case study in conservation biology

This page has been archived and is no longer updated

Conservation Biology

What is Conservation Biology?

Conservation biology, said to be a "mission-oriented crisis discipline" (Soulé 1986), is a multidisciplinary science that has developed to address the loss of biological diversity. Conservation biology has two central goals: 1. to evaluate human impacts on biological diversity and 2. to develop practical approaches to prevent the extinction of species (Soulé 1986, Wilson 1992). The field seeks to integrate conservation policy with theories from the fields of ecology, demography, taxonomy, and genetics. The principles underlying each of these disciplines have direct implications for the management of species and ecosystems, captive breeding and reintroduction, genetic analyses, and habitat restoration.

The concept of conservation biology was introduced by Dasmann (1968) and Ehrenfeld (1970). Soulé & Wilcox's (1980) contribution, Conservation Biology: An Evolutionary Ecological Perspective , served as an impetus for the development of the discipline. Over the next six years, many scientists began to refer to themselves as conservation biologists. Conservation Biology: The Science of Scarcity and Diversity was published, a Society for Conservation Biology formed, and a journal was established (Soulé 1986).

Several factors contributed to the development of the field. Scientists began to realize that virtually all natural systems have been damaged by what Diamond (1986) referred to as the "Evil Quartet": habitat loss and fragmentation, overharvesting, introduced predators and competitors, and the indirect effects of these threats on ecological interactions. None of the traditional applied disciplines, such as wildlife management, agriculture, forestry and fisheries, were comprehensive enough by themselves to address critical threats to biological diversity (Primrack 1993). Also, these traditional applied disciplines often overlooked threatened species that were of little economic or aesthetic value. Theories and field studies in community ecology, island biogeography, and population ecology were subjects of major investigation and development in the 1960s and 1970s, and while these disciplines have direct relevance to conservation, they traditionally emphasized the study of species in their natural environments, in the absence of human activity. The growing separation of "applied" and "basic" disciplines prohibited the exchange of new ideas and information between various academic assemblages and to management circles (Soulé 1980).

Conservation biology as a discipline aims to provide answers to specific questions that can be applied to management decisions. The main goal is to establish workable methods for preserving species and their biological communities. Specific methods have been developed for determining the best strategies for protecting threatened species, designing nature reserves, initiating breeding programs to maintain genetic variability in small populations, and reconciling conservation concerns with the needs of local people (Primrack 1993). For this to be successful, communication among all sectors of the conservation community is necessary. The interface between theory and practice in conservation biology, especially from the point of view of resource managers, has been somewhat neglected (Soulé 1986). Because we do not understand community and ecosystem structure and function well enough to make reliable predictions, uncertainty has inhibited scientists from providing concrete answers to managers. The availability of statistical and computational tools has been integral in the development of analytical methods critical to addressing the issue of uncertainty in conservation biology. Management tools such as population viability analysis (PVA), Bayesian statistics, and decision analysis have been developed to provide "objective" methods for making conservation decisions. These approaches have been key in the transformation of conservation biology from an idea to a discipline.

Statistical and Computational Tools Used in Conservation Biology

Population viability analysis (pva).

PVA is a process used to evaluate the likelihood that a population will persist for some particular time in a particular environment.

Gilpin and Soulé (1986) conceived of population vulnerability analysis as an integrative approach to evaluate the full range of forces impinging on populations and to make determinations about viability. PVAs have become a cornerstone of conservation biology, and it is likely that their importance will increase in the future. The precise role of PVA in conservation biology is still emerging.

Minimum Viable Population: What's the Magic Number?

In the 1970s, empirical studies and ecological and genetic theory converged on the idea that a species becomes exceptionally vulnerable to extinction when it includes only a few small populations (MacArthur & Wilson 1967, Richter-Dyn & Goel 1972, Leigh 1975). The observation that once a population was reduced below a certain threshold, it began to dwindle toward extinction led to the concept of minimum viable population size (MVP), the smallest number of individuals necessary to prevent a population from going extinct. The concept of MVP officially emerged in response to an injunction from the United States Congress to the US Forest Service to maintain "viable populations" of all native vertebrate species in National Forests (National Forest Management Act of 1976, 16 USC 1600-1614; Gilpin & Soulé 1986). The concept encompasses theories that had been developed and tested to varying degrees in the fields of population genetics and demography. The critical feature of MVP is that it allows a quantitative "rule of thumb" estimate of minimum population size to be made. MVP remains a tenuous concept among conservation biologists. In light of the complex and dynamic nature of single species population dynamics, conservation biologists have frowned upon the "magic number" concept. They argue that the job of conservation biologists should be to recommend or provide more than just the minimum number necessary for a species' persistence (Soulé 1987). Yet the term has not been abandoned and actually remains a central theme in conservation biology. As human population growth continues to encroach upon the habitat of endangered and threatened species, the MVP concept is likely to become a critical tool for conservation biologists to assure the continued existence of species.

Decision Analysis and Multiple-Criteria Approaches

Decision analysis, which was developed for guiding business decisions under uncertainty, has been proposed as a useful tool for endangered species management (Raiffa 1968, Behn & Vaupel 1982, Maguire 1986). Statistical approaches make explicit the logic by which a decision is reached under conditions of uncertainty. Mace & Lande (1991) and the International Union for Conservation of Nature (IUCN) have attempted to apply decision analysis theory to put the MVP and PVA concepts into practice for determining a species' status on the Red List of threatened and endangered wildlife.

Broad Speculation on the Future of Conservation Biology

Conservation biology has become a burgeoning discipline since it originated in the early 1980s. Theories from the fields of island biogeography, genetics, demography, and population ecology have been broadly applied to the design and management of reserves, captive breeding programs, and the classification of endangered species. Since 1980 we have witnessed the rapid expansion of a professional society and the emergence of active graduate programs.

Nonetheless, the course of development of the discipline has not altogether been smooth sailing; lack of adequate funding remains a critical problem. The financial and institutional supports for conservation biology, in both its research and educational roles, need to be strengthened (Soulé 1986). Furthermore, while some advances have been made in the realm of interdisciplinary cooperation and communication between scientists and managers, significant progress is necessary before the original goals of conservation biology can be met.

The caveats with various analytical methods necessitate further research in order to reach their full potential as predictors of extinction. It has become clear that PVA is not currently a viable method for predicting the precise time to extinction for a species. Further, requiring quantitative data for conservation decisions may unduly place the burden of proof on scientists in a manner detrimental to the species of concern. PVA is useful, however, for comparing the relative extinction risks among species and populations, and for prioritizing research and management actions. Similarly, the MVP concept has thus far been limited in its potential for application to conservation decisions. Because lack of genetic variability does not generally pose extinction risks for large populations, the concept is only relevant to small populations. However, even for small populations, a temporary reduction below any MVP does not necessarily imply a high probability of extinction. Consensus among conservation biologists about the selection of appropriate assumptions for estimating effective population size and about the timeframe under which we are concerned about extinction, offers potential for the use of MVP as a tool in conservation biology. Because conservation decisions are often confounded by uncertainty, decision analysis appears to be a particularly useful method for conservation biologists. The IUCN classification scheme offers a risk-averse approach to species classification in its use of multiple criteria, wherein data would typically be available to evaluate at least one of the criteria. However, additional analyses are necessary to develop and refine analytical tools suggested by the IUCN as status determination criteria.

Until these issues are resolved, the status of conservation biology as a predictive science will remain in serious doubt (Soulé 1986). Given the imperfect nature of the analytical tools integral to the field of conservation biology, the apparent gap between theory and practice, and the continued loss of biodiversity, what is the future for conservation biology? The models of today may undoubtedly become the "broken stick models . . . and other strange and wonderful debris" that Soulé (1987) envisions as littering the field of mathematical population biology. Nonetheless, population models will continue to evolve as critical tools to conservation biologists. The gap between theory and practice is narrowing as a function of the prominence of conservation biology as a field of study. Because the field is interdisciplinary, it necessarily unites basic and applied scientists with natural resource managers. Scientists will continue to work with policy makers in developing appropriate and workable approaches to species conservation. A central theme in conservation biology is developing compromises between conservation priorities and human needs. However, the precise role of conservation biologists as advocates has yet to be formalized. Soulé himself disobliges scientists from taking on an advocacy role: "Most biologists and most economists are not trained to be advocates. They're trained to think and teach, to encourage students and support and advance their disciplines. So to expect that most scientists will turn themselves into effective community activists, politicians, or managers is unfair and unrealistic." Instead, the role of the conservation biologist remains simply to advocate for good science and to make salient findings available to managers and scientists in other fields. Advocating "values" under the auspices of doing science undermines the objectivity of science. The distinction between advocacy and science should be clear for conservation biology to persist as a legitimate discipline. Finally, the dichotomy referred to by Caughley (1994) as the "small population paradigm," which needs more empirical evidence, and the "declining population paradigm," which needs more theoretical development, has generated substantial debate among conservation biologists about where the field is going. Caugley pointed out that many of the theoretical underpinnings of conservation biology are misguided in that they treat an effect, such as small population size, as if it were a cause. He suggested that conservation efforts should instead be focused on determining causes of population declines and the means by which agents of a decline can be identified (Caughley 1994). This idea has reoriented many theoreticians to consider the broader scope of their work and has encouraged field biologists to more closely align their research to conservation-related questions. Thus, the stage has been set for the future development of both the theoretical constructs and the natural history investigations critical to the persistence of conservation biology as a scientific discipline.

References and Recommended Reading

Caughley, G. Directions in conservation biology. Journal of Animal Ecology 63 , 215–244 (1994).

Dashman, R. F. Environmental Conservation . New York, NY: John Wiley and Sons, 1968.

Ehrenfeld, D. W. Biological Conservation . New York, NY: Holt, Rinehart, and Winston, 1970.

Gilpin, M. E. & Soulé, M. E. "Minimum viable populations: Processes of species extinction." In Conservation Biology: The Science of Scarcity and Diversity , ed. M. E. Soulé (Sunderland: Sinauer & Associates, 1986): 19–34.

Ginzburg, L. R. et al . Quasiextinction probabilities as a measure of impact on population growth. Risk Analysis 2 , 171–181 (1982).

Leigh, E. G. "Population fluctuations and community structure." In Ecology and Evolution of Communities , eds. J. M. Diamond & M. L. Cody (Cambridge, MA: Harvard University Press, 1975): 51–73.

MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography . Princeton, NJ: Princeton University Press, 1967.

Mace, G. M. & Lande, R. Assessing extinction threats: Toward a reevaluation of IUCN threatened species categories. Conservation Biology 5 , 148–157 (1991).

Primack, R. B. Essentials of Conservation Biology . Sunderland, MA: Sinauer & Associates, 1993.

Richter-Dyn, N. & Goel, N. S. On the extinction of a colonizing species. Theoretical Population Biology 3 , 406–433 (1972).

Soulé, M. E. "Thresholds for survival: Maintaining fitness and evolutionary potential." In Conservation Biology: An Evolutionary-Ecological Perspective , eds. M. E. Soulé & B. A. Wilcox (Sunderland: Sinauer & Associates, 1980) 151–169.

Soulé, M. E. Conservation Biology: The Science of Scarcity and Diversity . Sunderland, MA: Sinauer & Associates, 1996.

Wilson, E. O. The Diversity of Life . Cambridge, MA: The Belknap Press of Harvard University Press, 1992.

Flag Inappropriate

Email your Friend

•  |  Lead Editor:  Sigurdur Greipsson

Within this Subject (12)

• Basic (8)
• Intermediate (4)

Other Topic Rooms

• Ecosystem Ecology
• Physiological Ecology
• Population Ecology
• Community Ecology
• Global and Regional Ecology
• Conservation and Restoration
• Animal Behavior
• Teach Ecology
• Earth's Climate: Past, Present, and Future
• Terrestrial Geosystems
• Marine Geosystems
• Scientific Underpinnings
• Paleontology and Primate Evolution
• Human Fossil Record
• The Living Primates

© 2014 Nature Education

• Press Room |
• Terms of Use |
• Privacy Notice |

Visual Browse

Advertisement

A case study of a conservation flagship species: the monarch butterfly

• Original Paper
• Open access
• Published: 04 May 2021
• Volume 30 , pages 2057–2077, ( 2021 )

Cite this article

You have full access to this open access article

• Stephanie D. Preston 1 ,
• Julia D. Liao 1 ,
• Theodore P. Toombs 2 ,
• Rainer Romero-Canyas 2 ,
• Julia Speiser 1 &
• Colleen M. Seifert   ORCID: orcid.org/0000-0001-5889-5167 1  

5961 Accesses

22 Citations

41 Altmetric

Explore all metrics

What makes a flagship species effective in engaging conservation donors? Large, charismatic mammals are typically selected as ambassadors, but a few studies suggest butterflies—and monarchs in particular—may be even more appealing. To gather more information about people’s responses to monarchs, we conducted an empirical study of member submissions to a successful conservation campaign, the Monarch Story Campaign, conducted by the Environmental Defense Fund (EDF). The set of 691 stories along with their associated demographic and donation data was analyzed in a mixed-methods study using qualitative analysis and tests of association. The results showed that people often described encounters with monarchs in childhood and as adults. They expressed strong, positive emotions, and lauded the monarch’s beauty and other “awe-inspiring” qualities and expressed wonder at their lifecycle (i.e., metamorphosis and migration). They also raised conservation themes of distress at monarch loss, calls for action, and caretaking, such as being “fragile” and “in need.” Sharing personal encounters was associated with current efforts to save the species and more past financial donations, while a second pattern tied more donations to awe at the monarch’s mass migration. These results imply that conservation campaigns built around species people encounter may build lifelong awareness, concern, and actions towards conservation.

Similar content being viewed by others

Effect and difference between the threatened and endemic status on the general public support towards wildlife species in a biodiversity hotspot

Conservation Biologists and the Representation of At-Risk Species: Navigating Ethical Tensions in an Evolving Discipline

Money, Myths and Man-Eaters: Complexities of Human–Wildlife Conflict

Avoid common mistakes on your manuscript.

Introduction

Monarch butterflies ( Danaus plexippus ) are among the most popular insect species in the world, and are easily recognizable in gardens and fields across North America (Oberhauser et al. 2018 ). Articles about monarchs appear frequently in the popular press; for example, the New York Times published (on average) one each month from 1995 to 2015 (cf. Gustafsson et al. 2015 ). In the 1950s, Fred and Norah Urquhart chose monarchs for the first citizen science research project on, “Where do monarchs go in the winter?” (Urquhart and Urquhart 1976 ). Monarch migration and overwintering sites now draw thousands of ecotourists each year (Lemelin and Jaramillo-López 2019 ; Lemelin et al. 2019 ). Thanks to school programs and large-scale monitoring projects, public awareness of monarchs has grown over generations who are interacting with monarchs “in the wild” (Young-Isebrand et al. 2015 ; Gustafson et al. 2015 ; Lewandowsky and Oberhauser 2017 ).

But since the turn of the century, wildlife habitat loss, herbicide use, and climate change have caused a rapid decline in the monarch population (Thogmartin et al. 2017 ). In 2014, U.S. President Barack Obama requested the establishment of a federal strategy to save the monarch, which initiated a status assessment by the U.S. Fish and Wildlife Service (White House 2014 ). Concurrently, a wide array of longstanding and new conservation groups (from local to national in scope) have coalesced around this cause through a new organization: The Monarch Joint Venture (Monarch Joint Venture 2020 ). Monarch conservation efforts also align with sustainable farming practices to address habitat, water quality, and erosion through changes like vegetated field buffers, which also provide food for migrating butterflies (Gustafsson et al. 2017 ). Based on this unprecedented coalition of conservation activity, the monarch came to represent the decline of biodiversity and broader environmental issues across North America (Gustafsson et al. 2015 , 2017 ).

The monarch’s recovery will require an unprecedented collaborative conservation effort (Jepsen et al. 2015 ). Efforts to save the species from extinction will be expensive, as feeding habitats must be restored across a wide swath of North America through planting milkweed and nectar-producing plants (Thogmartin et al. 2017 ) and through changes to agricultural policies (Nail et al. 2015 ). These efforts will require large financial contributions and broad societal support, from agriculture, industry, citizens group, conservation organizations, and all levels of government, which will likely cost hundreds of millions of dollars (Thogmartin et al. 2017 ). Conservation organizations rely upon varied sources of financial support, including public funding, private donors, foundations, and individual annual memberships. Without strong public support, these funding sources may fall short of what is needed to save the monarch.

Fortunately, the general public, scientists, and conservationists appear to be rallying and uniting to save the monarch (Gustafsson et al. 2015 ). Efforts to save the monarch also benefit from the fact that it is a well-known and beloved creature. For example, the monarch butterfly is the only insect described as “iconic” by the National Wildlife Federation, the Natural Resource Defense Council, and the World Wildlife Fund (Horsley et al. 2020 ). What is special about the monarch? Can the monarch’s popularity be applied to generate broader conservation support?

• Flagship species

Species surrogacy is a conservation fundraising strategy (Simberloff 1998 ) where a single “flagship” species is marketed in conservation magazines and environmental non-governmental organization (ENGO) campaigns to the general public, generating interest and revenue (Verissimo et al. 2011 ). Flagship species draw people’s interest; for example, people playing an online game donated more to campaigns featuring flagship (e.g., elephants, polar bears, and tigers) than non-flagship (e.g., frogs, cods, and stoneflies) species (Thomas-Walters and Raihani 2017 ). Most flagship campaigns employ large mammals or charismatic megafauna due to their popularity with donors (Caro et al. 2004 ; MacDonald et al. 2015 ); for example, polar bears have become icons for climate change (Born 2019 ; World Wildlife Fund 2020 ). Because of this focus, the majority of conservation publications feature mammals, while invertebrates representing over 90% of species are underrepresented (Barua 2011 ). Flagship species can serve as “ambassadors” by drawing attention to biodiversity within their distribution (Bennett et al. 2015 ; Macdonald et al. 2017 ). However, the assumption that the wealth spreads to other species may be mistaken, as these campaigns may suggest that other species are less valuable (Douglas and Winkel 2014 ), and 61% of flagship campaigns raised funds for only the target species (Smith et al. 2012 ).

Researchers have called for a more rigorous and objective approach to selecting flagship species by using marketing research to compare people’s preferences across species (Verissimo et al. 2011 ). Flagship species possess greater perceived charisma, larger geographical distribution, more threatened conservation status, better visibility, and larger body size (Barua, 2012 ). An empirical study with over 1500 people from five continents assessed the relative charisma of different mammals and found that: (1) large body size is a key selection feature; (2) big cats and primates are most preferred; and (3) the tiger ( Panthera tigris ) was the top species by a wide margin (Macdonald et al. 2015 ). Research funding shares this bias, as more money is allocated to larger species without considering conservation status or geographic range (Tensen 2018 ). Conservation communications and environmental non-governmental organizations (ENGO) also show this body size bias (Barua 2011 ; Horsley et al. 2020 ). Preferences are also predicted by familiarity (Schlegel and Rupf 2010 ), at both global and local levels (Macdonald et al. 2015 ). Flagship species are also defined by their aesthetic appeal or “cuddliness,” and these features fit a broader range of species (Smith et al. 2012 ). Despite these findings, theorists note that we have little understanding about, “…why certain species have appeal, galvanize action, and have staying power” to influence conservation outcomes (Jepson and Barua 2015 , p. 95).

Butterflies as flagship species

Based on the fact that preferred flagship species are usually large mammals with forward facing eyes (Smith et al. 2012 ), the monarch would appear to be a poor choice as a campaign focus. However, they are beautiful, fairly familiar, and threatened, which suggests that they are a good candidate for an overlooked “Cinderella species,” as defined by Smith and colleagues ( 2012 ). It is also beneficial for the monarch that they tap deeply into North American cultural concepts and associations, allowing them to speak for broader conservation goals (DeMello 2012 ; Jepson and Barua 2015 ). The monarch has been identified as a socially constructed “icon” that connects public, scientific, and conservationist interests as a symbol of broader environmental concerns in the U.S. (Gustafsson et al. 2015 ; 2017 ).

However, to our knowledge, there is little empirical evidence to support this culturally constructed view of people’s thoughts, feelings, and associations in response to butterflies. A U.K. study found that people reported higher levels of benefit and satisfaction with charismatic species like birds and butterflies than with beetles and bugs (McGinley et al. 2017 ). Comparisons across species show that along with mammals, people prefer butterflies and birds over reptiles, insects, and amphibians (Schlegel and Rupf 2010 ; Roberge 2014 ), with butterflies the most favored animal in the study (Schlegel and Rupf 2010 ). A study of invertebrate species in northeast India found preferences for butterflies, honeybees, and dragonflies over competitors because of their aesthetic appeal and harmlessness (Barua et al. 2012 ). However, people in that study also had negative views of caterpillars, attributing harm and economic damage to them, and only 63% said butterflies benefitted humans.

These findings suggest that butterflies have potential as flagship species for conservation programs, but we must better understand people’s responses to them. An empirical field study examining people’s perceptions, attitudes and associations with monarchs may suggest how they may influence conservation engagement. While the monarch’s plight has clearly grabbed broad attention (Gustafsson et al. 2017 ), the question of whether and why it may spur donations for conservation programs remains.

The monarch as flagship species

To examine why people are drawn toward monarchs and whether these attributes promote conservation aid, we conducted a case study of a conservation campaign by Environmental Defense Fund, Inc. (EDF), an international ENGO that has publicized the decline of monarchs and worked closely with agricultural groups to implement on-the-ground conservation projects (Environmental Defense Fund 2020 ). Like many other organizations, EDF is reliant upon donations to fund its actions, and fundraising from private donors requires contact with the public through social media, their website, and email campaigns. In a recent campaign—the “Monarch Story Campaign”—EDF created a website focused on the monarch butterfly (EDF 2018 ). Through EDF email lists, members were encouraged to visit the website to, “Tell your Monarch story” by writing about, “What does the Monarch mean to you?” EDF members were strongly engaged by The Monarch Story Campaign, as measured through website traffic and a higher than usual number of donations.

While this online engagement was high, it is unclear why. Monarch butterflies are renowned for their beauty; on the campaign website, appealing images signaled opportunities to donate (Nail et al. 2015 ; Gustafson et al. 2015 ). Monarchs are also familiar to people in the United States, and people protect familiar species (Schlegel and Rupf 2010 ). Monarchs may also benefit from their link to familiar places, which creates positive cultural associations (Jepson and Barua 2015 ). People also have personal experiences with monarchs or their migration, which creates memories that may motivate conservation (Bandura 1999 , 2001 , 2018 ). School programs and science projects like raising and releasing monarchs also expose people directly to the species (Young-Isebrand et al. 2015 ; Gustafson et al. 2015 ). The monarch also has a unique life-history including metamorphosis, massing, and annual migration crossing national borders in North America (Gustafsson et al. 2015 ; Simaika and Samways 2018 ), heightening their political and geographic prominence.

In addition, the monarch symbolizes cultural values, including beauty, natural wonder, scientific discovery, conservation imperatives, and civic duty (Gustafson et al. 2015 , 2017 ). These cultural themes may create a shared, “animal as constructed” (see DeMello 2012 ) view of monarchs without first-hand experiences. For example, their metamorphosis from caterpillar to butterfly has been tied to spiritual and religious symbolism, such as the loss of loved ones and their souls returning on the Day of the Dead (Gustafsson et al. 2015 ). Finally, people may want to help the monarch because they share features with helpless neonates in need, signaling caregiving responses in human evolution (Preston 2013 ). The monarch’s threatened status, delicate and attractive appearance, and helplessness as a prey species may potentiate people’s motivation to help. Thus, there are many possible reasons that people may want to become involved in monarch conservation, but little evidence about the factors responsible for their engagement.

For these reasons, we conducted a case study of the EDF Monarch Story Campaign as a distinct instance of conservation programs (Abercrombie et al. 1984 ; Greene and Shepard 2003 ; Flyvbjerg 2011 ). Our research goal was to identify why people engaged with this campaign by observing how their open-ended stories reflected their responses to monarchs. Our critical case approach included a qualitative analysis with an interpretivist epistemological perspective (Flyvbjerg 2001 , 2006 ; Patton 2002 ), recognizing that the outcomes depend on the context, and the context is integrated into the analysis of findings (Creswell 1994 ; Patton 2002 ). This qualitative analysis of emergent themes in submitted stories was followed by statistical analyses of relationships among themes, conservation actions, and demographic variables. This mixed-methods approach (Creswell 2017 ) was aimed at determining which associations to monarchs inspired people to participate in the campaign. We hypothesized that monarch engagement would be particularly tied to their beauty, to their familiar (but unique) life history which people directly observe, and to the drive to take care of the endangered, helpless, and fragile.

EDF sent two separate email prompts to their list of prior donors. The first offered a detailed Monarch Story from a staff member (Appendix A) and invited the recipient to follow a link to an EDF web page where they entered and submitted their story in an open text response box (Fig.  1 ) and (optionally) entered their name and email. Four months later, a follow-up email invited the same email recipients to revisit the site to view anonymized story submissions that were pinned to a national map onto which they could add their own story:

“Monarch butterflies—just hearing the words brings a beautiful, black and orange miracle of nature fluttering through your mind. For me, the monarch was one of my first connections to nature— potentially what led me to EDF all these years later. And when I asked for your Monarch stories, you made it clear: the Monarch has played a crucial role for you, as well. For some, it's a connection to a lost loved one—a reminder of times you shared. For others, it's proof that we can always metamorphose, always become better versions of ourselves. And for many, it's a passion, a creature you're working hard to bring back from the brink.”

The EDF Monarch Story Campaign materials included a staff member’s story in each of two emails. Images in the emails (left) linked to the EDF campaign web page with a story prompt (right)

Further information about monarchs and EDF campaigns was available on EDF webpages.

The dataset for the study included the 691 monarch butterfly stories submitted by members of the public to the EDF website over the five-month campaign. The stories’ length averaged 453.66 characters (SD = 391.90), with a range from 6 (e.g., one response include a single word, “beauty”) to 4,422 characters. Some stories were entered into the EDF web page anonymously, but the majority included email addresses. EDF researchers retrieved linked demographic data for 517 of the entries through these emails. This demographic data (ethnicity or race) included gender (74% female with no nonbinary reported), age (75% ages 45–64), education (78% college graduates), homeowner status (78% homeowners), household income (median 50,000 to 75,000), net worth (median 250,000 to 500,000), location (e.g., rural vs. urban), and donation history. The remaining 174 stories were either anonymous or did not match past donor email addresses. Importantly, no data was available for donations in direct response to the Monarch Story campaign; consequently, donor characteristics from past EDF contributions served as an index of broader environmental giving.

Qualitative coding of themes

In order to document the content described in the stories, we created a qualitative codebook beginning with candidate themes adapted from prior studies as described above. Following Creswell ( 2017 ), the stories were also analyzed for emergent themes from an initial review of a random subset of 100 stories, followed by an iterative, detailed revision of the set of codes to improve their accuracy and remove duplication (Boeij 2002 ). The codebook was refined to 43 themes, and three coders independently scored a subset of 100 stories for the presence of each theme. Any discrepancies were discussed, and the coding criteria clarified or adjusted as needed. The coders then proceeded to independently score the remaining 591 stories. Statistical tests showed high interrater agreement for each individual theme code (all 43 had agreement above 0.87) (shown in Table 1 ). The three coders discussed any differences to agreement to determine the final codes. We also coded the two emails sent out by EDF for any of the themes and found that 20 of 43 themes (46%) appeared in at least one of the two Monarch Story campaign emails.

Qualitative analyses

Factor analysis.

To statistically identify relationships among these coded themes based on their co-occurrence in the stories, we conducted a factor analysis on all 43 coded themes using Principal Components Analysis (PCA). We examined an eigenvalue scree plot to determine the point of deflection that indicates a switch from explaining more to less variance. Based on this, we extracted a 5-factor solution that explained 25% of the variance, with Promax rotation (allowing individual factors to be correlated with each other). We report all themes loading over 0.5 on each of the five factors. We then averaged all themes loading > 0.5 for a single composite score to represent each of the five PCA factors in correlational analyses.

Correlational analyses

Our quantitative analysis plan included statistical tests to identify correlations among all observed themes, PCA composite factors, and demographic variables. However, conducting many statistical tests with the full set of 43 themes, five composite factors, and nine demographic variables greatly increases the risk of observing significance by chance (as a “false positive,” Type 1 error). To avoid this in our correlational analyses, we limited the number of variables included. We grouped similar themes based on content similarity into 13 theme clusters (shown in Appendix C), each of which occurred in more than 10% of stories. The few themes that fell into more than one cluster (e.g., personal experience with migration was included in both the Migration and Personal experiences theme clusters) were removed from both to avoid artificially inflating those correlations. Thus, tests of association were conducted for the five identified composite factors, 13 theme clusters, and nine demographic variables. Finally, we tested whether the mention of a theme in the EDF email prompts predicted their appearance in people’s stories. All correlational analyses used Pearson’s r (equivalent to a categorical phi coefficient when both variables are binary; Warner, 2008 ) and all categorical variables were considered with t-tests.

Frequency of observed themes

The 691 submitted stories averaged 453.66 characters (SD = 391.90) (approximately 80 words). While the stories posted on the webpage were fairly short, they included (on average) around 7 coded themes ( M  = 7.29; SD = 3.55). As shown in Fig.  2 , the set of stories ranged from 11 stories with only a single theme to one story including 21 themes. The longest story (792 words, 4422 characters) is shown in Appendix B.

Frequency distribution with number of themes (out of 43) coded in each submitted monarch story

Many of the most common coded themes were mentioned in one or both EDF emails, including beauty, planting milkweed, personal experiences, and knowledge of metamorphosis, migration, and reduction (see Appendix C for a complete list). The frequency of these email mentions (0, 1, 2) was correlated with their presence in people’s monarch stories, r (43) = 0.47, p  < 0.01. Even so, over half of the coded themes emerged without any prompting in emails. These novel themes included personal experiences in home gardens and yards, monarchs alighting on oneself or other people, and its role as a harbinger of other negative environmental changes, as well as being fragile, precious or treasured, as suggested by theories of altruism that derive from caregiving (Preston 2013 ).

In Table 1 , the 43 coded themes are shown with their frequency of occurrence across stories, rank order of frequency, and interrater agreement for each theme.

The most frequent theme reported (of the 43 identified) was beauty , observed in over 35% of stories . The beauty of the monarch species was mentioned in a much higher proportion of stories than any other individual theme. For example, one story was simply, “The monarch to me represents an iconic image of nature and beauty.” Across many themes, conservation concerns were reported, with planting to feed the monarchs mentioned in over 25% of stories; for example, “I love butterflies and have milkweed, butterfly weed, butterfly bushes and many other butterfly happy plants in my 2-acre yard with fruit orchard in the hills south of Syracuse NY. I do not use pesticides.” Other conservation themes were personal experiences observing monarch reduction (17%):

I love the beauty of the Monarchs. Every year I see less and less of them in my yard which breaks my heart. I try to plant flowers that are butterfly and bee friendly. I let the milkweed grow and spread in my yard.

A subset of these conservation stories admonished human actions (e.g., corporate greed, pesticides , harbinger of broad decline) , and described the monarch as a proverbial “canary in a coal mine.” Moreover, even though most stories included positive emotions (83%), some of these stories also expressed anger at the actions of corporations and practices related to farming. For example:

Living in rural Massachusetts in the 1950s, there were other butterflies to see, but the Monarch was always the most awesome. What losing the Monarch means to me is that we have finally lost...the greed of the companies that only want to rape the land, the animals for profit. They've been allowed or bribed their way into winning...not just in the USA. I think the use of glyphosphate is just too pervasive, but we don't seem to be able to stop it here. I'm just sad and feel that the Monarch is another "canary" to show that living things are being killed off.

For the majority of contributors, writing “your Monarch Story” drew people in to write first-hand accounts of their personal experiences with the species. These themes emphasized personal encounters with monarchs, reflected in the 3rd most frequent theme of Childhood memories (23%) in many contexts (e.g., in the yard, at school, during migration):

When I was in second grade, I found a monarch egg on a milkweed leaf, so I brought it home and raised the caterpillar. I named it Tracy because that is a gender-neutral name. When Tracy emerged as a butterfly, I found it was a female. I let her go back into nature and then prepared a timeline of her life to present to my classmates. It was a big hit.

Adult experiences were also frequently reported:

One of the most moving experiences in my life was going to El Rosario Monarch Butterfly Preserve in Mexico where monarch butterflies overwinter. So rarely do we see such an assemblage of so many individuals of one species in such a tiny area. The trees were completely ornamented with monarch butterflies. When the monarchs would take flight, it was like being in an orange and black blizzard. So infrequently do wildlife interact with us humans other than by turning tail and running, but I had multiple monarchs alight on my arms and head. This experience wasn't just moving, it was life-defining.

The 4th most frequent theme was positive emotions (22%), including joy, happiness, delight; for example, “I worked at a domestic violence shelter, and every year one beautiful monarch would visit the garden, and it brought me such happiness! Imagine what a multitude would do.” The stories also frequently expressed a sense of awe and magic arising from monarch encounters:

I just remember that as a child I would see lots and lots of Monarchs passing through our city of Covina, CA each year and I always marveled at their ethereal, colorful beauty. It was somehow awe-inspiring and almost magical. Fast forward 50 years and I'm lucky if I see more than a handful each year. A world without Monarchs altogether would be a world lacking their magic and that would be sad indeed.

Many stories reflected species-specific qualities such as metamorphosis and mass migration; for example:

Monarch butterflies are beautiful, amazing creatures - but strangely they always remind me of my brother Dan. I was riding with my sister and brother-in-law in South Dakota from my brother's wedding to his reception when we saw a flock of monarch butterflies, and my brother-in-law explained to me their amazing migration habits. I realized that they're not only beautiful and fragile, but also strong in many ways. Actually, just seeing one makes me smile.

The monarch’s important role in the ecosystem as a pollinator and sign of ecological balance was also reflected in the stories:

I live in GMO farming country. We no longer have common brown bats, wild honey bees, little milkweed either. Last year my wife and I planted a pollinator garden and half of it was planted with milkweed that I started from seed. We were pleasantly surprised, having only seen 2 monarchs all summer, to witness the formation of 12 chrysalis under our shed eave and all 12 hatched. HABITAT IS EVERYTHING WHEN IT COMES TO NATURE! If you plant it they will come. We also were successful in convincing one landowner to plant timothy hay rather than GMO crops on his leased land. We will continue the good fight and yes the pollinator garden has already been expanded.

While these most frequent themes represent commonalities in the stories, many other themes emerged to reflect a great diversity among the submitted stories. Some included figurative references to the monarch’s association with freedom (8%) and springtime (7%), spirituality (4%), and its value as an artistic symbol ( appear in art or poems, 2% ). Other stories captured stories about missing loved ones (5%), reflecting loss or remembrance of a loved one when seeing a Monarch:

My story starts with when my mother passed. I watched her body transform into the spirit. After her death the monarch butterfly would often fly in circles around me reminding me of her transformation with her spirit and presence changing from this shell she lived in as the butterfly transforms into a new form.

Though submitted on a public website, the recorded stories are striking in their revelation of personal, heart-felt memories and experiences, specific knowledge about monarchs, and concern for conservation efforts on their behalf. The wealth of specific associations in the submitted monarch stories suggests monarch are a touchstone in the story writers’s lives over time.

Factor analysis of observed themes

The 43 themes resulted in a five-factor solution from the Principal Components Analysis (PCA) with four factors including three subsumed themes and one factor including only one theme (see Table 2 ). We labelled the extracted factors as: (1) Raising Monarchs, with themes about raising butterflies (10), personal experiences with metamorphosis (7), and learning in science classes and schools (32); Denounces Reduction, with themes of loss and sadness over reduction (9), anger about greed and influence of corporations (33) and money interests; 3) Awe at Migration, with themes of awe and wonder (5), personal experiences with massing monarchs (8) and migration (12); (4) Planting Milkweed , with a single theme of planting to feed butterflies (2); and 5) Species Attributes, with themes of strength (e.g., resilience and perseverance) (36), amazing abilities (e.g., “incredible”) (30), and fragility (e.g., “delicate”) (28).

Among these five composite factors, Raising Monarchs and Planting Milkweed ( r  = 0.14, p  < 0.001) were positively correlated, as might be expected. Awe at Mass Migration increased with mentions of Species Attributes ( r  = 0.11, p < 0.01) and decreased with mentions of Raising Monarchs ( r  = -0.09, p  < 0.05) and Planting Milkweed ( r  = -0.17, p  < 0.001). No other significant correlations were observed.

Correlational analyses with theme clusters

Next, we examined intercorrelations for the 13 theme clusters (compiled from the 43 observed themes). To predict conservation efforts, we focused on three theme clusters describing motivations and actions directed toward monarch conservation: Calls to act, Working to save, and Distress at loss. The Calls to act theme cluster stories spoke out about the need for collective action:

Butterflies are magical to me. Every single time I see one, I smile. I absolutely love them and the habitat loss due to increased use of pesticides must stop immediately.

Stories including the Working to save theme cluster included actions such as planting:

We have planted a demonstration Pollinator Meadow on our complex of 142 acres and have distributed over two hundred milkweed plants to residents for their own gardens and planters. Also, we have encouraged our grounds staff to stop cutting back wild milkweed where ever possible when they manicure the grounds.

About a third of the stories expressed Distress at loss from monarch reduction; for example , “ There used to be a lot of butterflies and bees around. I do not see any more. Scary!” We tested whether each of these three conservation themes were associated with one another and the remaining theme clusters (see Table 3 ).

Several significant associations were revealed among the three conservation-related theme clusters and with the remaining clusters. Stories expressing Distress at loss and Calls to act were positively correlated ( r  = 0.13, p  < 0.001), and both mentioned Role in the ecosystem more often, suggesting that more knowledge about broader environmental issues is tied to both. The conservation theme of Working to save the monarch was predicted by both Personal experiences and Positive emotions; however, Working to save stories were less likely to also mention Calls to act and were unrelated to Distress at loss. A potential explanation for the inconsistent relationship between conservation themes is the negative spillover effect (Raimi 2017 ), whereby people who take one type of active response to an environmental concern are less enthusiastic about supporting larger policy or systemic solutions.

Relationships with demographic variables

Finally, we tested for correlations between the nine demographic variables (Table 4 ) and the five composite factors and 13 theme clusters.

Several patterns of associations with attributes of the story writers emerged across these correlational analyses. The majority of story writers were women, and they were more likely to mention the special qualities of the monarch species, its beauty, their experiences raising monarchs and positive emotions about them. This group was also more likely to call for collective action to save the monarch. Mentions of monarch beauty were less frequent for those with more education and more donation history.

A second pattern of association centered on descriptions of personal awe at mass migration. This theme was more likely for older, more educated writers with higher incomes and net worth, and more donation history (number of gifts and dollars). Older respondents may more frequently discuss mass migration because it was easier to experience before recent reduction. This association is reflected in both the factor scores and the migration theme cluster, and the size of the correlations are larger than for other patterns.

A third pattern groups writers reporting experiences of raising monarchs, planting milkweed, and working to save the monarch. These stories are associated with older, female, and more affluent homeowners who are already active donors. This pattern may reflect those interested and able to manage garden projects to support monarchs.

A final pattern associates stories expressing distress at the loss of monarchs and denouncing their reduction with writers in rural areas. A higher likelihood of seeing natural populations of monarchs may have made rural residents better able to personally note the current reduction in monarch populations. Interestingly, these patterns appear distinct; for example, the mass migration factor is negatively related to raising and planting for monarchs, and the Call to action theme cluster is negatively related to Working to save monarchs. While the demographics suggest different uses of themes based on story writer characteristics, the small size of the correlations suggests there are many overlaps in story themes across demographic categories.

In sum, both quantitative and qualitative analyses identified monarch-specific qualities (e.g., metamorphosis, milkweed, migration, and species attributes) together with concern for their conservation as prominent themes. The qualitative analysis offers additional information about what story writers think about monarchs; notably, many describe personal experiences as adults and in childhood memories, along with strong emotions and with the appeal of the monarch’s beauty. Interestingly, different patterns of association occurred for writers reflecting distress at monarch loss with calls for action compared to those with higher donations. Those with more resources included a pattern of personal efforts such as planting milkweed while others were monarch enthusiasts who were not engaged in conservation actions. The mixed methods approach in our study utilized qualitative analysis of themes to suggest meaning behind the findings from quantitative methods, producing a richer account of people’s monarch stories contributed to the campaign.

Whereas previous empirical studies compared perceptions of flagships across species (Caro et al. 2004 ; Schlegel and Rupf 2010 ; Barua 2011 ; Barua et al. 2012 ; Roberge 2014 ; MacDonald et al. 2015 ), this study is the first to examine people’s in-depth responses to a single flagship species both qualitatively and quantitatively. The results show that monarch butterflies have special appeal that differs among individuals. Taking a broad perspective, distinctive patterns of relationships in theme clusters, factors, and demographic variables are evident across the Monarch Stories. These patterns emerge from considering the intercorrelations among the five identified PCA factors (Table 2 ), the theme clusters arising from the qualitative analysis (Table 3 ), and the significant correlations with demographic variables (Table 4 ). These patterns suggest that groups of Monarch Story contributors differed in the qualities emphasized in their stories and in their conservation actions.

The role of personal connection

The finding that personal encounters with monarchs powerfully influence conservation themes is consistent with Bandura’s ( 1999 , 2018 ) theory of motivation tying personal experiences to people’s later actions. That is, people’s conservation interests and actions may reflect their acquired, self-relevant learning experiences. Many people living in the U.S. have personal memories of monarch encounters, along with childhood memories about caring for monarchs from school programs (Young-Isebrand et al. 2015 ; Gustafsson et al. 2015 ). People’s responses to monarch reduction may also be structured by shared cultural history and associations (DeMello 2012 ; Jepson and Barua 2015 ; Gustafsson et al. 2017 ) and place-specific ties (Jepson and Barua 2015 ; Horsley et al. 2020 ) to their experiences. Early positive experiences may motivate later conservation interest and actions (see Bandura 2018 ).

The monarch stories also describe powerful feelings associated with monarchs, such as “joy,” and “awe,” as in a sense of wonder and magic, along with other attributes like strength and perseverance (Gustafsson et al. 2015 ; Simaika and Samways 2018 ). Encounters with monarchs may thus lead to more intimate emotional connections to them based on their familiarity from experience (Schlegel and Rupf 2010 ; Macdonald et al. 2015 ). Studies have shown a link between positive feelings of awe and intentions (Keltner and Haidt 2003 ), and awe toward nature leads spiritual people to express feelings of oneness with others (Van Cappellen and Saroglu 2012 ). Awe has also been shown to serve as a precursor to science learning (Valdesolo et al. 2017 ), so the pervasive presence of awe around mass migration may elicit openness to learning, as documented by the frequent descriptions of learning about monarchs in the stories. Awe has also been associated with altruism (Stellar et al. 2017 ), suggesting that awe might promote interest and giving to environmental campaigns.

Altruistic themes in the monarch stories—a novel finding—emerged as many stories focused upon current caretaking actions for monarchs, such as planting milkweed to feed them, raising monarchs through their early life cycle, joining conservation monitoring groups and volunteering to help them. These results are consistent with theories of altruism related to caregiving (Preston 2013 ), which predict that people are motivated by a perceived need to care for attractive, vulnerable others in immediate need. Females as a demographic group also more often mentioned raising butterflies, planting milkweed, and the need for action, consistent with this theory. Lewandowski and Oberhauser ( 2017 ) found that monarch waystation volunteers planned to donate at the same or higher levels afterwards, further indicating that altruistic conservation actions and donations are related. The identification of needs and the provision of first-hand support for the species may be more appealing for those with caregiving motivations and may remain unfulfilled by other forms of altruism, such as financial donations toward land conservation. Further, asking contributors to identify their current conservation actions may increase awareness of potential “negative spillover” (Raimi 2017 ), wherein people may react to proposed environmental interventions with their own, individual efforts in front of mind.

Implications

This study may offer insights for future conservation campaigns. While previous studies found that people prefer larger, charismatic mammals (Schlegel and Rupf 2010 , Barua 2012 ; Roberge 2014 ; Macdonald et al. 2015 , 2017 ) with aesthetic appeal (Smith et al. 2012 ), our findings documented people’s positive feelings for an insect. Though Schlegel and Rupf ( 2010 ) had found that butterflies were preferred even over mammals, invertebrates are rarely selected as flagship species. Our study found evidence that monarchs draw people in to respond to their conservation needs based upon the monarch’s beauty, the emotions they evoke, their familiarity, and memories of positive personal encounters. Monarchs also feature distinctive species attributes that are observed in school programs, citizen science projects, and cultural communications. Moreover, based upon these early experiences, many people are already knowledgeable about and interested in monarch conservation that, as Bandura ( 2018 ) argues, may establish a motivation to engage in their conservation. A challenge for future research is to identify other species with similar personal and experiential ties within other regional populations.

An important implication of this study is that personal, direct experiences with a flagship species may motivate later action. The monarch’s accessibility in the U.S. seems a key factor in their appeal: currently, people are still encountering monarchs in their gardens, parks, and schools (or noting their absence). Often, conservation campaigns are planned from the reverse direction: they provide new information to stir emotions in order to motivate people to act. Our findings suggest that conservation programs might instead engage people in conservation actions first in order to build awareness, positive feelings, and personal memories. Experiences occurring as precursors may build the link to later conservation actions like making donations. Positive experiences (e.g., studying monarchs in grade school) can be strong motivators in and of themselves, and can stimulate a positive link between emotions, awareness and further conservation actions (Singleton 2016 ).

Conservation campaigns may promote this by providing opportunities to interact with species first-hand, creating personal knowledge and experiences with specific species encountered in local areas. Segmenting campaigns to highlight species encounters based on geographic region may be better able to build more personal experiences and commitment. Increasing animal contact for children has been shown to increase propensity for biophilia and decreases biophobia, along with enhancing pro-conservation attitudes (Zhang et al. 2014 ). Our findings suggest that adult groups may also benefit from continued encounters with local species, helping people remain engaged and informed about why and how to be active in the process of their conservation. In particular, the themes that center around caretaking, such as raising monarchs and helping animals in need, may elicit support from people who are motivated by nurturing in ways that are unfulfilled by financial donations.

While many species are now difficult to encounter in the wild, technological advances may increase exposure and familiarity; for example, people can see what an animal sees in the field through animal-borne video and environmental data collection systems (AVEDs) (Moll et al, 2007 ), and camera trap technology may allow even real-time observations of threatened species by the public (Belbachir et al. 2015 ). Opportunities through social media campaigns offer new ways of engagement with more region- or interest-specific encounters. For environmental organizations, engaging donors and program stakeholders in interconnected actions over time may increase commitment and investment (Lewandowski and Oberhauer 2017 ). Developing public engagement campaigns that are “personal” may prove instrumental in reaching a common goal to preserve biodiversity.

This study also highlights the importance of learning more about differences in people’s responses to flagship species in order to more effectively incorporate them into conservation campaigns. Are species attributes (beauty or mass migration) or experiences with them (near home, “hands-on”) more important to individuals? If positive experiences and personal memories are most impactful, campaigns can be designed with regional foci leading to greater personal investment in engaging, helping, and donating on behalf of a species. Appreciation of animals is constructed within a sociocultural milieu (Gustafsson et al. 2017 ), with positive cultural associations shaped by history and the specifics of place (Jepson and Barua 2015 ). DeMello ( 2012 ) stressed the importance of the spaces animals occupy in human social and cultural worlds, and the interactions humans have with them. Further research should explore how people within regional cultures respond to specific species, and what kinds of experience-based learning methods inspire people to make the leap from awareness to understanding to action.

These findings support the claim by Gustafsson and colleagues ( 2015 , 2017 ) that the monarch has been perhaps uniquely positioned over many years to serve as a symbol for conservation in the U.S. (Gustafsson et al. 2015 ). For those responding to the EDF’s Monarch Stories campaign, the monarch’s beauty, natural wonder in mass migration, and familiarity from individual encounters has led to deep ties and a strong motivation to help them. In future studies, ENGOs willing to provide data from campaigns may document the relationships to flagship species suggested in this study. Considering flagship-specific data may support innovative social media campaigns and identify alternate forms of engagement that are effective for distinct groups of donors.

Finally, a key finding emerging from the monarch stories was the emotion reflected in people’s stories about individual monarchs. Conservation organizations may avoid emotional appeals because they seem “alarmist” or too “touchy-feely” for science-based programs. Yet in this study, deep emotions arising from precious memories were readily offered by the public engaging in the campaign. Our study suggests that conservationists should seek to evoke, not avoid, emotion as part of conservation campaigns in order to motivate action. Nuanced communication that weaves meaningful emotional experiences into science-based appeals may increase the effectiveness of conservation campaigns.

EDF’s Monarch Stories Campaign included innovations that successfully engaged their members. By seeing a personal story from EDF staff in an email, people were “primed” to discuss both the same and novel topics in their own stories. These social interactions may serve to scaffold the development of people’s views of conservation, increasing their sense of community and commitment to environmental concerns. And their novel approach of asking, “What does the Monarch mean to you?” encouraged people to think about a conservation issue as their personal concern. This low-investment activity may be an effective means of drawing people into the campaign and the EDF website, influencing their further interaction with organizational materials and potentially their financial support for the campaign.

Limitations

This mixed methods study investigated a single campaign as a case study with an interpretivist epistemological perspective (Flyvbjerg 2001 , 2006 ; Patton 2002 ) where the outcomes depend on the context, and the context is integrated into the analysis of findings (Creswell 1994 ; Patton, 2002 ). The outcomes are not intended for generalization across campaign contexts differing substantially from this case. Our findings are strictly associational, and no causal conclusions can be drawn. While the associations reported are statistically significant, most account for only a small proportion of the variance; for example, the positive correlation between the theme clusters, “distress at loss” and “role in the ecosystem” accounts for approximately five percent of the variance. However, across a large sample of potential donors, small influences leading individuals to act are of practical significance.

Available demographic information for the sample was also limited, and participants were existing members at EDF (likely to be U.S. residents, already committed to conservation, and interested in EDF’s pragmatic and solutions-focused approach). As noted above, the campaign materials included two example stories with themes that appeared often in the collected stories; however, more than half of the themes observed were not mentioned at all in EDF materials.

Overall, our findings show that people share awe-inspired, joyous memories of their personal encounters with beautiful monarchs. However, this experiential point of contact may be only infrequently engaged when designing conservation campaigns. Selecting flagship species for campaigns by assessing preferences in the abstract (Schlegel and Rupf 2010 ; Verissimo et al. 2011 ; MacDonald et al. 2015 ; Tensen 2018 ) may fail to capture the strong draw of lived experiences with specific species in local environments. Drawing on personal experiences with wildlife builds awareness and associations with species that may increase later motivation to help in their conservation.

As Richard Louv ( 2005 ) suggested, childhood experiences in the natural world are predictors of conservation activism in adulthood. In the Monarch Story campaign, a quarter of adults described childhood encounters with monarchs through school programs that predicted their current efforts to save monarchs. Children exposed to monarchs in science classes are not only learning about science: They are also building intimate connections to individual monarchs through personal experiences that echo through encounters with the species throughout their lives. Outreach programs, classes, and field trips foster memorable one-on-one encounters between species, building personal engagement and creating future conservationists.

Data availability

Story data is available upon request.

Abercrombie N, Hill S, Turner BS, Erofeev SA (1984) The Penguin dictionary of sociology. Penguin, Harmondsworth, UK

Bandura A (1999) Social cognitive theory of personality. Handbook Personal 2:154–196

Google Scholar  

Bandura A (2001) Social cognitive theory: An agentic perspective. Annu Rev Psychol 52:1–26. https://doi.org/10.1146/annurev.psych.52.1.1

Article   PubMed   CAS   Google Scholar  

Bandura A (2018) Toward a psychology of human agency: Pathways and reflections. Perspect Psychol Sci 13(2):130–136. https://doi.org/10.1177/1745691617699280

Article   PubMed   Google Scholar  

Barua M (2011) Mobilizing metaphors: the popular use of keystone, flagship and umbrella species concepts. Biodiv Conserv 20:1427. https://doi.org/10.1007/s10531-011-0035-y

Article   Google Scholar  

Barua M, Gurdak DJ, Ahmed RA, Tamuly J (2012) Selecting flagships for invertebrate conservation. Biodiv Conserv 21:1457–1476. https://doi.org/10.1007/s10531-012-0257-7

Belbachir F, Pettorelli N, Wacher T, Belbachir-Bazi A, Durant SM (2015) Monitoring rarity: the critically endangered Saharan cheetah as a flagship species for a threatened ecosystem. PLoS One, 10(1)

Bennett JR, Maloney R, Possingham HP (2015) Biodiversity gains from efficient use of private sponsorship for flagship species conservation. Proceed Royal Soc B: Biol Sci 282(1805):20142693

Boeije H (2002) A purposeful approach to the constant comparative method in the analysis of qualitative interviews. Qual Quant 36(4):391–409

Born D (2019) Bearing witness? Polar bears as icons for climate change communication in National Geographic . Environ Commun 13(5):649–663

Caro T, Engilis A Jr, Fitzherbert E, Gardner T (2004) Preliminary assessment of flagship species concept at a small scale. Anim Conserv 7:63–70

Creswell JW (1994) Research design: Qualitative and quantitative approaches. Sage, Thousand Oaks, CA

Creswell, J. W. (2017). Research design: Qualitative, quantitative, and mixed methods approaches . Sage Publications.

DeMello M (2012) Animals and society: an introduction to human-animal studies. Columbia UP, New York

Douglas LR, Winkel G (2014) The flipside of the flagship. Biodivers Conserv 23(4):979–997

Environmental Defense Fund (2018). Monarch stories. https://www.edf.org/what-you-can-do-help-Monarchs . 12 Jan 2018

Environmental Defense Fund (2020). Why we need a variety of ways to protect wildlife. https://www.edf.org/ecosystems/why-we-need-variety-ways-protect-wildlife . 25 March 2020

Flyvbjerg B (2001) Making social science matter: Why social inquiry fails and how it can succeed again. Cambridge University Press, Cambridge, UK

Book   Google Scholar  

Flyvbjerg B (2006) Five misunderstandings about case-study research. Qual Inq 12(2):219–245

Flyvbjerg B (2011) Case study. In: Denzin NK, Lincoln YS (eds) The Sage handbook of qualitative research, 4th edn. Sage, Thousand Oaks, CA, pp 301–316

Greene RW, Shepard J (2003) Sociology and you . Glencoe Mc Graw-Hill, Ohio, pp A–22

Gustafsson KM, Agrawal AA, Lewenstein BV, Wolf SA (2015) The monarch butterfly through time and space: The social construction of an icon. Bioscience 65(6):612–622

Gustafsson KM, Agrawal AA, Wolf SA (2017) Science-policy-practice interfaces: emergent knowledge and monarch butterfly conservation. Environ Policy Gov 27:521–533

Horsley S, Hohbein R, Morrow K, Green GT (2020) What’s in a name? A content analysis of environmental NGOs’ use of “iconic species” in press releases. Biodiv Conserv 29:2711–2728. https://doi.org/10.1007/s10531-020-01995-7(0123456789

Jepson P, Barua M (2015) A theory of flagship species action. Conserv Soc 13(1):95–104

Keltner D, Haidt J (2003) Approaching awe, a moral, spiritual, and aesthetic emotion. Cogn Emot 17(2):297–314

Lemelin RH, Jaramillo-López PF (2019) Orange, black, and a little bit of white is the new shade of conservation: the role of tourism in Monarch Butterfly conservation in Mexico. J Ecotourism 1–13.

Lemelin RH, Boileu EYS, Russell C (2019) Entomotourism: the allure of the arthropod. Soc Anim 27:733–750

Lewandowski EJ, Oberhauser KS (2017) Contributions of citizen scientists and habitat volunteers to monarch butterfly conservation. Hum Dimens Wildl 22(1):55–70. https://doi.org/10.1080/10871209.2017.1250293

Louv R (2005) Last child in the woods: Saving our children from nature-deficit disorder. Workman Publishing Company, New York

Macdonald EA, Burnham D, Hinks AE, Dickman AJ, Malhi Y, Macdonald DW (2015) Conservation inequality and the charismatic cat: Felis felicis. Global Ecol Conserv 3:851–866

Macdonald EA, Hinks A, Weiss DJ, Dickman A, Burnham D, Sandom CJ, Macdonald DW (2017) Identifying ambassador species for conservation marketing. Global Ecol Conserv 12:204–214

McGinlay JM, Parsons DJ, Morris J, Hubatova M, Graves A, Bradbury RB, Bullock JM (2017) Do charismatic species groups generate more cultural ecosystem service benefits? Ecosyst Serv 27A:15–24

Moll RJ, Millspaugh JJ, Beringer J, Sartwell J, He Z (2007) A new ‘view ‘of ecology and conservation through animal-borne video systems. Trends Ecol Evol 22(12):660–668

Monarch Joint Venture (2020). About Us. https://Monarchjointventure.org/ . 27 March 2020

Nail KR, Altizer S, Oberhauser KS (2015) Monarchs in a changing world: Biology and conservation of an iconic butterfly. Cornell University Press, United States

Oberhauser KS, Nail KR, Altizer S (Eds) (2018) Monarchs in a changing world: biology and conservation of an iconic butterfly . Cornell University Press

Patton MQ (2002) Qualitative evaluation and research methods, 3rd edn. Sage, Thousand Oaks, CA

Preston SD (2013) The origins of altruism in offspring care. Psychol Bull 139(6):1305–1341. https://doi.org/10.1037/a0031755

Raimi K (2017) Negative spillover to policy. Nat Clim Change 7:473–474. https://doi.org/10.1038/nclimate3317

Roberge JM (2014) Using data from online social networks in conservation science: which species engage people the most on Twitter? Biodivers Conserv 23(3):715–726

Schlegel J, Rupf R (2010) Attitudes towards potential animal flagship species in nature conservation: a survey among students of different educational institutions. J Nat Conserv 18(4):278–290

Simaika JP, Samways MJ (2018) Insect conservation psychology. J Insect Conserv 22:635–642. https://doi.org/10.1007/s10841-018-0047-y

Simberloff D (1998) Flagships, umbrellas, and keystones: Is single-species management passe in the landscape era? Biodivers Conserv 83:247–257

Singleton, J. (2016). Environmental literacy and sustainability values: A content analysis of environmental education standards.  ECO-THINKING ,  1 . https://eco-thinking.org/index.php/journal/article/view/984

Smith RJ, Verissimo D, Isaac NJB, Jones KE (2012) Identifying Cinderella species: uncovering mammals with conservation flagship appeal. Conserv Lett 5:205–212

Stellar JE, Gordon AM, Piff PK, Cordaro D, Anderson CL, Bai Y, Maruskin LA, Keltner D (2017) Self-transcendent emotions and their social functions: compassion, gratitude, and awe bind us to others through prosociality. Emot Rev 9(3):200–207

Tensen L (2018) Biases in wildlife and conservation research, using felids and canids as a case study. Global Ecol Conserv 15:e00423. https://doi.org/10.1016/j.gecco.2018.e00423

Thogmartin WE, Wiederholt R, Oberhauser K, Drum RG, Diffendorfer JE, Altizer S, Taylor OR, Pleasants J, Semmens D, Semmens B, Erickson R, Libby K, Lopez-Hoffman L (2017) Monarch butterfly population decline in North America: identifying the threatening processes. Royal Soc Open Sci 4(9):170760. https://doi.org/10.1098/rsos.170760

Thomas-Walters L, Raihani NJ (2017) Supporting conservation: the roles of flagship species and identifiable victims. Conserv Lett 10(5):581–587. https://doi.org/10.1111/conl.12319

Urquhart FA, Urquhart NR (1976) The overwintering site of the eastern population of the monarch butterfly ( Danaus P. Plexippus ; Danaidae) in southern Mexico. J Lepidopterists’ Soc 30:153–158

Valdesolo P, Shtulman A, Baron AS (2017) Science is awe-some: the emotional antecedents of science learning. Emot Rev 9(3):215–221

Van Cappellen P, Saroglou V (2012) Awe activates religious and spiritual feelings and behavioral intentions. Psychol Relig Spiritual 4(3):223

Verissimo D, MacMillan DC, Smith RJ (2011) Toward a systematic approach for identifying conservation flagships. Conserv Lett 4:1–8

Warner RM (2008) Applied statistics: From bivariate through multivariate techniques. Sage, New York

The White House (2014) Presidential memorandum -- Creating a federal strategy to promote the health of honey bees and Other pollinators . Office of the Press Secretary. https://obamawhitehouse.archives.gov/the-press-office/2014/06/20/presidential-memorandum-creating-federal-strategy-promote-health-honey-b . 20 June 2014

World Wildlife Fund (2020). Adopt a polar bear. https://www.worldwildlife.org/species/polar-bear . 1 June 2020

Young-Isebrand, E., Oberhauser, K. S., Bailey, K., Charest, S., Hayes, B., Howard, E., Lovett, J,, Meyers, S., Mollenhauer, E., Montesiños-Patino, E. B., Ryan, A., Taylor, O. R., & Treviño, R. (2015). Environmental education and monarchs: Reaching across disciplines, generations, and nations. In K. S. Oberhauser, K. R., Nail & S. Altizer (Eds.). (2015). Monarch s in a changing world: Biology and conservation of an iconic butterfly (pp. 5–12). Cornell University Press.

Zhang W, Goodale E, Chen J (2014) How contact with nature affects children’s biophilia, biophobia and conservation attitude in China. Biol Cons 177:109–116

Download references

Acknowledgements

We thank Audrey Archer at the Environmental Defense Fund for her assistance with data access. We also thank Skylar Burkhardt and Amanda Szczesniak, undergraduate research assistants at the University of Michigan, for their contributions to the project. We are grateful to the Environmental Defense Fund for their willingness to contribute anonymized web page entries and demographic information.

A grant to support data analyses was provided by Environmental Defense Fund and the Graham Sustainability Institute to S. D. Preston and C. M. Seifert at the Department of Psychology, University of Michigan, Ann Arbor.

Author information

Authors and affiliations.

University of Michigan, Ann Arbor, USA

Stephanie D. Preston, Julia D. Liao, Julia Speiser & Colleen M. Seifert

Environmental Defense Fund, New York, USA

Theodore P. Toombs & Rainer Romero-Canyas

You can also search for this author in PubMed   Google Scholar

Corresponding author

Correspondence to Colleen M. Seifert .

Ethics declarations

Conflict of interest.

Two of the authors (Theodore Toombs and Rainer Romero-Canyas) are currently employed as scientists at the Environmental Defense Fund.

Consent for publication

All authors agree.

Additional information

Communicated by Peter Bridgewater.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 36 kb)

Rights and permissions.

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ .

Reprints and permissions

About this article

Preston, S.D., Liao, J.D., Toombs, T.P. et al. A case study of a conservation flagship species: the monarch butterfly. Biodivers Conserv 30 , 2057–2077 (2021). https://doi.org/10.1007/s10531-021-02183-x

Download citation

Received : 30 August 2020

Revised : 23 March 2021

Accepted : 12 April 2021

Published : 04 May 2021

Issue Date : June 2021

DOI : https://doi.org/10.1007/s10531-021-02183-x

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

• Conservation
• Conservation marketing
• Environmental psychology, environmental attitudes
• Mixed methods
• Monarch butterflies
• Find a journal
• Publish with us
• Track your research

An official website of the United States government

The .gov means it’s official. Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

The site is secure. The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

• Publications
• Account settings
• My Bibliography
• Collections
• Citation manager

Save citation to file

Email citation, add to collections.

• Create a new collection
• Add to an existing collection

Add to My Bibliography

Your saved search, create a file for external citation management software, your rss feed.

• Search in PubMed
• Search in NLM Catalog
• Add to Search

Genomics in Conservation: Case Studies and Bridging the Gap between Data and Application

Affiliations.

• 1 Flathead Lake Biological Station, Fish and Wildlife Genomic Group, Division of Biological Sciences, University of Montana, Polson, MT 59860, USA; Wildlife Program, Fish and Wildlife Genomic Group, College of Forestry and Conservation, University of Montana, Missoula, MT 59812, USA.
• 2 Flathead Lake Biological Station, Fish and Wildlife Genomic Group, Division of Biological Sciences, University of Montana, Polson, MT 59860, USA. Electronic address: [email protected].
• 3 Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, QC G1V 0A6, Canada.
• 4 Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, NH 03824, USA.
• 5 Molecular Genetics Laboratory, Pacific Biological Station, Nanaimo, BC V9T 6N7, Canada.
• 6 Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 8901 La Jolla Shores Drive, La Jolla, CA 92037, USA.
• 7 Columbia River Inter-Tribal Fish Commission, Hagerman Fish Culture Experiment Station, 3059-F National Fish Hatchery Road, Hagerman, ID 83332, USA.
• 8 Theodosius Dobzhansky Center for Genome Bioinformatics, St Petersburg State University, 41 Sredniy Prospect, St Petersburg, Russia.
• 9 Alaska Department of Fish and Game, Division of Wildlife Conservation, 802 3rd Street, Douglas, AK 99824, USA.
• 10 Gene Conservation Laboratory, Alaska Department of Fish and Game, 333 Raspberry Road, Anchorage, AK 99518, USA.
• 11 School of Biological Sciences, Monash University, Melbourne, VIC 3800 Australia.
• 12 Washington Department of Fish and Wildlife, Molecular Genetics Laboratory, 600 Capitol Way N., Olympia, WA 98501, USA.
• 13 Conservation Genetics Laboratory, 1011 East Tudor Road, MS 331, Anchorage, AK 99503, USA.
• PMID: 26654124
• DOI: 10.1016/j.tree.2015.10.009

Keywords: conservation biology; conservation genomics; conservation practice; genetic monitoring; natural resource management; next-generation sequencing; population genomics.

PubMed Disclaimer

• Reply to Garner et al. Shafer ABA, Wolf JBW, Alves PC, Bergström L, Colling G, Dalén L, De Meester L, Ekblom R, Fior S, Hajibabaei M, Hoezel AR, Hoglund J, Jensen EL, Krützen M, Norman AJ, Österling EM, Ouborg NJ, Piccolo J, Primmer CR, Reed FA, Roumet M, Salmona J, Schwartz MK, Segelbacher G, Thaulow J, Valtonen M, Vergeer P, Weissensteiner M, Wheat CW, Vilà C, Zieliński P. Shafer ABA, et al. Trends Ecol Evol. 2016 Feb;31(2):83-84. doi: 10.1016/j.tree.2015.11.010. Epub 2015 Dec 17. Trends Ecol Evol. 2016. PMID: 26704456 No abstract available.
• Genomics and the challenging translation into conservation practice. Shafer AB, Wolf JB, Alves PC, Bergström L, Bruford MW, Brännström I, Colling G, Dalén L, De Meester L, Ekblom R, Fawcett KD, Fior S, Hajibabaei M, Hill JA, Hoezel AR, Höglund J, Jensen EL, Krause J, Kristensen TN, Krützen M, McKay JK, Norman AJ, Ogden R, Österling EM, Ouborg NJ, Piccolo J, Popović D, Primmer CR, Reed FA, Roumet M, Salmona J, Schenekar T, Schwartz MK, Segelbacher G, Senn H, Thaulow J, Valtonen M, Veale A, Vergeer P, Vijay N, Vilà C, Weissensteiner M, Wennerström L, Wheat CW, Zieliński P. Shafer AB, et al. Trends Ecol Evol. 2015 Feb;30(2):78-87. doi: 10.1016/j.tree.2014.11.009. Epub 2014 Dec 17. Trends Ecol Evol. 2015. PMID: 25534246

Similar articles

• Life on Earth to have its DNA analysed in the name of conservation. [No authors listed] [No authors listed] Nature. 2018 Nov;563(7730):155-156. doi: 10.1038/d41586-018-07323-y. Nature. 2018. PMID: 30401859 No abstract available.
• Multiple Facets of Marine Invertebrate Conservation Genomics. Lopez JV, Kamel B, Medina M, Collins T, Baums IB. Lopez JV, et al. Annu Rev Anim Biosci. 2019 Feb 15;7:473-497. doi: 10.1146/annurev-animal-020518-115034. Epub 2018 Nov 28. Annu Rev Anim Biosci. 2019. PMID: 30485758 Review.
• A Bigger Toolbox: Biotechnology in Biodiversity Conservation. Corlett RT. Corlett RT. Trends Biotechnol. 2017 Jan;35(1):55-65. doi: 10.1016/j.tibtech.2016.06.009. Epub 2016 Jul 13. Trends Biotechnol. 2017. PMID: 27424151 Review.
• Integrating population genetics and conservation biology in the era of genomics. Ouborg NJ. Ouborg NJ. Biol Lett. 2010 Feb 23;6(1):3-6. doi: 10.1098/rsbl.2009.0590. Epub 2009 Sep 2. Biol Lett. 2010. PMID: 19726442 Free PMC article.
• Reversing the decline of threatened koala ( Phascolarctos cinereus ) populations in New South Wales: Using genomics to enhance conservation outcomes. Lott MJ, Frankham GJ, Eldridge MDB, Alquezar-Planas DE, Donnelly L, Zenger KR, Leigh KA, Kjeldsen SR, Field MA, Lemon J, Lunney D, Crowther MS, Krockenberger MB, Fisher M, Neaves LE. Lott MJ, et al. Ecol Evol. 2024 Jul 31;14(8):e11700. doi: 10.1002/ece3.11700. eCollection 2024 Aug. Ecol Evol. 2024. PMID: 39091325 Free PMC article.
• Integration of genomic and ecological methods inform management of an undescribed, yet highly exploited, sardine species. Coelho JFR, Mendes LF, Di Dario F, Carvalho PH, Dias RM, Lima SMQ, Verba JT, Pereira RJ. Coelho JFR, et al. Proc Biol Sci. 2024 Mar 13;291(2018):20232746. doi: 10.1098/rspb.2023.2746. Epub 2024 Mar 6. Proc Biol Sci. 2024. PMID: 38444338
• Integration of fluorescence in situ hybridization and chromosome-length genome assemblies revealed synteny map for guinea pig, naked mole-rat, and human. Romanenko SA, Kliver SF, Serdyukova NA, Perelman PL, Trifonov VA, Seluanov A, Gorbunova V, Azpurua J, Pereira JC, Ferguson-Smith MA, Graphodatsky AS. Romanenko SA, et al. Sci Rep. 2023 Nov 29;13(1):21055. doi: 10.1038/s41598-023-46595-x. Sci Rep. 2023. PMID: 38030702 Free PMC article.
• Resolving a nearly 90-year-old enigma: The rare Fagus chienii is conspecific with F. hayatae based on molecular and morphological evidence. Li DQ, Jiang L, Liang H, Zhu DH, Fan DM, Kou YX, Yang Y, Zhang ZY. Li DQ, et al. Plant Divers. 2023 Jan 12;45(5):544-551. doi: 10.1016/j.pld.2023.01.003. eCollection 2023 Sep. Plant Divers. 2023. PMID: 37936819 Free PMC article.
• Estimating microhaplotype allele frequencies from low-coverage or pooled sequencing data. Delomas TA, Willis SC. Delomas TA, et al. BMC Bioinformatics. 2023 Nov 3;24(1):415. doi: 10.1186/s12859-023-05554-z. BMC Bioinformatics. 2023. PMID: 37923981 Free PMC article.

Publication types

• Search in MeSH

LinkOut - more resources

Full text sources.

• Elsevier Science

Other Literature Sources

• scite Smart Citations

Miscellaneous

• NCI CPTAC Assay Portal
• Citation Manager

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

An official website of the United States government

The .gov means it’s official. Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

The site is secure. The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

• Publications
• Account settings

Preview improvements coming to the PMC website in October 2024. Learn More or Try it out now .

• Advanced Search
• Journal List
• v.9(1); 2016 Jan

Why evolution matters for species conservation: perspectives from three case studies of plant metapopulations

Isabelle olivieri.

1 Institut des Sciences de l'Evolution, Université Montpellier, CNRS, IRD, EPHE, CC65, Place Eugène Bataillon, 34095, Montpellier cedex 5, France

Jeanne Tonnabel

2 Department of Ecology and Evolution, Le Biophore, UNIL‐SORGE, University of Lausanne, Lausanne, Switzerland

Ophélie Ronce

Agnès mignot.

We advocate the advantage of an evolutionary approach to conservation biology that considers evolutionary history at various levels of biological organization. We review work on three separate plant taxa, spanning from one to multiple decades, illustrating extremes in metapopulation functioning. We show how the rare endemics Centaurea corymbosa (Clape Massif, France) and Brassica insularis in Corsica (France) may be caught in an evolutionary trap: disruption of metapopulation functioning due to lack of colonization of new sites may have counterselected traits such as dispersal ability or self‐compatibility, making these species particularly vulnerable to any disturbance. The third case study concerns the evolution of life history strategies in the highly diverse genus Leucadendron of the South African fynbos. There, fire disturbance and the recolonization phase after fires are so integral to the functioning of populations that recruitment of new individuals is conditioned by fire. We show how past adaptation to different fire regimes and climatic constraints make species with different life history syndromes more or less vulnerable to global changes. These different case studies suggest that management strategies should promote evolutionary potential and evolutionary processes to better protect extant biodiversity and biodiversification.

Introduction

This study belongs to a special issue on women's contribution to evolutionary biology. Through the review of past work of our group, led by Isabelle Olivieri (Box  1 ), we seek to illustrate why evolution needs to be considered in conservation biology, based on extensive studies of the recent evolutionary history in three plant taxa. Conservation biology should not only consist in conserving habitats, species richness or species, but it should be about promoting evolutionary potential and evolutionary processes at all levels of biodiversity (Box  2 ). We first briefly review general ideas about why conservation biology benefits from an evolutionary perspective, and then introduce three case studies that will illustrate how our work contributed to this debate.

Personal reflections.

Our group started its investigations in evolutionary conservation biology in 1993. Conservation biology then largely ignored evolutionary considerations. At best, in the nineties, population viability analyses included inbreeding depression (Lacy 1993 ). Genetic studies were rare, and then, only neutral molecular diversity was considered (Allendorf and Servheen 1986 ), often at a single point in time (but see Noss 1990 ). A new concept was then gaining much influence on the paradigms of conservation biology, that of metapopulations. In 1983, while IO was doing a postdoc at Stanford University, metapopulation was a big word in conservation biology, but studied from the demographic point of view only (Harrison et al. 1988 ). There was at that time no evolution being considered. It was around that time that IO initiated a new line of research investigating how a metapopulation functioning affects the evolution of dispersal and other life history traits, joined by several students and collaborators (among which OR) throughout the years (e.g. Olivieri and Gouyon 1985 , 1997 ; Olivieri et al. 1990 , 1995 ; Gandon et al. 1996 ; Ronce and Olivieri 1997 ; Godelle et al. 1998 ; Brachet et al. 1999 ; Ronce et al. 2000a , b ; Olivieri 2000 , 2001 ; Mathias et al. 2001 ; Ravigné et al. 2004 ; Ravigné et al. 2006 ; Ravigné et al. 2009 ; Vitalis et al. 2004 , 2014 ). This research was in large part theoretical, but also included experimental studies of dispersal in thistles and of plant genetics, much inspired by the metapopulation concept (Manicacci et al. 1992 ; Colas et al. 2001 ; Vitalis et al. 2001 , 2002 ). Several opportunities allowed our group to initiate what were then pioneering studies in evolutionary conservation biology with a metapopulation perspective.

Opportunity to work on Centaurea corymbosa occurred when IO was asked to study some endemic rare species of the Languedoc–Roussillon region by Louis Olivier, then Head of the National Botanical Mediterranean Conservatory of Porquerolles (CBNMP), a conservation structure in Southern France. At that time, she was asked to perform an allozyme study for five endemics of the region. Instead, thanks to the work of Bruno Colas who started a PhD, she focused on only one of them, C. corymbosa , and, joined by Miquel Riba, they started a programme on plant evolutionary conservation biology. They aimed at understanding rarity in this species. This question was further explored by several other PhDs and postdoctorates within and then outside the group as former students continued working on this fascinating model.

Opportunity to work on Brassica insularis was similarly due to rather contingent circumstances. IO was asked by the French Ministry of Research to work on a protected Corsican species, which might be a useful genetic resource. Studies on B .  insularis , which our group initiated in 1998, thus allowed us to examine the generality of patterns found in C. corymbosa , and to examine further some questions that arose in our study of C. corymbosa due to the availability of genetic resources in Brassica . First, collections of plants from different populations maintained ex situ by the CBNMP were available for us to measure traits in controlled conditions. Second, close relatedness to the domestic cabbage allowed us to use genetic resources, which were not available for nonmodel species such as C. corymbosa , and in particular to study the genetics of self‐incompatibility*, which was of particular interest for AM.

In 1999, IO was asked by the Centre National de la Recherche Scientifique (CNRS) to organize a Biodiversity workshop in South Africa, where apartheid had ceased and the French government wanted to seed new scientific collaborations. IO and AM participated at the workshop, where contacts were initiated with South African researchers (in particular Jeremy Midgley, Anthony Rebelo, William Bond, with whom the collaboration went further) on the evolution of diversity and life histories in the fynbos. The PhD of JT allowed these projects to make a significant step forward in recent years.

These biographical elements illustrate how exciting science can be born from fortuitous meetings and circumstances, how solicitations from conservation structure and political powers can seed rich long‐term research programme with high interest both for basic and applied science. Most of all, it illustrates that good science emerges from cooperation of many students, young and experienced researchers. This research was the achievement of a group with strong bonds, complementary skills and high diversity. Working in this group was scientifically, but also personally, enlightening. This is our experience of research, as female scientists at various stages of their career: we feel very lucky having worked in an environment where cooperation was always valued above competition, and where friendship was intricately mixed with high intellectual stimulation.

Conservation of biodiversity beyond species.

More than 300 years ago, Carl Linnaeus offered a system of classification (Linnæus 1735 ). Species played a central role, and were viewed as fixed entities created by God. A hundred and fifty years later, Charles Darwin discovered a major evolutionary process (selection) and suggested a new way of classifying living organisms. Darwin wrote that the characters which naturalists consider as showing true affinity between any two or more species, are those which have been inherited from a common parent, and, in so far, all true classification is genealogical (Darwin 1859 ). It was then clear that species were not to be defined on the basis of what they did, but on the basis of what they were and where they came from (Lecointre 2011 ; Jetz et al. 2014 ). Darwin wrote I am often in despair in making the generality of naturalists even comprehend me. Intelligent men who are not naturalists and have not a bigoted idea of the term species, show more clearness of mind (Darwin 1859 ). Species exist, just as other levels of classification, because we invented them. They are one arbitrary level in the Tree of life. There is often as much diversity within a species as between species (Helms et al. 2015 ; Realini et al. 2015 ), so that one could have cut the Tree of life elsewhere to define taxonomical units to be preserved.

Evolution and ecology can operate on the same time scale. There are many examples of rapid contemporary evolution in nature (e.g. Hansen et al. 2012 ; see special issue introduced by Merilä and Hendry 2014 ) and in experimentally evolving populations (Kawecki et al. 2012 ; Rosenzweig and Sherlock 2014 ). Evolutionary conservation biology emerged recently as a new discipline (Ferrière et al. 2004 ; Whiteley et al. 2015 ), in part because of the growing awareness that evolutionary changes can proceed sufficiently fast to affect demographic functioning. Understanding the threats on population viability requires considering not only population sizes but also the genetic diversity of populations. This idea was early recognized by studies of impacts of inbreeding depression on population viability, now enriched by our increasing understanding of the feedbacks between demography and genetics (Keller and Waller 2002 ; Cheptou and Donohue 2011 ). Preserving genetic diversity among populations, in particular that linked to local adaptations, implies understanding the evolutionary forces that have shaped this diversity (Hansen et al. 2012 ; Santamaria and Mendez 2012 ). The development of genomics offers new insights into answering these questions (Ouborg 2010 ; Thomson et al. 2010 ; Angeloni et al. 2012 ; Mc Mahon et al. 2014 ; but see Shaffer et al. 2015 ). Awareness about forecasted increases in population extinction and species range contraction has renewed interest on the concept of evolutionary rescue (see special issue introduced by Gonzalez et al. 2013 ; see also Orr and Unckless 2014 ), a process by which a declining population evolves adaptation to new stressful conditions and escapes extinction. Threatened lineages need to evolve to persist in the context of global changes, but often have small population sizes and evolutionary histories that constrain their ability to adapt to new conditions, making evolutionary rescue particularly unlikely (van der Wal et al. 2013 ). Past evolution can indeed explain the vulnerability of species to threats (Corey and Waite 2008 ; Baker et al. 2010 ; van Woesik et al. 2012 ; Lavergne et al. 2013 ).

The contribution of our group (Box  1 ) to the development of the field of evolutionary conservation biology was much inspired by the concept of metapopulations. The term metapopulation was first coined by Levins ( 1968 ) in the context of island biogeography (‘a population of local populations which are established by colonists, survive for a while, send out migrants, and eventually disappear’), then by Slatkin and Wade ( 1978 ) in the context of population genetics, and initially used in conservation biology as a pure demographic tool by Hanski ( 1989 ) (see Couvet et al. 1985 ; Olivieri et al. 1990 for reviews). We will illustrate, through three case studies, how concepts about evolution in metapopulations may allow us to understand the vulnerability of different populations, and propose management strategies to better protect populations and their diversity of ecological traits. In return, these investigations enriched and stimulated our conceptual understanding of evolutionary biology in metapopulations. These different case studies represent some extremes in metapopulation functioning.

The first case study concerns the biology of the rare endemic Centaurea corymbosa , which has an extremely restricted range (see Box  3 for a description about the biology and natural history of this species). It illustrates the conservation issues associated with sets of populations that do not function as metapopulations but still live in patchy habitats, that is where dispersal between extant populations and colonization of new patches are absent, and where founding of new populations cannot balance potential local extinctions. Our research suggested how evolution of dispersal, mating system and life history traits in the landscape inhabited by C.  corymbosa may have worsened its persistence prospects in the long term, a potential concrete case of evolutionary suicide. The same types of challenges associated with the combination of strong isolation and small population sizes were illustrated by our research on another narrow endemic with a highly fragmented habitat, Brassica insularis (Box  4 ). The third case study, discussed in the second part of this review, reflects the opposite extreme in metapopulation functioning and concerns the evolution of fire‐related traits, and more generally of life history strategies, in the highly diverse genus Leucadendron (Box  5 ) of the South African fynbos, a world hot spot of biodiversity. There, fire disturbance and the recolonization phase after fires are so integral to the functioning of populations that the recruitment of new individuals in the populations is conditioned by the occurrence of fire. Combining theory and comparative analyses based on phylogenies, our results suggest that the large diversity of life history traits has evolved jointly with fire regimes and climatic conditions. Examining evolutionary history, we are able to predict which traits are currently most threatened by changes in climate and fire regimes. Finally, we discuss how an evolutionary perspective could affect management in these different case studies and conclude by defining a research agenda for evolutionary conservation biology.

Centaurea corymbosa, a cliff‐dwelling species tottering on the brink of extinction.

Our work on Centaurea corymbosa has become a model in conservation biology (e.g. Wilson and Rannala 2003 ). The species, from the family Asteraceae , is endemic of the Clape Massif (France). Only six populations of C. corymbosa have been described since 1783. They all are on the south‐western slope of the Massif, occupying less than 10% of the area. The species range is thus limited to three km 2 . Populations are restricted to cliffs and the edge of cliffs, on rocky and open areas with very shallow soils. The species appears as a poor competitor, restricted to open areas with very little vegetation cover (Imbert et al. 2012 ). Distance between populations varies from 300 to 2300 m, but populations are separated by what represents a hostile environment for C. corymbosa (Colas et al. 1997 ). Centaurea corymbosa is a monocarpic* plant: it flowers after several years of vegetative growth as a rosette (between 3 and 12 years, with a mean of 5.5 years; Fréville et al. 2004 ). Centaurea corymbosa is a self‐incompatible and insect‐pollinated plant (Kirchner et al. 2005 ).

The species is thus very rare and, as such, endangered. It is listed under Bern Convention and under Annex II of EC Habitats Directive, as well as under the list of plants protected in France (Ministerial Order of 20 January, 1982, published 13 May, 1982), and under Volume I (Priority Species) of the National Red List of Threatened Plants in France (Olivier et al. 1995 ).

Brassica insularis, another endangered cliff species.

The insular cabbage Brassica insularis, which is closely related to the cultivated cabbage, Brassica oleracea, is considered as vulnerable at the national and international levels, and listed under different nature protection mechanisms. As C. corymbosa , B. insularis is an endemic species, found mainly in some Mediterranean Isles (Corsica, Sardinia, Pantelleria) and also in Tunisia and Algeria (Snogerup et al. 1990 ). Its habitat is restricted to limestone cliffs, and it occurs in isolated populations of various sizes. As C. corymbosa and B .  oleracea , B. insularis is a perennial*, self‐incompatible plant, pollinated by insects (Snogerup et al. 1990 ). It is however polycarpic* with a life span of 5–7 years and an age at first reproduction of 2 or 3 years. The strong morphological differentiation between Corsican populations has led to the distinction of six varieties (Widler and Bocquet 1979 ), five of them existing only in one population.

Life history traits of perennial* plants in the South African fynbos, the special case of the genus Leucadendron .

The genus Leucadendron , or Conebushes, belongs to the Proteaceae family, one of the most prominent flowering plant families in the southern hemisphere. This genus is mostly distributed in a restricted area, the South African fynbos, known to display a large environmental variation both for climate and for fire regimes (Schulze 1997 ). Moreover, environments inhabited by each Leucadendron species are very well characterized (Rebelo 1992 ). All 96 taxa in the genus are dioecious* shrubs. Some species show no morphological differences between males and females, whereas other species exhibit the highest degrees of sexual dimorphism in angiosperms. Once mature, female plants produce every year flowerheads that form woody cones in which fruits are borne. Species are either serotinous, retaining seeds in cones for several years, or display a soil‐stored seed bank*. Fire triggers seed recruitment: in serotinous species, it leads to seed release from cones, and in soil‐stored seed bank* species, it breaks seed dormancy. In this genus as in many other Proteaceae , keeping cones closed requires providing them with some resources, mainly water. Death of the plants results in premature opening of the cones and in seed release under unfavourable conditions for recruitment. Some species are able to regrow from protected buds after a fire: these resprouting* individuals will thus experience several fires. On the contrary, individuals of non‐resprouting* species are killed by fire events. In the genus Leucadendron , these fire‐related traits are found in different species: 45.7% and 8.6% of species are, respectively, serotinous non‐resprouting* and serotinous resprouting*, while 42.0% and 3.7% display underground‐stored seed banks and are, respectively, non‐resprouting* and resprouting*. No species is known to have both a serotinous and a soil‐stored seed bank*. Pollination mode varies between Leucadendron species: pollen can be dispersed either by wind or by insects. When seeds are released from the cones, they can be dispersed by wind, mammals, ants or gravity.

Part 1: Are rare species caught in an evolutionary trap?

Rarity and extinction vortex.

Species rarity may be defined according to population size, geographical range and habitat range: there is a single way to be common (i.e. large populations, large distribution and wide range of habitats), but there are seven forms of rarity (Rabinowitz 1981 ). We studied two rare species, C. corymbosa (Box  3 ) and B. insularis (Box  4 ), both characterized by a narrow distribution and small populations (with some exceptions for B. insularis ). We performed studies coupling genetics, demography, ecology and reproduction biology to identify the causes of rarity on one hand, and to be able to provide pragmatic solutions on the other hand. Very small populations can be caught in an extinction vortex, where demographic vulnerability is accentuated by the lack of genetic diversity, inbreeding depression and fixation load, leading to even smaller population sizes and greater genetic problems (Oostermeijer et al. 2003 ; Frankham 2005 ; Fagan and Holmes 2006 ; Wagenius et al. 2007 ; Leducq et al. 2010 ). Life history traits of C. corymbosa and B. insularis further increase their demographic vulnerability. Evolutionary rescue through the evolution of different life history traits, which could boost population dynamics, is prevented not only by the lack of genetic variability associated with small population size, but also by selection pressures associated with demographic functioning and habitat structure (Colas et al. 1997 ; Noel et al. 2010 ).

Centaurea corymbosa : demographic threats

Centaurea corymbosa has an extremely narrow range, with only six populations (Box  3 ). Demographic surveys have revealed that populations are declining (Colas et al. 1996 , 1997 ; Riba et al. 2001 ). Population size (number of flowering plants) varies among populations and years (e.g. between one and 36 individuals per year in the smallest population, and between 76 and 351 in the largest). Demographic surveys in permanent quadrats performed every 3 months allowed the estimation of transition rates between different stages of the life cycle, and the modelling of population dynamics using matrix models to predict long‐term population growth rates (Fréville et al. 2004 ). Based on modelling results, we predict decline in three populations of the six known populations. The predicted growth rates however vary among populations and years. Demographic analyses have revealed that demographic stochasticity, due to small population size, and environmental stochasticity, due to varying environmental conditions in space and time, explain this high variability in population growth (Fréville et al. 2004 ). We predicted extinction for at least two populations within the next 100 years (Fréville 2001 ).

An evolutionary hypothesis: Fragmentation of favourable habitat and associated dispersal cost has counterselected traits favouring dispersal.

The habitat of C. corymbosa is naturally highly fragmented, with rare patches of favourable habitat on rocky cliffs, surrounded by vast areas where germination and life cycle completion is impossible. The degree of fragmentation is also probably influenced by human activities in a complex manner (see Part 3). Dispersal of seeds in such a landscape is an extremely risky venture, with a very small probability of landing in a suitable patch of habitat. Theoretical studies have predicted that a high cost of dispersal in such fragmented landscapes can counterselect traits enhancing seed dispersal distances (e.g. van Valen 1971 ; Olivieri et al. 1995 ; see a review in Ronce 2007 ). Empirical support for this theoretical prediction has been found in two other Asteraceae species (Cheptou et al. 2008 ; Riba et al. 2009 ), showing that the consequences of habitat fragmentation can be aggravated by the evolution of dispersal for species remaining in these fragments.

Dispersal is indeed very limited in C. corymbosa

Fruits of C. corymbosa bear a pappus* (see glossary in Box  6 ), which is usually characteristic of adaptation to seed dispersal by wind in Asteraceae . The peculiar morphology of the pappus* in C. corymbosa makes seed dispersal by wind very inefficient: falling velocity of fruits, which is inversely related to seed dispersal distance under a given height of release, is four times higher than for dandelions fruits (Riba et al. 2005 ). Dispersal thus occurs mostly by gravity, which is consistent with the estimation of very short average dispersal distances, as measured by in situ direct methods ( d  = 32 cm, Colas et al. 1997 ). Additionally, there is no evidence that the elaiosome* facilitates dispersal by ants (Imbert 2006 ).

Dioecious: species with distinct male and female plants.

Elaiosome : an external structure that belongs to a seed or a fruit, rich in nutrients, and that is attractive to ants.

Monocarpic: a plant that produces seeds only once before dying.

Pappus: a parachute‐like structure on fruits of Asteraceae that facilitates dispersal by wind.

Polycarpic: a plant that flowers and sets seeds several times in its lifetime.

Perennial: a plant that lives more than one year. Monocarpy and polycarpy are two different strategies that exist in perennial plants.

Resprouting: the ability of an organism to regrow from burgeons after that aerial parts were killed, e.g. after a fire.

Self‐incompatibility: inability for a fertile hermaphrodite plant to produce viable seeds by self‐pollination. There are different genetic self‐incompatibility systems, but they all exhibit a large number of alleles at each locus, called S‐alleles , maintained by frequency‐dependent selection. An S‐allele cannot fertilize the same S‐allele.

Serotiny : the retention of seeds within closed cones in the plant canopy after seed maturation. Seeds are normally released after fire (i.e. when cones die) and are short‐lived after release. They germinate with the first following rains.

Soil‐stored seed bank: dormant seeds are released every year and stored in the soil. In the specific case of species living in fire‐prone environment, seeds generally germinate when a fire occurs.

In the context of the highly fragmented structure of the habitat, this very limited dispersal capacity of seeds explains the demographic isolation of the different populations, which function as independent entities. Fine‐scale analysis of spatial patterns of gene flow through pollen within the Auzils population has shown that the average dispersal distance of pollen was lower than 22 m, and has revealed the quasi‐absence of immigrant pollen from other populations (Hardy et al. 2004a ). Together with limited pollen dispersal, short seed dispersal distance thus contributes to the genetic isolation and large genetic distance among populations despite the small geographical distances between them ( F st  = 0.23 for microsatellites and 0.35 for allozymes; Fréville et al. 2000 , 2001 ). Genetic assignation tests also revealed that immigrants within populations were rare (209 of 228 individuals were assigned to their own population) and came from populations within a distance of 300–600 m (Fréville et al. 2001 ).

The range of C. corymbosa is limited by its poor dispersal capacity

During our 20‐year demographic survey, we recorded no new populations in the area. Five of the six populations of C. corymbosa have been known for more than a century, and even if the sixth population was discovered in 1994, it may well have existed before that. The absence of colonization of new sites could be due to dispersal limitation or to the absence of favourable patches of habitats. We tested the latter hypothesis by introducing seeds of C. corymbosa in two new sites. We found that plants had a better survival in those new sites than in the previously occupied sites (probably because we established the seeds in what we evaluated as favourable microsites), but had a lower fecundity (probably because of Allee effects due to the small number of introduced plants, Colas et al. 2008 ). This experiment should be repeated, in particular because one of the introduced populations went extinct in 2014, but it however showed unambiguously that empty favourable sites do exist in the area, where plants can survive, but cannot be reached by C. corymbosa due to its poor dispersal capacity.

The absence of colonizations has many evolutionary consequences

The combination of perenniality, monocarpy and self‐incompatibility* (which are traits shared by closely related species in the genus Centaurea , see Fréville et al. 1998 ) makes the populations of C. corymbosa particularly vulnerable to any disturbance that would strongly decrease population density, resulting in strong Allee effects. The late age at first reproduction slows down population growth, and successful reproduction requires finding synchronous and compatible partners, which could be really challenging in a small population, as exemplified by our introduction attempts. Paternity analyses in the Auzils population showed that seeds from a single plant were sired on average by five different pollen donors only (Hardy et al. 2004b ). We further found that seed set increased with the density of neighbouring plants, and showed that it was likely due to the self‐incompatibility* system (Kirchner et al. 2005 ). Self‐compatibility has evolved many times from self‐incompatibility* in angiosperms (Igic et al. 2003 ). Self‐pollination experiments have shown that a few individuals of C. corymbosa are partially self‐compatible (10–15%) or fully self‐compatible (1%, unpublished results). So why did the populations not evolve greater self‐compatibility given the threats on persistence that such a reproductive system entails in small, declining populations? Similar questions arise about the evolution of lower flowering age and iteroparity.

Theoretical studies on the evolution of life history traits and mating systems (reviewed in Ronce and Olivieri 2004 ) shed some light on these questions. In a metapopulation, selection pressures on mating and life history strategies differ during phases of recolonization after disturbance, where populations are small but growing, from selection pressures in stable populations. As a result, organisms living in metapopulations with a higher population turnover have been predicted to evolve lower age at maturity (de Jong et al. 2000 ), higher selfing rates (Pannell and Barrett 2001 ), higher fecundities (Ronce and Olivieri 1997 ; Crowley and McLetchie 2002 ) and higher dispersal ability (e.g. Olivieri et al. 1995 ). In C. corymbosa , such a metapopulation functioning is disrupted: in the absence of colonization, there is simply no selection pressures favouring other life history and mating strategies. If a rare colonization occurred, the present combination of traits would result in large Allee effects, making it even less likely that such a colonization would succeed and establish a viable population. Theoretical studies have shown how such evolutionary traps could ultimately lead to extinction, a process called ‘evolutionary suicide’ (reviewed in Ferrière and Legendre 2013 ). Centaurea corymbosa (Fig.  1 ) could well be a concrete example of a species on the verge of such evolutionary suicide (Ferrière et al. 2004 ), with all populations in decline and short‐term extinction predicted for two of six. Many other species that evolved life history traits that increase their demographic vulnerability may be in the same situation, but the combination of traits increasing extinction risk will depend on environmental pressures that the species confront (see e.g., Fréville et al. 2007 for experimental results on grassland communities).

The extinction vortex of C . corymbosa . The plant traits, because they act on demography (arrow from left to right, top), induce a poor colonizing ability, which in return (other arrow) determines plant traits.

Brassica insularis : another endemic rare cliff species with similar conservation challenges

Do the demographic and evolutionary challenges faced by C. corymbosa represent an isolated and even pathological case, or could our understanding of these challenges inform the conservation biology of other species facing similar challenges? Studies on B. insularis , which shares many characteristics of its biology and demography with C. corymbosa, allowed us to evaluate what could be transferred from a system to another and how a different species reacts to similar challenges (Box  4 ). Our studies on five Corsican populations, distant from each other by eight to 105 km, revealed a strong genetic differentiation, with no pattern of isolation by distance (Glémin et al. 2005 ). More than 10 years of demographic survey on these same populations showed a large variability of population growth among years and populations and a clear tendency of decline (Noel et al. 2010 ).

The role of diversity of self‐incompatibility* alleles in the demography of B. insularis

The number of S‐alleles at the self‐incompatibility* locus in a population was positively correlated with population size, as expected under genetic drift. Indeed, in the smallest population surveyed, which harbours only 50 reproducing individuals, we found only three distinct S‐alleles, with one of them having a frequency greater than 90% (Glémin et al. 2005 ). Self‐incompatibility* represents a serious demographic handicap in small populations, but also in larger populations where patch structure may reduce locally the diversity of S‐alleles, and thus the availability of compatible mates (Mignot et al. 2005 ; Glémin et al. 2008 ).

Inbreeding depression in B. insularis

In such a situation where the reproductive success of self‐incompatible individuals is strongly limited by the rarity of compatible mates, self‐compatible genotypes could be at an advantage. Evolution towards self‐compatibility would be facilitated by a low inbreeding depression. A small difference in fitness between selfed and outcrossed progeny (which measures inbreeding depression in plants) is expected in small populations, because recessive deleterious mutations of small effect can spread to fixation, while those of strong effect are purged (Glémin et al. 2001 ). We measured inbreeding depression in controlled conditions, performing crosses with individuals in ex situ collections. Contrary to theoretical predictions, we found a large inbreeding depression on survival at different stages of the life cycle (inbred individuals suffered from a 25–30% decrease in survival compared to outbred individuals before first flowering, and a 40–50% decrease after first flowering), which could be explained by the accumulation of mutations during the long life span of the plants (Glémin et al. 2006 ). Evolution towards self‐compatibility could thus be halted by the large inbreeding depression, despite the constraints associated with the rarity of compatible mates.

Genetic rescue: risks and benefits

Introduction of individuals with additional S‐alleles in small populations could help improve the reproductive success, by increasing the number of compatible mates. Gene flow could also alleviate the negative genetic consequences of small population size, by restoring genetic diversity at other loci, and making selection against deleterious mutations more efficient. Genetic rescue has been used with success in a few emblematic examples in conservation biology (Hedrick and Fredrickson 2010 ). Artificial gene flow between isolated populations is however not without risk: isolated populations may have evolved genetic incompatibilities leading to outbreeding depression, and/or have patterns of local adaptation that could be disrupted by gene flow (Tallmon et al. 2004 ). The five studied Corsican populations of B. insularis belong to five different subspecies, raising questions about the genetic entities that are the target of conservation. Would restoring some level of gene flow between populations in B. insularis provide demographic benefits that would compensate for the associated risk or loss of genetic originality?

Experimental and theoretical studies provide some insights into this question. On the theoretical side, stimulated by the previous case studies, we investigated the antagonistic effects of gene flow in fragmented populations when both inbreeding and local adaptation affect plant fitness (Lopez et al. 2008 ). Simulations showed that gene flow had net positive effects in very small populations (with effective size less than 100) because (i) such populations suffer from high drift load and inbreeding depressing their mean fitness, and (ii) local adaptation is generally absent in such small populations as they are too small and genetically depauperate to respond to local selection pressures, consistent with meta‐analyses showing that local adaptation emerges more readily in large populations (Leimu and Fischer 2008 ). Large populations do not suffer from inbreeding and have higher level of local adaptation, so gene flow is predicted to have less beneficial effects in larger populations. Large numbers of migrants are however necessary to significantly alter the genetic composition of such large populations. Whatever the size of populations, we found that an optimal number of one to two migrants per generation maximized plant fitness, being sufficient to alleviate much of the negative consequences of complete isolation, without severely disrupting local adaptation (Lopez et al. 2008 ). On the experimental side, in C. corymbosa and in the studied Corsican populations of B. insularis, we found no evidence for differentiation of functional traits among populations when grown in a common garden, which would be expected in the presence of local adaptation (Petit et al. 2001 ). These results obtained on the juvenile stage of plants should be confirmed by further analyses of adult traits (because the former are more likely to be affected by maternal effects), and by the study of potential genetic incompatibilities.

Part 2. Evolution in fire‐prone environments and conservation issues

The two previous endemics seem particularly vulnerable when facing new threats and disturbances, possibly because they have traits adapted to dynamics with very little turnover. In contrast, in the South African fynbos, species are subjected to recurrent natural fires, which burn all above‐ground vegetation and are followed by massive regeneration. Are species adapted to recurrent disturbances more resilient in the context of anthropogenic changes? Our studies of life history traits evolution in the fire‐prone fynbos suggest that the existence of recurrent disturbance in a metapopulation (as opposed to undisturbed habitats) is not sufficient to understand patterns of vulnerability or resilience. Species adapt to specific disturbance regimes, rather than to disturbance per se , through different strategies. These specific strategies make some species more resilient or vulnerable than others to changes in the disturbance regime, to climate change, and to other forms of global change.

The metapopulation concept is useful to understand the evolution of life history traits in fire‐prone ecosystems because it sheds light on selective and ecological processes in populations that are far from any demographic equilibrium (Ronce and Olivieri 2004 ). In the fynbos in particular, the recruitment of many species is conditioned by the occurrence of fire. The age of individuals is then tightly correlated with the time since the last disturbance, which was theoretically shown to select for specific ageing strategies in a metapopulation (Ronce et al. 2005 ; Cotto et al. 2013 , 2014 ). In addition to seed dispersal, recurrent fires also select for alternative strategies to recolonize burnt sites, such as various types of seed banks (Box  5 ). The extent of gene flow and dispersal among populations, and their role in the ecological and evolutionary dynamics in the fynbos, are the subject of ongoing investigations. We will here focus on other aspects of metapopulation functioning, those associated with selection pressures in populations subject to recurrent disturbances, which represent both opportunities in terms of recruitment and constraints in terms of completion of the life cycle.

Conservation issues in the fynbos

The South African fynbos is one of the five existing fire‐prone ecosystems in the world, known for their high levels of endemism and diversity (Myers et al. 2000 ). Plants from the South African fynbos, and from other fire‐prone ecosystems, display an important diversity in their life history strategies (Rebelo 2001 ). Such diversity has been attributed to variation in environmental aspects such as soil fertility and components of the fire regime such as fire frequencies, intensities or sizes (Keeley et al. 2011 ; Keeley 2012 ), which may have shaped the evolution of these traits in these metapopulations (Box  5 ). Because of climate warming and human activities, fire frequencies are expected to increase in the future in all fire‐prone ecosystems (Syphard et al. 2009 ) and could affect the persistence of some life history traits.

Exaptations versus adaptations: a relevant debate for conservation biology?

The existence of an adaptive link between these life history traits and fire regimes was however challenged by Bradshaw et al. ( 2011 ). They proposed that the emergence of serotiny* was not linked to fire, but rather responded to factors such as low nutrient availability and high seed predation. Bradshaw et al. ( 2011 ) indeed argued that the emergence of some of these traits predated periods with recurrent fires, and their presence was not restricted to fire‐prone environments. They concluded that the so‐called fire adaptations were most likely ‘exaptations’ – traits that enhance fitness in the presence of a given factor, but which emergence was caused by another factor (Gould and Vrba 1982 ). Bradshaw et al. ( 2011 ) argued that, because some species might be adapted to something else than fire, managing fire regimes may not be the best solution for their conservation.

As suggested by Keeley et al. ( 2011 ), an exaptation is a trait that has been shaped by natural selection throughout its entire evolutionary history, and is very likely to be adapted to the conditions experienced currently (see also Gomez‐Gonzalez et al. 2011 ; Simon and Pennington 2012 ; Crisp and Cook 2013 ; Oliver et al. 2013 ). Keeley et al. ( 2011 ) argued that observing that fire‐related traits have evolved multiple times independently (but see Losos 2011 ), or that they coevolved (as shown by He et al. 2011 in the genus Banksia ), suggests that fire played a significant role in the selection of such traits. Using phylogenies of Pinus and Proteaceae respectively, He et al. ( 2012 ) and Lamont and He ( 2012 ) found that fire‐related traits arose jointly with an important increase of atmospheric O 2 concentration during the Cretaceous, which probably increased fire frequency on Earth (Bergman et al. 2004 ). More convincing evidence that fire has shaped the evolution of such traits was provided by models of joint evolution of plant traits and habitat type (i.e. fire‐prone vs nonfire‐prone) along phylogenies, such as was found in the Proteaceae family (Lamont and He 2012 ).

A different perspective on fire adaptations

In this context, we started to investigate which selective pressures shaped, in the past, the evolution of life history traits in fire‐prone metapopulations and how such knowledge could inform us about potential effects of change in climate and fire regimes. Although understanding what caused the first emergence of a particular life history trait is an interesting question for an evolutionary biologist (e.g. see Bena et al. 1998 ), it might be irrelevant for conservation purposes. We therefore investigated the more recent evolutionary past of plant groups in fire‐prone environments to understand what is currently maintaining such a large diversity of fire‐related traits, pollination strategies, seed dispersal strategies and degrees of sexual dimorphism (Box  5 ), combining theoretical studies with comparative analyses.

Adaptation to fire or to fire regimes? Theoretical considerations

The persistence of serotinous species is supposed to be strongly linked to the distribution of fire intervals. In some fire‐prone environments, recruitment between two fires is supposed to be very rare due to competition with already established plants (Cowling and Lamont 1987 ; Enright et al. 1998 ; but see Enright and Goldblum 1999 for an example of interfire recruitment). Thus, serotinous species need to keep their cones closed until fire arrives because their seeds are short‐lived in the soil (Weiss 1984 ). The degree of serotiny*, defined as the average cone age on the plant, strongly varies among species and among populations of the same species (Cowling and Lamont 1987 ; Enright and Lamont 1989 ; Lamont et al. 1991 ; Midgley 2000 ; Cramer and Midgley 2009 ), and is much shorter than the typical mean fire interval, especially in the South African fynbos. Low degrees of serotiny* thus appear as an evolutionary paradox. We used a model of life history evolution in fire‐prone environments, inspired by the biology of the genus Leucadendron and other Proteaceae in the fynbos, to investigate what the optimal life history of serotinous plants should be under a given fire regime characterized by a distribution of fire return intervals (Tonnabel et al. 2012 ). We considered that plants allocated resources yearly to growth and survival, seed production, and maintenance of seed canopy. We found that weak levels of serotiny* evolved even in the absence of interfire recruitment. This was because we assumed that resources were limited, generating a trade‐off between current seed production and maintaining past seed production (Tonnabel et al. 2012 ). We also showed that the variance in fire intervals strongly affects the evolution of the degree of serotiny*: when the predictability about fire intervals is low, the optimal strategy consists in increasing allocation towards current reproduction at the expense of cone maintenance. This is because the optimal strategy is to produce a certain number of seeds every year. This model does not explicitly describe dispersal between burnt and unburnt sites. More recent theoretical investigation showed that low dispersal does not significantly alter the predicted relationships between fire frequency, fire predictability and the evolved life history traits in serotinous species when recruitment between fires is rare (A. Kubisch, J. Tonnabel, F. M. Schurr, and O. Ronce, unpublished manuscript).

Does the evolutionary history of species inform us about their vulnerability under changing fire regimes?

We used our evolutionary model of life history to predict the demographic consequences of changes in fire regime, assuming that life history traits have been shaped by past historical fire regime. We manipulated both the mean time interval between fires (fire frequency) and the predictability in fire occurrence (the variance of time intervals between fires at a same location). Deviations from the historical mean fire interval always negatively affects population growth and persistence prospects, but populations with larger historical variances are more resilient to a change in mean fire interval (Fig.  2 ). Whatever the historical variance of fire intervals, a smaller variance in the new fire regime ameliorates the survival of the population if the mean fire interval is unchanged (Tonnabel et al. 2012 ). Populations with larger historical variances are also more resilient to increased variance. To maintain an adapted life history, one should thus maintain the population historical fire regime. But to maintain biodiversity and biodiversification , it is important to maintain a diversity of fire regimes, considering the mean fire interval but also its variance. There are other examples about how knowledge of historical fire regimes can help conservation (see the general review of Dellasala et al. 2004 ), for instance in mammals (Bilney 2014 ; Augustine and Derner 2015 ), birds (Fuhlendorf et al. 2006 ; Augustine and Derner 2012 , 2015 ), insects (Schlesinger and Novak 2011 ) and other plants (Menges and Dolan 1998 ; Marchin et al. 2009 ; Radies et al. 2009 ; Weekley et al. 2010 ).

Effect of changes in the mean ( μ ) of the probability distribution of fire intervals (uniform distribution) on the probability of extinction at 50 years for three serotinous populations adapted to different historical fire regimes. For each population, the life history was optimized with a historical mean fire interval of 16 years. Each population had evolved under a given variance of fire intervals. Stochastic simulations were run using the ULM software (Legendre and Clobert 1995 ).

Comparative analyses: insights on joint evolution of traits, fire regime and climatic niche

We tested hypotheses about the adaptive value of different fire‐related traits using macro‐evolutionary comparative analyses. Our goal was to characterize the joint evolution of fire‐related traits and environmental niches to predict how these traits might be affected by potential future changes in climate and fire regimes. We inferred the joint evolution of the environmental niche, for example the mean temperature of the coldest quarter, and that of life history traits along the branches of the phylogeny (J. Tonnabel, F. M. Schurr, F. Boucher, W. Thuiller, J. Renaud, E. M. P. Douzery, and O. Ronce, unpublished manuscript). We expected serotinous species without the ability to resprout after fire to be more sensitive to extreme environments than other trait combinations because their reproduction relies on a single fire event, until which females need to stay alive, and because cone maintenance is costly. We found that the evolution of serotiny* is indeed associated with the evolution of environmental niches characterized by less extreme climatic events, allowing both drought and frost avoidance, and by shorter mean fire intervals (or shorter variance of fire intervals as this aspect of fire regimes is strongly correlated with mean fire interval) compared to species with soil‐stored seed banks* (Fig.  3 ). The evolution of resprouting* after fire was associated with the evolution of niches with more extreme climates, including more extreme droughts and frosts (Fig.  3 ). As expected, species combining serotiny* and inability to resprout evolved niches with the lowest exposition to droughts and frosts. We suggest that all combinations of life history traits do not form an even threat in the context of climate change. According to climate change projections, the climate in Southern Africa should become warmer and drier (Tyson et al. 2002 ). Those serotinous species without resprouting* ability would particularly suffer if summers became warmer, but would benefit from milder winters. Our comparative analyses also showed that life history traits evolved in a correlated manner (Tonnabel et al. 2014 ): species with greater seed dispersal distances tended to evolve lower pollen dispersal distance, insect‐pollinated species evolved decreased sexual dimorphism compared to wind‐pollinated species, and species with a persistent soil seed bank evolved towards reduced adult resprouting* ability after fire compared to serotinous species. This suggests that environmental changes would probably threaten suites of traits rather than single traits.

Summary of the results about effects of intrinsic and extrinsic factors on the evolution of life history traits of plants in fire‐prone environments. Dashed blue and continuous red arrows correspond respectively to positive and negative effects. Note that the probabilities of drought and frost were used in the comparative analysis as proxies for factors affecting plant survival and cost of serotiny*.

Part 3. Implications for management

Halting decline and founding new populations in centaurea corymbosa.

The Clape Massif, where all populations of C. corymbosa are found, belongs to the European network of nature protection areas Natura 2000. The management plan for this site in the context of Natura 2000 was written jointly by researchers, experts (National Botanical Mediterranean Conservatory of Porquerolles CBNMP) and managers (Narbonnaise in Méditerranée Natural regional Park, Coastal Protection Agency, Forests National Office, Gruissan City). The demographic survey in C. corymbosa shows a clear decline of populations, with a high risk of extinction within 50 years. Population decline is linked with the progressive encroachment of dense vegetation on the habitat of the poor competitor C. corymbosa , at the edges of cliffs, due to the abandonment of agricultural practices, the decline in sheep grazing, and fire control. Management should therefore aim at actions favouring more open habitat, through, for example, controlled clearings, to first halt the decline of extant populations. More open habitat on the plateau could also help connecting different patches of favourable habitats, allowing the colonization of empty patches from occupied patches. Colonization of new patches of habitat would in turn result in different selection pressures on life history traits and mating system, allowing the maintenance of greater diversity in the populations, slowing the downward evolutionary spiral in which this species seems to be caught.

A second line of action concerns the new populations created in 1994 and 1995: one which just maintained itself with 67 individuals in 2014, while the other one went extinct in 2014. Reinforcement or reintroduction of large numbers of seeds would be necessary to overcome Allee effects, but would require a phase of multiplication and seed production in controlled conditions to avoid collecting too many seeds in situ in already declining populations. A protocol for the reintroduction programme has been elaborated jointly with managers, and plans for its funding are under discussion. Demographic reinforcement may increase the probability of successful establishment of these new populations, but will diminish the strength of selection on genotypes with alternative mating and life history tactics during such artificial colonization.

Reinforcement of populations in Brassica insularis

Our demographic surveys in B. insularis allowed us to identify specific threats (or the absence of immediate threats) acting on the different surveyed populations, which include disturbances by climbers, overgrazing, herbivore attacks and fires (Noel et al. 2010 ). The National Botanical Conservatory of Corsica has in particular implemented a communication campaign towards users of the sites to reduce those threats. In the very small populations, these direct demographic threats may be aggravated by the lack of compatible mates, due to the loss of genetic diversity at the S locus. Reinforcement of populations has been proposed in management plans of the species. Our single attempt to introduce a new population in an empty site has failed, due to unfavourable weather, but reinforcement of extant populations through the establishment of additional individuals has been successful (unpublished data). How should we choose the genetic origin of the plants used for reinforcement of extant populations? There exists an ex situ conservation scheme in B. insularis consisting in a seed collection of diverse origins managed by the CBNMP. Because genetic diversity at the S locus may be instrumental for the positive effect of such reinforcement, it would be interesting to evaluate how the collection maintains this diversity both within and between populations. When local diversity has been lost both in situ and ex situ , the use of nonlocal material should be discussed, balancing the costs and benefits of such interventions.

Consequences of fire management in the genus Leucadendron

The South African Cape Floristic Region (CFR) is a priority for conservation (Myers et al. 2000 ), in which both national and provincial conservation organizations (i.e. SANParks and CapeNature) have invested great efforts. CapeNature, a provincial public entity of the Western Cape Government, is a key conservation unit responsible for managing and monitoring fires in protected areas of the CFR. Conservation policies are thus greatly affecting fire regimes. In the South African fynbos, fire suppression was adopted at the beginning of the 20th century and later abandoned for a management strategy called prescribed burning, which consists in burning patches of land with a fixed mean fire interval (van Wilgen et al. 2010 ). These management strategies ignore the fact that many organisms and their life history strategies might be adapted to specific fire regimes that they experienced in the past. Our studies on Leucadendron suggest that information about historical fire regimes should be incorporated into prescribed burning strategies when they are implemented. Serotinous species were found to have evolved jointly with shorter mean fire intervals or shorter variances of fire intervals, which may make them particularly sensitive to management practices decreasing frequencies or predictability of fires. So far, prescribed burning practices lack a scientific method when choosing an artificial mean fire interval (but see Kraaij et al. 2013 ). Managers and scientists should work together to build an integrative method for prescribed burning strategies while accounting for past fire regimes, site specific diversity of life history traits, and potential threats to human populations.

Overall, our results, both theoretical and empirical, suggest that a diversity of environments and disturbance regimes have selected for a diversity of life history traits and strategies adapted to these different conditions. Thus, it is crucial to maintain a diversity of environments in the fynbos to maintain the extraordinary diversity of life history traits in this ecosystem. Uniform fire regimes through prescribed burning with similar artificial mean fire intervals may allow the maintenance of only those species which by chance evolved under similar regimes, or those adapted to very variable fire intervals, which we predict to be more resilient to change in fire regimes.

We think that conservation of biodiversity should aim at conserving evolutionary processes that generate biodiversity. To maintain processes leading to biodiversity, it is essential to maintain a diversity of landscapes. The case studies presented in this study illustrate how we identify the threats on biodiversity at different scales of organization, integrate eco‐evolutionary feedbacks in our evaluation of risks, propose new indices of vulnerability and imagine different management practices. The application of genetics in the management of threatened species in the wild is still in its infancy (Laikre et al. 2009 ). According to Frankham ( 2010 ), this is not due to a lack of scientific guidelines, but to the failure to consider genetic issues in wild management (Fig. ​ (Fig.4 4 ).

Planning research in Evolutionary conservation biology. Blue boxes correspond to demographic, ecological and genetic surveys (i.e. monitoring over several years), yellow boxes correspond to calculations, and orange boxes correspond to experiments. Arrows indicate that the box it is starting from should be taken into account in the box towards which it is pointing.

Integrating evolutionary considerations in conservation practices is not an easy task. Defining a research programme for evolutionary conservation biology requires integrating many different complementary approaches, including nonevolutionary ones (see attempts to define such an ideal programme in Fig.  4 ). Adaptive evolution is mainly concerned with the diversity of life history traits (Hansen et al. 2012 ). How should we monitor genetic diversity for adaptive traits? In the optimal situation, one can follow a gene (see examples from pesticide resistance: Weill 2013 ; McNair 2015 ). But usually, there is no candidate gene: monitoring phenotypic diversity is then necessary. Controlled conditions experiments should be set up whenever possible to measure quantitative genetic variation for adaptive traits both within and between populations (Petit et al. 2001 ). Genetic monitoring (surveys through time) should be done on quantitative traits as well as on neutral and non‐neutral genes in several populations. Neutral genes will inform us on evolutionarily significant units, mating systems and gene flow. Quantitative genetics and non‐neutral genes will inform us on adaptive diversity. Genomics offer new powerful tools for genetic monitoring. Demographic survey (i.e. identifying and counting the various ages or stages at every census , on several occasions, as we did on C. corymbosa and B. insularis ) will allow us to perform viability analyses, complemented by data from crosses on inbreeding and outbreeding depressions. Together with ecological survey (i.e. following the habitat), demographic and genetic surveys (i.e. following genes) will allow us predicting the consequences of management actions. These predictions then need to be tested.

Through our studies on C. corymbosa , B. insularis and the genus Leucadendron , we explored several facets of these complex interactions and feedbacks between genetics, evolution and ecology: each facet enriched considerably our understanding of the functioning of threatened species and ecosystems. This was an exciting experience, and we hope that many will embark on such a research programme with great both scientific benefits and benefits for the protection of biodiversity.

Acknowledgements

Demographic surveys of C. corymbosa and B. insularis still go on, with the particular involvement of Eric Imbert, David Carbonell, Christophe Petit and Sandrine Maurice. We thank them all for being such precious team members. Fabienne Justy has been instrumental in the genetic surveys and the molecular biology formation of the many students that contributed to these studies, so is now Elodie Flaven, who helped with Leucadendron molecular work. More generally, the ‘Metapopulation group’ at ISEM has hosted many visitors and students throughout the years, who all contributed to ideas, models, data collection, analyses and discussion, as synthesized in this study. They are too numerous to be cited individually, but we thank them collectively for having made work and life in our laboratory such a great experience. This is publication ISEM 2015‐196.

Literature cited

• Allendorf, F. W. , and Servheen C. 1986. Genetics and the conservation of grizzly bears . Trends in Ecology and Evolution 1 :88–89. [ Google Scholar ]
• Angeloni, F. , Wagemaker N., Vergger P., and Ouborg J. 2012. Genomic toolboxes for conservation biologists . Evolutionary Applications 5 :130–143. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Augustine, D. J. , and Derner J. D. 2012. Disturbance regimes and mountain plover habitat in shortgrass steppe: large herbivore grazing does not substitute for prairie dog grazing or fire . Journal of Wildlife Management 76 :721–728. [ Google Scholar ]
• Augustine, D. J. , and Derner J. D. 2015. Patch burn grazing management in a semiarid grassland: consequences for pronghorn, plains pricklypear, and wind erosion . Rangeland Ecology & Management 68 :40–47. [ Google Scholar ]
• Baker, J. A. , Wund M. A., Chock R. Y., Ackein L., Elsemore R., and Foster S. A. 2010. Predation history and vulnerability: conservation of the stickleback adaptive radiation . Biological Conservation 143 :1184–1192. [ Google Scholar ]
• Bena, G. , Lejeune B., Prosperi J. M., and Olivieri I. 1998. Molecular phylogenetic approach for studying life‐history evolution: the ambiguous example of the genus Medicago L . Proceedings of the Royal Society B‐Biological Sciences 265 :1141–1151. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Bergman, N. M. , Lenton T. M., and Watson A. J. 2004. COPSE: a new model of biogeochemical cycling over Phanerozoic time . American Journal of Science 304 :397–437. [ Google Scholar ]
• Bilney, R. H. 2014. Poor historical data drive conservation complacency: the case of mammal decline in south‐eastern Australian forests . Austral Ecology 39 :875–886. [ Google Scholar ]
• Brachet, S. , Olivieri I., Godelle B., Klein E., Frascaria‐Lacoste N., and Gouyon P.‐H. 1999. Dispersal and metapopulation viability in a heterogeneous landscape . Journal of Theoretical Biology 198 :479–495. [ PubMed ] [ Google Scholar ]
• Bradshaw, S. , Dixon K., Hopper S., Lambers H., and Turner S. 2011. Little evidence for fire‐adapted plant traits in Mediterranean climate regions . Trends in Plant Science 16 :69–76. [ PubMed ] [ Google Scholar ]
• Cheptou, P.‐O. , and Donohue K. 2011. Environment‐dependent inbreeding depression: its ecological and evolutionary significance . New Phytologist 189 :395–407. [ PubMed ] [ Google Scholar ]
• Cheptou, P.‐O. , Carrue O., Rouifed S., and Cantarel A. 2008. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta . Proceedings of the National Academy of Sciences of the United States of America 105 :3796–3799. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Colas, B. , Riba M., and Molina J. 1996. Demographic status of Centaurea corymbosa Pourret ( Asteraceae ), Hormatophylla pyrenaica (Lapeyr) Cullen&Dudley ( Brassicaceae ) and Marsilea strigosa Willd ( Marsileaceae‐Pieridophyta ), three rare plants in the South of France . Acta Botanica Gallica 143 :191–198. [ Google Scholar ]
• Colas, B. , Olivieri I., and Riba M. 1997. Centaurea corymbosa , a cliff‐dwelling species tottering on the brink of extinction: a demographic and genetic study . Proceedings of the National Academy of Sciences of the United States of America 94 :3471–3476. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Colas, B. , Olivieri I., and Riba M. 2001. Spatio‐temporal variation of reproductive success and conservation of the narrow‐endemic Centaurea corymbosa (Asteraceae) . Biological Conservation 99 :375–386. [ Google Scholar ]
• Colas, B. , Kirchner F., Riba M., Olivieri I., Mignot A., Imbert E., Beltrame C. et al. 2008. Restoration demography: a 10‐year demographic comparison between introduced and natural populations of endemic Centaurea corymbosa (Asteraceae) . Journal of Applied Ecology 45 :1468–1476. [ Google Scholar ]
• Corey, S. J. , and Waite T. A. 2008. Phylogenetic autocorrelation of extinction threat in globally imperilled amphibians . Diversity and Distributions 14 :614–629. [ Google Scholar ]
• Cotto, O. , Olivieri I., and Ronce O. 2013. Optimal life‐history schedule in a metapopulation with juvenile dispersal . Journal of Evolutionary Biology 26 :944–954. [ PubMed ] [ Google Scholar ]
• Cotto, O. , Kubisch A., and Ronce O. 2014. Optimal life history strategy differs between philopatric and dispersing individuals in a metapopulation . American Naturalist 183 :384–393. [ PubMed ] [ Google Scholar ]
• Couvet, D. , Gouyon P.‐H., Kjellberg F., Olivieri I., Pomente D., and Valdeyron G. 1985. From metapopulation to neighborhood – genetics of unbalanced populations . Genetics Selection Evolution 17 :407–413. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Cowling, R. M. , and Lamont B. B. 1987. Post‐fire recruitment of four co‐occurring Banksia species . Journal of Applied Ecology 24 :645–658. [ Google Scholar ]
• Cramer, M. D. , and Midgley J. J. 2009. Maintenance costs of serotiny do not explain weak serotiny . Austral Ecology 34 :653–662. [ Google Scholar ]
• Crisp, M. D. , and Cook L. G. 2013. How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective . Annual Review of Ecology, Evolution, and Systematics 44 :303–324. [ Google Scholar ]
• Crowley, P. H. , and McLetchie D. N. 2002. Trade‐offs and spatial life‐history strategies in classical metapopulations . American Naturalist 159 :190–208. [ PubMed ] [ Google Scholar ]
• Darwin, C. 1859. On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle of Life . Murray, London. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Dellasala, D. A. , Williams J. E., Williams C. D., and Franklin J. E. 2004. Beyond smoke and mirrors: a synthesis of fire policy and science . Conservation Biology 18 :976–986. [ Google Scholar ]
• Enright, N. J. , and Goldblum D. 1999. Demography of a non‐sprouting and resprouting Hakea species (Proteaceae) in fire‐prone Eucalyptus woodlands of southeastern Australia in relation to stand age, drought and disease . Plant Ecology 144 :71–82. [ Google Scholar ]
• Enright, N. J. , and Lamont B. B. 1989. Seed banks, fire season, safe sites and seedling recruitment in five co‐occurring Banksia species . Journal of Ecology 77 :1111–1122. [ Google Scholar ]
• Enright, N. J. , Marsala R., Lamont B. B., and Wissel C. 1998. The ecological significance of canopy seed storage in fire‐prone environments: a model for non‐sprouting shrubs . Journal of Ecology 86 :946–949. [ Google Scholar ]
• Fagan, W. F. , and Holmes E. E. 2006. Quantifying the extinction vortex . Ecology Letters 9 :51–60. [ PubMed ] [ Google Scholar ]
• Ferrière, R. , and Legendre S. 2013. Eco‐evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory . Philosophical Transactions of the Royal society B‐Biological Sciences 368 :20120081. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Ferrière R., Dieckmann U., and Couvet D., eds. 2004. Evolutionary Conservation Biology. Cambridge Studies in Adaptive Dynamics . Cambridge University Press, Cambridge. [ Google Scholar ]
• Frankham, R. 2005. Genetics and extinction . Biological Conservation 126 :131–140. [ Google Scholar ]
• Frankham, R. 2010. Challenges and opportunities of genetic approaches to biological conservation . Biological Conservation 143 :1919–1927. [ Google Scholar ]
• Fréville, H. 2001. La Centaurée de la Clape: Biologie d'une espèce rare et réflexions méthodologiques . Doctorat de l'Université de Montpellier II.
• Fréville, H. , Colas B., Ronfort J., Riba M., and Olivieri I. 1998. Predicting endemism from population structure of a widespread species: case study in Centaurea maculosa Lam. (Asteraceae) . Conservation Biology 12 :1269–1278. [ Google Scholar ]
• Fréville, H. , Imbert E., Justy F., Vitalis R., and Olivieri I. 2000. Isolation and characterization of microsatellites in the endemic species Centaurea corymbosa Pourret (Asteraceae) and other related species . Molecular Ecology 9 :1671–1672. [ PubMed ] [ Google Scholar ]
• Fréville, H. , Justy F., and Olivieri I. 2001. Comparative allozyme and microsatellite population structure in a narrow endemic plant species, Centaurea corymbosa Pourret (Asteraceae) . Molecular Ecology 10 :879–889. [ PubMed ] [ Google Scholar ]
• Fréville, H. , Colas B., Riba M., Caswell H., Mignot A., Imbert E., and Olivieri I. 2004. Spatial and temporal demographic variability in the endemic plant species Centaurea corymbosa (Asteraceae) . Ecology 85 :694–703. [ Google Scholar ]
• Fréville, H. , McConway K., Dodd M., and Silvertown J. 2007. Prediction of extinction in plants: interaction of extrinsic threats and life history traits . Ecology 88 :2662–2672. [ PubMed ] [ Google Scholar ]
• Fuhlendorf, S. D. , Harrell W. C., Engle D. M., Hamilton R. G., Davis C. A., and Leslie D. M. 2006. Should heterogeneity be the basis for conservation? Grassland bird response to fire and grazing . Ecological Applications 16 :1706–1716. [ PubMed ] [ Google Scholar ]
• Gandon, S. , Capowiez Y., Dubois Y., Michalakis Y., and Olivieri I. 1996. Local adaptation and gene‐for‐gene coevolution in a metapopulation model . Proceedings of the Royal Society B‐Biological Sciences 263 :1003–1009. [ Google Scholar ]
• Glémin, S. , Bataillon T., Ronfort J., Mignot A., and Olivieri I.. 2001. Inbreeding depression in small populations of self‐incompatible plants . Genetics 159 :1217–1229. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Glémin, S. , Gaude T., Guillemin M. L., Lourmas M., Olivieri I., and Mignot A. 2005. Balancing selection in the wild: testing population genetics theory of self‐incompatibility in the rare species Brassica insularis . Genetics 171 :279–289. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Glémin, S. , Vimond L., Ronfort J., Bataillon T., and Mignot A. 2006. Marker‐based investigation of inbreeding depression in an endangered species of Brassica . Heredity 97 :304–311. [ PubMed ] [ Google Scholar ]
• Glémin, S. , Petit C., Maurice S., and Mignot A. 2008. Consequences of low mate availability in the rare self‐incompatible species Brassica insularis (Brassicaceae) . Conservation Biology 22 :216–221. [ PubMed ] [ Google Scholar ]
• Godelle, B. , Austerlitz F., Brachet S., Colas B., Cuguen J., Gandon S., Gouyon P.‐H. et al. 1998. The genetic system, selected genes and neutral polymorphism: implications for conservation biology . Genetics Selection Evolution 30 :S15–S28. [ Google Scholar ]
• Gomez‐Gonzalez, S. , Torres‐Diaz C., Bustos‐Schindler C., and Gianoli E. 2011. Anthropogenic fire drives the evolution of seed traits . Proceedings of the National Academy of Sciences of the United States of America 108 :18743–18747. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Gonzalez, A. , Ronce O., Ferrière R., and Hochberg M. E. 2013. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution . Philosophical Transactions of the Royal Society B‐Biological Sciences 368 :20120404. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Gould, S. J. , and Vrba E. S. 1982. Exaptation – a missing term in the science of forms . Paleobiology 8 :4–15. [ Google Scholar ]
• Hansen, M. M. , Olivieri I., Waller D. M., Nielsen E. E., and the GeM working group . 2012. Monitoring adaptive genetic responses to environmental change . Molecular Ecology 21 :1311–1329. [ PubMed ] [ Google Scholar ]
• Hanski, I. 1989. Metapopulation dynamics – does it help to have more of the same? Trends in Ecology and Evolution 4 :113–114. [ PubMed ] [ Google Scholar ]
• Hardy, O. J. , González‐Martínez S. C., Colas B., Fréville H., Mignot A., and Olivieri I. 2004a. Fine‐scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships . Genetics 168 :1601–1614. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Hardy, O. J. , Gonzalez‐Martinez S. C., Fréville H., Boquien G., Mignot A., Colas B., and Olivieri I. 2004b. Fine‐scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae) I. Pattern of pollen dispersal . Journal of Evolutionary Biology 17 :795–806. [ PubMed ] [ Google Scholar ]
• Harrison, S. , Murphy D. D., and Ehrlich P. R. 1988. Distribution of the bay checkerspot butterfly, Euphydryas editha bayensis – evidence for a metapopulation model . American Naturalist 132 :360–382. [ Google Scholar ]
• He, T. , Lamont B. B., and Downes K. S. 2011. Banksia born to burn . New Phytologist 191 :184–196. [ PubMed ] [ Google Scholar ]
• He, T. , Pausas J. G., Belcher C. M., Schwilk D. W., and Lamont B. B. 2012. Fire‐adapted traits of Pinus arose in the fiery Cretaceous . New Phytologist 194 :751–759. [ PubMed ] [ Google Scholar ]
• Hedrick, P. W. , and Fredrickson R. 2010. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers . Conservation Genetics 11 :615–626. [ Google Scholar ]
• Helms, B. S. , Vaught R. C., Suciu S. K., and Santos S. R. 2015. Cryptic diversity within two endemic crayfish species of the Southeastern US revealed by molecular genetics and geometric morphometrics . Hydrobiologia 755 :283–298. [ Google Scholar ]
• Igic, B. , Bohs L., and Kohn J. R. 2003. Historical inferences from the self‐incompatibility locus . New Phytologist 161 :97–105. [ Google Scholar ]
• Imbert, E. 2006. Dispersal by ants in Centaurea corymbosa : what is the elaiosome for ? Plant Species Biology 21 :109–117. [ Google Scholar ]
• Imbert, E. , Youssef S., Carbonell D., and Baumel A. 2012. Do endemic species always have a low competitive ability? A test for two Mediterranean plant species under controlled conditions . Journal of Plant Ecology 5 :305–312. [ Google Scholar ]
• Jetz, W. , Thomas G. H., Joy J. B., Redding D. W., Hartmann K., and Mooers A. O. 2014. Global distribution and conservation of evolutionary distinctness in Birds . Current Biology 24 :919–930. [ PubMed ] [ Google Scholar ]
• de Jong, T. J. , Klinkhamer P. G. L., and de Heiden J. H. L. 2000. The evolution of generation time in metapopulations of monocarpic perennial plants: some theoretical considerations and the example of the rare thistle Carlina vulgaris . Evolutionary Ecology 14 :213–231. [ Google Scholar ]
• Kawecki, T. J. , Lenski R. E., Ebert D., Hollis B., Olivieri I., and Whitlock M. C. 2012. Experimental evolution . Trends in Ecology and Evolution 27 :547–560. [ PubMed ] [ Google Scholar ]
• Keeley, J. E. 2012. Fire in Mediterranean climate ecosystems – a comparative overview . Israel Journal of Ecology and Evolution 58 :123–135. [ Google Scholar ]
• Keeley, J. E. , Pausas J. G., Rundel P. W., Bond W. J., and Bradstock R. A.. 2011. Fire as an evolutionary pressure shaping plant traits . Trends in Plant Science 16 :406–411. [ PubMed ] [ Google Scholar ]
• Keller, L. F. , and Waller D. M. 2002. Inbreeding effects in wild populations . Trends in Ecology and Evolution 17 :230–241. [ Google Scholar ]
• Kirchner, F. , Luijten S. H., Imbert E., Riba M., Mayol M., González‐Martínez S. C., Mignot A. et al. 2005. Effects of local density on insect visitation and fertilization success in the narrow‐endemic Centaurea corymbosa . Oikos 111 :130–142. [ Google Scholar ]
• Kraaij, T. , Cowling R., and Van Wilgen B.. 2013. Fire regimes in eastern coastal fynbos: Imperatives and thresholds in managing for diversity . Koedoe; 55 : UNSP 1104. [ Google Scholar ]
• Lacy, R. C. 1993. Vortex – a computer‐simulation model for population viability analysis . Wildlife Research 20 :45–65. [ Google Scholar ]
• Laikre, L. , Allendorf F. W., Aroner L. C., Baker C. S., Gregovich D. P., Hansen M. M., Jackson J. A. et al. 2009. Neglect of genetic diversity in implementation of the convention on biological diversity . Conservation Biology 24 :86–88. [ PubMed ] [ Google Scholar ]
• Lamont, B. B. , and He T. 2012. Fire‐adapted Gondwanan angiosperm floras evolved in the Cretaceous . BMC Evolutionary Biology 12 :1–10. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Lamont, B. B. , Le Maitre D. C., Cowling R. M., and Enright N. J. 1991. Canopy seed storage in woody plants . Botanical Review 57 :277–317. [ Google Scholar ]
• Lavergne, S. , Evans M. E. K., Burfield I. J., Jiguet F., and Thuiller W. 2013. Are species’ responses to global change predicted by past niche evolution? Philosophical Transactions of the Royal Society B‐Biological Sciences 368 :20120091. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Lecointre, G. 2011. One‐eyed biodiversity . Comptes Rendus Palevol 10 :331–334. [ Google Scholar ]
• Leducq, J. B. , Gosset C. G., Poiret M., Hendoux F., Vekemans X., and Billiard S. 2010. An experimental study of the S‐Allee effect in the self‐incompatible plant Biscutella neustriaca . Conservation Genetics 11 :497–508. [ Google Scholar ]
• Legendre, S. , and Clobert J. 1995. ULM, a software for conservation and evolutionary biologists . Journal of Applied Statistics 22 :817–834. [ Google Scholar ]
• Leimu, R. , and Fischer M. 2008. A meta‐analysis of local adaptation in plants . PLoS ONE 3 :e4010. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Levins, R. 1968. Evolution in Changing Environments. Monographs in Population Biology 2 . Princeton University Press, Princeton, NJ. [ Google Scholar ]
• Linnæus, C. 1735. Systema naturæ, sive regna tria naturæ systematice proposita per classes, ordines, genera, & species ., pp. 1–12. Lugduni Batavorum. Haak, Leiden. [ Google Scholar ]
• Lopez, S. , Rousset F., Shaw F. H., Shaw R. G., and Ronce O.. 2008. Migration load in plants: role of pollen and seed dispersal in heterogeneous landscapes . Journal of Evolutionary Biology 21 :294–309. [ PubMed ] [ Google Scholar ]
• Losos, J. B. 2011. Convergence, adaptation, and constraint . Evolution 65 :1827–1840. [ PubMed ] [ Google Scholar ]
• Manicacci, D. , Olivieri I., Perrot V., Atlan A., Gouyon P.‐H., Prosperi J.‐M., and Couvet D. 1992. Landscape ecology – population genetics at the metapopulation Level . Landscape Ecology 6 :147–159. [ Google Scholar ]
• Marchin, R. M. , Bhandari R. K., Wall W. A., Hohmann M. G., Gray J. B., and Hoffmann W. A. 2009. Are rare species less shade tolerant than common species in the fire prone environment? A test with seven Amorpha (Fabaceae) species . Plant Ecology 205 :249–260. [ Google Scholar ]
• Mathias, A. , Kisdi E., and Olivieri I. 2001. Divergent evolution of dispersal in a heterogeneous landscape . Evolution 55 :246–259. [ PubMed ] [ Google Scholar ]
• Mc Mahon, B. , Teeling E. C., and Hoglund J. 2014. How and why should we implement genomics into conservation? Evolutionary Applications 7 :999–1007. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• McNair, C. 2015. Ectoparasites of medical and veterinary importance: drug resistance and the need for alternative control methods . Journal of Pharmacy and Pharmacology 67 :351–363. [ PubMed ] [ Google Scholar ]
• Menges, E. S. , and Dolan R. W. 1998. Demographic viability of populations of Silene regia in midwestern prairies: relationships with fire management, genetic variation, geographic location, population size and isolation . Journal of Ecology 86 :63–78. [ Google Scholar ]
• Merilä, J. , and Hendry A. P. 2014. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence . Evolutionary Applications 7 :1–14. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Midgley, J. J. 2000. What are the relative costs, limits and correlates of increased degree of serotiny? Australian Journal of Ecology 25 :65–68. [ Google Scholar ]
• Mignot, A. , Glemin S., Gaude T., Boillot F., and Olivieri I. 2005. Succès reproducteur du chou insulaire ( Brassica insularis Moris), espèce endémique auto‐incompatible: importance de la dérive . Les Actes du BRG 5 :37–51. [ Google Scholar ]
• Myers, N. , Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. B., and Kent J. 2000. Biodiversity hotspots for conservation priorities . Nature 403 :853–858. [ PubMed ] [ Google Scholar ]
• Noel, F. , Maurice S., Mignot A., Glemin S., Carbonell D., Justy F., Guyot I. et al. 2010. Interaction of climate, demography and genetics: a ten‐year study of Brassica insularis , a narrow endemic Mediterranean species . Conservation Genetics 11 :509–526. [ Google Scholar ]
• Noss, R. F. 1990. Indicators for Monitoring Biodiversity – a Hierarchical Approach . Conservation Biology 4 :355–364. [ Google Scholar ]
• Oliver, A. K. , Brown S. P., Callaham M., and Jumpponen A. 2013. Ectomycorrhizal community responses to recurring prescribed fires in yellow pine forests: effects of fire intervals and season . Phytopathology 103 :107. [ Google Scholar ]
• Olivier, L. , Galland J. P., Maurin H., and Roux J. P.. 1995. Livre rouge de la Flore menace en France. Tome 1: Espèces prioritaires . Museum National d'Histoire Naturelle, Paris. [ Google Scholar ]
• Olivieri, I. 2000. Preface – Special issue on plant metapopulations . Evolutionary Ecology 14 :iii–vii. [ Google Scholar ]
• Olivieri, I. 2001. The evolution of seed heteromorphism in a metapopulation: interactions between dispersal and dormancy In: Silvertown J., and Antonovics J., eds. Integrating Ecology and Evolution in a Spatial Context. British Ecological Society Volume , pp. 245–266. Blackwell Science, Oxford. [ Google Scholar ]
• Olivieri, I. , and Gouyon P.‐H.. 1985. Seed dimorphism for dispersal: theory and implications In Haeck J., and Woldendorp J., eds. Structure and Functioning of Plant Populations , pp. 77–90. North‐Holland Pub.‐Co, Amsterdam. [ Google Scholar ]
• Olivieri, I. , and Gouyon P.‐H.. 1997. Evolution of migration rate and other traits: the metapopulation effect In Hanski I., and Gilpin M. E., eds. Metapopulation Biology: Ecology, Genetics and Evolution , pp. 293–323. Academic Press, San Diego. [ Google Scholar ]
• Olivieri, I. , Couvet D., and G ouyon P.‐H. 1990. The genetics of transient populations – research at the metapopulation level . Trends in Ecology and Evolution 5 :207–210. [ PubMed ] [ Google Scholar ]
• Olivieri, I. , Michalakis Y., and Gouyon P.‐H. 1995. Metapopulation genetics and the evolution of dispersal . American Naturalist 146 :202–228. [ Google Scholar ]
• Oostermeijer, J. G. B. , Luijten S. H., and den Nijs J. C. M. 2003. Integrating demographic and genetic approaches in plant conservation . Biological Conservation 113 :389–398. [ Google Scholar ]
• Orr, H. A. , and Unckless R. L. 2014. The population genetics of evolutionary rescue . Plos Genetics 10 :e1004551. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Ouborg, N. J. 2010. Integrating population genetics and conservation biology in the era of genomics . Biology Letters 6 :3–6. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Pannell, J. R. , and Barrett S. C. H. 2001. Effects of population size and metapopulation dynamics on a mating‐system polymorphism . Theoretical population Biology 59 :145–155. [ PubMed ] [ Google Scholar ]
• Petit, C. , Fréville H., Mignot A., Colas B., Riba M., Imbert E., Hurtrez‐Bousses S. et al. 2001. Gene flow and local adaptation in two endemic plant species . Biological Conservation 100 :21–34. [ Google Scholar ]
• Rabinowitz, D. 1981. Seven forms of rarity In: Synge H., ed. The Biological Aspects of Rare Plant Conservation , pp. 205–217. Wiley, New York. [ Google Scholar ]
• Radies, D. , Coxson D., Johnson C., and Konwicki K. 2009. Predicting canopy macrolichen diversity and abundance within old‐growth inland temperate rainforests . Forest Ecology and Management 259 :86–97. [ Google Scholar ]
• Ravigné, V. , Olivieri I., Gonzalez‐Martinez S. C., and Rousset F. 2006. Selective interactions between short‐distance pollen and seed dispersal in self‐compatible species . Evolution 60 :2257–2271. [ PubMed ] [ Google Scholar ]
• Ravigné, V. , Diekmann U., and Olivieri I. 2004. Implications of habitat choice for protected polymorphism . Evolutionary Ecology Research 6 :125–145. [ Google Scholar ]
• Ravigné, V. , Olivieri I., and Dieckmann U. 2009. Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity . American Naturalist 174 :E141–E169. [ PubMed ] [ Google Scholar ]
• Realini, M. F. , Gonzalez G. E., Font F., Picca P. I., Poggio L., and Gottlieb A. M. 2015. Phylogenetic relationships in Opuntia (Cactaceae, Opuntioideae) from southern South America . Plant Systematics and Evolution 30 :1123–1134. [ Google Scholar ]
• Rebelo, A. G. 1992. Protea Atlas manual: Instruction Booklet to the Protea Atlas Project . National Botanical Institute, Claremont, South Africa. [ Google Scholar ]
• Rebelo, A. G. 2001. A Field Guide to the Proteas of Southern Africa . Fernwood Press, Vlaeberg, Cape Town. [ Google Scholar ]
• Riba, M. , Colas B., Fréville H., Henry J.‐P., Mignot A., Petit C., Ronce O. et al. 2001. Diagnostic de la situation de Centaurea corymbosa ( Asteraceae ), endémique du massif de la Clape (Aude, France) . Bocconea 13 :173–179. [ Google Scholar ]
• Riba, M. , Mignot A., Fréville H., Colas B., Imbert E., Vile D., Virevaire M. et al. 2005. Variation in dispersal traits in a narrow‐endemic plant species, Centaurea corymbosa Pourret. ( Asteraceae ) . Evolutionary Ecology 19 :241–254. [ Google Scholar ]
• Riba, M. , Mayol M., Giles B. E., Ronce O., Imbert E., van der Velde M., Chauvet S. et al. 2009. Darwin's wind hypothesis: does it work for plant dispersal in fragmented habitats? New Phytologist 183 :667–677. [ PubMed ] [ Google Scholar ]
• Ronce, O. 2007. How does it feel to be like a rolling stone? Ten questions about dispersal evolution . Annual Review of Ecology Evolution and Systematics 38 :231–253. [ Google Scholar ]
• Ronce, O. , and Olivieri I. 1997. Evolution of reproductive effort in a metapopulation with local extinctions and ecological succession . American Naturalist 150 :220–249. [ PubMed ] [ Google Scholar ]
• Ronce, O. , and Olivieri I.. 2004. Life‐history evolution in metapopulations In Hanski I., and Gaggiotti O. E., eds. Ecology, Genetics, and Evolution of Metapopulations , pp. 227–258. Academic Press, Amsterdam. [ Google Scholar ]
• Ronce, O. , Perret F., and Olivieri I. 2000a. Evolutionarily stable dispersal rates do not always increase with local extinction rates . American Naturalist 155 :485–496. [ PubMed ] [ Google Scholar ]
• Ronce, O. , Perret F., and Olivieri I. 2000b. Landscape dynamics and evolution of colonizer syndromes: interactions between reproductive effort and dispersal in a metapopulation . Evolutionary Ecology 14 :233–260. [ Google Scholar ]
• Ronce, O. , Brachet S., Olivieri I., Gouyon P.‐H., and Clobert J. 2005. Plastic changes in seed dispersal along ecological succession: theoretical predictions from an evolutionary model . Journal of Ecology 93 :431–440. [ Google Scholar ]
• Rosenzweig, F. , and Sherlock G.. 2014. Experimental evolution: prospects and challenges . Genomics 104 :V–VI. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Santamaria, L. , and Mendez P. F. 2012. Evolution in biodiversity policy – current gaps and future needs . Evolutionary Applications 5 :202–218. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Schlesinger, M. D. , and Novak P. G. 2011. Status and conservation of an imperiled tiger beetle fauna in New York State, USA . Journal of Insect Conservation 15 :839–852. [ Google Scholar ]
• Schulze, R. E. 1997. South African Atlas of Agrohydrology and Climatology . Water Research Commission Report TT82/96. Pretoria, South Africa. [ Google Scholar ]
• Shaffer, A. B. A. , Wolf J. B. W., Alves P. C., Bergstrom L., Bruford M. W., Brannstrom I., Colling G. et al. 2015. Genomics and the challenging translation into conservation practice . Trends in Ecology & Evolution 30 :78–87. [ PubMed ] [ Google Scholar ]
• Simon, M. F. , and Pennington T.. 2012. Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado . International Journal of Plant Sciences 173 :711–723. [ Google Scholar ]
• Slatkin, M. , and Wade M. J. 1978. Group selection on a quantitative character . Proceedings of the National Academy of Sciences of the United States of America 75 :3531–3534. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Snogerup, S. , Gustafsson M., and Von Bothmer R. 1990. Brassica sect. Brassica (Brassicaceae) I. Taxonomy and variation . Willdenowia 19 :271–365. [ Google Scholar ]
• Syphard, A. D. , Radeloff V. C., Hawbaker T. J., and Stewart S. I. 2009. Conservation threats due to human‐caused increases in fire frequency in Mediterranean climate ecosystems . Conservation Biology 23 :758–769. [ PubMed ] [ Google Scholar ]
• Tallmon, D. A. , Luikart G., and Waples R. S. 2004. The alluring simplicity and complex reality of genetic rescue . Trends in Ecology and Evolution 19 :489–496. [ PubMed ] [ Google Scholar ]
• Thomson, R. C. , Wang I. J., and Johnson J. R. 2010. Genome‐enabled development of DNA markers for ecology, evolution and conservation . Molecular Ecology 19 :21–84. [ PubMed ] [ Google Scholar ]
• Tonnabel, J. , Van Dooren T., Midgley J., Haccou P., Mignot A., Ronce O., and Olivieri I. 2012. Optimal resource allocation in a serotinous non‐sprouting plant species under different fire regimes . Journal of Ecology 100 :1464–1474. [ Google Scholar ]
• Tonnabel, J. , Mignot A., Douzery E. J. P., Rebelo A. G., Schurr F. M., Midgley J., Illing N. et al. 2014. Convergent and correlated evolution of major life history traits in the angiosperm genus Leucadendron (Proteaceae) . Evolution 68 :2775–2792. [ PubMed ] [ Google Scholar ]
• Tyson, P. , Fuchs R., Fu C., Lebel L., Mitra A. P., Odada E., Jerry J. et al. 2002. Global–Regional Linkages in the Earth System , pp. 3–73. Springer, Berlin. [ Google Scholar ]
• van Valen, L. 1971. Group selection and the evolution of dispersal . Evolution 25 :591–598. [ PubMed ] [ Google Scholar ]
• Vitalis, R. , Dubois M. P., and Olivieri I. 2001. Characterization of microsatellite loci in the endangered species of fern Marsilea strigosa Willd. (Marsileaceae, Pteridophyta) . Molecular Ecology Notes 1 :64–66. [ Google Scholar ]
• Vitalis, R. , Riba M., Colas B., Grillas P., and Olivieri I. 2002. Multilocus genetic structure at contrasted spatial scales of the endangered water fern Marsilea strigosa Willd. (Marsileaceae, Pteridophyta) . American Journal of Botany 89 :1142–1155. [ PubMed ] [ Google Scholar ]
• Vitalis, R. , Glemin S., and Olivieri I. 2004. When genes go to sleep: the population genetic consequences of seed dormancy and monocarpic perenniality . American Naturalist 163 :295–311. [ PubMed ] [ Google Scholar ]
• Vitalis, R. , Rousset F., Kobayashi Y., Olivieri I., and Gandon S. 2014. The joint evolution of dispersal and dormancy in a metapopulation with local extinctions and kin competition . Evolution 67 :1676–1691. [ PubMed ] [ Google Scholar ]
• Wagenius, S. , Lonsdorf E., and Neuhauser C. 2007. Patch aging and the S‐Allee effect: breeding system effects on the demographic response of plants to habitat fragmentation . American Naturalist 169 :383–397. [ PubMed ] [ Google Scholar ]
• van der Wal, E. , Garant D., Festa‐Bianchet M., and Pelletier F. 2013. Evolutionary rescue in vertebrates: evidence, applications and uncertainty . Philosophical transactions of the Royal Society of London. Series B, Biological sciences 368 :20120090. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Weekley, C. W. , Zaya D. N., Menges E. S., and Faivre A. E. 2010. Multiple causes of seedling rarity in scrub plum, Prunus geniculata (Rosaceae), an endangered shrub of the Florida scrub . American Journal of Botany 97 :144–155. [ PubMed ] [ Google Scholar ]
• Weill, M. 2013. Overview of 40 years of insecticide resistance genes evolution in the mosquito Culex pipiens . Pathogens and Global Health 107 :433–434. [ Google Scholar ]
• Weiss, P. W. 1984. Seed characteristics and regeneration of some species in invaded coastal communities . Austral Ecology 9 :99–106. [ Google Scholar ]
• Whiteley, A. R. , Fitzpatrick S. W., Funk W. C., and Tallmon D. A. 2015. Genetic rescue to the rescue . Trends in Ecology and Evolution 30 :42–49. [ PubMed ] [ Google Scholar ]
• Widler, B. E. , and Bocquet G. 1979. Brassica insularis , an example of a Messinian pattern of distribution . Candollea 34 :133–152. [ Google Scholar ]
• van Wilgen, B. W. , Forsyth G. G., De Klerk H., Das S., Khuluse S., and Schmitz P. 2010. Fire management in Mediterranean‐climate shrublands: a case study from the Cape Fynbos, South Africa . Journal of Applied Ecology 47 :631–638. [ Google Scholar ]
• Wilson, G. A. , and Rannala B. 2003. Bayesian inference of recent migration rates using multilocus genotypes . Genetics 163 :1177–1191. [ PMC free article ] [ PubMed ] [ Google Scholar ]
• van Woesik, R. , Franklin E. C., O'Leary J., McClanahan T. R., Klaus J. S., and Budd A. F. 2012. Hosts of the Plio‐Pleistocene past reflect modern‐day coral vulnerability . Proceedings of the Royal Society B‐Biological Sciences 279 :2448–2456. [ PMC free article ] [ PubMed ] [ Google Scholar ]

• Search Menu

Sign in through your institution

• Browse content in Arts and Humanities
• Browse content in Archaeology
• Anglo-Saxon and Medieval Archaeology
• Archaeological Methodology and Techniques
• Archaeology by Region
• Archaeology of Religion
• Archaeology of Trade and Exchange
• Biblical Archaeology
• Contemporary and Public Archaeology
• Environmental Archaeology
• Historical Archaeology
• History and Theory of Archaeology
• Industrial Archaeology
• Landscape Archaeology
• Mortuary Archaeology
• Prehistoric Archaeology
• Underwater Archaeology
• Zooarchaeology
• Browse content in Architecture
• Architectural Structure and Design
• History of Architecture
• Residential and Domestic Buildings
• Theory of Architecture
• Browse content in Art
• Art Subjects and Themes
• History of Art
• Industrial and Commercial Art
• Theory of Art
• Biographical Studies
• Byzantine Studies
• Browse content in Classical Studies
• Classical Numismatics
• Classical Literature
• Classical Reception
• Classical History
• Classical Philosophy
• Classical Mythology
• Classical Art and Architecture
• Classical Oratory and Rhetoric
• Greek and Roman Archaeology
• Greek and Roman Epigraphy
• Greek and Roman Law
• Greek and Roman Papyrology
• Late Antiquity
• Religion in the Ancient World
• Social History
• Digital Humanities
• Browse content in History
• Colonialism and Imperialism
• Diplomatic History
• Environmental History
• Genealogy, Heraldry, Names, and Honours
• Genocide and Ethnic Cleansing
• Historical Geography
• History by Period
• History of Agriculture
• History of Education
• History of Emotions
• History of Gender and Sexuality
• Industrial History
• Intellectual History
• International History
• Labour History
• Legal and Constitutional History
• Local and Family History
• Maritime History
• Military History
• National Liberation and Post-Colonialism
• Oral History
• Political History
• Public History
• Regional and National History
• Revolutions and Rebellions
• Slavery and Abolition of Slavery
• Social and Cultural History
• Theory, Methods, and Historiography
• Urban History
• World History
• Browse content in Language Teaching and Learning
• Language Learning (Specific Skills)
• Language Teaching Theory and Methods
• Browse content in Linguistics
• Applied Linguistics
• Cognitive Linguistics
• Computational Linguistics
• Forensic Linguistics
• Grammar, Syntax and Morphology
• Historical and Diachronic Linguistics
• History of English
• Language Variation
• Language Families
• Language Acquisition
• Language Evolution
• Language Reference
• Lexicography
• Linguistic Theories
• Linguistic Typology
• Linguistic Anthropology
• Phonetics and Phonology
• Psycholinguistics
• Sociolinguistics
• Translation and Interpretation
• Writing Systems
• Browse content in Literature
• Bibliography
• Children's Literature Studies
• Literary Studies (Modernism)
• Literary Studies (Asian)
• Literary Studies (European)
• Literary Studies (Eco-criticism)
• Literary Studies (Romanticism)
• Literary Studies (American)
• Literary Studies - World
• Literary Studies (1500 to 1800)
• Literary Studies (19th Century)
• Literary Studies (20th Century onwards)
• Literary Studies (African American Literature)
• Literary Studies (British and Irish)
• Literary Studies (Early and Medieval)
• Literary Studies (Fiction, Novelists, and Prose Writers)
• Literary Studies (Gender Studies)
• Literary Studies (Graphic Novels)
• Literary Studies (History of the Book)
• Literary Studies (Plays and Playwrights)
• Literary Studies (Poetry and Poets)
• Literary Studies (Postcolonial Literature)
• Literary Studies (Queer Studies)
• Literary Studies (Science Fiction)
• Literary Studies (Travel Literature)
• Literary Studies (War Literature)
• Literary Studies (Women's Writing)
• Literary Theory and Cultural Studies
• Mythology and Folklore
• Shakespeare Studies and Criticism
• Browse content in Media Studies
• Browse content in Music
• Applied Music
• Dance and Music
• Ethics in Music
• Ethnomusicology
• Gender and Sexuality in Music
• Medicine and Music
• Music Cultures
• Music and Culture
• Music and Religion
• Music and Media
• Music Education and Pedagogy
• Music Theory and Analysis
• Musical Scores, Lyrics, and Libretti
• Musical Structures, Styles, and Techniques
• Musicology and Music History
• Performance Practice and Studies
• Race and Ethnicity in Music
• Sound Studies
• Browse content in Performing Arts
• Browse content in Philosophy
• Aesthetics and Philosophy of Art
• Epistemology
• Feminist Philosophy
• History of Western Philosophy
• Meta-Philosophy
• Metaphysics
• Moral Philosophy
• Non-Western Philosophy
• Philosophy of Action
• Philosophy of Law
• Philosophy of Religion
• Philosophy of Science
• Philosophy of Language
• Philosophy of Mind
• Philosophy of Perception
• Philosophy of Mathematics and Logic
• Practical Ethics
• Social and Political Philosophy
• Browse content in Religion
• Biblical Studies
• Christianity
• East Asian Religions
• History of Religion
• Judaism and Jewish Studies
• Qumran Studies
• Religion and Education
• Religion and Health
• Religion and Politics
• Religion and Science
• Religion and Law
• Religion and Art, Literature, and Music
• Religious Studies
• Browse content in Society and Culture
• Cookery, Food, and Drink
• Cultural Studies
• Customs and Traditions
• Ethical Issues and Debates
• Hobbies, Games, Arts and Crafts
• Natural world, Country Life, and Pets
• Popular Beliefs and Controversial Knowledge
• Sports and Outdoor Recreation
• Technology and Society
• Travel and Holiday
• Visual Culture
• Browse content in Law
• Arbitration
• Browse content in Company and Commercial Law
• Commercial Law
• Company Law
• Browse content in Comparative Law
• Systems of Law
• Competition Law
• Browse content in Constitutional and Administrative Law
• Government Powers
• Judicial Review
• Local Government Law
• Military and Defence Law
• Parliamentary and Legislative Practice
• Construction Law
• Contract Law
• Browse content in Criminal Law
• Criminal Procedure
• Criminal Evidence Law
• Sentencing and Punishment
• Employment and Labour Law
• Environment and Energy Law
• Browse content in Financial Law
• Banking Law
• Insolvency Law
• History of Law
• Human Rights and Immigration
• Intellectual Property Law
• Browse content in International Law
• Private International Law and Conflict of Laws
• Public International Law
• IT and Communications Law
• Jurisprudence and Philosophy of Law
• Law and Society
• Law and Politics
• Browse content in Legal System and Practice
• Courts and Procedure
• Legal Skills and Practice
• Legal System - Costs and Funding
• Primary Sources of Law
• Regulation of Legal Profession
• Medical and Healthcare Law
• Browse content in Policing
• Criminal Investigation and Detection
• Police and Security Services
• Police Procedure and Law
• Police Regional Planning
• Browse content in Property Law
• Personal Property Law
• Restitution
• Study and Revision
• Terrorism and National Security Law
• Browse content in Trusts Law
• Wills and Probate or Succession
• Browse content in Medicine and Health
• Browse content in Allied Health Professions
• Arts Therapies
• Clinical Science
• Dietetics and Nutrition
• Occupational Therapy
• Operating Department Practice
• Physiotherapy
• Radiography
• Speech and Language Therapy
• Browse content in Anaesthetics
• General Anaesthesia
• Browse content in Clinical Medicine
• Acute Medicine
• Cardiovascular Medicine
• Clinical Genetics
• Clinical Pharmacology and Therapeutics
• Dermatology
• Endocrinology and Diabetes
• Gastroenterology
• Genito-urinary Medicine
• Geriatric Medicine
• Infectious Diseases
• Medical Oncology
• Medical Toxicology
• Pain Medicine
• Palliative Medicine
• Rehabilitation Medicine
• Respiratory Medicine and Pulmonology
• Rheumatology
• Sleep Medicine
• Sports and Exercise Medicine
• Clinical Neuroscience
• Community Medical Services
• Critical Care
• Emergency Medicine
• Forensic Medicine
• Haematology
• History of Medicine
• Medical Ethics
• Browse content in Medical Dentistry
• Oral and Maxillofacial Surgery
• Paediatric Dentistry
• Restorative Dentistry and Orthodontics
• Surgical Dentistry
• Browse content in Medical Skills
• Clinical Skills
• Communication Skills
• Nursing Skills
• Surgical Skills
• Medical Statistics and Methodology
• Browse content in Neurology
• Clinical Neurophysiology
• Neuropathology
• Nursing Studies
• Browse content in Obstetrics and Gynaecology
• Gynaecology
• Occupational Medicine
• Ophthalmology
• Otolaryngology (ENT)
• Browse content in Paediatrics
• Neonatology
• Browse content in Pathology
• Chemical Pathology
• Clinical Cytogenetics and Molecular Genetics
• Histopathology
• Medical Microbiology and Virology
• Patient Education and Information
• Browse content in Pharmacology
• Psychopharmacology
• Browse content in Popular Health
• Caring for Others
• Complementary and Alternative Medicine
• Self-help and Personal Development
• Browse content in Preclinical Medicine
• Cell Biology
• Molecular Biology and Genetics
• Reproduction, Growth and Development
• Primary Care
• Professional Development in Medicine
• Browse content in Psychiatry
• Addiction Medicine
• Child and Adolescent Psychiatry
• Forensic Psychiatry
• Learning Disabilities
• Old Age Psychiatry
• Psychotherapy
• Browse content in Public Health and Epidemiology
• Epidemiology
• Public Health
• Browse content in Radiology
• Clinical Radiology
• Interventional Radiology
• Nuclear Medicine
• Radiation Oncology
• Reproductive Medicine
• Browse content in Surgery
• Cardiothoracic Surgery
• Gastro-intestinal and Colorectal Surgery
• General Surgery
• Neurosurgery
• Paediatric Surgery
• Peri-operative Care
• Plastic and Reconstructive Surgery
• Surgical Oncology
• Transplant Surgery
• Trauma and Orthopaedic Surgery
• Vascular Surgery
• Browse content in Science and Mathematics
• Browse content in Biological Sciences
• Aquatic Biology
• Biochemistry
• Bioinformatics and Computational Biology
• Developmental Biology
• Ecology and Conservation
• Evolutionary Biology
• Genetics and Genomics
• Microbiology
• Molecular and Cell Biology
• Natural History
• Plant Sciences and Forestry
• Research Methods in Life Sciences
• Structural Biology
• Systems Biology
• Zoology and Animal Sciences
• Browse content in Chemistry
• Analytical Chemistry
• Computational Chemistry
• Crystallography
• Environmental Chemistry
• Industrial Chemistry
• Inorganic Chemistry
• Materials Chemistry
• Medicinal Chemistry
• Mineralogy and Gems
• Organic Chemistry
• Physical Chemistry
• Polymer Chemistry
• Study and Communication Skills in Chemistry
• Theoretical Chemistry
• Browse content in Computer Science
• Artificial Intelligence
• Computer Architecture and Logic Design
• Game Studies
• Human-Computer Interaction
• Mathematical Theory of Computation
• Programming Languages
• Software Engineering
• Systems Analysis and Design
• Virtual Reality
• Browse content in Computing
• Business Applications
• Computer Games
• Computer Security
• Computer Networking and Communications
• Digital Lifestyle
• Graphical and Digital Media Applications
• Operating Systems
• Browse content in Earth Sciences and Geography
• Atmospheric Sciences
• Environmental Geography
• Geology and the Lithosphere
• Maps and Map-making
• Meteorology and Climatology
• Oceanography and Hydrology
• Palaeontology
• Physical Geography and Topography
• Regional Geography
• Soil Science
• Urban Geography
• Browse content in Engineering and Technology
• Agriculture and Farming
• Biological Engineering
• Civil Engineering, Surveying, and Building
• Electronics and Communications Engineering
• Energy Technology
• Engineering (General)
• Environmental Science, Engineering, and Technology
• History of Engineering and Technology
• Mechanical Engineering and Materials
• Technology of Industrial Chemistry
• Transport Technology and Trades
• Browse content in Environmental Science
• Applied Ecology (Environmental Science)
• Conservation of the Environment (Environmental Science)
• Environmental Sustainability
• Environmentalist Thought and Ideology (Environmental Science)
• Management of Land and Natural Resources (Environmental Science)
• Natural Disasters (Environmental Science)
• Nuclear Issues (Environmental Science)
• Pollution and Threats to the Environment (Environmental Science)
• Social Impact of Environmental Issues (Environmental Science)
• History of Science and Technology
• Browse content in Materials Science
• Ceramics and Glasses
• Composite Materials
• Metals, Alloying, and Corrosion
• Nanotechnology
• Browse content in Mathematics
• Applied Mathematics
• Biomathematics and Statistics
• History of Mathematics
• Mathematical Education
• Mathematical Finance
• Mathematical Analysis
• Numerical and Computational Mathematics
• Probability and Statistics
• Pure Mathematics
• Browse content in Neuroscience
• Cognition and Behavioural Neuroscience
• Development of the Nervous System
• Disorders of the Nervous System
• History of Neuroscience
• Invertebrate Neurobiology
• Molecular and Cellular Systems
• Neuroendocrinology and Autonomic Nervous System
• Neuroscientific Techniques
• Sensory and Motor Systems
• Browse content in Physics
• Astronomy and Astrophysics
• Atomic, Molecular, and Optical Physics
• Biological and Medical Physics
• Classical Mechanics
• Computational Physics
• Condensed Matter Physics
• Electromagnetism, Optics, and Acoustics
• History of Physics
• Mathematical and Statistical Physics
• Measurement Science
• Nuclear Physics
• Particles and Fields
• Plasma Physics
• Quantum Physics
• Relativity and Gravitation
• Semiconductor and Mesoscopic Physics
• Browse content in Psychology
• Affective Sciences
• Clinical Psychology
• Cognitive Neuroscience
• Cognitive Psychology
• Criminal and Forensic Psychology
• Developmental Psychology
• Educational Psychology
• Evolutionary Psychology
• Health Psychology
• History and Systems in Psychology
• Music Psychology
• Neuropsychology
• Organizational Psychology
• Psychological Assessment and Testing
• Psychology of Human-Technology Interaction
• Psychology Professional Development and Training
• Research Methods in Psychology
• Social Psychology
• Browse content in Social Sciences
• Browse content in Anthropology
• Anthropology of Religion
• Human Evolution
• Medical Anthropology
• Physical Anthropology
• Regional Anthropology
• Social and Cultural Anthropology
• Theory and Practice of Anthropology
• Browse content in Business and Management
• Business History
• Business Strategy
• Business Ethics
• Business and Government
• Business and Technology
• Business and the Environment
• Comparative Management
• Corporate Governance
• Corporate Social Responsibility
• Entrepreneurship
• Health Management
• Human Resource Management
• Industrial and Employment Relations
• Industry Studies
• Information and Communication Technologies
• International Business
• Knowledge Management
• Management and Management Techniques
• Operations Management
• Organizational Theory and Behaviour
• Pensions and Pension Management
• Public and Nonprofit Management
• Social Issues in Business and Management
• Strategic Management
• Supply Chain Management
• Browse content in Criminology and Criminal Justice
• Criminal Justice
• Criminology
• Forms of Crime
• International and Comparative Criminology
• Youth Violence and Juvenile Justice
• Development Studies
• Browse content in Economics
• Agricultural, Environmental, and Natural Resource Economics
• Asian Economics
• Behavioural Finance
• Behavioural Economics and Neuroeconomics
• Econometrics and Mathematical Economics
• Economic Methodology
• Economic Systems
• Economic History
• Economic Development and Growth
• Financial Markets
• Financial Institutions and Services
• General Economics and Teaching
• Health, Education, and Welfare
• History of Economic Thought
• International Economics
• Labour and Demographic Economics
• Law and Economics
• Macroeconomics and Monetary Economics
• Microeconomics
• Public Economics
• Urban, Rural, and Regional Economics
• Welfare Economics
• Browse content in Education
• Adult Education and Continuous Learning
• Care and Counselling of Students
• Early Childhood and Elementary Education
• Educational Equipment and Technology
• Educational Strategies and Policy
• Higher and Further Education
• Organization and Management of Education
• Philosophy and Theory of Education
• Schools Studies
• Secondary Education
• Teaching of a Specific Subject
• Teaching of Specific Groups and Special Educational Needs
• Teaching Skills and Techniques
• Browse content in Environment
• Applied Ecology (Social Science)
• Climate Change
• Conservation of the Environment (Social Science)
• Environmentalist Thought and Ideology (Social Science)
• Management of Land and Natural Resources (Social Science)
• Natural Disasters (Environment)
• Pollution and Threats to the Environment (Social Science)
• Social Impact of Environmental Issues (Social Science)
• Sustainability
• Browse content in Human Geography
• Cultural Geography
• Economic Geography
• Political Geography
• Browse content in Interdisciplinary Studies
• Communication Studies
• Museums, Libraries, and Information Sciences
• Browse content in Politics
• African Politics
• Asian Politics
• Chinese Politics
• Comparative Politics
• Conflict Politics
• Elections and Electoral Studies
• Environmental Politics
• Ethnic Politics
• European Union
• Foreign Policy
• Gender and Politics
• Human Rights and Politics
• Indian Politics
• International Relations
• International Organization (Politics)
• Irish Politics
• Latin American Politics
• Middle Eastern Politics
• Political Theory
• Political Methodology
• Political Communication
• Political Philosophy
• Political Sociology
• Political Behaviour
• Political Economy
• Political Institutions
• Politics and Law
• Politics of Development
• Public Administration
• Public Policy
• Qualitative Political Methodology
• Quantitative Political Methodology
• Regional Political Studies
• Russian Politics
• Security Studies
• State and Local Government
• UK Politics
• US Politics
• Browse content in Regional and Area Studies
• African Studies
• Asian Studies
• East Asian Studies
• Japanese Studies
• Latin American Studies
• Middle Eastern Studies
• Native American Studies
• Scottish Studies
• Browse content in Research and Information
• Research Methods
• Browse content in Social Work
• Addictions and Substance Misuse
• Adoption and Fostering
• Care of the Elderly
• Child and Adolescent Social Work
• Couple and Family Social Work
• Direct Practice and Clinical Social Work
• Emergency Services
• Human Behaviour and the Social Environment
• International and Global Issues in Social Work
• Mental and Behavioural Health
• Social Justice and Human Rights
• Social Policy and Advocacy
• Social Work and Crime and Justice
• Social Work Macro Practice
• Social Work Practice Settings
• Social Work Research and Evidence-based Practice
• Welfare and Benefit Systems
• Browse content in Sociology
• Childhood Studies
• Community Development
• Comparative and Historical Sociology
• Disability Studies
• Economic Sociology
• Gender and Sexuality
• Gerontology and Ageing
• Health, Illness, and Medicine
• Marriage and the Family
• Migration Studies
• Occupations, Professions, and Work
• Organizations
• Population and Demography
• Race and Ethnicity
• Social Theory
• Social Movements and Social Change
• Social Research and Statistics
• Social Stratification, Inequality, and Mobility
• Sociology of Religion
• Sociology of Education
• Sport and Leisure
• Urban and Rural Studies
• Browse content in Warfare and Defence
• Defence Strategy, Planning, and Research
• Land Forces and Warfare
• Military Administration
• Military Life and Institutions
• Naval Forces and Warfare
• Other Warfare and Defence Issues
• Peace Studies and Conflict Resolution
• Weapons and Equipment

Conservation Biology for All

• Cite Icon Cite
• Permissions Icon Permissions

This book provides cutting-edge but basic conservation science for the inhabitants of both developing as well as developed countries. Authoritative chapters are written by top names in conservation biology. Important topics such as balancing conversion and human needs, climate change, conservation planning, designing and analyzing conservation research, ecosystem services, endangered species management, extinctions, fire, habitat loss, and invasive species are covered. Numerous textboxes describing additional relevant material or case studies are also included. The book is written for undergraduate and graduate students as well as scientists, managers, and personnel in governmental and non-governmental organizations. The book has all the necessary topics to become a required reading for various undergraduate and graduate conservation-related courses. English is kept at a level comprehensible to people with English as a second language. Overall, this book represents a project that the conservation community has deemed worthy of support by donations of time and effort.

Personal account

• Sign in with email/username & password
• Get email alerts
• Save searches
• Purchase content
• Activate your purchase/trial code
• Add your ORCID iD

Institutional access

Sign in with a library card.

• Sign in with username/password
• Recommend to your librarian
• Institutional account management
• Get help with access

Access to content on Oxford Academic is often provided through institutional subscriptions and purchases. If you are a member of an institution with an active account, you may be able to access content in one of the following ways:

IP based access

Typically, access is provided across an institutional network to a range of IP addresses. This authentication occurs automatically, and it is not possible to sign out of an IP authenticated account.

Choose this option to get remote access when outside your institution. Shibboleth/Open Athens technology is used to provide single sign-on between your institution’s website and Oxford Academic.

• Click Sign in through your institution.
• Select your institution from the list provided, which will take you to your institution's website to sign in.
• When on the institution site, please use the credentials provided by your institution. Do not use an Oxford Academic personal account.
• Following successful sign in, you will be returned to Oxford Academic.

If your institution is not listed or you cannot sign in to your institution’s website, please contact your librarian or administrator.

Enter your library card number to sign in. If you cannot sign in, please contact your librarian.

Society Members

Society member access to a journal is achieved in one of the following ways:

Sign in through society site

Many societies offer single sign-on between the society website and Oxford Academic. If you see ‘Sign in through society site’ in the sign in pane within a journal:

• Click Sign in through society site.
• When on the society site, please use the credentials provided by that society. Do not use an Oxford Academic personal account.

If you do not have a society account or have forgotten your username or password, please contact your society.

Sign in using a personal account

Some societies use Oxford Academic personal accounts to provide access to their members. See below.

A personal account can be used to get email alerts, save searches, purchase content, and activate subscriptions.

Some societies use Oxford Academic personal accounts to provide access to their members.

Viewing your signed in accounts

Click the account icon in the top right to:

• View your signed in personal account and access account management features.
• View the institutional accounts that are providing access.

Signed in but can't access content

Oxford Academic is home to a wide variety of products. The institutional subscription may not cover the content that you are trying to access. If you believe you should have access to that content, please contact your librarian.

For librarians and administrators, your personal account also provides access to institutional account management. Here you will find options to view and activate subscriptions, manage institutional settings and access options, access usage statistics, and more.

Our books are available by subscription or purchase to libraries and institutions.

• About Oxford Academic
• Publish journals with us
• University press partners
• What we publish
• New features  
• Open access
• Rights and permissions
• Accessibility
• Advertising
• Media enquiries
• Oxford University Press
• Oxford Languages
• University of Oxford

Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide

• Copyright © 2024 Oxford University Press
• Cookie settings
• Cookie policy
• Privacy policy
• Legal notice

This Feature Is Available To Subscribers Only

Sign In or Create an Account

This PDF is available to Subscribers Only

For full access to this pdf, sign in to an existing account, or purchase an annual subscription.

An official website of the United States government

Here's how you know

Official websites use .gov A .gov website belongs to an official government organization in the United States.

Secure .gov websites use HTTPS A lock ( ) or https:// means you’ve safely connected to the .gov website. Share sensitive information only on official, secure websites.

•   Facebook
•   Twitter
•   Linkedin
•   Digg
•   Reddit
•   Pinterest
•   Email

Latest Earthquakes |    Chat Share Social Media  

Integrating ecological value and charismatic species habitats to prioritize habitats for conservation: A case study from Greater Yellowstone

Expanding human pressure has reduced natural habitats globally and motivated strategies to conserve remaining natural habitats. Decisions about conservation on private lands, however, are typically made by local stakeholders who are motivated by the elements of nature they most highly value. Thus, national prioritization for conservation should be complemented by local analysis of species or habitats that most influence local landowner decisions. We demonstrate within the Greater Yellowstone Ecosystem how quantitative mapping of wildlife species that are highly valued by local residents can be integrated with indices of ecosystem integrity to prioritize private lands for conservation. We found that natural vegetation cover (NVC) comprised 81% of the private lands. Some watersheds have lost 6% of NVC since 2001 and developed lands now cover >40% of their areas. Locations high in ecological value, elk habitat, and grizzly habitat occurred in different biophysical settings. Consequently, only 2% of the NVC supports high levels of all three biodiversity measures and 26% of this area was within conservation easements. The remaining areas of high biodiversity value that are unprotected are priorities for conservation. We suggest that national-scale conservation planning will be most effective on private lands if additional within-ecoregion analyses are done on the elements of biodiversity that are most valued by local people.

Citation Information

Related Content

Shannon brewer, phd, research fish biologist, frank t van manen, ph.d., supervisory research wildlife biologist, mark haroldson, supervisory wildlife biologist.

Academia.edu no longer supports Internet Explorer.

To browse Academia.edu and the wider internet faster and more securely, please take a few seconds to  upgrade your browser .

Enter the email address you signed up with and we'll email you a reset link.

• We're Hiring!
• Help Center

An Inquiry-based Case Study for Conservation Biology

Case studies provide an important tool for inquiry-based science education but require careful consideration of how class activities promote specific learning objectives. Here, we present a case study of the implementation of the Clean Water Act in Stroubles Creek, Virginia. In contrast to a lecture format, our approach achieves learning objectives by requiring students to ask and answer a series of questions related to the case study. First, we present a “teaching case” to be distributed to students.

Related Papers

Southeastern Naturalist

Andrew Edelman

Inquiry-based instruction has been shown to increase student motivation, engagement, and achievement in biology education. In this paper, we describe how we used an open-inquiry-based approach to engage undergraduate and graduate students in an upper-level conservation-biology class. As part of this course, students designed and implemented a research project using camera traps to examine questions related to wildlife conservation on their local campus. Students derived their research question through introductory readings and discussion regarding on-campus conservation issues. This approach allowed students to take ownership of the project, fueling enthusiasm and motivation, and promoting the development of core scientific skills. The students organized themselves into research teams at the beginning of the semester, a technique that mimicked how realworld conservation biologists collaborate on large-scale projects that require a range of knowledge and skills. In addition, teamwork allowed students to develop collaboration and communication skills and made them accountable to their peers for class performance. Given the applied nature of this course, the students also engaged in public outreach related to their research via social media and public presentations. These activities gave students the opportunity to learn how to interact with multiple stakeholders and deal with controversial issues in conservation biology.

Bioscience Education

Christopher M. Ernst

Natural history, defined in this context as the observation and description of the natural world, is fundamental to the broad discipline of ecology, yet is rarely integrated formally into undergraduate curricula; natural history is not often included in an academic program as a hands-on field-based research experience. There is a growing recognition that problem-based, situational projects are an important goal in higher education, but can be challenging to integrate into introductory biology courses, especially those that take students outside the classroom. Using a case study approach, we explore the challenges and opportunities when incorporating group-based natural history research projects into a required, introductory environmental biology course at McGill University in Quebec, Canada. Using an active learning, student-centered model of pedagogy, groups of students developed natural history research projects based on species that occur in a local forest. Students completed the entire research process: they developed their research question, designed field-based experiments, collected data, interpreted their findings and communicated the results. We present a full overview of the course and the mechanics of running complex, group-based research projects with undergraduate students. We present a model that is feasible, meeting the learning objectives, and creating a unique learning opportunity for students – a model we hope can be adopted by other instructors. We argue that field-based courses are as important as traditional indoor courses in any biology degree, and as such they require sustained support.

The American Biology Teacher

Helena Puche

This semi-guided inquiry activity explores the macroinvertebrate fauna in water sources affected by different levels of pollution. Students develop their ability to identify macroinvertebrates, compare aquatic fauna from different sources of water samples, evaluate water quality using an index, document and analyze data, raise questions and hypotheses, and discuss other possible issues that could be investigated at a later time. These sets of activities were designed for freshman high school students but are applicable to middle school students as well.

Education Inquiry

Maria Entezari

Case Studies in the Environment

Carole Griffiths

Critical thinking (CT) underpins the analytical and systems-thinking capacities needed for effective conservation in the 21st century but is seldom adequately fostered in most postsecondary courses and programs. Many instructors fear that devoting time to process skills will detract from content gains and struggle to define CT skills in ways relevant for classroom practice. We tested an approach to develop and assess CT in undergraduate conservation biology courses using case studies to address both challenges. We developed case studies with exercises to support content learning goals and assessment rubrics to evaluate student learning of both content and CT skills. We also developed a midterm intervention to enhance student metacognitive abilities at a light and intensive level and asked whether the level of the intervention impacted student learning. Data from over 200 students from five institutions showed an increase in students’ CT performance over a single term, under both lig...

Presented here is an inquiry-based unit on biogeochemical principles taught to tenth grade Ecology students that was designed and implemented by a teacher-graduate student part- nership who were supported by the National Science Foundation GK-12 program. Course content was based on results from local environmental research efforts, with students playing the role of scientists. The unit was framed as a crime scene investigation, in which students were tasked with determining the main culprits behind a widespread fish kill event in a local watershed, Hood Canal, Washington, a sub-basin of the Puget Sound estuary. Students were given sequential pieces of evidence (e.g. scientific plots, lab exercises, and simulations) to learn fundamental biogeochemical principles and were allowed to move on to the next piece of evidence after showing an understanding of the underlying concept, and how it fit in with the mystery as a whole. The graduate student was present two days per week and led self-designed warm-up exercises, lessons, and lab activities, while the teacher remained responsible for student discipline. This disciplinary dynamic made students generally feel comfortable working with the graduate student, strength- ening the student-mentor relationship. The teaching pair collaborated on the unit during a one-hour planning period twice weekly and corresponded remotely. This framework was successful in engaging local researchers with the K-12 STEM community, enhancing opportunities available for high school students, and providing diverse training for future educators. Although the NSF GK-12 program has been archived, we encourage educators and researchers to work towards the goal of creating sustainable STEM networks by lever- aging state STEM programs and soliciting new partnerships.

Madeleine Abrandt Dahlgren , Gunilla Oberg

This short paper describes BioScann, a high school STEM inquiry curriculum that uses a CSCL environment to support an interrupted case studies (ICS) method. This technologyenhanced curriculum supports autonomous, sustained student engagement, scientific argumentation, conceptual understanding, and the development of student self-efficacy and career awareness. The BioScann technology platform scaffolds student activities, collects student artifacts, and helps the teacher advance the curriculum through various stages. We discuss how our designs were improved across multiple pilot studies, including two major versions of the curriculum and technology. Each new pilot allowed us to improve the materials and technology environment, as well as student engagement, career awareness, and collaborative data-based decision-making. Major issues addressed Scholars, visionaries, and policymakers have called for education that prepares students to face the complex challenges of an increasingly tech...

amanda gonczi

This study analyzes 143 6 th -grade students’ open-ended responses prior to and following their participation in a three-dimensional, problem-based ecology curriculum unit. By the end of the unit, students were more likely to make accurate claims about the direct ( p = 0.003) and indirect effects ( p = 0.000) of a decrease in size of a top predator population. In addition, on a near-transfer assessment question, students were more likely to articulate long-term effects and feedback loops that reflected systems reasoning on the post-test as compared to the pre-test ( p = 0.015). Students were also more likely to make comparisons between graphs on the post-test than pre-test ( p = 0 .000). There was evidence of far-transfer learning in regards to the mediating effect of food abundance on a predator population, but not in regards to the influence of an abiotic factor on populations. In light of these findings, ecology learning progressions may need to be more fine-grained to distinguis...

American Institute of Biological Sciences

Clyde Herreid

RELATED PAPERS

Limnology and Oceanography Bulletin

Jennifer Klug

Franco Pirrami

Sonja Lopez Arnak

Helen Walkington

Norris Armstrong

Iowa Science Teachers Journal

Journal of Computing in Higher Education

Paula Jackson

Science Teacher

Lindy Brigham

Cognition and instruction: …

Brian K Smith , Brian J. Reiser

Journal of Food Science Education

Tracy Irani

Trends in Ecology &amp; Evolution

Peter Feinsinger

Journal of Natural Resources and Life …

Zonnetje Auburn

Journal of College Science Teaching

Nancy Schiller , Clyde Herreid , Mary Lundeberg

Claudia Hinojosa

Sarah Bunnell

Research in Science Education

Anat Abramovich

Journal of Physics: Conf. Series 1157 (2019) 022100

Evi Roviati

•   We're Hiring!
•   Help Center
• Find new research papers in:
• Health Sciences
• Earth Sciences
• Cognitive Science
• Mathematics
• Computer Science
• Academia ©2024