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  1. Response to G. Lente's E-Letter

    In the E-Letter by G. Lente, he criticized the use of the term turnover frequencies (TOFs) as a means to characterize the activity of a given molecular-defined catalyst in our recent Report (1) as well as in other publications. Clearly, this term has been applied in catalysis for several decades and it is commonly used and defined in catalysis textbooks (2–5). More specifically, in recent decades more than a thousand publications have appeared using this term, including publications in the journal Reaction Kinetics, Mechanisms and Catalysis for which Lente is the Managing Editor (6, 7).

    However, as Lente notes, one should be cautious using this term because it is not well-defined and, interestingly, even varies in catalysis. In homogeneous catalysis, TOF is simply the number of cycles the catalysts run divided by a period of time—indeed which should be also given by the authors (8). In heterogeneous catalysis, the TOF also depends on the active site. Finally, to complete this confusing picture, the TOF in biocatalysis is derived from the rate measured when all enzyme molecules are coordinated to a reactant, divided by the enzyme concentration (9). Comparing activities of heterogeneous catalysts is far from being trivial, given that not only the conditions (T, p, [S], [cat]) must be specified but the exact number of active sites must be taken into consideration.

    Nevertheless, although we agree with Lente that the term TOF is often used in an ill-defined form, it clearly allows for a simple quantitative comparison of different catalysts if the reaction conditions are appropriately defined. And for simple reactions such as decomposition reactions (A to B and C) exhibiting first-order kinetics, the TOF can facilitate exploring details of the reaction (10). Particularly in the chemical industry, TOFs are widely used to define the lifetime of a catalyst (11). For instance, the TOF reported by us (1) was obtained under constant conditions and observed for at least 20 hours. Thus, TOFs, as time derivatives of turnover numbers with time intervals significantly shorter than the observation time, are useful for describing the catalytic efficiency as a function of time.

    In summary, one should not use catalyst TOFs without knowing the kinetic rate of the reaction, and one must be clear about the conditions of the reaction. However, under these premises it's an additional characterization tool for characterizing catalysts even though they do not fit into the pure concept of chemical kinetics.

    Albert Boddien

    Leibniz-Institut für Katalyse e.V. an der Universität Rostock, Albert-Einstein Strasse 29a, Rostock, 18059, Germany, and Institut des Sciences et Ingénierie Chimiques, École Polytechnique Fédérale de Lausanne (EPFL), 1015, Lausanne, Switzerland.

    Dörthe Mellmann, Felix Gärtner, Ralf Jackstell, Henrik Junge, Matthias Beller

    Leibniz-Institut für Katalyse e.V. an der Universität Rostock, Albert-Einstein Strasse 29a, Rostock, 18059, Germany.

    Paul J. Dyson, Gábor Laurenczy

    Institut des Sciences et Ingénierie Chimiques, École Polytechnique Fédérale de Lausanne (EPFL), 1015, Lausanne, Switzerland.

    Ralf Ludwig

    Universität Rostock, Institut für Chemie, Abteilung Physikalische Chemie, Dr.-Lorenz-Weg 1, Rostock, 18059, Germany.

    References

    1. A. Boddien et al., Science 333, 1733 (2011).

    2. I. Chorkendorff, J. W. Niemantsverdrient in Concept of Modern Catalysis and Kinetics (Wiley-VCH, Weinheim, 2003).

    3. A. Behr, Angewandte Homogenkatalyse (Wiley-VCH Verlag, Weinheim, 2008).

    4. B. Heaton, Mechanisms in Homogeneous Catalysis (Wiley-VCH Verlag, Weinheim, 2005).

    5. M. Boudart, Chem. Rev. 95, 661 (1995).

    6. H. Zhao, L. Chou, H. Song, React. Kinet. Mech. Catal. 104, 451 (2011).

    7. G. Wang, Y. Zuo, M. Han, J. Wang, React. Kinet. Mech. Catal. 101, 443 (2010).

    8. P. W. N. M. van Leeuwen in Homogeneuos Catalysis (Kluwer Academic Publishers, Dordrecht, 2004).

    9. I. Chorkendorff, J. W. Niemantsverdrient in Concept of Modern Catalysis and Kinetics (Wiley-VCH, Weinheim, 2003).

    10. A. S. Bommarius, B. R. Riebel in Biocatalysis (Wiley-VCH, Weinheim, 2004).

    11. S. Fukuzumi, T. Kobayashi, T. Suenobu, J. Am. Chem. Soc. 132, 1496 (2010).

    Conflict of Interest:

    None declared

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  2. The Fallacy of Turnover Frequencies

    Turnover frequencies (TOFs) are frequently used in catalysis research such as that of A. Boddien et al. ("Efficient dehydrogenation of formic acid using an iron catalyst," Reports, 23 September 2011, p. 1733) and other recent Reports in Science magazine (1–4). TOFs are supposed to characterize the catalytic efficiency of a substance. It is quite interesting to note that the concept of TOF is not defined in most textbooks about chemical kinetics (5). There is a sound reason for this omission: TOFs do not make any kinetic sense. We will demonstrate this here with no intent to discredit the particular authors or to dispute the importance of the reported phenomena in the cited articles.

    TOF is usually defined as the amount of product formed in a catalytic reaction divided by the amount of the catalyst and the reaction time. This is the same as dividing a quantity resembling the formation rate of the product with the concentration of the catalyst. Here lies the first pitfall: Reaction rates are dependent on concentrations, normally including that of the substrate of a catalytic reaction as well. The usual unit of TOF is inverse time, the same as for a first-order rate constant. Alas, it is a rate constant given without any attempt to explore the rate law, and it usually is the first-order rate constant of a process that is not first order at all. A TOF cannot be used to characterize the catalytic efficiency of a substance in a reaction because it is not characteristic of a substance. It is characteristic of a single experiment in which the substance is used.

    This is already bad enough, but things get worse. The common definition given above uses a finite difference instead of a rate (a derivate). Consequently, TOFs do not only depend on the concentrations but also on the time for which the experiment was monitored. Fig. 1 of Boddien et al. shows TOF values as a function of time and initial concentrations calculated from data presented in their Report. In general, reaction rates tend to fall as time proceeds because reactants are depleted, but in this special example, there is an added complicating effect of an induction period. In any case, the authors' reported TOF value was the maximum of curve (5390) shown in Fig. 1.

    Even more dubious is the practice of using TOF values to derive activation energies. Concentration and time dependences apart, this is problematic because activation parameters are only meaningful for elementary reactions. In the example quoted here, a mechanism composed of seven steps was proposed: It should have seven sets of activation parameters instead of the single activation energy calculated in the Report.

    The science of chemical kinetics gives clear advice to all sorts of users. For those not interested in sound science: Use the highest possible substrate concentration and the shortest possible reaction time, and your turnover frequencies will look good. For others: Forget turnover frequencies—determine and report rate laws and rate constants instead.

    Gábor Lente

    Department of Inorganic and Analytical Chemistry, University of Debrecen, H-4010 Debrecen, Hungary.

    References and Notes

    1. L. Kesavan et al., Science 331, 195 (2011).

    2. M. L. Helm, M. P. Stewart, R. M. Bullock, M. R. DuBois, D. L. DuBois, Science 333, 863 (2011).

    3. D. H. Lee, K.-H. Kwon, C. S. Lee, Science 333, 1613 (2011).

    4. B. N. Zope, D. D. Hibbitts, M. Neurock, R. J. Davis, Science 330, 74 (2010).

    5. For example, one of the most authoritative textbooks on chemical kinetics is Chemical Kinetics and Reaction Mechanisms by J. H. Espenson (McGraw-Hill, New York, 2nd ed., 1995). Only turnover number is defined, but its meaning is quite different from the one used in catalysis research; it is a rate constant in the Michaelis-Menten mechanism.

    Conflict of Interest:

    None declared

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  3. Response to D. Currie's E-Letter

    D. Currie presents three main criticisms of our recent Report (1). First, he says that we focus most of our attention on the role of climate-change velocity, when in fact the strongest predictor of endemism is the extent of analogous contemporary climate. Here, our philosophical viewpoints seem fundamentally different. Currie refers to velocity and extent as competing explanations, whereas we see them as complementary, based on our expectation that patterns of endemism in amphibians, mammals, and birds would not be entirely attributable to any one explanatory variable (2, 3). We were thus not interested in eliminating all but one explanation, but rather in assessing the support for several possible explanations and the interactions among them. If models must compete against one another, we suggest comparing the model sets with and without each candidate predictor variable, as we did when calculating the summed Akaike weights for each variable (2). This gives a measure of the indispensability of each predictor variable, and shows that multiple factors, both historical and contemporary, are needed to adequately describe endemism patterns.

    Second, Currie notes that, to the extent that historical and contemporary climate variables are collinear, it is difficult to assess their relative importance; this is a general problem in comparative studies. However, there was not a strong multicollinearity between velocity and our other predictor variables (tolerance values for velocity: amphibians = 0.51, mammals = 0.49, birds = 0.52, values differ due to the use of different predictor variable subsets). As always, it is impossible to ever be certain that any particular predictor is causally connected with a response; there could always be an unmeasured collinear explanation. Thus, the best practice is to consider and test such possible alternative explanations, as we did with topographic heterogeneity and temperature anomaly. This challenge is by no means limited to our study, nor to historical explanations in particular. We also note that the within-region r values reported in our Report and quoted by Currie are global means. We argue that the local importance of velocity should vary strongly, as indeed it does [Fig. 3A (1)]. Under conditions where velocity was predicted to be most important, the local relationships do become much stronger [Fig. 3, B–D (1)].

    Finally, Currie suggests that our explanation demands numerous species extinctions since the Last Glacial Maximum (LGM). There is little evidence for massive numbers of global species extinctions during this time period, except for megafaunal extinctions, whose causes are only controversially linked to climate change (4). However, as stated in our Report (1), the spatial pattern of warming from the LGM to the current period is likely to resemble warming patterns following previous glacial periods (5, 6). The climate-change velocity used in our Report thus likely reflects a much longer period than 21,000 years, probably the whole Late Quaternary, and perhaps even beyond. Additionally, extinctions below the species level are documented in this time period (e.g., 7) and, as argued in our Report, may contribute to the observed velocity-endemism relationship.

    We do not claim that a historical explanation for endemism patterns should supplant a contemporary one. Rather, we show that adding a mechanistically based historical predictor greatly improves our ability to explain modern endemism patterns.

    B. Sandel, J.-C. Svenning

    Ecoinformatics and Biodiversity Group, Department of Bioscience, Aarhus University, Aarhus 8000 C, Denmark.

    L. Arge

    Center for Massive Data Algorithmics (MADALGO), Department of Computer Science, Aarhus University, Aarhus 8000 C, Denmark.

    B. Dalsgaard, W. J. Sutherland

    Conservation Science Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.

    R. G. Davies

    School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK.

    K. J. Gaston

    Environment and Sustainability Institute, University of Exeter, Cornwall TR10 9EZ, UK.

    References and Notes

    1. B. Sandel et al., Science 334, 660 (2011).

    2. K. P. Burnham, D. R. Anderson, Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach (Springer, New York, ed. 2, 2002).

    3. J. B. Johnson, K. S. Omland, Trends Ecol. Evol. 19, 101 (2004).

    4. A. D. Barnosky, P. L. Koch, R. S. Feranec, S. L. Wing, A. B. Shabel, Science 306, 70 (2004).

    5. R. Jansson, Proc. R. Soc. London Ser. B 270, 1515 (2003).

    6. Records of sea surface temperature from oceanic sediment cores, for example, show that the magnitude of warming following several previous glaciations are well-correlated (www.ncdc.noaa.gov/paleo/recons.html).

    7. L. Dalén et al., Proc. Natl. Acad. Sci. U.S.A. 104, 6726 (2007).

    Conflict of Interest:

    None declared

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  4. Does Climate-Change Velocity Determine Endemic Species' Survival?

    B. Sandel et al. recently argued that areas of the Earth where rates of climate change since the Last Glacial Maximum (LGM) were largest have few endemic (small-ranged) species due to elevated extinction rates ("The influence of Late Quaternary climate-change velocity on species endemism," Reports, 4 November 2011, p. 660, published online 6 October 2011). The hypothesis is intriguing. However, Sandel et al. focus on results that support their hypothesis, rather than testing it against its most obvious competitor: that endemic species occur in places where contemporary patches of climatically appropriate habitat are small. In this light, Sandel et al. found that endemism is more strongly correlated with the area of analogous contemporary climate (r2 = 0.415 - 0.538) than with climate change velocity (r2 = 0.283 - 0.385) for all taxa they studied. In multiple regressions, effect sizes for contemporary patch size were nearly twice those for historical climate change. Sandel et al. report that "models incorporating velocity were always strongly preferred over equivalent models without velocity." However, the same is true for several contemporary habitat variables. Given that historical and contemporary variables are strongly collinear, there is no reason to attribute causation to any one of them. Analyses that were restricted to 10° x 10° regions showed that "high velocity areas within regions were associated with low endemism." In fact, within regions where collinearity between climate change and contemporary climate is likely weaker, the correlation between endemism and climate change nearly disappears: r2 = 0.008 - 0.026.

    Finally, if extinctions produced the gradients of endemism observed in this study, then very large numbers of species would have to have gone extinct since the LGM. Published literature shows dramatic shifts in species' ranges as glaciers retreated, but little evidence of mass extinctions during that period (1). If, however, extinctions were only local, then species distributions simply shifted in response to shifting climate. In sum, the study presents no evidence to favor a historical explanation of endemism over a contemporary one.

    David Currie

    Biology Department, University of Ottawa, Ottawa, ON K1N 6N5, Canada.

    Reference

    1. J. W. Williams, B. N. Shuman, T. Webb, P. J. Bartlein, P. L. Leduc, Ecol. Monogr. 74, 309 (2004).

    Conflict of Interest:

    None declared

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  5. Post-Stroke Cholinergic Biomarkers

    We read with great interest the C. H. Y. Wong et al. Report of the immune suppressing innervation of hepatic iNKT cells following stroke ( "Functional innervation of hepatic iNKT cells is immunosuppressive following stroke," 7 October 2011, p. 101, published online 15 September 2011), and would like to highlight its relevance to previous predictions of a critical functional role for the changes in circulation cholinesterases in post-stroke patients.

    M. Rosas-Ballina and co-workers show in the same Science issue that action potentials originating in the vagus nerve regulate splenic T cells, which in turn produce acetylcholine (ACh) and intercept pro-inflammatory cytokine production (1). Given that ACh is rapidly and efficiently hydrolyzed by the closely related hydrolytic enzymes acetyl- and butyrylcholinesterase (AChE, BChE) (2), measuring these enzymes' activity provides an effective biomarker of the immunosuppressive power of the autonomous nervous system.

    In patients, after acute ischemic stroke, declined serum AChE activity predicts the neurological outcome, survival, and inflammatory reactions (3). Additionally, M. Sykora et al. recently reported decreases in the autonomous system's measure of baroreflex sensitivity (BRS) as an independent predictor for post-stroke infections (4), and both the BRS and serum AChE activity correlated with multiple inflammatory biomarkers. Together, these different yet interrelated approaches to estimate the cholinergic suppression of inflammation demonstrate its value for assessing the consequent risk of infection. An emerging controller of the cholinergic effect of inflammation is micro-RNA-132 (5), whose involvement with post-stroke recovery awaits further studies and might open new venues for more rigorous assessment of the post-stroke risk of survival and systematic infection and the identification of conceptually novel targets for therapeutic interference.

    Shani Shenhar-Tsarfaty

    The Institute of Life Sciences and the Edmond and Lily Safra Center of Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel, and Departments of Neurology and Internal Medicine "E", Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.

    Einor Ben Assayag

    Departments of Neurology and Internal Medicine "E", Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.

    Natan M. Bornstein, Shlomo Berliner

    Departments of Neurology and Internal Medicine "E", Tel Aviv Sourasky Medical Center, Tel Aviv, Israel, and Sackler Faculty of Medicine, Tel Aviv University, Tel-Aviv, Israel.

    Hermona Soreq

    The Institute of Life Sciences and the Edmond and Lily Safra Center of Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel.

    References

    1. M. Rosas-Ballina et al., Science 334, 98 (2011).

    2. H. Soreq, S. Seidman, Nat. Rev. Neurosci. 2, 294 (2001).

    3. E. Ben Assayag et al., Mol. Med. 16, 278 (2010).

    4. M. Sykora et al., Stroke 42, 1218 (2011).

    5. I. Shaked et al., Immunity 31, 965 (2009).

    Conflict of Interest:

    None declared

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  6. Research Funding for International Projects

    A. Cho's story "Commitments, ideology clash over research spending" (News Focus, 11 November 2011, p. 754) points out far-reaching priority choices that may have to be made by the Office of Science in a flat budget scenario that cannot accommodate ongoing domestic projects as well as the increasing contribution to the $23 billion international fusion experiment, ITER, in France.

    Of the five domestic projects discussed in the article, the Facility for Rare Isotope Beams (FRIB) project at Michigan State University (MSU) is furthest along with an approved conceptual design and a baseline–start of civil construction review planned for April 2012, enabling civil construction to start in summer 2012. Other projects in the works (NextGeneration Light Source and Long Baseline Neutrino Experiment) are in earlier stages of development and do not yet have an approved conceptual design.

    It is also worth noting that MSU is sharing about $100 million of the FRIB project cost, thus reducing the cost to the Department of Energy. In addition, MSU will contribute over $250 million in real and personal property to the future FRIB laboratory. It would be tragic if such a cost-effective opportunity to create new science would be delayed by the desire to carve out more funding for the cost increases being encountered by ITER. All of these issues are arising in the face of a constrained budget.

    Domestic projects like FRIB generate important intellectual capital in our country and contribute strongly to the education of our future engineers and scientists—they are key to our nation's future prosperity. In the shorter term, the FRIB project also brings important new work to the Michigan community, which like much of the United States, is struggling in difficult economic times.

    Lorenz A. Kull

    Retired President, Science Applications International Corporation (SAIC), Silverthorne, CO 80498, USA.

    Conflict of Interest:

    None declared

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  7. Response to B. Riegl and S. Purkis's E-Letter

    B. Riegl and S. Purkis's E-Letter on our recent Review (1) focuses on promoting assisted migration, based on a belief that local adaptation and (unassisted) migration will be insufficient to allow corals to cope with the effects of global warming and ocean acidification. We do not believe any potential approach to mitigating effects of climate change should be dismissed a priori. However, Riegl and Purkis misrepresent our view of the role of evolution in understanding the response of reefs to climate change, and falsely equate our Review (1) with a previous Review that specifically disputed the potential for evolution to play a significant role in response to climate change (2). They also criticize a model in our Review (1), based on the erroneous claim that we proposed it as a basis for management decisions, while simultaneously invoking a very similar model in support of an interventionist management program of unparalleled scale in marine habitats.

    Riegl and Purkis make the erroneous claim of our Review (1) that "the rates of change, rather than absolute magnitude, are seen as ultimately determining the impact since they allow or disallow evolution and adaptation to take place." However, rates of climate change will not "allow or disallow evolution"; they will allow or disallow persistence while some evolution inevitably occurs (3). We were careful to note that evolution will not be a panacea, and that the costs of adaptation are poorly understood for reefs, but we also review a growing body of literature showing that thermal adaptation can occur on much shorter time scales than assumed in some recent reviews of effects of climate change (2).

    Riegl and Purkis state that "Some of the optimism regarding the evolutionary capacity of corals is based on population dynamic consequences evaluated from a modified Lotka-Volterra–type model that provides survival scenarios for differently susceptible taxa." However, none of our assessment of the likely role of evolution was based on our Lotka-Volterra (LV) model. That model does not include evolution at all, and it is focused solely on ecological processes. The point of our model was to show that one cannot simply assume a priori that the most bleaching-susceptible species are the most vulnerable to climate change, even though, as we clearly state in the main text, this is the more common medium-term response to bleaching [but see (4)]. In any event, contrary to their assertion, we do not advocate using that model as a basis for management.

    Riegl and Purkis refer to an earlier Review (2) as similar to ours, stating that "Pandolfi et al. (1) and Hoegh-Guldberg et al. (2) agree that the rates of change in heat and OA [ocean acidification] will determine survivability via adaptation of corals." However, Hoegh-Guldberg et al. (2) specifically discount the potential for adaptation or evolution to play an appreciable role in coral reef response to climate change, in direct contradiction to our Review (1). In contrast, Riegl and Purkis's main recommendation (assisted migration) rests on an uncritical acceptance of the paradigm of (2), where local adaptation (and presumably unassisted migration) is assumed to be negligible over the relevant time scales, and therefore that immediate intervention using assisted migration is necessary. However, our Review (1) considers abundant evidence that corals do and will respond evolutionarily to climate change, because they are living things. The consequences of those changes under different scenarios should not be dismissed a priori; rather, they should be a major priority for future research.

    In their final section, Riegl and Purkis assert that Arabian Gulf populations are special because they provide important information about "present limits of adaptability." However, the basis for this claim is not at all clear. The Arabian Gulf populations are an example of the capacity for local adaptation to allow corals to cope with conditions that prevail in the Arabian Gulf; this pattern tells us little about the limits of adaptability. One of Riegl and Purkis's arguments for assisted migration comes in the form of environmental equivalence between present-day conditions in some places and future projected climate change conditions. However, their comparisons are problematic. For example, contrary to their assertion, current conditions in the eastern Pacific are almost the antithesis of projected conditions for most reef systems under global warming and ocean acidification. The only analogy is that of low pH, but in many other respects, such as temperature, nutrients, and seasonal variability, many reefs will likely experience the opposite environmental effects.

    We believe that Riegl and Purkis provide an overly optimistic view of assisted migration, advocating the introduction of warm-adapted strains of coral hosts and symbionts to a place that is cooler to assist with adaptation, and fail to acknowledge some important potential problems. First, locally adapted strains are likely to suffer higher mortality when they are moved to very different conditions—local adaptation is a product of directional selection such that adapting to one environment is likely to reduce performance in another environment (5, 6). Indeed, the weight of evidence suggests that tolerance (i.e., generalist strategies) comes at the expense of performance in a particular environment: the-jack-of-all-trades-is-master-of-none paradigm (3, 7). Given that Arabian Gulf corals are likely to be adapted to idiosyncrasies of the Arabian Gulf environment, such as extreme fluctuations in temperature and salinity, they are likely to have low fitness in the Indo-Pacific, relative to resident populations.

    Second, if the transplant did succeed, Riegl and Purkis do not acknowledge the potentially negative consequences of interbreeding between introduced and native individuals. Introducing individuals with very different genetic backgrounds could disrupt co-adapted gene complexes and cause "outbreeding depression," a situation in which grandchildren from crosses between individuals from different populations have lower fitness than those from the same population (8). A successful translocation would introduce some migration load into the resident population, reducing its viability to some degree (9). Whereas increasing genetic variability in a population, and increasing the proportion of adapted genotypes might facilitate rapid adaptation, mixing very different populations can lead to unexpected and deleterious outcomes (10). There is a rich and complex literature that wrestles with the consequences of mixing locally adapted populations (8–10), but these issues are not considered in the E-Letter.

    We are surprised that Riegl and Purkis criticize our LV model for the potential hazards of applying it to management (something we don't do, or recommend), then argue for a global-scale biological introduction experiment based upon simulations from a single model (11). Importantly, their model incorporates species interactions of LV form, like our model, but unlike our model, considers only a single set of parameter values. Their model assumes no evolution, interbreeding, or exchange of symbionts between introduced and native populations. It also ignores the well-known dependence of growth and metabolism on temperature, assuming that Gulf corals will retain the same demographic rates after being transported to a new environment whose temperature mean and variance is considerably different from the environment to which they have adapted. Moreover, potential risks of biological introductions, such as the introduction of novel coral pathogens associated with Gulf corals, are not considered.

    We are not opposed to research into assisted migration as a potential, last-ditch response to climate change, particularly if the rate of warming is such that a rapid decline in coral cover occurs. However, in our view, the standard of evidence required, including experimental work on the consequences of cross-infection of symbionts, interbreeding, the physiological performance of Gulf corals under several environmental conditions that prevail elsewhere (not just temperature), and an assessment of the risk of co-introduction of microbial or viral pathogens to which native coral populations may be poorly adapted, should be considerably higher than that suggested in the E-Letter and (11).

    John M. Pandolfi

    Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies, St. Lucia, QLD 4072, Australia, and School of Biological Sciences, University of Queensland, St. Lucia, QLD 4072, Australia.

    Sean R. Connolly

    Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies and School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4011, Australia.

    Dustin J. Marshall

    School of Biological Sciences, University of Queensland, St. Lucia, QLD 4072, Australia.

    Anne L. Cohen

    Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

    References

    1. J. M. Pandolfi, S. R. Connolly, D. J. Marshall, A. L. Cohen, Science 333, 418 (2011).

    2. O. Hoegh-Guldberg et al., Science 318, 1737 (2007).

    3. R. Gomulkiewicz, M. Kirkpatrick, Evolution 46, 390 (1992).

    4. R. van Woesik, K. Sakai, A. Ganase, Y. Loya, Mar. Ecol. Prog. Ser. 434, 67 (2011).

    5. D. J. Marshall, K. Monro, M. Bode, M. J. Keough, S. Swearer, Ecol. Lett. 13, 128 (2010).

    6. J. G. Kingsolver, Am. Nat. 174, 755 (2009).

    7. M. Lynch, W. Gabriel, Am. Nat. 129, 283 (1987).

    8. M. Lynch, Evolution 45, 622 (1991).

    9. O. Rance, M. Kirkpatrick, Evolution 55, 1520 2001).

    10. P. Nosil, D. J. Funk, D. Ortiz-Barrientos, Mol. Ecol. 18, 375 (2009).

    11. B. M. Riegl, S. J. Purkis, A. S. Al-Cibahy, M. A. Abdel-Moati, O. Hoegh-Guldberg, PLoS One 6, e24802 (2011); 10.1371/journal.pone.0024802.

    Conflict of Interest:

    None declared

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  8. Methods to Preserve Coral Reef Futures

    J. M. Pandolfi et al. project reef futures and provide management considerations for coral reefs with the aim of assisting their survival ("Projecting coral reef futures under global warming and ocean acidification," Review, 22 July 2011, p. 418). They believe that the threats posed from ocean acidification (OA) and ocean warming can, at least to some extent, be balanced by adaptation and evolution. While we agree with their findings, we warn that "passive" management, seeking purely to minimize anthropogenic impacts is likely to be insufficient, given the local and large-scale inevitable pressures created by an unabatedly expanding human population. We argue that "active" management using assisted migration of holobionts adapted to the known extremes in temperature and acidity should be considered. This could help avoid their own local extinction due to ever-increasing habitat degradation in their original range, could provide potentially robust stock for denuded areas, and assist in shortening the time needed for adaptation of stocks yet naïve to such extremes.

    Pandolfi and colleagues review the threats posed to coral reefs by increased ocean heat content and acidification and point to the role of evolution in buffering populations. Evidence from the fossil record is provided that in some periods with much higher extremes, coral growth could nonetheless persist. In agreement with an earlier, similar Review (1), the rates of change, rather than absolute magnitude, are seen as ultimately determining the impact since they allow or disallow evolution and adaptation to take place.

    Some of the optimism regarding the evolutionary capacity of corals is based on population dynamic consequences evaluated from a modified Lotka-Volterra–type model that provides survival scenarios for differently susceptible taxa. An analytical solution of the equations shows that, at least theoretically, it is possible that bleaching-susceptible species suffering severe population reduction may rebound due to reduced carrying-capacity limitations. However, the theoretically beneficial effect of increased space availability is in nature frequently negated by several factors that act non-linearly and are difficult to predict, let alone model. Disease outbreaks that often preferentially disadvantage the most bleaching-sensitive taxa are known to follow bleaching events (2), predator concentration can lead to significant post-bleaching losses (3), and coral settlement processes (implicit in the model's parameter r) are often characterized by spatial and temporal stochasticity, making any sort of analytical solution or prediction difficult. Competition with other benthos than corals (i.e., algae) can rapidly arise in the immediate aftermath of coral mortality, adding to the unpredictability of settlement success (parameter r). These factors were not included in the presented model, and are difficult to solve analytically, but their importance has been demonstrated using simulations based on similar LV-based models that did include these variables and their importance was verified by field monitoring (4). Reliance on such models for management purposes bears the danger of unforeseen surprises, precisely because some key parameters may not be included or impossible to model. Unfortunately already the optimistic outlook promised by Pandolfi et al. does not seem to be borne out by the majority of bleaching-sensitive (especially Acropora) populations that continue to decline, albeit at highly variable rates across the world's oceans (5).

    The management considerations by Pandolfi et al. focus on slowing the rate of climate change and reducing anthropogenic impacts such as fishing and coastal developments. It is likely that such an approach alone might not give corals enough time or space to survive in enough numbers to adapt, even if they prove as adaptable as the Review suggests. This is due to the unabated upward trends in human population growth (6), atmospheric heat content, and OA (2). Most of the world's coral reefs are situated in areas with maximum human population growth and therefore impending important expansion of extractive and development-related local pressures. The projected increases in human population also cast doubt on whether the emission goals can be reached at all. We suggest taking a more aggressive approach to coral reef management and beginning to consider assisting corals in speeding up evolution. Without an aggressive, hands-on approach to wildlife management most big, charismatic mammals would today be extinct. We believe that coral reefs deserve similar attention and action.

    Important gradients in stress levels, and therefore local adaptation of the coral holobiont exist on coral reefs across today’s oceans. Some coral populations in peripheral seas (or extreme environments such as tide pools) live today in environments that climate change projections expect for the tropical ocean in about a century. The thermal environment in today’s Arabian Gulf is equal to IPCC predictions for 2099 (7), and acidity in today’s eastern Pacific allows a glimpse into the future (8). These coral populations provide important information about the present limits of adaptability and could also help to either speed up adaptation in populations that have yet to experience such extremes, or be used to repopulate reef areas that have recently been denuded due to unprecedented environmental extremes. For example, the hot climate of the Arabian Gulf has over the past 6 ky selected for uniquely heat-adapted local strains of corals with higher bleaching thresholds and far longer exposure tolerance to extreme heat [>3 months of exposure tolerance to temperatures that would kill all known tropical corals (7)]. Population models have shown that introducing these corals to bleaching-damaged areas could lead to their complete dominance within ~20 years without requiring them to change their temperature adaptation, whereas the local strains would go extinct unless they adapt. These corals could survive the next 100 years of climate change in the tropics, and kick-start the region's adaptation and evolution, thereby providing genetic material selected for heat resistance over 6 ky. However, unless drastic action is taken soon, they may be lost in their natural habitat. In the Gulf, extreme heat events that stress corals beyond their tolerance are becoming increasingly common and have led to significant population reduction (7). Additionally, local development practices have altered ~40% of the Gulf's coastline and destroyed a similar percentage of coral reefs (9). The outlook for these uniquely adapted holobionts is bleak. We therefore contend that these corals should be considered for assisted migration from their endangered, extreme habitats to the tropical Indo-Pacific.What would amount to ex-situ conservation for the moved populations, could amount to in-situ conservation of the recipient populations, if the new genetic material assists in adaptation to higher environmental extremes.

    Both Pandolfi et al. and Hoegh-Guldberg et al. (1) agree that the rates of change in heat and OA will determine survivability via adaptation of corals. We contend that the rate of adaptation might also increase to match that of environmental degradation by carefully selecting coral populations from extreme environments and introducing them to areas that are only now beginning to experience such extremes. Since the species at the edge of a coral reef distribution are the same as those in the center (the Gulf coral fauna is, for example, a 10% subset of the typical Indo-Pacific reef fauna, with only three endemic species that should not be considered for relocation), the genetic integrity of species could conceivably be maintained despite assisted migration. Especially if denuded areas are chosen for repopulation by migrated stocks, the risks for genetic contamination can be reduced further.

    While hotly contested and anathema to some, intensive population management of rare species has a long and successful history in forestry and wildlife management and is in wide use. We believe that it should at least be critically evaluated as one of many strategies to ensure or enhance the survival of coral reefs.

    Bernhard Riegl and Sam Purkis

    National Coral Reef Institute, Nova Southeastern University, Dania Beach, Florida 33004, USA.

    References

    1. O. Hoegh-Guldberg et al., Science 318, 1737 (2007).

    2. J. Bruno et al., PLoS Biol. 5(6), e124 (2007); 10.1371/journal.pbio.0050124.

    3. P. Glynn, Coral Reefs 12, 1 (1993).

    4. B. Riegl et al., Mar. Pollution Bull. 58, 24 (2009).

    5. K. E. Carpenter et al., Science 321, 560 (2008).

    6. L. Roberts, Science 333, 540 (2011).

    7. B. Riegl et al., PLoS One 6(9), e24802 (2011); 10.1371/journal.pone.0024802.

    8. D. Manzello et al., PNAS 105(3), 10450 (2008).

    9. C. Sheppard et al, Mar. Pollution Bull. 60, 13 (2010).

    Conflict of Interest:

    None declared

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  9. Biological Errors

    The Perspective by M. A. Norell contains two biological errors—one major, one minor ("Fossilized feathers," 16 September 2011, p. 1590).

    The first is Norell's statement that melanosomes are "specialized cells." They are not. Melanosomes are intracellular pigment granules assembled in the cytoplasm of melanocytes. The latter are pigment cells derived developmentally from the neural crest. This fundamental error colors Norell's next several paragraphs and leaves an erroneous impression of the nature of the very significant work by R. A. Wogelius et al. (1) (with whom I have no connection). Melanosomes are actively transferred from melanocytes to differentiating keratinocytes of the skin, including feathers. The surviving remnants of melanosomes are what Wogelius et al. have analyzed.

    The second error is Norell's characterization of one melanosome category as "phenomelanosomes." He uses this term in reference to several publications, and it is wrong. The term is "pheomelanosome." It refers to the nature of the melanin assembled within it.

    John R. Coleman

    Brown University, Providence, RI 02912, USA.

    Reference

    1. R. A. Wogelius et al., Science 333, 1622 (2011).

    Conflict of Interest:

    None declared

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  10. Doubts About a Serial Founder-Effect Model of Language Expansion

    Research on human language published in Science usually relies on computational methods, and is often criticized by linguists. We attempt to explain why this is the case with Q. D. Atkinson's recent Report ("Phonemic diversity supports a serial founder–effect model of language expansion from Africa," 15 April 2011, p. 346).

    Atkinson shows a negative correlation between the number of phonemes in a language and its distance from Africa, and, assuming that phonemic diversity is subject to a serial founder effect, claims that this finding supports an African origin of language.

    Linguists have trouble accepting Atkinson's conclusion for two main reasons. First, they view the idea that a founder effect exists in language transmission to be an audacious hypothesis, at best. Most of the evidence Atkinson provides of its existence is circumstantial or highly speculative, the only exception being the positive correlation between modern population sizes and number of phonemes in modern languages. The correlation, however, does not necessarily imply a causal link, especially since it is unknown whether it held true in the past when population numbers were dramatically different. Atkinson does not offer any plausible mechanism for the disappearance of phonemes when the founder population splits off the parent one. Moreover, the founder-effect assumption contradicts the hypothesis that small languages should be more complex than large ones, which benefits from the support of solid theoretical reasoning (1), and some statistical corroboration as well (2).

    Second, linguists worry that Atkinson's data and methods might be subject to various biases. As regards the data, the traditions and quality of grammatical description vary among scholars of different linguistic areas. As regards the methods, it is unclear whether weights assigned by Atkinson to different components of phonemic diversity (consonants, vowels, tones) are appropriate.

    Aleksandrs Berdicevskis

    Department of Foreign Languages, University of Bergen, Bergen, 5020, Norway.

    Alexander Ch. Piperski

    Lomonosov Moscow State University, Moscow, 119991, Russia.

    References

    1. A. Wray, G. Grace, Lingua 117, 543 (2007).

    2. G. Lupyan, R. Dale, PLoS ONE 5, e8559 (2010); 10.1371/journal.pone.0008559.

    Conflict of Interest:

    None declared

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