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Local buffer mechanisms for population persistence

2023 / https://doi.org/10.1016/j.tree.2023.06.006 / Trends in Ecology & Evolution, Month 2023

Assessing and predicting the persistence of populations is essential for the conservation and control of species. Here, we argue that local mechanisms require a better conceptual synthesis to facilitate a more holistic consideration along with regional mechanisms known from metapopulation theory. We summarise the evidence for local buffer mechanisms along with their capacities and emphasise the need to include multiple buffer mechanisms in studies of population persistence. We propose an accessible framework for local buffer mechanisms that distinguishes between damping (reducing fluctuations in population size) and repelling (reducing population declines) mechanisms. We highlight opportunities for empirical and modelling studies to investigate the interactions and capacities of buffer mechanisms to facilitate better ecological understanding in times of ecological upheaval.

Long transient response of vegetation dynamics after four millennia of anthropogenic impacts in an island ecosystem

2023 / https://doi.org/10.1111/gcb.16363 / Glob Change Biol. 2022;28:6318–6332.

Factors affecting survival and dispersal of the comma butterfly in a high mountain deciduous forest habitat

2022 / htpps://doi.org/10.32800/abc.2023.46.0001 / Animal Biodiversity and Conservation 46(1): 1-11

Daniel Oro, Constantino Stefanescu, Marina Alba, José Capitán, Andreu Ubach, Meritxell Genovart

Interspecific synchrony on breeding performance and the role of anthropogenic food subsidies

2022 / https://doi.org/10.1371/journal.pone.0275569 / PloS one 17, 10, e0275569

Ana Payo-Payo, José-Manuel Igual, Ana Sanz-Aguilar, Enric Real, Meritxell Genovart, Daniel Oro, Giacomo Tavecchia

Inferring the age of breeders from easily measurable variables

2022 / https://doi.org/10.1038/s41598-022-19381-4 / Scientific reports 12 (1), 1-9

Meritxell Genovart, Katarina Klementisová, Daniel Oro, Pol Fernández-López, Albert Bertolero, Frederic Bartumeus

The first genome of the Balearic shearwater (Puffinus mauretanicus) provides a valuable resource for conservation genomics and sheds light on adaptation to a pelagic lifestyle

2022 / https://doi.org/10.1093/gbe/evac067 / Genome Biology and Evolution 14, 5, evac067

Cristian Cuevas-Caballé, Joan Ferrer Obiol, Joel Vizueta, Meritxell Genovart, Jacob Gonzalez-Solís, Marta Riutort, Julio Rozas

Sharp decreases in survival probabilities in the long-finned pilot whales in Strait of Gibraltar

2022 / https://doi.org/10.1007/s00227-022-04030-1 / Marine Biology 169 (4), 1-9

Miquel Pons, Renaud De Stephanis, Philippe Verborgh, Meritxell Genovart.

Short-term gain, long-term loss: how a widely-used conservation tool could further threaten sea turtles

2022 / https://doi.org/10.1016/j.biocon.2021.109260 Get rights and content Abstract Sea turtles nest on tropical and subtropical beaches, where developmental success of egg clutches depends on nest temperature. Higher nest temperatures increase embryo and hatchling mortalities and produce female hatchlings. Nest shading has been used on some beaches to reduce nest temperatures, and thereby increase number of hatchlings and reduce female-biased sex ratios. We modeled short- and long-term effects of reducing mean nest temperatures on a leatherback turtle (Dermochelys coriacea) population for which the effect of temperature on sex ratios and emergence success (# hatchlings emerged/ # eggs) is well-established. We simulated mean nest temperature reductions of −0.5 °C, −1 °C, −1.5 °C and −2 °C in relation to current mean (30.4 °C) and projected population responses over 100 years. Additionally, we run climate change simulations of +0.5 °C, +1.0 °C and +2.0 °C to assess if shading could be needed after passing a certain threshold. Emergence success increased with reduced nest temperatures. However, lowering nest temperatures ultimately caused long-term declines in number of nesting females and total population size, because the number of female hatchlings was reduced. Because hatcheries are a widely-used conservation tool, caution must be used to avoid reducing the number of female hatchlings by lowering nest temperatures. Nest cooling may only be needed under critically low hatchling production and extremely biased female sex ratios that we only found at +2.0 °C. If nest shading is to be used, it should be applied strategically to optimize hatchling production with natural sex ratios to achieve both short-term conservation goals and long-term population sustainability. Introduction Climate change is among the main threats sea turtles are likely to face in the near future (Fish et al., 2005; Hawkes et al., 2007; Jensen et al., 2018). Global air temperatures are projected to increase from 1.5 °C to 2 °C above pre-industrial levels by the end of the 21st century, with a likely increase in the frequency of high-temperature extreme events (Collins et al., 2013). High nest temperatures increase the rate of embryonic mortality during development and hatchling mortality during emergence (Santidrián Tomillo et al., 2009; Valverde et al., 2012). In sea turtles, typical incubation periods range between 43 and 94 days for temperatures between 24 °C and 33 °C, but with differences among species (Booth, 2017). Maximum temperatures that allow development are ~35 °C (Howard et al., 2014), although eggs from some species (e.g., leatherback (Dermochelys coriacea) and olive ridley turtles (Lepidochelys olivacea)) are less tolerant to high temperatures than others (e.g., green turtles (Chelonia mydas) and loggerhead turtles (Caretta caretta)) (Howard et al., 2014; Santidrián Tomillo et al., 2020). Nest temperatures during the middle third of development determine sex in sea turtles (Morreale et al., 1982; Yntema and Mrosovsky, 1982). During that thermosensitive period, higher temperatures produce a higher proportion of female hatchlings, whereas male gonads develop at lower temperatures (Standora and Spotila, 1985), though the range of temperatures within which hatchlings are produced at all is relatively narrow (~5 to 8 °C). Female-biased sex ratios have been reported for many nesting sea turtle populations around the world (Binckley et al., 1998; Hawkes et al., 2007; Zbinden et al., 2007, and reviewed in Hays et al., 2014) and extremely female-biased sex ratios (> 90% female) for a few (Godfrey et al., 1999; Broderick et al., 2000; Jensen et al., 2018). There has been some speculation about the potentially negative effect of continued warming on sex ratios, but female biased primary sex ratios appear to be natural at most nesting beaches and female-biased sex ratios may also be beneficial as they can increase the size of the nesting population under certain conditions (Laloë et al., 2014), compensating for mortality of early life-stages (Santidrián Tomillo and Spotila, 2020). However, this compensation may not work at extremely high nest temperatures, as hatchling production may reach critically low levels (Santidrián Tomillo et al., 2015; Hays et al., 2017). As many sea turtle populations around the world are endangered, and there are several threats to developing sea turtle egg clutches, it is a common conservation practice to relocate clutches to safer areas where embryos can complete development and emerge from nests (Wyneken et al., 1988; Tuttle and Rostal, 2010). For example, illegal harvest of eggs is a major threat to sea turtles in many countries, especially in remote areas where beaches extend over many kilometers that are difficult to access and protect (Chacón-Chaverri and Eckert, 2007; Mutalib and Fadzly, 2015), necessitating egg relocation to safe areas that can sometimes include 100% of clutches. Moreover, sea turtles do occasionally nest below the high tide line, where incubating embryos are likely to die from regular tidal inundation and beach erosion. These ‘doomed clutches’ are often relocated. Doomed clutches are most often relocated to beach hatcheries where nests can be monitored and protected from people and predators (Van de Merwe J et al., 2006; Patino-Martinez et al., 2012). Because there is growing concern on the negative effect of climate warming on hatchling production, measures to reduce nest temperatures, such as shading and watering nests, have been implemented or proposed as climate mitigation strategies in some locations (Maulany et al., 2012; Hill et al., 2015; Jourdan and Fuentes, 2015; Mutalib and Fadzly, 2015). In particular, these widely used interventions are commonly justified by the assumption that production of hatchlings and reduction of the female bias in hatchling sex ratios will promote improved population status. However, there could be important unintended consequences of lowering nest temperatures, and whether reducing female biases actually benefits population dynamics remains an open question. Although Morreale et al. (1982) warned several decades ago about the potential negative effect of clutch relocation on sex ratios, the effectiveness of this very common conservation strategy—particularly when coupled with intentional reductions of nest temperatures— warrants robust examination. Sea turtles are long-lived and late-maturing species characterized by high adult survival and low and variable survival of early life-stages (Heppell et al., 2003). Females can mate with multiple males in a season and the occurrence of multiple paternity is common (Crim et al., 2002; Lee et al., 2018). Additionally, although primary sex ratios are female biased at most beaches, the sex ratio of adult reproductive individuals seems to be balanced (Stewart and Dutton, 2011; Wright et al., 2012; Gaos et al., 2018) or male biased (Howe et al., 2018; Lasala et al., 2013; Turkozan et al., 2019). Because males can reproduce more frequently than females (i.e., annually vs semi-annually), and one male could potentially mate with several females, it is likely that population dynamics in sea turtles are largely driven by the number of females (Hays et al., 2017). In fact, altering sex ratios to female biases could increase the size of animal populations in the long-term when the number of eggs limits the population growth (Wedekind, 2002). Therefore, we hypothesize that lowering female biased sex ratios, could have negative impacts on sea turtle populations in the long-term, thus potentially undermining the stated goals of many conservation projects focused on nesting beaches. To test this hypothesis and evaluate potentially negative, unintended consequences of measures to cool nest temperatures, we used the known effects of nest temperature on embryo and hatchling mortalities and on sex ratios in a population of sea turtles to examine the potential impacts of shading or irrigating nests in hatcheries. We use the leatherback turtle population that nests in Pacific Costa Rica as an example, because models have been previously used for this population and model parameters have been defined (Santidrián Tomillo et al., 2015; Laúd OPO network, 2020). Specifically, we assessed the effect of reducing nest temperatures, as if nests were artificially shaded or watered, on emergence success, primary sex ratios, number of nesting turtles, number of adult males, total population size, and asymptotic population growth rate (λs). To complete the picture, we additionally simulated the effect of increasing mean nest temperatures under climate change scenarios to determine if shading could become needed if temperatures passed a certain threshold. Ultimately, our results will help guide future management actions for sea turtle populations and could inform management of other species with TSD. Section snippets Methods To assess the potential negative effect of decreasing nest temperatures when relocating sea turtle clutches, we used data from leatherback turtles nesting at Playa Grande, Costa Rica, which belong to the eastern Pacific (EP) leatherback regional management unit (Wallace et al., 2010). The EP leatherbacks have precipitously declined due to a combination of bycatch and egg harvest (Spotila et al., 2000; Sarti Martínez et al., 2007; Laúd OPO Network, 2020). Pacific Costa Rican leatherbacks have Effect of decreasing mean nest temperatures Relative to mean in situ nest temperatures, both current and historical model scenarios incorporating effects of reducing nest temperatures resulted in increased emergence success and reduction of the female bias in primary sex ratios. The lower the nest temperature, the higher the emergence success in all cases and consequently, the higher the number of hatchlings (Table 1). The increase in emergence success when temperatures were reduced by 2.0 °C would translate into an increase in the Discussion The ostensible goal of cooling sea turtle nests is to produce more hatchlings. Our results confirmed that lowering nest temperature increased hatching and emergence successes, as found in operating hatcheries in Indonesia and Malaysia where shading has been implemented (Maulany et al., 2012; Mutalib and Fadzly, 2015). This apparently positive outcome from reductions in nest temperature can, however, negatively affect sea turtle populations causing long-term abundance declines, if nest Implications for nest management under climate warming Our results indicate that nest shading may only be needed to conserve sea turtles under extreme female biases that could result in non-fertilized eggs and that are accompanied by high embryo and hatchling mortality, as we found in the highest future mean nest temperature increases, but not in the scenarios of low and intermediate temperature increases. Some populations such as the green turtles that nest in the northern beaches of the Great Barrier Reef are already extremely female biased (> CRediT authorship contribution statement Pilar Santidrián Tomillo: Conceptualization, methodology, writing-original draft, supervision; Bryan P Wallace: Conceptualization, methodology, writing-reviewing editing; Frank V Paladino: writing-reviewing editing, supervision; James R Spotila: writing-reviewing editing, supervision; Meritxell Genovart: methodology, population model development, writing-reviewing editing. Declaration of competing interest The authors have no competing interests to declare. Acknowledgements We thank all field assistants and volunteers that contributed to the data collection at Playa Grande over the years. We also thank Parque Nacional Marino Las Baulas and the Tempisque Conservation Area for supporting research on sea turtles. Funding for this study came from the Earthwatch Institute, The Leatherback Trust, the Disney Conservation Fund and the Spanish Ministry of Science (CGL2017-85210) (MICINN/FEDER, UE). References (68) D.L. Dutton et al. Increase of a Caribbean leatherback turtle Dermochelys coriacea nesting population linked to long-term nest protection Biol. Conserv. (2005) A.R. Gaos et al. Prevalence of polygyny in a critically endangered marine turtle population J. Exp. Mar. Biol. Ecol. (2018) M. Girondot et al. Delimitation of the embryonic thermosensitive period for sex determination using an embryo growth model reveals a potential bias for sex ratio prediction in turtles.Journal of Thermal Biology (2018) T.T. Jones et al. Growth of captive leatherback turtles, Dermochelys coriacea, with inferences on growth in the wild: implications for population decline and recovery J. Exp. Mar. Biol. Ecol. (2011) P.L.M. Lee et al. Chapter one – a review of patterns of multiple paternity across sea turtle rookeries Adv. Mar. Biol. (2018) A. Lolavar et al. Experimental assessment of the effects of moisture on loggerhead sea turtle hatchling sex ratios Zoology (2017) N. Mrosovsky et al. Temperature dependence of sexual differentiation in sea turtles: implications for conservation practices Biological Conservation (1980) I. Reboul et al. Artificial and natural shade: implications for green turtle (Chelonia mydas) rookery management Ocean Coast. Manag. (2021) P. Santidrián Tomillo et al. High beach temperatures increased female-biased primary sex ratios but reduced output of female hatchlings in the leatherback turtle Biol. Conserv. (2014) O. Turkozan et al. Multiple paternity at the largest green turtle (Chelonia mydas) rookery in the Mediterranean Reg. Stud. Mar. Sci. (2019) Cited by (6) Temperature-based modeling of incubation period to protect loggerhead hatchlings on an urban beach in Northwest Florida 2022, Journal of Experimental Marine Biology and Ecology Operational sex ratio estimated from drone surveys for a species threatened by climate warming 2022, Marine Biology A review of the effects of incubation conditions on hatchling phenotypes in non-squamate reptiles 2022, Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology RELOCATING GREEN TURTLE (CHELONIA MYDAS) EGGS TO OPEN BEACH AREAS PRODUCES HIGHLY FEMALE-BIASED HATCHLINGS 2021, Herpetological Conservation and Biology Are Sea Turtle Hatcheries in India Following Best Practices? 2021, Herpetological Conservation and Biology Effects of moisture during incubation on green sea turtle (Chelonia mydas) development, morphology and performance 2021, Endangered Species Research Recommended articles (6) Research article Compassion and moral inclusion as cornerstones for conservation education and coexistence Biological Conservation, Volume 261, 2021, Article 109253 Research article The mitigation hierarchy in environmental impact assessment and related legislation as a tool for species conservation: A case study of western chimpanzees and mining development Biological Conservation, Volume 261, 2021, Article 109237 Research article Satellite tracking improves conservation outcomes for nesting hawksbill turtles in Solomon Islands Biological Conservation, Volume 261, 2021, Article 109240 Research article Using systems thinking to inform management of imperiled species: A case study with sea turtles Biological Conservation, Volume 260, 2021, Article 109201 Research article Effectiveness and design of marine protected areas for migratory species of conservation concern: A case study of post-nesting hawksbill turtles in Brazil Biological Conservation, Volume 261, 2021, Article 109229 Research article Identifying future sea turtle conservation areas under climate change Biological Conservation, Volume 204, Part B, 2016, pp. 189-196 View full text © 2021 Elsevier Ltd. 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Santidrián Tomillo, Pilar; Wallace, Bryan; Paladino, Frank; Spotila, James; Genovart, Meritxell
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