Not all that glitters is gold in the science supporting shark conservation

The international exploitation of elasmobranch species (sharks and rays) has increased consistently over recent decades, mainly to satisfy the Asian market demand for shark fin.

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Moreover, shark species are generally characterized by high levels of bycatch in commercial fishery and this bycatch issue, most of the time, has been managed ineffectively. Long story short, the conservation status of several large and medium-sized shark species has been a recent matter of concern, which led to several conservation organizations calling for national governments to take actions to limit or to close directed commercial fisheries on some shark species. Overall, there are some preliminary successes, such as the listing of five shark species (great hammerhead -Sphyrna mokarran; scalloped hammerhead – Sphyrna lewini; smooth hammerhead – Sphyrna zigaena; oceanic whitetip – Carcharhinus longimanus; and porbeagle – Lamna nasus) and manta rays (Mantaspp.) into the Appendix II of CITES in 2013. This listing requires for each country to provide a certificate of sustainability for the fishery on those species to permit their export. Still, this is not necessarily a regulation forcing fishery closures, but it can hopefully motivate national governments to devote more effort for the conservation of sharks, while providing their sustainable exploitation. I want to point out that the productivity of shark varies by species, and I believe that by taking into consideration the life history of the species at hand and the fishery characteristics, there are good examples of shark fisheries that can be sustainable (e.g. spiny dogfish in the U.S. North Atlantic).

The sustainability of a fishery is measured by parameters (called reference points) drawn from stock assessments conducted by national or regional fishery authorities. These stock assessments, which are fishery-independent, need to be conducted for a sufficiently long time so to analyze changes in species abundance over time. In turn, these changes might suggest excessive fishery exploitation for a given species. However, such sampling effort can be prohibitively expensive for the majority of countries, which forces fishery managers to often rely on other sources of available information, collectively known as fishery-dependent surveys. For example, quantitative information on fish catch can be collected from fishermen logbooks or from catch data provided by each government to international agencies and boards, such as FAO. Although this type of data represents an important source of information for fishery managers, the issue originates in “what” data are used for the analysis (i.e. the criteria used to choose the data),and “how” they are analyzed (i.e. the specific statistics used to analyze the data).

The discussion for the “what” and “how” in the analysis of fishery-dependent data might be particularly controversial for hot-topic species, such as sharks, that can capture media and people attention more easily than for other, less charismatic species. In light of that, the scientific community should provide good stewardship on the conservation status of natural resources by producing and disseminating results from reliable, unbiased, and scientifically accountable studies. Recently, a heated dispute flared up in the scientific realm of fishery management, which Ray Hilborn (2007), professor at the School of Aquatic and Fisheries Science at the University of Washington, USA described as a “Great Divide” between marine ecologists and fishery scientists. Marine ecologists, who are mainly academic marine scientists and statisticians, claim that fishery managers have failed in fully recognizing the importance of ecological aspects when managing fishing resources and propose the introduction of marine protected areas (MPAs) as the primary management tool to maintain healthy ecosystems and to rebuild overfished stocks. On the contrary, fishery scientists, who are represented by a group of fishery managers working in fishery agencies and also many marine scientists from academia, believe that fisheries management are also represented by successful stories for which we can get valuable knowledge on how to develop effective strategies to stop overfishing and to maintain sustainable fisheries, mainly by working within fishery governance systems.

The dispute has being revolving around shark species conservation as well, after a series of controversial papers were published by a group of marine ecologists from the Department of Biology at Dalhousie University in Halifax, Canada. Two of these papers, which were published by Baum et al. (2003) and Baum and Myers (2004), deal specifically with shark species, and claimed the occurrence of recent alarming collapses for the population of several shark species in the northwest Atlantic Ocean (Baum et al. 2003) and in the Gulf of Mexico (Baum and Myers 2004).For the purpose of this blog I will focus my discussion just on the first of these two papers, using it as a good example of what I mean when I say that the scientific community should be at the forefront of good stewardship of shark conservation by providing reliable, unbiased, and scientifically accountable studies. From the tone of my words you might have already recognized my disagreement with conclusions provided by these two papers. With this, however, I don’t intend to say that shark populations are not in danger and that overfishing for some species is not occurring in several coastal and pelagic areas around the world. At the incipit of this blog I clearly said that increased fishing pressures on shark species is occurring and I believe that it is unquestionably affecting the conservation status of several species, but not for all species and not for all marine regions. What I am personally concerned about are the consequences for possible wrong overestimations of this scenario, which I believe is the case for the conclusions provided by these two papers. However, as my grandmother was used to say: “variety is the spice of life”; and everybody in the scientific community has the right to maintain his/her beliefs and opinions until, hopefully, somebody will be able to challenge them from a scientific standpoint.

The reason for my skepticism on Baum et al. (2003) conclusions is based on a series of scientifically sound critics provided by another paper by Burgess et al. (2005) that was written right after the former paper was published. Now, due to space restrictions, I am not going to describe in details each single aspect of this paper for which I disagree, as this would be a merely repetition of concepts already brilliantly described in the original rebuttal paper. Therefore, I limit myself to report the list of argumentations provided by Burgess et al. (2005) to claim that conclusions reached by Baum et al. (2003) are most likely inconsistent and overstated, which is based on six main points: 1) the analyses were based on a limited number of data sets; 2) the data sets used for the analysis were inadequate to describe the status of all shark populations in the study area; 3) there existed available data sets that could have produced different conclusions that were not utilized; 4) other factors that could have potentially biased the results were not considered by authors; 5) no alternative hypothesis to explain other potential causes of the perceived declines in abundance were discussed; and 6) the authors did not consider results from other available stock assessments suggesting, in several cases, that the conservation status of some shark species was considerably healthier than asserted.

That being said, I invite you to first read the original paper by Baum et al. (2003), the rebuttal by Burgess et al. (2005), and also the answer to this rebuttal provided by Baum et al. (2005) to defend their conclusions.Furthermore, for the sake of completeness, I also invite you to read another paper questioning some of Baum and colleagues’ conclusions that was written by Aires-da-Silva et al. (2008). Then, after having plunged yourself into what I hope was a genuine and impartial “analytical and critical” reading of these papers, you should be prepared for what I am trying to explain you in the last part of this blog.

For those of you who still consider conclusions by Baum et al. (2003) correct and robust, I guess I can’t add anything more to convince you of the contrary. Again, constructive discussion is one of the milestones of science, and I believe that critical thinking should be always encouraged and generated within this discussion process. This is particularly true for science, which is inherently affected by some degree of uncertainty for which both marine ecologists and fishery managers have to cope with. For those of you who were convinced by arguments provided by Burgess et al. (2005), I would like to put the discussion further and let you notice that this rebuttal paper was not published in the same scientific peer-reviewed journal of Baum et al. (2003). The majority of papers coming from the Dalhousie University scientific group were published in Science and Nature, which are by far the most influential journals within the scientific community. The rebuttal by Burgess and colleagues was instead published in Fisheries, which is a journal of the American Fisheries Society with a significantly lower impact factor than Science or Nature. At this point you might ask yourself why the authors did not think about try to publish their rebuttal directly on Science. Well, the truth is that they tried, but the editor considered these argumentations likely inconsistent or, perhaps, not of sufficient merit or interest to be published. This might surprises you, but it really should not. In fact, I noticed that it is not that uncommon for high-impact scientific journals to publish quite disputable papers, and I suspect this is mainly because of the species or topic discussed and the controversy that might stem from it. In fact, a recent paper by Banobi et al. (2011) was able to raise questions about the effectiveness of the whole rebuttal process for some of these highly quoted papers. This paper considered seven original studies on fisheries, of which one was published in Nature and six in Science, including the one by Baum and colleagues. Considering that each of these seven papers was followed by at least one rebuttal paper describing substantial flaws in these original studies, the authors examined how successful these rebuttals were at changing or correcting scientific perceptions of the original articles. Their results indicated that in the majority of cases rebuttals were not able to change scientific perceptions on the original papers, which I personally find extremely worrisome. Based on their results the authors suggest, and agree with them, that most scientists tend to accept a paper’s conclusions uncritically, which I believe has become a particularly common practice for articles published in Science and Nature. The punch line is that if an article is published on these two journals there is a high chance for scientists taking for granted that conclusions are scientifically correct and meaningful. I personally found this result alarming because these two journals have a higher chance to influence the scientific community, society and, most of all, the mind of the new generation of scientists joining the so called Great Divide compared to other scientific journals. Therefore, if distortion of the truth is provided and published, there is probably no such filter that could avoid dissemination of biased and unaccountable study results. In this regard, it is important to highlight that although Baum and colleagues, as much as any other scientist, have the right to submit a manuscript if they are genuinely convinced of the robustness, scientific accountability, and appropriateness of their conclusions, it is a mandatory requirement of the editor of the journal and reviewers to carefully check for the good scientific quality of the manuscript during the reviewing process. Perhaps, this is something that scientific journals with high-impact factors have not being fully provided, which can dangerously hamper the effective dissemination of scientific truth. Luckily enough, scrupulous scientists still exists and thanks to them some of these questionable papers were challenged on the ground of science, which is a vital aspect for the scientific debate and the fishery management process that can originate from this debate. For instance, after repeated criticisms for the type of data used and analysis performed, Baum et al. (2010) were finally convinced to examine changes in abundance of shark populations in the Northwest Atlantic by using more reliable data sources than fisherman logbooks, such as the data from the U.S. Atlantic pelagic longline fishery’s observer monitoring program. Their new conclusions indicated that for some species the estimated rate of decline were less than those previously reported in their 2003’s article, also pointing at some inherent difficulties in interpreting results from complex generalized linear models analysis. Although I believe this should be considered an important step toward enhancing dissemination of good science, I am still wondering why this new re-analysis of shark abundances was not published in Science and ended up instead in being published in Fisheries Research, which is still a highly cited scientific journals but definitely does not hold an impact factor as high as the one for Science. Maybe that Science is more interested in publishing articles that can more easily attract attention from the media, press, and the public?

The case for the conservation of white shark (Carcharodon carcharias) in this sense is an excellent example. The study by Baum et al. (2003) in the Northwest Atlantic concluded also that, among the shark species whose abundance have declined by more than 75% over the study period, white shark was one of those species.The fact that this paper was published in Science gave it unquestionably more attention in the scientific community and in the media, potentially increasing the chances that this article could influence fishery management decisions pertinent to the conservation of white sharks on a global scale. In fact, this paper was used to prove alarming decreases in white shark abundance in order to support the listing of the species in Appendix II of CITES in 2004 (CoP13 Prop. 32. 2004). Listing in CITES is based on quantitative criteria. Therefore, overestimation of decline can potentially bias the listing process by incorrectly shifting thresholds to the level for which species meet the criteria for listing. In the case of white sharks, it is worth noting that the members of the FAO Expert Advisory Panel who were charged to review the proposal for listing opportunely noticed that, based on arguments that were similar to those provided by Burgess et al. (2005) one year later, the estimated decline described by Baum and colleagues was most likely too large, convincing them to assign a reliability index of zero to this estimate of decline (FAO 2004). Nevertheless, conclusions from this study may have influenced the listing process at some level. In fact, the species was listed in Appendix II although several aspects of this listing process are still now considered particularly controversial. Both the FAO Expert Advisory Panel and the CITES Secretariat were not able to confirm or exclude the possibility that white shark met the criteria for a listing in Appendix II. However, the CITES Secretariat recommended the species to be listed, although concluding that this recommendation was extraordinarily cautious and based on evidence that white sharks are naturally rare in nature and are characterized by life histories that make them particularly susceptible to overfishing. For those of you interested in the whole controversy about the CITES listing on white shark I will suggest you to read the article by Gehring and Ruffing (2008), which provides a very good analysis of potential controversies affecting the CITES listing process.

That being said, it is clear to me that Baum et al. (2003) conclusions on white shark declines might have influenced the decision making process to conserve the species. Now, I am a shark researcher and a conservationist, so I could not be happier to know that shark species are included in conservation management measures at international level. However, such management measures should be based on reliable and accountable scientific results, otherwise there will be serious consequences affecting the whole conservation process for natural resources. This means that science should not be necessarily the armed wing of conservation, but instead it should be the guarantor for dissemination of the truth. It might really be that white shark populations have being severely depleted in some regions of the world and that fishery managers and national governments should devote more effort in evaluating the existence of these scenario exploitations, but still on an indisputable and unbiased scientific basis. If the dissemination of the truth is not provided, the consequence would be the shift of economic resources, effort, and burden on developing and maintaining conservation measures for the species needing management measures less urgently. I believe that for elasmobranch this is particularly true for large charismatic species, which are not necessarily the one in need for more serious attention; although this does not mean that fishery managers should all of a sudden disregard those species or start to believe that they are not threatened by extinction. However, a recent study by Dulvy et al. (2013) suggests that the elasmobranch species more likely threated by the highest extinction risks are those living in coastal, shallow waters, such as sawfishes, rays and less iconic small-medium sized sharks, mainly because they are more prone to fishery exploitation and bycatch compared to larger offshore species. Consequently, within the elasmobranch group those species should be assigned the highest priorities for conservation measures. Of course, we all wish that sharks and rays may be effectively protected and their habitat preserved, but we live in a world of limiting funding for which effective conservation efforts and measures should be seriously prioritized, and the criteria should always be good science.

In summary, I hope that by reading this blog I was able to convey three main key messages:

1. The fact that a study was published in a scientific peer-reviewed journal doesn’t necessarily mean that its conclusions are true or set in stone. You should always read a paper using YOUR critical thinking.
2. The fact that a study was published in Science or Nature doesn’t imply that its conclusions should be regarded at a higher level of consideration compared to other studies published in journals with a lower impact factors. Again, use YOUR critical thinking and judgment.
3. Science should not be a matter of self-recognition, but only the search for the truth.

To expand further on the controversial aspects of scientific papers published by the Dalhousie University’s group I invite the reader to look at the following web-page, which collects lot of good information about the exaggerated claims of collapse that those papers reported and various responses to these same papers http://www.soest.hawaii.edu/PFRP/large_pelagics/large_pelagic_predators.html

Literature cited:
Aires-da-Silva A.M., Hoey J.J., Gallucci V.F. (2008) A Historical Index of Abundance for the Blue Shark (Prionaceglauca) in the Western North Atlantic.Fisheries Research92: 41-52.

Banobi J.A., Branch T.A., Hilborn R. (2011) Do rebuttals affect future science? Ecosphere 2(3): 1-11.

Baum J.K., Myers R.A., Kehler D.G., Worm B., Harley S.J., Doherty P.A. (2003) Collapse and Conservation of Shark Populations in the Northwest Atlantic. Science 299: 389-392.

Baum J.K., Myers R.A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters7: 135-145.

Baum J.K., Kehler D., Myers, R.A. (2005) Robust Estimates of Decline for Pelagic Shark Populations in the Northwest Atlantic and gulf of Mexico. Fisheries 30(10): 27-29.

Burgess G.H., Beerkircher L.R., Cailliet G.M., Carlson J.K., Cortés E., Goldman K.J., Grubbs R.D., Musick J.A., Musyl M.K., Simpfendorfer C.A. (2005) Is the Collapse of Shark Populations in the Northwest Atlantic Ocean and Gulf of Mexico Real? Fisheries 30(10): 19-26.

CITES(2004) Conference of the Parties to the Convention 2004: Proposal 32.Convention on International Trade in Endangered Species of Wild Fauna and Flora. Available at http://www.cites.org/eng/cop/13/prop/E13-P32.pdf

CoP13 Prop. 32. 2004. Conference of the Parties to the Convention 2004: Proposal 32. Convention on International Trade in Endangered Species of Wild Fauna and Flora. Available at http://www.cites.org/eng/cop/13/prop/E13-P32.pdf

Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2013) Extinction Risk and Conservation of the World’s Sharks and Rays. eLife 2014;3:e00590. DOI: 10.7554/eLife.00590

FAO (2004) Report of the FAO Ad Hoc Expert Advisory Panel for the Assessment of Proposals to Amend Appendices I and II of CITES Concerning Commercially-exploited Aquatic Species. Rome, 13-16 July 2004. FAO Fisheries Report No. 748. Rome, FAO, 51 p.

Gehring T., Ruffing E. (2008) When Arguments Prevail Over Power: the CITES Procedure for the Listing of Endangered Species. Global Environmental Politics 8: 123-148.

Hilborn R. (2007) Moving to Sustainability by Learning from Successful Fisheries.Ambio 36(4): 296-303.