marine Science, Townsville.

Veron, J.E.N., Hoegh-Guldberg, O., Lenton, T.M., Lough, J.M., Obura, D.O., Pearce-Kelly, P., Sheppard, C.R.C., Spalding, M., Stafford-Smith, M.G., and Rogers, A.D. (2009) The coral reef crisis: The critical importance of <350 ppm CO2. Marine Pollution Bulletin 58(10):1428-1436.

Inside a coral nursery

Tanks
Here is a behind the scenes look at coral propagation at the Husbandry Center of Taiwan’s National Museum of Marine Biology and Aquarium (NMMBA). This facility is used for a wide variety of purposes including culturing of live foods, isolation of new animals, breeding area, nursery environment for animals born here, medical care for animals that may need it as well as the propagation of corals – the latter will be focused on in this post.  You could call this a coral farm, parent colonies are maintained and continue to grow in this facility, and the branches of these colonies are propagated by fragmentation – similar to the way new plants are grown from cuttings of existing plants.

The fragments -or ‘frags’- are affixed to a base, soft corals are sewn onto terracotta tiles (15 x 15 cm), on the rugose side as they prefer surface irregularity. As the frags grow, they will attach themselves and encrust onto the base structure and start to develop several branches.
Coral_Spats

After reaching a larger size they can be put into tanks inside of plastic planter pots.

Hard coral frags on the other hand are suspended in tanks by monofilament lines. When they are big enough they can be epoxied to a hard substrate.hard_smallHard_Large

Why should we grow corals when wild-harvested corals are available right out the front door of the Museum?  It’s our social responsibility to reduce the pressure on the world’s coral reefs.  Every coral fragment we can grow in the facility is one less taken from a natural reef.

At NMMBA coral propagation is used for Aquarium as well as the natural products research they do here. Around 2008 they did a study to see if they should undertake restoration efforts; however, they found that recruitment was high enough that they did not need to. Unfortunately, this is not the case globally and a number of agencies in various other countries are involved in these operations. Frags are attached onto natural live rocks using cyanacrylate glues, which will eventually, naturally, establish their foothold on the live rocks.  Restoration efforts began in the 1970s-1980s (Maragos 1974, Harriot and Fisk 1988) and have been increasingly implemented in the Caribbean targeting threatened staghorn coral, Acropora cervicornis (Lamarck, 1816) and elkhorn coral, Acropora palmate (Lamarck, 1816), which were once the dominant reef-building taxa in the region.  Due to the combination of biological and human induced stressors, Acropora has suffered significant degradation with estimated population declines of up to 95% in some areas (Porter and Meier 1992) leading to their listing as threatened in the US under the Endangered Species Act in 2006 and as critically endangered in the International Union for Conservation of Nature (IUCN) Red List of Threatened Species in 2008.

Although a number of projects are now getting significant funding, using considerable technical expertise and field efforts to establish coral nurseries, and plant out small colonies, the success is varied. While there is a lot of news about how well corals do in the nursery there is little evidence of long-term success once planted out. However, the University of Miami researchers report 92% survival of all outplanted corals since 2007.  Frame1frame2

Other critics of these efforts mention that selection of “resistant” corals are ones that survive in the nursery. The coral reef restoration project Dr Sarah Frias-Torres is running in the Seychelles is a bit different. During the 1998 massive El Nino, which coincided with the Indian Ocean Dipole (the “Indian El Nino”), about 97% of the shallow coral reefs in the tinner granitic island died. This project uses frag from the 3% that survived the massive coral bleaching. This means, they are not growing corals that survive in the open ocean nurseries, but are growing fragments of the corals that survived a major warming event. There is hope that the restored coral reef will have a better chance of survival this time.

Indeed, some doubt that such efforts will be successful, for example these so called “artificial reefs” are often displaced by hurricanes and typhoons (Vize, personal communication). Wave heights can exceed 10m and can move steel frame boxes (average height 5m) lashed together with steel cable that are attached to steel beams and concrete bridge pilings functioning as anchors can be displaced up to 1200m (Turpin and Bortone, 2002). However, it depends on how these structures are installed. Reef Balls is a non-profit and international environmental NGO that has deployed over 1/2 million artificial reefs, which have been noted to have not been displaced by Hurricane Georges in 1993 (Harris, 1998).
ReefBall

In the past 5 years coral nurseries have expanded to ecologically meaningful levels and are beginning to have a considerable impact on the localized recovery of coral reefs (RinkevichForrester et al., 2014). I’m aware the pie of conservation dollars is small and we don’t want to see any slices going into ill-conceived projects that promise restoration with no solid scientific support. Nonetheless, I think we can make the pie bigger, involve public and private sources of funding while working at the same time in science-based conservation and science-based restoration.

Curmudgeons are quick to point out that this is only a local approach (and costly at that) and will not be an effective long-term solution. Sadly, they may be right. As long energy production continues to release C02, oceans will continue to suffer. Nonetheless, in many coral tourism and coral aquaculture areas, including the Maldives, Thailand, Indonesia, Philippines and some Pacific Island States, etc, there are many sound commercial reasons why resort companies and other commercial ventures should and do support local coral nursery and plant-out projects, and personally I support this type activity.

“The time is always right to do what is right” – Martin Luther King

References:

Forrester, G.E., Ferguson, M.A., O’Connell-Rodwell, C.E., Jarecki, L.L. (2014) Long-term survival and colony growth of Acropora palmata fragments transplanted by volunteers for restoration. Aquatic Conservation: Marine and Freshwater Ecosystems 24:81-91.

Harriot, V.J. and Fisk, D.A. (1988) Coral transplantation as a reef management option. Proc 6 Int. Coral Reef Symp. Vol. 2

Harris, L.E. (1988). Post-hurricane site inspection of the reef ball artificial reef submerged breakwater at Gran Dominicus beach resort near La Romana, Dominican Republic. Status report for reef ball

Maragos, J.E. (1974). Coral transplantation: a method to create preserve and manage coral reefs. Sea grant advisory report 74-03-COR-MAR-14. University of Hawaii, Honolulu.

Porter, J.W. and Meier, O.W. (1992) Quantification of loss and change in the Floridian reef coral populations. American Zoologist 32(6): 625-640.

Rinkevich, B. (2013) Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Current Opinion in Environmental Sustainability 7:28-36.

Turpin, R.K. and Bortone, S.A. (2002) Pre- and post-hurrican assesment of artificial reefs: evidence for potential use a refugia in a fishery management strategy. Journal of Marine Science 59: S74-S82.

Investigating Circadian and Circalunar Systems in Cnidarians

578764-coral-spawning-at-ningaloo-reefOur lab is particularly interested in how broadcast-spawning in corals is temporally regulated, and how solar and lunar illumination control the time at which spawning occurs.  Perhaps the most well known synchronized spawning event is the mass spawning behavior of corals on the Great Barrier Reef where over a hundred species spawn within a few hours after sunset on the nights surrounding the full moon once a year.  The time (hour and minutes) of gamete release is directly controlled by sunset time and not an entrained clock (Brady et al., 2009; Levitan et al., 2011).  However, it has been suggested that the level of lunar irradiance could provide a cue to synchronize the night of spawning in cnidarians (Vize et al., 2012).

Circadian clocks allow organisms to anticipate environmental changes with seasonal cycles of day and night.  There are many similarities between the bilaterian and the cnidarian clocks suggesting that molecular components of the endogenous clock are highly conserved (Reitzel et al., 2013).  The potential that lunar illumination may interact with the circadian clock to set the date of spawning is still open to question. To address this issue we will exploit environmental, pharmacological and genetic means to test the interdependence of circadian and circalunar timekeeping.

Corals detect light via photoreceptors that alter signal transduction pathways, controlling the levels of second messenger calcium, which is responsible for entraining light-driven circadian rhythms. When Hilton et al. (2012) treated coral larvae kept in the dark with thapsigargin, a compound that raise the level of cytoplasmic calcium, patterns of proteins shifted to a day pattern. Melatonin has been found in all multicellular animals, including the cnidarians (Anctil et al., 1991),where a circadian pattern of production was observed (Peres et al. SICB 2012). My working hypothesis is that light induced calcium inhibits melatonin production, and that low levels of melatonin production in response to the full moon set the spawning date, which occurs as night time illumination tapers off. Pharmacologically altering night time melatonin levels in coral and anemones should generate the same responses as the phase of the moon.

The field of cnidarian circadian biology provides an opportunity to test the hypothesis on roles of circadian clocks regulating physiology as well as the evolutionary conservation of circadian regulatory pathways. Spawning synchrony is a complex phenomenon dependent upon the physiological response to several environmental cues which vary both spatially and temporally. By experimentally manipulating cycles of lunar illumination and molecular pathways (using thapsigargin and melatonin) will allow us to determine whether corals display circalunar transcription cycles or if circadian cycles intersect with lunar illumination in some other fashion.  If our results demonstrate circadian and circalunar rhythms are responsible for setting the spawn date, management during lunar cycles prior to spawning will be essential. Findings could potentially encourage researchers to focus on the development of mitigation measures in areas of high risk. This may include monitoring and limiting run-off and human activities such as artificial illumination during period prior to spawning.

References:

Anctil, M., Pani, A.K., Ali, M.A. (1991) Modulation of rhythmic contractions by melatonin via cyclic GMP in the coelenterate Renilla keollikeri. J. Comp. Physiol. B 161:569-575.

Brady, A.K., Hilton, J.D., Vize, P.D. (2009) Coral spawn timing is a direct response to solar light cycles and is not an entrained circadian response. Coral Reefs 28:677-680.

Hilton, J.D., Brady, A.K., Spaho, S.A., Vize, P.D. (2012) Photoreception and signal transduction in corals: proteomic and behavioral evidence for cytoplasmic calcium as a mediator of light responsivity. Biol. Bull. 223: 291-299

Levitan, D.R., Fogarty, N.D., Jara, J., Lotterhos, K.E., Knowlton, N. (2011) Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65(5):1254-1270.

Vize, P.D. (2009). Transcriptome analysis of the circadian regulatory network in the coral Acropora millepora. Biol. Bull. 216: 131-137.

Vize, P.D., Hilton, J.D., Brady, A.K. (2012) Biological clock driven circadian transcription cycles in Acropora millepora. Proceedings of the 12th International Coral Reef Symposium.

Xu, Y., Padiath, Q.S. Shapiro, R.E., Jones, C.R., Wu, S.C., Saigoh, N.,Saigoh, K., Ptacek, L.J., Fu, Y.H. (2005) Functional consequences of a CK1 mutation causing familial advanced sleep phase syndrome. Nature 434: 640-644.