Next Article in Journal
Identification and Functional Analysis of Known and New Mutations in the Transcription Factor KLF1 Linked with β-Thalassemia-like Phenotypes
Previous Article in Journal
Inputs and Outputs of the Mammalian Circadian Clock
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Biology
Volume 12
Issue 4
10.3390/biology12040509
biology-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Assessing Global Efforts in the Selection of Vertebrates as Umbrella Species for Conservation

by
Nan Yang
1,†,
Megan Price
2,†,
Yu Xu
3,
Yun Zhu
3,
Xue Zhong
4,*,
Yuehong Cheng
5 and
Bin Wang
4
1
Institute of Qinghai-Tibetan Plateau, Southwest Minzu University, Chengdu 610225, China
2
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China
3
Key Laboratory of National Forestry and Grassland Administration on Biodiversity Conservation in Karst Mountainous Areas of Southwestern China, School of Life Sciences, Guizhou Normal University, Guiyang 550001, China
4
Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong 637009, China
5
Wolong National Nature Reserve Administration Bureau, Wenchuan 623006, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Biology 2023, 12(4), 509; https://doi.org/10.3390/biology12040509
Submission received: 9 February 2023 / Revised: 15 March 2023 / Accepted: 24 March 2023 / Published: 28 March 2023
(This article belongs to the Section Conservation Biology and Biodiversity)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Conservation funds and resources have long been globally inadequate, and methods that could maximize conservation outcomes with limited investment, such as umbrella-species strategies, are thus needed to address the current biodiversity crisis. In this study, we summarized 242 published scientific articles and found 213 terrestrial vertebrates that were recommended as umbrella species. We summarized global trends in umbrella species selection and research during the past four decades, with North America, Europe, and Asia over-representing umbrella-related studies, and thus, more umbrella species recommendations have occurred in the Northern Hemisphere. Generally, there has been a bias toward recommending bird and mammal species, wide-ranging species, and non-threatened species, such as umbrellas, and grouses (order Galliformes) and large carnivores have often been recommended as umbrellas across different continents by multiple studies. Given observed biases and trends, we raise concerns about neglecting amphibians and reptiles, the over-preference for wide-ranging and non-threatened species, and recommend little-known species. We argue that conservation umbrella strategies can be cost-effective and successful given that appropriate species are chosen in the right location, and our findings could inform future conservation research and practices using conservation umbrella strategies.

Abstract

The umbrella-species strategy has been proposed as an attainable tool to achieve multi-species and community conservation with limited investment. There have been many umbrella-related studies since the concept’s inception; thus, a summary of global study efforts and recommended umbrella species is important for understanding advances in the field and facilitating conservation applications. Here, we collated 213 recommended umbrella species of terrestrial vertebrates from 242 scientific articles published during 1984–2021 and analyzed their geographic patterns, biological features, and conservation statuses to identify global trends in the selection of umbrella species. We found a considerable geographic bias: most studies and, consequently, recommended umbrella species are from the Northern Hemisphere. There is also a strong taxonomic bias, with grouses (order Galliformes) and large carnivores being the most popular umbrella species and amphibians and reptiles being largely overlooked. In addition, wide-ranging and non-threatened species were frequently recommended as umbrella species. Given the observed biases and trends, we caution that appropriate species need to be chosen for each location, and it is important to confirm that popular, wide-ranging species are effective umbrella species. Moreover, amphibians and reptiles should be investigated for their potential as umbrella species. The umbrella-species strategy has many strengths and, if applied appropriately, may be one of the best options in today’s conservation research and funding landscape.

1. Introduction

The rapid loss of global biodiversity is one of the most urgent challenges facing humanity [1]. Unfortunately, given that global conservation has long been inadequately funded, limiting outcomes [2], addressing the global biodiversity crisis is quite challenging. Therefore, it may be prudent to revisit strategies that could protect more species more economically and effectively [3]. The umbrella-species strategy has been proposed as a shortcut to achieving broader conservation aims while overcoming funding and information constraints [4,5]. Essentially, the concept is that conserving one umbrella species confers protection to a large number of co-occurring species [6,7]. Compared with the other conservation surrogates, such as flagship species (species that can be used as a symbol of conservation campaigns to attract public awareness and investment) and keystone species (species that have great impacts on many other species, communities, or ecosystems), the umbrella-species concept reflects the notions and practices of protection more directly [5,8]. Certainly, these terms often overlap in several species. For example, the charismatic giant panda (Ailuropoda melanoleuca) has become a successful flagship species raising public appeal, driving government policy, and attracting conservation funds throughout the world [9]; meanwhile, it has also been recommended as an umbrella species because by conserving vast areas of the intact bamboo forest it meets the giant panda’s dietary requirements and many other bamboo-dependent forest species are protected [10,11]. The umbrella effect of protecting sympatric species has been documented by numerous empirical studies, suggesting that it is an attainable and efficient strategy for maximizing conservation outcomes under limited resources [10,12,13,14].
Although there is debate as to when the umbrella-species concept was first proposed, we consider the first use of the term ‘umbrella species’ by Wilcox [15] as the key starting point. Since then, diverse criteria for the selection of umbrella species have been developed, such as selection based on body size [16], home range [17], geographic range [18], relationships with sympatric species [19], or representativeness for taxonomic and functional diversity [20]. Consequently, diverse taxa have been recommended as umbrellas, and umbrella species lists have been compiled to prioritize conservation management by governments and non-governmental organizations [21,22]. A comprehensive understanding of global research and the umbrella species they have recommended, especially their biological features and conservation statuses, is fundamental for understanding advances in this field and facilitating future conservation applications. However, no study has systematically reviewed existing umbrella species in the past nearly four decades since the concept’s inception, except for Roberge and Angelstam [6], who summarized the key studies prior to 2004.
Terrestrial biodiversity and ecosystems are highly related to sustainable development and human wellbeing. However, terrestrial vertebrates have been threatened by multiple intrinsic and extrinsic pressures and are thus at unprecedented extinction risks globally, raising concerns and demands to maximize the effectiveness and accuracy of global conservation efforts [1,23]. In this study, we scanned scientific articles focused on umbrella species published since 1984 and collated those terrestrial vertebrates (amphibians, reptiles, birds, and mammals) that were recommended as umbrella species. We aimed to determine any overall trends in the study efforts and umbrella species recommendations from a global-scale perspective by analyzing geographic patterns, biological features, and the conservation statuses of recommended umbrella species. Given the taxonomic and/or geographic imbalances in the identities of the species that were proposed as umbrella taxa could potentially limit the usefulness of this strategy and thereby undermine effective conservation policy, we then provided guidance for future conservation research and practices using this strategy based on the potential biases or inadequacies we revealed in this study.

2. Materials and Methods

We conducted a literature search using Web of ScienceTM (Science Citation Index Expanded; https://www.webofscience.com/ (accessed on 1 June 2022)), with the search topic “umbrella species” and a timespan from 1984 to 2021. We included those early view articles (without an assigned volume, issue, and pages) that were published online in advance of formal publication as well. In total, we obtained 735 articles and scanned them manually. We only considered articles that explicitly recommended one or several terrestrial vertebrate species (classes Amphibia, Reptilia, Aves, and Mammalia) that were studied as umbrella species and so excluded (1) reviews and meta-analyses, (2) studies on plants and invertebrates, (3) studies on aquatic-obligative vertebrates (such as fishes and whales), and (4) studies that considered all species within a guild or taxon as an umbrella species (e.g., recommending all parrots as umbrella species). We strictly distinguished umbrella species from other conservation surrogate terms and excluded the articles that only stated their study species as flagship species, keystone species, indicator species, or other surrogates while including the articles that recommended the species as umbrella species and other surrogates simultaneously. For the studies that selected umbrella species from a set of candidates, we only recorded the final and optimal selections.
We recorded study locations, the year of publication, and the umbrella species recommended from each retained article. We analyzed the number of studies conducted on each continent that were published each year to reveal the spatial and temporal distribution of the study efforts and identified the representative umbrella species for each continent by counting the number of studies on each species. Then, each umbrella species’ threatened category at the time when it was first proposed was recorded by searching the IUCN (International Union for Conservation of Nature) Red List of Threatened Species, published in the year that was closest to the year of the species’ first recommendation as an umbrella species. We also recorded their threatened categories, which were assessed by the latest version of the IUCN Red List [24], and compared the potential changes from their first recommendations. We obtained the biological information and current conservation status of each species from the latest IUCN Red List, including taxonomy, population trend, habitat, threats, general use and trade, the conservation actions already in place, and the conservation actions needed. We analyzed the proportions of recommended umbrella species across different biological features and conservation statuses to reveal global trends in the selection of umbrella species.
In addition, we downloaded the distribution polygons of global vertebrates from the IUCN dataset [24]. To generate a global distribution map with higher certainty for each species, we trimmed each species’ ranges according to their attributes [25] and retained the sections whose presence was extant, had a native origin, or were reintroduced, introduced, or had assisted colonization; were seasonally resident or resident through the breeding season, non-breeding season, and passage. Then, each species’ distribution range was clipped to the Earth’s land surface using a layer of land range from the World Borders Dataset 0.3 (https://thematicmapping.org/ (accessed on 20 June 2022)) as a mask. The species that were extinct and extinct in the wild were removed as their spatial data were not available in the IUCN dataset. Finally, we compiled geographic ranges for 6685 amphibian, 6979 reptile, 10,909 avian, and 5647 mammal species. To determine if the recommended umbrella species had larger geographic ranges than global terrestrial vertebrate species, we compared the terrestrial ranges of recommended umbrella species with all vertebrate species using a two-tailed Mann–Whitney U test as the data were non-normal (Kolmogorov–Smirnov tests, both p < 0.001). We applied a rejection criterion of α = 0.05. Species distribution polygons were processed using ArcGIS 10.6 (ESRI, Redlands, CA, USA) under the World Mercator projected coordinate system, and statistical analyses were conducted using R 4.2.2 [26].

3. Results

3.1. Geographic Distribution

In total, we summarized 242 articles published since 1984 that were directly related to umbrella species. These articles collectively recommended 213 terrestrial vertebrate species as umbrella species (refer to Table S1 for a full list). The first scientific article with an umbrella species as a study species indexed by the Science Citation Index Expanded was published in 1995, after which the total number of studies and newly recommended umbrella species increased rapidly over time and peaked in 2019 (Figure 1A). The research was dominated by studies from North America, followed by Europe and Asia. There were fewer studies from Africa, South America, and Oceania and none from Antarctica (Figure 2). Consequently, there were considerably more umbrella species recommended in North America, Europe, and Asia than in other continents (Figure 2). The sage grouse (Centrocercus urophasianus) was the most extensively studied among the 213 species, as a representative umbrella in North America, followed by the tiger (Panthera tigris) in Asia and the western capercaillie (Tetrao urogallus) in Europe. The jaguar (P. onca) was a popular umbrella species in both North and South America.

3.2. Biological Features

Birds (46.9%) and mammals (45.1%) dominated the 213 recommended umbrella species, whereas reptiles (5.2%) and amphibians (2.8%) were rarely selected (Figure 1B). The distribution polygons were not available for four reptile species; thus, we calculated the terrestrial range area of 209 recommended umbrella species. The Persian fallow deer (Dama mesopotamica) had the smallest range area of 614 km2, whereas the migratory peregrine falcon (Falco peregrinus) and osprey (Pandion haliaetus) had the largest with over 90 million km2 ranges (including all seasonal ranges; Table S2). The median terrestrial range for the recommended umbrella species (4,365,049 km2) was significantly larger than the median range of all terrestrial vertebrates (80,756 km2; Mann–Whitney U test, U = 1,140,467, Z = −15.942, p < 0.001). Over 70% of the 209 species had ranges above the upper quartile of all terrestrial vertebrate ranges (760,527 km2). In total, the 213 recommended umbrella species used 17 types of habitats (Table S2), but a higher proportion of them occupied one to three types of habitats (Figure 1C), with forest, shrubland, and grassland being the most frequently used habitats (Figure 1D).

3.3. Threats and Conservation Statuses

The majority of the 213 recommended umbrella species faced different types of historical, on-going, and/or future threats (Figure 3A), with biological resource use, agriculture and aquaculture, and residential and commercial development being the most common threat types (Figure 3B). Generally, whole individuals, parts of individuals, or the products from individuals of those recommended umbrella species were consumptively used by humans for a diverse set of use and trade purposes (Figure 3C), with pets, food, and sport hunting as general types of end uses (Figure 3D). However, about 20% of species were neither threatened nor used, and most of them were least concern (LC) species (Table S2).
The threatened categories for nine recommended umbrella species (4.2%) were unknown at the time they were the first recommended, but all of them were assessed in the latest version of the IUCN Red List (Figure 4). At the time of first recommendation, LC species accounted for about half of the 213 recommended umbrella species, followed by vulnerable (VU) species, while critically endangered (CR) species were the rarest (Figure 4). The threatened categories of most species remained unchanged from the time that they were first proposed until the latest version of the Red List (Figure 4), but eight species were downlisted, and five species were uplisted since their first recommendation (Table S2). The global populations of most umbrella species were estimated to be currently decreasing (63.9%), whereas only 16.4% and 13.1% of species had stable or increasing populations, respectively. The population trend was not estimated for 6.6% of the umbrella species.
Over half of the recommended umbrella species were protected under three or four types of conservation actions (Figure 5A), and land or water protection and management are currently in place for 205 species (Figure 5B). Based on specialists’ assessments, over 70% of these umbrella species will need more or improved conservation actions in the future (Figure 5C), and land or water management and protection are still required by a large proportion of species (Figure 5D).

4. Discussion

4.1. Geographic Bias in Umbrella-Focused Research

Since the 1984 inception of the umbrella-species concept [15], a considerable number of studies targeting umbrella species have been undertaken. We found that there was a rapid increase in published studies before 2019 (Figure 1A). This likely reflects the concerns of the global community for conserving biodiversity and the use of umbrella species as popular conservation strategies. This increase in publications may also reflect the availability of funding for these strategies. It is hoped that the increase in published studies has equated to an increase in on-the-ground conservation actions. Nevertheless, it is likely that the number of empirical umbrella-focused studies, on-the-ground efforts, and publication declines since 2019 was due to global constraints in field studies and conservation funding shortages resulting from the SARS-CoV pandemic [27,28], and the recovery of study efforts will probably lag behind the global post-pandemic recovery.
Our analysis has demonstrated a considerable geographic bias in study efforts toward the Northern Hemisphere. The number of studies was not in agreement with the global diversity of terrestrial vertebrates, with Asia, South America, and Africa indicating the highest species richness [29,30] but with lower study efforts. This is similar to other studies that have found a North American and European bias in the literature, probably correlated to the density of publishing conservation scientists [31,32]. Di Marco, Chapman, Althor, Kearney, Besancon, Butt, Maina, Possingham, Rogalla von Bieberstein, and Venter and Watson [31] also found that approximately 40% of national or sub-national conservation studies published between 2011 and 2015 were from the United States, United Kingdom, and Australia. It appears that conservationists in Oceania are publishing more non-umbrella-related articles. Therefore, the observed bias is likely due to the density of publishing scientists rather than any reflection of biodiversity-related factors. Perhaps the umbrella-species concept is less widely considered a viable option in these continents due to their focus on other methods of protection (e.g., ecosystems and habitats). However, it is likely that for several areas with rich biodiversity in the Southern Hemisphere, especially those developing countries in global biodiversity hotspots [33], conservation funding is limited, and thus, cost-effective strategies are key for greater conservation outcomes [28]. Given the proven usefulness of umbrella species for conservation [14,34], policymakers in these countries should take these strategies into account when formulating conservation practices and designing protected areas, and there are already diverse approaches that can provide informed guidance for selecting umbrella species with higher effectiveness and representativeness in a given region [35,36,37].

4.2. Taxonomic Bias in Recommending Umbrella Species

We found that amphibians and reptiles were infrequently considered or chosen as umbrella species compared to birds and mammals. This strong taxonomic bias in umbrella species was also reported in a previous review [6] and a meta-analysis [34]. This consistent preference for birds and mammals as umbrellas over amphibians and reptiles is likely due to several main factors. Firstly, compared to the majority of amphibians and reptiles, birds and mammals might meet some conventional criteria of umbrella species more easily, such as large body size, large home range, and ease of monitoring [38], making them more likely to be preconceived as capable umbrella species. Secondly, our deficient understanding of amphibian [39] and reptile distributions [40] has probably limited their usefulness as umbrella species and hindered any selection process. In addition, humans have had a long-standing preference for charismatic animals with aesthetic appeal [41,42]. Several of the most popular umbrella species also act as flagship species (e.g., the tiger and giant panda) and therefore need to be charismatically appealing. However, previous studies have suggested that satisfying conventional criteria does not necessarily lead to better umbrella effects, and a rigorous assessment of umbrella species is required to ensure their conservation effectiveness [34,38]. Given that umbrella species generally provide more benefit to same-taxon co-occurring species due to their similar resource requirements and shared threats [43], amphibian and reptile umbrellas could potentially provide better protection to sympatric amphibians and reptiles than currently favored avian and mammalian umbrellas. For example, water pollution and drought are generalized threats for amphibian species because they are so dependent on water quality compared to other terrestrial vertebrates, so the management of water sources in habitats targeting an amphibian umbrella species should confer direct conservation benefits to sympatric amphibian species [44]. Consequently, we recommend that more amphibians and reptiles should be assessed for their appropriateness as umbrella species across habitats and ecosystems.

4.3. Cautions in Selecting Umbrella Species

We found that a large proportion of existing recommended umbrella species are undergoing global population decreases and facing diverse external threats, and thus, most of these species are under protection and/or need further conservation. According to IUCN’s documentation [24], a few recommended umbrella species currently lack direct and formal (or widely recognized and recorded) conservation actions (Table S2). Moreover, only a few umbrella species have been downlisted since their first recommendations due to successful conservation, and some have even been uplisted. Such disparities between scientific research and actual conservation practices using umbrella-species strategies are concerning, as an umbrella species can only open its conservation umbrella to shelter co-occurring species if it has been protected.
A good understanding of natural history and ecological information are predictors of how well an umbrella species can represent and confer conservation benefits to ecosystems and co-occurring species [45]. However, we found that basic and important information, such as geographic distribution, population trends, and habitat, are not available for several existing umbrella species. Moreover, IUCN assessments for several recommended umbrella species have not been updated in a long time. The most recent IUCN assessments for 13 umbrella species were published ten years ago, and worse, the little-known and/or less-concerned species, such as the European pond turtle (Emys orbicularis) and gopher tortoise (Gopherus polyphemus), have not been evaluated since 1996 (Table S2). This lack of up-to-date knowledge largely impedes the conservation practices targeting these species, such as the designation of protected areas, habitat protection, and population management, and could eventually reduce the usefulness and effectiveness of these little-known species as conservation umbrellas. Therefore, timely updates of IUCN assessments on those less-concerned species and taxa are warranted to fill knowledge gaps and address the lag in critical information.
We found that the 213 recommended umbrella species generally had large ranges. This is unsurprising, given that many umbrella species are chosen for their wide distributions, which encompass those of many co-occurring species [6,18]. However, wide-scale protection calls for vast resource investment [46] and international collaboration for conserving umbrellas throughout their extensive ranges; these are unrealistic requirements in most circumstances [43]. Alternatively, Ward, Rhodes, Watson, Lefevre, Atkinson, and Possingham [22] found that choosing a mix of traditional wide-ranging umbrella species and species with narrower ranges provided an increase in management efficiency within a set budget. In addition, given that the umbrella effect of a species may vary across spatial scales and sites, especially for migratory species that have distinct breeding and wintering ranges, a species with a satisfied umbrella effect in tested regions does not always perform well across its whole range [38]. Therefore, to maximize conservation outcomes while minimizing investment, a trade-off between wide- and narrow-range species should be taken into consideration when deciding which umbrellas are used for conservation schemes. Moreover, a rigorous assessment of potential umbrella effects is necessary prior to conservation practices in a new site.
Umbrella species appear to be most successful when they have similar threats with co-occurring beneficiaries, and thus, conservation actions targeting umbrellas could mitigate those shared threats [22,47]. However, we found that non-threatened species under the LC category dominated the recommended umbrellas of vertebrates. LC species may be more advantageous as umbrellas because they have relatively large populations that occur continuously (or nearly continuously) over their ranges [48], potentially enhancing active monitoring and management, especially when only one species is chosen as an umbrella [18]. However, species in this category are generally facing fewer threats. A large proportion of LC species that were recommended as umbrellas were neither threatened by any factor nor used by humans for any purpose. These species could probably not represent common threats of sympatric species very well, and their efficacy as umbrellas might be limited. Therefore, particular concerns about a species’ representativeness for the common threats to ecosystems or communities, besides their overlaps with regional biodiversity [49], should be raised when non-threatened species are selected and used as conservation umbrellas.

5. Conclusions

As an attainable strategy for maximizing conservation outcomes, the umbrella-species strategy has been studied for about 40 years, and 213 terrestrial vertebrate species have been recommended as umbrella species from 242 scientific articles published since the concept’s inception. We found a considerable geographic bias in global study efforts toward the Northern Hemisphere and also a remarkable taxonomic bias (toward birds and mammals) in the selection of umbrella species. In addition, wide-ranging and non-threatened species were preferred as umbrella species. Based on these revealed biases and trends, we have made some recommendations for the better application of umbrella-species strategies in the future. First, when conservation resources and funding are limited, policymakers in developing countries, especially those in the Southern Hemisphere, should not overlook umbrella species as viable strategies for maximizing conservation outcomes. Second, it is important to rigorously evaluate the effectiveness of different umbrella species with varying ranges and threats prior to conservation practices in a new site, and researchers should especially investigate the potential and appropriateness of amphibians and reptiles as umbrella species. Finally, the inadequate and/or outdated information and conservation statuses of umbrella species could impede their successful applications; therefore, IUCN specialists should update species assessments in a timely manner to fill our knowledge gaps and facilitate related conservation practices.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/biology12040509/s1, Table S1: A full list of the 242 scientific articles with umbrella species as study species published since 1984 to 2021, and the terrestrial vertebrate species they recommended as umbrella species [8,9,10,12,13,17,19,22,35,36,37,44,47,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185,186,187,188,189,190,191,192,193,194,195,196,197,198,199,200,201,202,203,204,205,206,207,208,209,210,211,212,213,214,215,216,217,218,219,220,221,222,223,224,225,226,227,228,229,230,231,232,233,234,235,236,237,238,239,240,241,242,243,244,245,246,247,248,249,250,251,252,253,254,255,256,257,258,259,260,261,262,263,264,265,266,267,268,269,270,271,272,273,274,275,276,277]; Table S2: Detailed biological features and conservation status of the 213 recommended umbrella species of terrestrial vertebrates.

Author Contributions

Conceptualization, X.Z.; methodology, N.Y.; formal analysis, N.Y.; investigation, Y.X., Y.Z., B.W. and Y.C.; writing—original draft preparation, N.Y. and B.W.; writing—review and editing, M.P. and Y.X.; visualization, N.Y.; project administration, X.Z.; funding acquisition, N.Y., Y.X., B.W. and X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province, grant number U1812401, the National Natural Science Foundation of China, grant number 32000354, the Natural Science Foundation of Sichuan Province, grant number 2022NSFSC0123, 2022NSFSC0130, 2022NSFSC1726.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in supplementary Tables S1 and S2.

Acknowledgments

We thank the International Union for Conservation of Nature for the species spatial data used in this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ceballos, G.; Ehrlich, P.R.; Dirzo, R. Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc. Natl. Acad. Sci. USA 2017, 114, E6089–E6096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Waldron, A.; Miller, D.C.; Redding, D.; Mooers, A.; Kuhn, T.S.; Nibbelink, N.; Roberts, J.T.; Tobias, J.A.; Gittleman, J.L. Reductions in global biodiversity loss predicted from conservation spending. Nature 2017, 551, 364–367. [Google Scholar] [CrossRef] [PubMed]
  3. Zhang, C.; Zhu, R.; Sui, X.; Chen, K.; Li, B.; Chen, Y. Ecological use of vertebrate surrogate species in ecosystem conservation. Glob. Ecol. Conserv. 2020, 24, e01344. [Google Scholar] [CrossRef]
  4. Rodrigues, A.S.; Brooks, T.M. Shortcuts for biodiversity conservation planning: The effectiveness of surrogates. Annu. Rev. Ecol. Evol. Syst. 2007, 38, 713–737. [Google Scholar] [CrossRef]
  5. Simberloff, D. Flagships, umbrellas, and keystones: Is single-species management passe in the landscape era? Biol. Conserv. 1998, 83, 247–257. [Google Scholar] [CrossRef]
  6. Roberge, J.M.; Angelstam, P. Usefulness of the umbrella species concept as a conservation tool. Conserv. Biol. 2004, 18, 76–85. [Google Scholar] [CrossRef]
  7. Minor, E.S.; Lookingbill, T.R. A multiscale network analysis of protected-area connectivity for mammals in the United States. Conserv. Biol. 2010, 24, 1549–1558. [Google Scholar] [CrossRef]
  8. Barua, M. Mobilizing metaphors: The popular use of keystone, flagship and umbrella species concepts. Biodivers. Conserv. 2011, 20, 1427–1440. [Google Scholar] [CrossRef]
  9. Wei, F.; Costanza, R.; Dai, Q.; Stoeckl, N.; Gu, X.; Farber, S.; Nie, Y.; Kubiszewski, I.; Hu, Y.; Swaisgood, R.; et al. The value of ecosystem services from giant panda reserves. Curr. Biol. 2018, 28, 2174–2180.e2177. [Google Scholar] [CrossRef] [Green Version]
  10. Li, B.; Pimm, S.L. China’s endemic vertebrates sheltering under the protective umbrella of the Giant Panda. Conserv. Biol. 2016, 30, 329–339. [Google Scholar] [CrossRef]
  11. Xu, W.; Viña, A.; Qi, Z.; Ouyang, Z.; Liu, J.; Liu, W.; Wan, H. Evaluating conservation effectiveness of nature reserves established for surrogate species: Case of a giant panda nature reserve in Qinling Mountains, China. Chin. Geogr. Sci. 2014, 24, 60–70. [Google Scholar] [CrossRef] [Green Version]
  12. Hawkes, R.W.; Smart, J.; Brown, A.; Jones, H.; Lane, S.; Wells, D.; Dolman, P.M. Multi-taxa consequences of management for an avian umbrella species. Biol. Conserv. 2019, 236, 192–201. [Google Scholar] [CrossRef]
  13. Suter, W.; Graf, R.F.; Hess, R. Capercaillie (Tetrao urogallus) and avian biodiversity: Testing the umbrella-species concept. Conserv. Biol. 2002, 16, 778–788. [Google Scholar] [CrossRef]
  14. Caro, T.M. Umbrella species: Critique and lessons from East Africa. Anim. Conserv. 2003, 6, 171–181. [Google Scholar] [CrossRef]
  15. Wilcox, B.A. In situ conservation of genetic resources: Determinants of minimum area requirements. In National Parks, Conservation, and Development: The Role of Protected Areas in Sustaining Society; McNeely, J.A., Miller, K.R., Eds.; Smithsonian Institution Press: Washington, DC, USA, 1984. [Google Scholar]
  16. Carrascal, L.M.; Cayuela, L.; Palomino, D.; Seoane, J. What species-specific traits make a bird a better surrogate of native species richness? A test with insular avifauna. Biol. Conserv. 2012, 152, 204–211. [Google Scholar] [CrossRef] [Green Version]
  17. Ozaki, K.; Isono, M.; Kawahara, T.; Iida, S.; Kudo, T.; Fukuyama, K. A mechanistic approach to evaluation of umbrella species as conservation surrogates. Conserv. Biol. 2006, 20, 1507–1515. [Google Scholar] [CrossRef] [PubMed]
  18. Caro, T.M.; O’Doherty, G. On the use of surrogate species in conservation biology. Conserv. Biol. 1999, 13, 805–814. [Google Scholar] [CrossRef]
  19. Stuber, E.F.; Fontaine, J.J. Ecological neighborhoods as a framework for umbrella species selection. Biol. Conserv. 2018, 223, 112–119. [Google Scholar] [CrossRef] [Green Version]
  20. Sattler, T.; Pezzatti, G.B.; Nobis, M.P.; Obrist, M.K.; Roth, T.; Moretti, M. Selection of multiple umbrella species for functional and taxonomic diversity to represent urban biodiversity. Conserv. Biol. 2014, 28, 414–426. [Google Scholar] [CrossRef]
  21. Moran-Lopez, R.; Ganan, E.C.; Tolosa, O.U.; Guzman, J.M.S. The umbrella effect of Natura 2000 annex species spreads over multiple taxonomic groups, conservation attributes and organizational levels. Anim. Conserv. 2020, 23, 407–419. [Google Scholar] [CrossRef]
  22. Ward, M.; Rhodes, J.R.; Watson, J.E.M.; Lefevre, J.; Atkinson, S.; Possingham, H.P. Use of surrogate species to cost-effectively prioritize conservation actions. Conserv. Biol. 2020, 34, 600–610. [Google Scholar] [CrossRef]
  23. Alroy, J. Current extinction rates of reptiles and amphibians. Proc. Natl. Acad. Sci. USA 2015, 112, 13003–13008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. IUCN The IUCN Red List of Threatened Species. Version 2022-2. 2022. Available online: https://www.iucnredlist.org (accessed on 25 February 2023).
  25. IUCN SSC Red List Technical Working Group. Mapping Standards and Data Quality for the IUCN Red List Spatial Data. Version 1.19. 2021. Available online: https://www.iucnredlist.org/resources/mappingstandards (accessed on 25 February 2023).
  26. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria 2022. Available online: https://www.R-project.org/ (accessed on 1 March 2023).
  27. Corlett, R.T.; Primack, R.B.; Devictor, V.; Maas, B.; Goswami, V.R.; Bates, A.E.; Koh, L.P.; Regan, T.J.; Loyola, R.; Pakeman, R.J.; et al. Impacts of the coronavirus pandemic on biodiversity conservation. Biol. Conserv. 2020, 246, 108571. [Google Scholar] [CrossRef] [PubMed]
  28. Lindsey, P.; Allan, J.; Brehony, P.; Dickman, A.; Robson, A.; Begg, C.; Bhammar, H.; Blanken, L.; Breuer, T.; Fitzgerald, K.; et al. Conserving Africa’s wildlife and wildlands through the COVID-19 crisis and beyond. Nat. Ecol. Evol. 2020, 4, 1300–1310. [Google Scholar] [CrossRef] [PubMed]
  29. Burgin, C.J.; Colella, J.P.; Kahn, P.L.; Upham, N.S. How many species of mammals are there? J. Mammal. 2018, 99, 1–14. [Google Scholar] [CrossRef] [Green Version]
  30. BirdLife International. BirdLife’s World Bird Database: Birds are Found Almost Everywhere in the World, from the Poles to the Equator. 2013. Available online: http://datazone.birdlife.org (accessed on 30 June 2022).
  31. Di Marco, M.; Chapman, S.; Althor, G.; Kearney, S.; Besancon, C.; Butt, N.; Maina, J.M.; Possingham, H.P.; Rogalla von Bieberstein, K.; Venter, O.; et al. Changing trends and persisting biases in three decades of conservation science. Glob. Ecol. Conserv. 2017, 10, 32–42. [Google Scholar] [CrossRef]
  32. Martin, L.J.; Blossey, B.; Ellis, E. Mapping where ecologists work: Biases in the global distribution of terrestrial ecological observations. Front. Ecol. Environ. 2012, 10, 195–201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Mittermeier, R.A.; Gil, P.R.; Hoffmann, M.; Pilgrim, J.; Brooks, T.; Mittermeier, C.G.; Lamoreux, J.; Da Fonseca, G.A.B. Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions; CEMEX: Mexico City, Mexico, 2004. [Google Scholar]
  34. Branton, M.; Richardson, J.S. Assessing the value of the umbrella-species concept for conservation planning with meta-analysis. Conserv. Biol. 2011, 25, 9–20. [Google Scholar] [CrossRef]
  35. Bani, L.; Massimino, D.; Bottoni, L.; Massa, R. A multiscale method for selecting indicator species and priority conservation areas: A case study for broadleaved forests in Lombardy, Italy. Conserv. Biol. 2006, 20, 512–526. [Google Scholar] [CrossRef]
  36. Breckheimer, I.; Haddad, N.M.; Morris, W.F.; Trainor, A.M.; Fields, W.R.; Jobe, R.T.; Hudgens, B.R.; Moody, A.; Walters, J.R. Defining and evaluating the umbrella species concept for conserving and restoring landscape connectivity. Conserv. Biol. 2014, 28, 1584–1593. [Google Scholar] [CrossRef]
  37. Maslo, B.; Leu, K.; Faillace, C.; Weston, M.A.; Pover, T.; Schlacher, T.A. Selecting umbrella species for conservation: A test of habitat models and niche overlap for beach-nesting birds. Biol. Conserv. 2016, 203, 233–242. [Google Scholar] [CrossRef]
  38. Seddon, P.J.; Leech, T. Conservation short cut, or long and winding road? A critique of umbrella species criteria. Oryx 2008, 42, 240–245. [Google Scholar] [CrossRef] [Green Version]
  39. Nori, J.; Villalobos, F.; Loyola, R. Global priority areas for amphibian research. J. Biogeogr. 2018, 45, 2588–2594. [Google Scholar] [CrossRef]
  40. Roll, U.; Feldman, A.; Novosolov, M.; Allison, A.; Bauer, A.M.; Bernard, R.; Böhm, M.; Castro-Herrera, F.; Chirio, L.; Collen, B. The global distribution of tetrapods reveals a need for targeted reptile conservation. Nat. Ecol. Evol. 2017, 1, 1677–1682. [Google Scholar] [CrossRef] [PubMed]
  41. Smith, R.J.; Verissimo, D.; Isaac, N.J.B.; Jones, K.E. Identifying Cinderella species: Uncovering mammals with conservation flagship appeal. Conserv. Lett. 2012, 5, 205–212. [Google Scholar] [CrossRef] [Green Version]
  42. Prokop, P.; Randler, C. Biological Predispositions and Individual Differences in Human Attitudes Toward Animals. In Ethnozoology; Alves, R.R.N., Albuquerque, U.P., Eds.; Academic Press: London, UK, 2018; pp. 447–466. [Google Scholar]
  43. Fleishman, E.; Blair, R.B.; Murphy, D.D. Empirical validation of a method for umbrella species selection. Ecol. Appl. 2001, 11, 1489–1501. [Google Scholar] [CrossRef]
  44. Denoël, M.; Perez, A.; Cornet, Y.; Ficetola, G.F. Similar local and landscape processes affect both a common and a rare newt species. PLoS ONE 2013, 8, e62727. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Andelman, S.J.; Fagan, W.F. Umbrellas and flagships: Efficient conservation surrogates or expensive mistakes? Proc. Natl. Acad. Sci. USA 2000, 97, 5954–5959. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Balmford, A.; Gaston, K.J.; Blyth, S.; James, A.; Kapos, V. Global variation in terrestrial conservation costs, conservation benefits, and unmet conservation needs. Proc. Natl. Acad. Sci. USA 2003, 100, 1046–1050. [Google Scholar] [CrossRef] [Green Version]
  47. Nekaris, K.A.I.; Arnell, A.P.; Svensson, M.S. Selecting a Conservation Surrogate Species for Small Fragmented Habitats Using Ecological Niche Modelling. Animals 2015, 5, 27–40. [Google Scholar] [CrossRef] [Green Version]
  48. IUCN. IUCN Red List Categories and Criteria: Version 3.1, 2nd ed.; IUCN: Gland, Switzerland; Cambridge, UK, 2012. [Google Scholar]
  49. Shi, X.W.; Gong, C.; Zhang, L.; Hu, J.; Ouyang, Z.Y.; Xiao, Y. Which species should we focus on? Umbrella species assessment in Southwest China. Biology 2019, 8, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Agha, M.; Lovich, J.E.; Ennen, J.R.; Todd, B.D. Wind, sun, and wildlife: Do wind and solar energy development ‘short-circuit’ conservation in the western United States? Environ. Res. Lett. 2020, 15, 075004. [Google Scholar] [CrossRef]
  51. Albert, C.; Luque, G.M.; Courchamp, F. The twenty most charismatic species. PLoS ONE 2018, 13, e0199149. [Google Scholar] [CrossRef] [Green Version]
  52. Alexander, J.S.; Cusack, J.J.; Pengju, C.; Kun, S.; Riordan, P. Conservation of snow leopards: Spill-over benefits for other carnivores? Oryx 2016, 50, 239–243. [Google Scholar] [CrossRef] [Green Version]
  53. Allen, M.L.; Sibarani, M.C.; Utoyo, L.; Krofel, M. Terrestrial mammalia community richness and temporal overlap between tigers and other carnivores in Bukit Barisan Selatan National Park, Sumatra. Anim. Biodivers. Conserv. 2020, 43, 97–107. [Google Scholar] [CrossRef] [Green Version]
  54. Alves, M.; Ferreira, J.P.; Torres, I.; Fonseca, C.; Matos, M. Habitat use and selection of the marsh harrier Circus aeruginosus in an agricultural-wetland mosaic. Ardeola-Int. J. Ornithol. 2014, 61, 351–366. [Google Scholar] [CrossRef]
  55. Andesner, P.; Vallant, S.; Seeber, T.; Lentner, R.; Arthofer, W.; Steiner, F.M.; Schlick-Steiner, B.C. A reference allelic ladder for Western Capercaillie (Tetrao urogallus) and Black Grouse (Tetrao tetrix) enables linking grouse genetic data across studies. Conserv. Genet. Resour. 2021, 13, 97–105. [Google Scholar] [CrossRef]
  56. Ashrafzadeh, M.R.; Khosravi, R.; Adibi, M.A.; Taktehrani, A.; Wan, H.Y.; Cushman, S.A. A multi-scale, multi-species approach for assessing effectiveness of habitat and connectivity conservation for endangered felids. Biol. Conserv. 2020, 245, 108523. [Google Scholar] [CrossRef]
  57. Banas, J.; Zieba, S.; Bujoczek, M.; Bujoczek, L. The Impact of Different Management Scenarios on the Availability of Potential Forest Habitats for Wildlife on a Landscape Level: The Case of the Black Stork Ciconia nigra (Linnaeus, 1758). Forests 2019, 10, 362. [Google Scholar] [CrossRef] [Green Version]
  58. Bar-David, S.; Saltz, D.; Dayan, T.; Shkedy, Y. Using spatially expanding populations as a tool for evaluating landscape planning: The reintroduced Persian fallow deer as a case study. J. Nat. Conserv. 2008, 16, 164–174. [Google Scholar] [CrossRef]
  59. Barichievy, C.; Altwegg, R.; Balfour, D.; Brett, R.; Gordon, C.; Henry, D.A.W.; Jeffries, G.; Khayale, C.; Wanyama, H.; Withers, O. A demographic model to support an impact financing mechanism for black rhino metapopulations. Biol. Conserv. 2021, 257, 109073. [Google Scholar] [CrossRef]
  60. Barlow, N.L.; Kirol, C.P.; Doherty, K.E.; Fedy, B.C. Evaluation of the Umbrella Species Concept at Fine Spatial Scales. J. Wildl. Manag. 2020, 84, 237–248. [Google Scholar] [CrossRef]
  61. Beazley, K.; Cardinal, N. A systematic approach for selecting focal species for conservation in the forests of Nova Scotia and Maine. Environ. Conserv. 2004, 31, 91–101. [Google Scholar] [CrossRef]
  62. Beier, P.; Majka, D.R.; Newell, S.L. Uncertainty analysis of least-cost modeling for designing wildlife linkages. Ecol. Appl. 2009, 19, 2067–2077. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Bell, D.; Hjalten, J.; Nilsson, C.; Jorgensen, D.; Johansson, T. Forest restoration to attract a putative umbrella species, the white-backed woodpecker, benefited saproxylic beetles. Ecosphere 2015, 6, 1–14. [Google Scholar] [CrossRef]
  64. Beranek, C.T.; Xu, G.; Clulow, J.; Mahony, M. Preliminary evidence for a two-for-one deal: Wetland restoration for a threatened frog may benefit a threatened bat. Ecol. Manag. Restor. 2021, 22, 32–39. [Google Scholar] [CrossRef]
  65. Berger, J. Population constraints associated with the use of black rhinos as an umbrella species for desert herbivores. Conserv. Biol. 1997, 11, 69–78. [Google Scholar] [CrossRef] [Green Version]
  66. Bergner, A.; Sunnergren, A.; Yesilbudak, B.; Erdem, C.; Jansson, N. Attributes of trees used by nesting and foraging woodpeckers (Aves: Picidae) in an area with old pollarded Oaks (Quercus spp.) in the Taurus Mountains, Turkey. Zool. Middle East 2016, 62, 288–298. [Google Scholar] [CrossRef]
  67. Bichet, O.; Dupuch, A.; Hebert, C.; Le Borgne, H.; Fortin, D. Maintaining animal assemblages through single-species management: The case of threatened caribou in boreal forest. Ecol. Appl. 2016, 26, 612–623. [Google Scholar] [CrossRef]
  68. Bifolchi, A.; Lode, T. Efficiency of conservation shortcuts: An investigation with otters as umbrella species. Biol. Conserv. 2005, 126, 523–527. [Google Scholar] [CrossRef]
  69. Blanco-Fontao, B.; Quevedo, M.; Obeso, J.R. Abandonment of traditional uses in mountain areas: Typological thinking versus hard data in the Cantabrian Mountains (NW Spain). Biodivers. Conserv. 2011, 20, 1133–1140. [Google Scholar] [CrossRef]
  70. Blicharska, M.; Baxter, P.W.J.; Mikusinski, G. Practical implementation of species’ recovery plans-lessons from the White-backed Woodpecker Action Plan in Sweden. Ornis Fenn. 2014, 91, 108–128. [Google Scholar]
  71. Booms, T.L.; Holroyd, G.L.; Gahbauer, M.A.; Trefry, H.E.; Wiggins, D.A.; Holt, D.W.; Johnson, J.A.; Lewis, S.B.; Larson, M.D.; Keyes, K.L.; et al. Assessing the status and conservation priorities of the short-eared owl in North America. J. Wildl. Manag. 2014, 78, 772–778. [Google Scholar] [CrossRef]
  72. Borghesio, L.; Ndang’ang’a, P.K. Habitat selection and the conservation status of Fischer’s turaco Tauraco fischeri on Unguja, Tanzania. Oryx 2003, 37, 444–453. [Google Scholar] [CrossRef] [Green Version]
  73. Bradsworth, N.; White, J.G.; Isaac, B.; Cooke, R. Species distribution models derived from citizen science data predict the fine scale movements of owls in an urbanizing landscape. Biol. Conserv. 2017, 213, 27–35. [Google Scholar] [CrossRef]
  74. Brambilla, M.; Bassi, E.; Bergero, V.; Casale, F.; Chemollo, M.; Falco, R.; Longoni, V.; Saporetti, F.; Vigano, E.; Vitulano, S. Modelling distribution and potential overlap between Boreal Owl Aegolius funereus and Black Woodpecker Dryocopus martius: Implications for management and monitoring plans. Bird Conserv. Int. 2013, 23, 502–511. [Google Scholar] [CrossRef] [Green Version]
  75. Brennan, A.; Beytell, P.; Aschenborn, O.; Du Preez, P.; Funston, P.J.; Hanssen, L.; Kilian, J.W.; Stuart-Hill, G.; Taylor, R.D.; Naidoo, R. Characterizing multispecies connectivity across a transfrontier conservation landscape. J. Appl. Ecol. 2020, 57, 1700–1710. [Google Scholar] [CrossRef]
  76. Brenner, S.J.; McWilliams, S.R. Independence day: Post-fledging movements and behavior of adult Eastern Towhees (Pipilo erythrophthalmus) in landscapes managed for American Woodcock (Scolopax minor). Wilson J. Ornithol. 2019, 131, 796–806. [Google Scholar] [CrossRef] [Green Version]
  77. Buffum, B.; Masse, R.; McWilliams, S.R. Novel Use of Species Distribution Modeling to Identify High Priority Sites for American Woodcock Habitat Management. Northeast. Nat. 2021, 28, 233–247. [Google Scholar] [CrossRef]
  78. Burgas, D.; Juutinen, A.; Byholm, P. The cost-effectiveness of using raptor nest sites to identify areas with high species richness of other taxa. Ecol. Indic. 2016, 70, 518–530. [Google Scholar] [CrossRef]
  79. Burivalova, Z.; Game, E.T.; Wahyudi, B.; Ruslandi Rifqi, M.; MacDonald, E.; Cushman, S.; Voigt, M.; Wich, S.; Wilcove, D.S. Does biodiversity benefit when the logging stops? An analysis of conservation risks and opportunities in active versus inactive logging concessions in Borneo. Biol. Conserv. 2020, 241, 108369. [Google Scholar] [CrossRef]
  80. Burnett, R.D.; Roberts, L.J. A Quantitative Evaluation of the Conservation Umbrella of Spotted Owl Management Areas in the Sierra Nevada. PLoS ONE 2015, 10, e0123778. [Google Scholar] [CrossRef]
  81. Burnham, D.; Hinks, A.E.; Macdonald, D.W. Life and Dinner under the Shared Umbrella: Patterns in Felid and Primate Communities. Folia Primatol. 2012, 83, 148–170. [Google Scholar] [CrossRef] [PubMed]
  82. Cadi, A.; Nemoz, M.; Thienpont, S.; Joly, P. Home range, movements, and habitat use of the European pond turtle (Emys orbicularis) in the Rhone-Alpes region, France. Biologia 2004, 59, 89–94. [Google Scholar]
  83. Carlisle, J.D.; Chalfoun, A.D.; Smith, K.T.; Beck, J.L. Nontarget effects on songbirds from habitat manipulation for Greater Sage-Grouse: Implications for the umbrella species concept. Condor 2018, 120, 439–455. [Google Scholar] [CrossRef] [Green Version]
  84. Carlisle, J.D.; Chalfoun, A.D. The abundance of Greater Sage-Grouse as a proxy for the abundance of sagebrush-associated songbirds in Wyoming, USA. Avian Conserv. Ecol. 2020, 15, 16. [Google Scholar] [CrossRef]
  85. Carlisle, J.D.; Keinath, D.A.; Albeke, S.E.; Chalfoun, A.D. Identifying Holes in the Greater Sage-Grouse Conservation Umbrella. J. Wildl. Manag. 2018, 82, 948–957. [Google Scholar] [CrossRef]
  86. Carlisle, J.D.; Stewart, D.R.; Chalfoun, A.D. An invertebrate ecosystem engineer under the umbrella of sage-grouse conservation. West. N. Am. Nat. 2017, 77, 450–463. [Google Scholar] [CrossRef]
  87. Carroll, C.; Dunk, J.R.; Moilanen, A. Optimizing resiliency of reserve networks to climate change: Multispecies conservation planning in the Pacific Northwest, USA. Glob. Chang. Biol. 2010, 16, 891–904. [Google Scholar] [CrossRef] [Green Version]
  88. Carroll, C.; Noss, R.F.; Paquet, P.C. Carnivores as focal species for conservation planning in the Rocky Mountain region. Ecol. Appl. 2001, 11, 961–980. [Google Scholar] [CrossRef]
  89. Carter, N.; Killion, A.; Easter, T.; Brand, J.; Ford, A. Road development in Asia: Assessing the range-wide risks to tigers. Sci. Adv. 2020, 6, 1–9. [Google Scholar] [CrossRef] [PubMed]
  90. Carvalho, J.S.; Meyer, C.F.J.; Vicente, L.; Marques, T.A. Where to Nest? Ecological Determinants of Chimpanzee Nest Abundance and Distribution at the Habitat and Tree Species Scale. Am. J. Primatol. 2015, 77, 186–199. [Google Scholar] [CrossRef] [PubMed]
  91. Castellon, T.D.; Sieving, K.E. Patch network criteria for dispersal-limited endemic birds of South American temperate rain forest. Ecol. Appl. 2007, 17, 2152–2163. [Google Scholar] [CrossRef]
  92. Chacon-Chaverri, D.; Martinez-Cascante, D.A.; Rojas, D.; Fonseca, L.G. Catch per unit effort and population structure of the Pacific green turtle (Chelonia mydas) in the Golfo Dulce, Costa Rica. Rev. Biol. Trop. 2015, 63, 363–373. [Google Scholar] [CrossRef]
  93. Chouteau, P. The impacts of logging on the microhabitats used by two species of couas in the western forest of Madagascar. Comptes Rendus Biol. 2004, 327, 1157–1170. [Google Scholar] [CrossRef]
  94. Ciudad, C.; Robles, H.; Matthysen, E. Postfledging habitat selection of juvenile middle spotted woodpeckers: A multi-scale approach. Ecography 2009, 32, 676–682. [Google Scholar] [CrossRef]
  95. Coates, P.S.; Casazza, M.L.; Ricca, M.A.; Brussee, B.E.; Blomberg, E.J.; Gustafson, K.B.; Overton, C.T.; Davis, D.M.; Niell, L.E.; Espinosa, S.P.; et al. Integrating spatially explicit indices of abundance and habitat quality: An applied example for greater sage-grouse management. J. Appl. Ecol. 2016, 53, 83–95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Collins, K.; du Toit, J.T. Population status and distribution modelling of the critically endangered riverine rabbit (Bunolagus monticularis). Afr. J. Ecol. 2016, 54, 195–206. [Google Scholar] [CrossRef] [Green Version]
  97. Comiskey, E.J.; Eller, A.C.; Perkins, D.W. Evaluating impacts to Florida panther habitat: How porous is the umbrella? Southeast. Nat. 2004, 3, 51–74. [Google Scholar] [CrossRef]
  98. Copeland, H.E.; Sawyer, H.; Monteith, K.L.; Naugle, D.E.; Pocewicz, A.; Graf, N.; Kauffman, M.J. Conserving migratory mule deer through the umbrella of sage-grouse. Ecosphere 2014, 5, 1–16. [Google Scholar] [CrossRef] [Green Version]
  99. Crespo-Gascon, S.; Guerrero-Casado, J. The role of the spectacled bear (Tremarctos ornatus) as an umbrella species for Andean ecoregions. Wildl. Res. 2019, 46, 176–183. [Google Scholar] [CrossRef]
  100. Cristescu, B.; Stenhouse, G.B.; Boyce, M.S. Grizzly bear diet shifting on reclaimed mines. Glob. Ecol. Conserv. 2015, 4, 207–220. [Google Scholar] [CrossRef] [Green Version]
  101. Crosby, A.D.; Elmore, R.D.; Leslie, D.M.; Will, R.E. Looking beyond rare species as umbrella species: Northern Bobwhites (Colinus virginianus) and conservation of grassland and shrubland birds. Biol. Conserv. 2015, 186, 233–240. [Google Scholar] [CrossRef]
  102. Cuadros-Casanova, I.; Zamora, C.; Ulrich, W.; Seibold, S.; Habel, J.C. Empty forests: Safeguarding a sinking flagship in a biodiversity hotspot. Biodivers. Conserv. 2018, 27, 2495–2506. [Google Scholar] [CrossRef]
  103. Curveira-Santos, G.; Sutherland, C.; Tenan, S.; Fernandez-Chacon, A.; Mann, G.K.H.; Pitman, R.T.; Swanepoel, L.H. Mesocarnivore community structuring in the presence of Africa’s apex predator. Proc. R. Soc. B-Biol. Sci. 2021, 288, 20202379. [Google Scholar] [CrossRef] [PubMed]
  104. Cushman, S.A.; Landguth, E.L. Multi-taxa population connectivity in the Northern Rocky Mountains. Ecol. Model. 2012, 231, 101–112. [Google Scholar] [CrossRef]
  105. Dahlgren, D.K.; Guttery, M.R.; Messmer, T.A.; Caudill, D.; Elmore, R.D.; Chi, R.; Koons, D.N. Evaluating vital rate contributions to greater sage-grouse population dynamics to inform conservation. Ecosphere 2016, 7, e01249. [Google Scholar] [CrossRef] [Green Version]
  106. Dahlgren, D.K.; Messmer, T.A.; Crabb, B.A.; Larsen, R.T.; Black, T.A.; Frey, S.N.; Thacker, E.T.; Baxter, R.J.; Robinson, J.D. Seasonal Movements of Greater Sage-grouse Populations in Utah: Implications for Species Conservation. Wildl. Soc. Bull. 2016, 40, 288–299. [Google Scholar] [CrossRef]
  107. Dai, Y.C.A.; Peng, G.C.A.; Wen, C.A.H.; Zahoor, B.; Ma, X.D.; Hacker, C.E.; Xue, Y.D. Climate and land use changes shift the distribution and dispersal of two umbrella species in the Hindu Kush Himalayan region. Sci. Total Environ. 2021, 777, 146207. [Google Scholar] [CrossRef]
  108. Dalerum, F.; Somers, M.J.; Kunkel, K.E.; Cameron, E.Z. The potential for large carnivores to act as biodiversity surrogates in southern Africa. Biodivers. Conserv. 2008, 17, 2939–2949. [Google Scholar] [CrossRef]
  109. Davis, M.L.; Kelly, M.J.; Stauffer, D.F. Carnivore co-existence and habitat use in the Mountain Pine Ridge Forest Reserve, Belize. Anim. Conserv. 2011, 14, 56–65. [Google Scholar] [CrossRef]
  110. De Vries, M.F.W. Large herbivores and the design of large-scale nature-reserves in western-europe. Conserv. Biol. 1995, 9, 25–33. [Google Scholar] [CrossRef]
  111. Dickman, A.J.; Hinks, A.E.; Macdonald, E.A.; Burnham, D.; Macdonald, D.W. Priorities for global felid conservation. Conserv. Biol. 2015, 29, 854–864. [Google Scholar] [CrossRef] [PubMed]
  112. Dinerstein, E.; Varma, K.; Wikramanayake, E.; Powell, G.; Lumpkin, S.; Naidoo, R.; Korchinsky, M.; Del Valle, C.; Lohani, S.; Seidensticker, J.; et al. Enhancing Conservation, Ecosystem Services, and Local Livelihoods through a Wildlife Premium Mechanism. Conserv. Biol. 2013, 27, 14–23. [Google Scholar] [CrossRef]
  113. Diniz, M.F.; Machado, R.B.; Bispo, A.A.; Brito, D. Identifying key sites for connecting jaguar populations in the Brazilian Atlantic Forest. Anim. Conserv. 2018, 21, 201–210. [Google Scholar] [CrossRef]
  114. Dinkins, J.B.; Beck, J.L. Comparison of conservation policy benefits for an umbrella and related sagebrush-obligate species. Hum.-Wildl. Interact. 2019, 13, 447–458. [Google Scholar]
  115. Drake, E.C.; Gignoux-Wolfsohn, S.; Maslo, B. Systematic Review of the Roost-Site Characteristics of North American Forest Bats: Implications for Conservation. Diversity 2020, 12, 76. [Google Scholar] [CrossRef] [Green Version]
  116. Drever, C.R.; Hutchison, C.; Drever, M.C.; Fortin, D.; Johnson, C.A.; Wiersma, Y.F. Conservation through co-occurrence: Woodland caribou as a focal species for boreal biodiversity. Biol. Conserv. 2019, 232, 238–252. [Google Scholar] [CrossRef]
  117. Dunk, J.R.; Zielinski, W.J.; Welsh, H.H. Evaluating reserves for species richness and representation in northern California. Divers. Distrib. 2006, 12, 434–442. [Google Scholar] [CrossRef]
  118. Duvall, A.L.; Metcalf, A.L.; Coates, P.S. Conserving the Greater Sage-Grouse: A Social-Ecological Systems Case Study from the California-Nevada Region. Rangel. Ecol. Manag. 2017, 70, 129–140. [Google Scholar] [CrossRef] [Green Version]
  119. Ebenhoch, K.; Thornton, D.; Shipley, L.; Manning, J.A.; White, K. Effects of post-release movements on survival of translocated sage-grouse. J. Wildl. Manag. 2019, 83, 1314–1325. [Google Scholar] [CrossRef]
  120. Edman, T.; Angelstam, P.; Mikusinski, G.; Roberge, J.M.; Sikora, A. Spatial planning for biodiversity conservation: Assessment of forest landscapes’ conservation value using umbrella species requirements in Poland. Landsc. Urban Plan. 2011, 102, 16–23. [Google Scholar] [CrossRef]
  121. Elliott, L.H.; Johnson, D.H. The grasshopper sparrow as an indicator species in tallgrass prairies. J. Wildl. Manag. 2018, 82, 1074–1081. [Google Scholar] [CrossRef]
  122. Epps, C.W.; Mutayoba, B.M.; Gwin, L.; Brashares, J.S. An empirical evaluation of the African elephant as a focal species for connectivity planning in East Africa. Divers. Distrib. 2011, 17, 603–612. [Google Scholar] [CrossRef]
  123. Favilli, F.; Hoffmann, C.; Elmi, M.; Ravazzoli, E.; Streifeneder, T. The BioREGIO Carpathians project: Aims, methodology and results from the “Continuity and Connectivity” analysis. Nat. Conserv. 2015, 11, 95–111. [Google Scholar] [CrossRef] [Green Version]
  124. Fedy, B.C.; Kirol, C.P.; Sutphin, A.L.; Maechtle, T.L. The Influence of Mitigation on Sage-Grouse Habitat Selection within an Energy Development Field. PLoS ONE 2015, 10, e0121603. [Google Scholar] [CrossRef]
  125. Figel, J.J.; Castaneda, F.; Calderon, A.P.; de la Torre, J.A.; Garcia-Padilla, E.; Noss, R.F. Threatened Amphibias sheltered under the big cat’s umbrella: Conservation of jaguars Panthera onca (Carnivora: Felidae) and endemic herpetofauna in Central America. Rev. Biol. Trop. 2018, 66, 1741–1753. [Google Scholar] [CrossRef] [Green Version]
  126. Forrest, J.L.; Wikramanayake, E.; Shrestha, R.; Areendran, G.; Gyeltshen, K.; Maheshwari, A.; Mazumdar, S.; Naidoo, R.; Thapa, G.J.; Thapa, K. Conservation and climate change: Assessing the vulnerability of snow leopard habitat to treeline shift in the Himalaya. Biol. Conserv. 2012, 150, 129–135. [Google Scholar] [CrossRef]
  127. Fourcade, Y.; Besnard, A.G.; Secondi, J. Evaluating interspecific niche overlaps in environmental and geographic spaces to assess the value of umbrella species. J. Avian Biol. 2017, 48, 1563–1574. [Google Scholar] [CrossRef]
  128. Freire Filho, R.; Palmeirim, J.M. Potential distribution of and priority conservation areas for the Endangered Caatinga howler monkey Alouatta ululata in north-eastern Brazil. Oryx 2020, 54, 794–802. [Google Scholar] [CrossRef]
  129. Gallo-Reynoso, J.P.; Ramos-Rosas, N.N.; Rangel-Aguilar, O. Aquatic bird predation by neotropical river otter (Lontra longicaudis annectens), at Rio Yaqui, Sonora, Mexico. Rev. Mex. Biodivers. 2008, 79, 275–279. [Google Scholar]
  130. Gamo, R.S.; Beck, J.L. Energy Disturbance and Productivity of Mule Deer Habitat in Sage-Grouse Core Areas. Rangel. Ecol. Manag. 2017, 70, 576–583. [Google Scholar] [CrossRef]
  131. Gangadharan, A.; Vaidyanathan, S.; St Clair, C.C. Categorizing species by niche characteristics can clarify conservation planning in rapidly-developing landscapes. Anim. Conserv. 2016, 19, 451–461. [Google Scholar] [CrossRef]
  132. Gerrard, R.; Stine, P.; Church, R.; Gilpin, M. Habitat evaluation using GIS—A case study applied to the San Joaquin Kit Fox. Landsc. Urban Plan. 2001, 52, 239–255. [Google Scholar] [CrossRef]
  133. Gomez-Catasus, J.; Perez-Granados, C.; Barrero, A.; Bota, G.; Giralt, D.; Lopez-Iborra, G.M.; Serrano, D.; Traba, J. European poplation trends and current conservation status of an endangered steppe-bird species: The Dupont’s lark Chersophilus duponti. Peerj 2018, 6, e5627. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  134. Gorfol, T.; Haga, K.; Dombi, I. Roost selection of barbastelle bats (Barbastella barbastellus) in an intensively managed floodplain forest: Implications for conservation. North-West. J. Zool. 2019, 15, 184–186. [Google Scholar]
  135. Gren, I.M.; Baxter, P.; Mikusinski, G.; Possingham, H.P. Cost-effective biodiversity restoration with uncertain growth in forest habitat quality. J. For. Econ. 2014, 20, 77–92. [Google Scholar] [CrossRef]
  136. Grigione, M.M.; Menke, K.; Lopez-Gonzalez, C.; List, R.; Banda, A.; Carrera, J.; Carrera, R.; Giordano, A.J.; Morrison, J.; Sternberg, M.; et al. Identifying potential conservation areas for felids in the USA and Mexico: Integrating reliable knowledge across an international border. Oryx 2009, 43, 78–86. [Google Scholar] [CrossRef] [Green Version]
  137. Hager, H.A.; Gorman, R.M.; Nudds, T.D. The relative performance of umbrella species for biodiversity conservation in island archipelagos of the Great Lakes, North America. Ecoscience 2006, 13, 475–484. [Google Scholar] [CrossRef]
  138. Hamalainen, K.; Junninen, K.; Halme, P.; Kouki, J. Managing conservation values of protected sites: How to maintain deciduous trees in white-backed woodpecker territories. For. Ecol. Manag. 2020, 461, 117946. [Google Scholar] [CrossRef]
  139. Hansbauer, M.M.; Storch, I.; Knauer, F.; Pilz, S.; Kuchenhoff, H.; Vegvari, Z.; Pimentel, R.G.; Metzger, J.P. Landscape perception by forest understory birds in the Atlantic Rainforest: Black-and-white versus shades of grey. Landsc. Ecol. 2010, 25, 407–417. [Google Scholar] [CrossRef]
  140. Hardy, M.A.; Broadway, M.S.; Pollentier, C.D.; Radeloff, V.C.; Riddle, J.D.; Hull, S.D.; Zuckerberg, B. Responses to land cover and grassland management vary across life-history stages for a grassland specialist. Ecol. Evol. 2020, 10, 12777–12791. [Google Scholar] [CrossRef] [PubMed]
  141. Hermes, C.; Segelbacher, G.; Schaefer, H.M. A framework for prioritizing areas for conservation in tropical montane cloud forests. Ecoscience 2018, 25, 97–108. [Google Scholar] [CrossRef]
  142. Herrera-Sanchez, F.J.; Gil-Sanchez, J.M.; Alvarez, B.; Cancio, I.; de Lucas, J.; Arredondo, A.; Diaz-Portero, M.A.; Rodriguez-Siles, J.; Saez, J.M.; Perez, J.; et al. Identifying priority conservation areas in a Saharan environment by highlighting the endangered Cuvier’s Gazelle as a flagship species. Sci. Rep. 2020, 10, 10. [Google Scholar] [CrossRef]
  143. Higa, M.; Yamaura, Y.; Senzaki, M.; Koizumi, I.; Takenaka, T.; Masatomi, Y.; Momose, K. Scale dependency of two endangered charismatic species as biodiversity surrogates. Biodivers. Conserv. 2016, 25, 1829–1841. [Google Scholar] [CrossRef]
  144. Hof, A.R.; Allen, A.M. An uncertain future for the endemic Galliformes of the Caucasus. Sci. Total Environ. 2019, 651, 725–735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Hof, A.R.; Hjalten, J. Are we restoring enough? Simulating impacts of restoration efforts on the suitability of forest landscapes for a locally critically endangered umbrella species. Restor. Ecol. 2018, 26, 740–750. [Google Scholar] [CrossRef]
  146. Hofman, M.P.G.; Hayward, M.W.; Kelly, M.J.; Balkenhol, N. Enhancing conservation network design with graph-theory and a measure of protected area effectiveness: Refining wildlife corridors in Belize, Central America. Landsc. Urban Plan. 2018, 178, 51–59. [Google Scholar] [CrossRef]
  147. Hurme, E.; Monkkonen, M.; Sippola, A.L.; Ylinen, H.; Pentinsaari, M. Role of the Siberian flying squirrel as an umbrella species for biodiversity in northern boreal forests. Ecol. Indic. 2008, 8, 246–255. [Google Scholar] [CrossRef]
  148. Ionescu, D.T.; Ciobota, M.; Milac, A.L.; Ciobota, A.; Murariu, D. New insights into fall passage ecology and behaviour of black storks (Ciconia nigra) at Dumbravita fishing complex (central Romania). North-West. J. Zool. 2019, 15, 101–106. [Google Scholar]
  149. Johnson, S.A.; Ober, H.K.; Adams, D.C. Are keystone species effective umbrellas for habitat conservation? A spatially explicit approach. J. Nat. Conserv. 2017, 37, 47–55. [Google Scholar] [CrossRef] [Green Version]
  150. Jones, J.; McLeish, W.J.; Robertson, R.J. Predicting the effects of Cerulean Warbler, Dendroica cerulea management on eastern Ontario bird species. Can. Field-Nat. 2004, 118, 229–234. [Google Scholar] [CrossRef] [Green Version]
  151. Kaczensky, P.; Adiya, Y.; von Wehrden, H.; Mijiddorj, B.; Walzer, C.; Guthlin, D.; Enkhbileg, D.; Reading, R.P. Space and habitat use by wild Bactrian camels in the Transaltai Gobi of southern Mongolia. Biol. Conserv. 2014, 169, 311–318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  152. Kajtoch, L.; Zmihorski, M.; Piestrzynska-Kajtoch, A. The Goosander as potential indicator of naturalness and biodiversity in submontane river valleys of northern Carpathians. Ecol. Indic. 2014, 45, 83–92. [Google Scholar] [CrossRef]
  153. Kerley, G.I.H.; Pressey, R.L.; Cowling, R.M.; Boshoff, A.F.; Sims-Castley, R. Options for the conservation of large and medium-sized mammalia in the Cape Floristic Region hotspot, South Africa. Biol. Conserv. 2003, 112, 169–190. [Google Scholar] [CrossRef]
  154. Keuroghlian, A.; Eaton, D.P. Importance of rare habitats and riparian zones in a tropical forest fragment: Preferential use by Tayassu pecari, a wide-ranging frugivore. J. Zool. 2008, 275, 283–293. [Google Scholar] [CrossRef]
  155. Khosravi, R.; Hemami, M.R. Identifying landscape species for ecological planning. Ecol. Indic. 2019, 99, 140–148. [Google Scholar] [CrossRef]
  156. Kiffner, C.; Albertini, M.; Ede, A.; Donnellan, B.; Hahn, N.; McGinnis, M.A.; Nietlisbach, N.A.; Tate, J.; Kioko, J. Performance of individual species as indicators for large mammalia species richness in Northern Tanzania. Ecol. Indic. 2015, 53, 70–77. [Google Scholar] [CrossRef]
  157. Kim, J.H.; Park, S.; Kim, S.H.; Lee, E.J. Identifying high-priority conservation areas for endangered waterbirds using a flagship species in the Korean DMZ. Ecol. Eng. 2021, 159, 106080. [Google Scholar] [CrossRef]
  158. Kittle, A.M.; Watson, A.C.; Cushman, S.A.; Macdonald, D.W. Forest cover and level of protection influence the island-wide distribution of an apex carnivore and umbrella species, the Sri Lankan leopard (Panthera pardus kotiya). Biodivers. Conserv. 2018, 27, 235–263. [Google Scholar] [CrossRef]
  159. Klinga, P.; Mikolas, M.; Delegan, I.V.; Danila, G.; Urban, P.; Paule, L.; Kanuch, P. Temporal landscape genetic data indicate an ongoing disruption of gene flow in a relict bird species. Conserv. Genet. 2020, 21, 329–340. [Google Scholar] [CrossRef]
  160. Klinga, P.; Mikolas, M.; Smolko, P.; Tejkal, M.; Hoglund, J.; Paule, L. Considering landscape connectivity and gene flow in the Anthropocene using complementary landscape genetics and habitat modelling approaches. Landsc. Ecol. 2019, 34, 521–536. [Google Scholar] [CrossRef]
  161. Koper, N.; Schmiegelow, F.K.A. Effects of habitat management for ducks on target and nontarget species. J. Wildl. Manag. 2006, 70, 823–834. [Google Scholar] [CrossRef]
  162. Koper, N.; Schmiegelow, F.K.A. Does management for duck productivity affect songbird nesting success? J. Wildl. Manag. 2007, 71, 2249–2257. [Google Scholar] [CrossRef]
  163. Kramer, G.R.; Peterson, S.M.; Daly, K.O.; Streby, H.M.; Andersen, D.E. Left out in the rain: Comparing productivity of two associated species exposes a leak in the umbrella species concept. Biol. Conserv. 2019, 233, 276–288. [Google Scholar] [CrossRef]
  164. Kumar, U.; Awasthi, N.; Qureshi, Q.; Jhala, Y. Do conservation strategies that increase tiger populations have consequences for other wild carnivores like leopards? Sci. Rep. 2019, 9, 14673. [Google Scholar] [CrossRef] [Green Version]
  165. Ladin, Z.S.; D’Amico, V.; Baetens, J.M.; Roth, R.R.; Shriyer, W.G. Predicting Metapopulation Responses to Conservation in Human-Dominated Landscapes. Front. Ecol. Evol. 2016, 4, 1–12. [Google Scholar] [CrossRef] [Green Version]
  166. Lamb, J.S.; Paton, P.W.C.; Osenkowski, J.E.; Badzinski, S.S.; Berlin, A.M.; Bowman, T.; Dwyer, C.; Fara, L.J.; Gilliland, S.G.; Kenow, K.; et al. Spatially explicit network analysis reveals multi-species annual cycle movement patterns of sea ducks. Ecol. Appl. 2019, 29, e01919. [Google Scholar] [CrossRef]
  167. Lee, S.M.; Moon, H.C.; Jeon, H.S.; Song, E.G.; Woo, D.; An, J.; Lee, M.Y. A core set of microsatellite loci for yellow-throated marten, Martes flavigula: A case of inferences of family relationships. Genes Genom. 2019, 41, 1457–1465. [Google Scholar] [CrossRef]
  168. Leech, T.J.; Gormley, A.M.; Seddon, P.J. Estimating the minimum viable population size of kaka (Nestor meridionalis), a potential surrogate species in New Zealand lowland forest. Biol. Conserv. 2008, 141, 681–691. [Google Scholar] [CrossRef]
  169. Li, S.; McShea, W.J.; Wang, D.J.; Gu, X.D.; Zhang, X.F.; Zhang, L.; Shen, X.L. Retreat of large carnivores across the giant panda distribution range. Nat. Ecol. Evol. 2020, 4, 1327–1331. [Google Scholar] [CrossRef]
  170. Li, W.W.; Yu, Y.; Liu, P.; Tang, R.C.; Dai, Y.C.; Li, L.; Zhang, L. Identifying climate refugia and its potential impact on small population of Asian elephant (Elephas maximus) in China. Glob. Ecol. Conserv. 2019, 19, e00664. [Google Scholar] [CrossRef]
  171. Linero, D.; Cuervo-Robayo, A.P.; Etter, A. Assessing the future conservation potential of the Amazon and Andes Protected Areas: Using the woolly monkey (Lagothrix lagothricha) as an umbrella species. J. Nat. Conserv. 2020, 58, 125926. [Google Scholar] [CrossRef]
  172. Litvaitis, J.A.; Reed, G.C.; Carroll, R.P.; Litvaitis, M.K.; Tash, J.; Mahard, T.; Broman, D.J.A.; Callahan, C.; Ellingwood, M. Bobcats (Lynx rufus) as a Model Organism to Investigate the Effects of Roads on Wide-Ranging Carnivores. Environ. Manag. 2015, 55, 1366–1376. [Google Scholar] [CrossRef] [PubMed]
  173. Lohmus, A.; Runnel, K.; Palo, A.; Leis, M.; Nellis, R.; Rannap, R.; Remm, L.; Rosenvald, R.; Lohmus, P. Value of a broken umbrella: Abandoned nest sites of the black stork (Ciconia nigra) host rich biodiversity. Biodivers. Conserv. 2021, 30, 3647–3664. [Google Scholar] [CrossRef]
  174. Longepierre, S.; Hailey, A.; Grenot, C. Home range area in the tortoise Testudo hermanni in relation to habitat complexity: Implications for conservation of biodiversity. Biodivers. Conserv. 2001, 10, 1131–1140. [Google Scholar] [CrossRef]
  175. Loyn, R.H.; McNabb, E.G.; Volodina, L.; Willig, R. Modelling landscape distributions of large forest owls as applied to managing forests in north-east Victoria, Australia. Biol. Conserv. 2001, 97, 361–376. [Google Scholar] [CrossRef]
  176. Lukacs, P.M.; Seglund, A.; Boyle, S. Effects of Gunnison Sage-Grouse habitat treatment efforts on associated avifauna and vegetation structure. Avian Conserv. Ecol. 2015, 10, 7. [Google Scholar] [CrossRef] [Green Version]
  177. Lynam, A.J.; Laidlaw, R.; Noordin, W.S.W.; Elagupillay, S.; Bennett, E.L. Assessing the conservation status of the tiger Panthera tigris at priority sites in Peninsular Malaysia. Oryx 2007, 41, 454–462. [Google Scholar] [CrossRef] [Green Version]
  178. Macdonald, D.W.; Bothwell, H.M.; Hearn, A.J.; Cheyne, S.M.; Haidir, I.; Hunter, L.T.B.; Kaszta, Z.; Linkie, M.; Macdonald, E.A.; Ross, J.; et al. Multi-scale habitat selection modeling identifies threats and conservation opportunities for the Sunda clouded leopard (Neofelis diardi). Biol. Conserv. 2018, 227, 92–103. [Google Scholar] [CrossRef]
  179. Macdonald, D.W.; Bothwell, H.M.; Kaszta, Z.; Ash, E.; Bolongon, G.; Burnham, D.; Can, O.E.; Campos-Arceiz, A.; Channa, P.; Clements, G.R.; et al. Multi-scale habitat modelling identifies spatial conservation priorities for mainland clouded leopards (Neofelis nebulosa). Divers. Distrib. 2019, 25, 1639–1654. [Google Scholar] [CrossRef] [Green Version]
  180. Maciantowicz, M.; Najbar, B. Distribution and active conservation of Emys orbicularis in Lubuskie province (West Poland). Biologia 2004, 59, 177–183. [Google Scholar]
  181. Mangas, J.G.; Lozano, J.; Cabezas-Diaz, S.; Virgos, E. The priority value of scrubland habitats for carnivore conservation in Mediterranean ecosystems. Biodivers. Conserv. 2008, 17, 43–51. [Google Scholar] [CrossRef]
  182. Martikainen, P.; Kaila, L.; Haila, Y. Threatened beetles in White-backed Woodpecker habitats. Conserv. Biol. 1998, 12, 293–301. [Google Scholar] [CrossRef]
  183. Masse, R.J.; Tefft, B.C.; McWilliams, S.R. Higher bird abundance and diversity where American woodcock sing: Fringe benefits of managing forests for woodcock. J. Wildl. Manag. 2015, 79, 1378–1384. [Google Scholar] [CrossRef]
  184. Matsuura, T.; Yokohari, M.; Azuma, A. Identification of potential habitats of gray-faced buzzard in Yatsu landscapes by using digital elevation model and digitized vegetation data. Landsc. Urban Plan. 2005, 70, 231–243. [Google Scholar] [CrossRef]
  185. McGranahan, D.A.; Engle, D.M.; Fuhlendorf, S.D.; Winter, S.L.; Miller, J.R.; Debinski, D.M. Inconsistent outcomes of heterogeneity-based management underscore importance of matching evaluation to conservation objectives. Environ. Sci. Policy 2013, 31, 53–60. [Google Scholar] [CrossRef] [Green Version]
  186. McKellar, A.E.; Kesler, D.C.; Walters, J.R. Resource selection reflects fitness associations for an endangered bird in restored habitat. Anim. Conserv. 2016, 19, 131–138. [Google Scholar] [CrossRef]
  187. McNew, L.B.; Winder, V.L.; Pitman, J.C.; Sandercock, B.K. Alternative Rangeland Management Strategies and the Nesting Ecology of Greater Prairie-Chickens. Rangel. Ecol. Manag. 2015, 68, 298–304. [Google Scholar] [CrossRef]
  188. Mena, J.L.; Yagui, H.; Tejeda, V.; Cabrera, J.; Pacheco-Esquivel, J.; Rivero, J.; Pastor, P. Abundance of jaguars and occupancy of medium- and large-sized vertebrates in a transboundary conservation landscape in the northwestern Amazon. Glob. Ecol. Conserv. 2020, 23, 13. [Google Scholar] [CrossRef]
  189. Mikolas, M.; Svitok, M.; Tejkal, M.; Leitao, P.J.; Morrissey, R.C.; Svoboda, M.; Seedre, M.; Fontaine, J.B. Evaluating forest management intensity on an umbrella species: Capercaillie persistence in central Europe. For. Ecol. Manag. 2015, 354, 26–34. [Google Scholar] [CrossRef]
  190. Mikolas, M.; Tejkal, M.; Kuemmerle, T.; Griffiths, P.; Svoboda, M.; Hlasny, T.; Leitao, P.J.; Morrissey, R.C. Forest management impacts on capercaillie (Tetrao urogallus) habitat distribution and connectivity in the Carpathians. Landsc. Ecol. 2017, 32, 163–179. [Google Scholar] [CrossRef]
  191. Mildenstein, T.L.; Stier, S.C.; Nuevo-Diego, C.E.; Mills, L.S. Habitat selection of endangered and endemic large flying-foxes in Subic Bay, Philippines. Biol. Conserv. 2005, 126, 93–102. [Google Scholar] [CrossRef]
  192. Mizsei, E.; Szabolcs, M.; Szabo, L.; Boros, Z.; Mersini, K.; Roussos, S.A.; Dimaki, M.; Ioannidis, Y.; Vegvari, Z.; Lengyel, S. Determining priority areas for an Endangered cold-adapted snake on warming mountaintops. Oryx 2021, 55, 334–343. [Google Scholar] [CrossRef] [Green Version]
  193. Moran-lopez, R.; Sanchez, J.M.; Costillo, E.; Corbacho, C.; Villegas, A. Spatial variation in anthropic and natural factors regulating the breeding success of the cinereous vulture (Aegypius monachus) in the SW Iberian Peninsula. Biol. Conserv. 2006, 130, 169–182. [Google Scholar] [CrossRef]
  194. Moran, M.D.; Monroe, A.; Stallcup, L. A proposal for practical and effective biological corridors to connect protected areas in northwest Costa Rica. Nat. Conserv. 2019, 36, 113–137. [Google Scholar] [CrossRef] [Green Version]
  195. Morelli, F.; Moller, A.P.; Nelson, E.; Benedetti, Y.; Tichit, M.; Simova, P.; Jerzak, L.; Moretti, M.; Tryjanowski, P. Cuckoo as indicator of high functional diversity of bird communities: A new paradigm for biodiversity surrogacy. Ecol. Indic. 2017, 72, 565–573. [Google Scholar] [CrossRef]
  196. Moreno-Opo, R.; Fernandez-Olalla, M.; Guil, F.; Arredondo, A.; Higuero, R.; Martin, M.; Soria, C.; Guzman, J. The role of ponds as feeding habitat for an umbrella species: Best management practices for the black stork Ciconia nigra in Spain. Oryx 2011, 45, 448–455. [Google Scholar] [CrossRef] [Green Version]
  197. Mortelliti, A.; Sanzo, G.S.; Boitani, L. Species’ surrogacy for conservation planning: Caveats from comparing the response of three arboreal rodents to habitat loss and fragmentation. Biodivers. Conserv. 2009, 18, 1131–1145. [Google Scholar] [CrossRef]
  198. Mukherjee, T.; Sharma, L.K.; Kumar, V.; Sharief, A.; Dutta, R.; Kumar, M.; Joshi, B.D.; Thakur, M.; Venkatraman, C.; Chandra, K. Adaptive spatial planning of protected area network for conserving the Himalayan brown bear. Sci. Total Environ. 2021, 754, 142416. [Google Scholar] [CrossRef]
  199. Muller, J.; Pollath, J.; Moshammer, R.; Schroder, B. Predicting the occurrence of Middle Spotted Woodpecker Dendrocopos medius on a regional scale, using forest inventory data. For. Ecol. Manag. 2009, 257, 502–509. [Google Scholar] [CrossRef]
  200. Natsukawa, H.; Mori, K.; Komuro, S.; Shiokawa, T.; Umetsu, J.; Wakita, N. Forest cover and open land drive the distribution and dynamics of the breeding sites for urban-dwelling Northern Goshawks. Urban For. Urban Green 2020, 53, 126732. [Google Scholar] [CrossRef]
  201. Navedo, J.G.; Garaita, R. Do systematic daily counts reflect the total number of birds using stopover sites during migration? A test with Eurasian Spoonbill. J. Nat. Conserv. 2012, 20, 242–246. [Google Scholar] [CrossRef]
  202. Nekhay, O.; Arriaza, M. Restoration of abandoned agricultural lands toward habitats for umbrella species. Span. J. Agric. Res. 2009, 7, 375–389. [Google Scholar] [CrossRef] [Green Version]
  203. Nikolakaki, P. A GIS site-selection process for habitat creation: Estimating connectivity of habitat patches. Landsc. Urban Plan. 2004, 68, 77–94. [Google Scholar] [CrossRef]
  204. Noss, R.F.; Quigley, H.B.; Hornocker, M.G.; Merrill, T.; Paquet, P.C. Conservation biology and carnivore conservation in the Rocky Mountains. Conserv. Biol. 1996, 10, 949–963. [Google Scholar] [CrossRef]
  205. Onorato, D.P.; Criffield, M.; Lotz, M.; Cunningham, M.; McBride, R.; Leone, E.H.; Bass, O.L.; Hellgren, E.C. Habitat selection by critically endangered Florida panthers across the diel period: Implications for land management and conservation. Anim. Conserv. 2011, 14, 196–205. [Google Scholar] [CrossRef]
  206. Ortiz-Urbina, E.; Diaz-Balteiro, L.; Iglesias-Merchan, C. Influence of Anthropogenic Noise for Predicting Cinereous Vulture Nest Distribution. Sustainability 2020, 12, 503. [Google Scholar] [CrossRef] [Green Version]
  207. Osipova, L.; Sangermano, F. Surrogate species protection in Bolivia under climate and land cover change scenarios. J. Nat. Conserv. 2016, 34, 107–117. [Google Scholar] [CrossRef]
  208. Overdijk, O.; Navedo, J.G. A massive spoonbill stopover episode: Identifying emergency sites for the conservation of migratory waterbird populations. Aquat. Conserv.-Mar. Freshw. Ecosyst. 2012, 22, 695–703. [Google Scholar] [CrossRef]
  209. Pakkala, T.; Pellikka, J.; Linden, H. Capercaillie Tetrao urogallus—A good candidate for an umbrella species in taiga forests. Wildl. Biol. 2003, 9, 309–316. [Google Scholar] [CrossRef]
  210. Penjor, U.; Kaszta, Z.; Macdonald, D.W.; Cushman, S.A. Prioritizing areas for conservation outside the existing protected area network in Bhutan: The use of multi-species, multi-scale habitat suitability models. Landsc. Ecol. 2021, 36, 1281–1309. [Google Scholar] [CrossRef]
  211. Petersen, W.J.; Savini, T.; Ngoprasert, D. Strongholds under siege: Range-wide deforestation and poaching threaten mainland clouded leopards (Neofelis nebulosa). Glob. Ecol. Conserv. 2020, 24, e01354. [Google Scholar] [CrossRef]
  212. Pilliod, D.S.; Jeffries, M.I.; Arkle, R.S.; Olson, D.H. Reptilia Under the Conservation Umbrella of the Greater Sage-Grouse. J. Wildl. Manag. 2020, 84, 478–491. [Google Scholar] [CrossRef]
  213. Poiani, K.A.; Merrill, M.D.; Chapman, K.A. Identifying conservation-priority areas in a fragmented minnesota landscape based on the umbrella species concept and selection of large patches of natural vegetation. Conserv. Biol. 2001, 15, 513–522. [Google Scholar] [CrossRef]
  214. Poulin, J.F.; Villard, M.A.; Hache, S. Short-term demographic response of an old forest specialist to experimental selection harvesting. Ecoscience 2010, 17, 20–27. [Google Scholar] [CrossRef]
  215. Pratt, A.C.; Smith, K.T.; Beck, J.L. Prioritizing seasonal habitats for comprehensive conservation of a partially migratory species. Glob. Ecol. Conserv. 2019, 17, e00594. [Google Scholar] [CrossRef]
  216. Proctor, M.F.; Nielsen, S.E.; Kasworm, W.F.; Servheen, C.; Radandt, T.G.; Machutchon, A.G.; Boyce, M.S. Grizzly Bear Connectivity Mapping in the Canada-United States Trans-Border Region. J. Wildl. Manag. 2015, 79, 544–558. [Google Scholar] [CrossRef]
  217. Pruett, C.L.; Patten, M.A.; Wolfe, D.H. It’s Not Easy Being Green: Wind Energy and a Declining Grassland Bird. Bioscience 2009, 59, 257–262. [Google Scholar] [CrossRef]
  218. Puri, M.; Srivathsa, A.; Karanth, K.K.; Kumar, N.S.; Karanth, K.U. Multiscale distribution models for conserving widespread species: The case of sloth bear Melursus ursinus in India. Divers. Distrib. 2015, 21, 1087–1100. [Google Scholar] [CrossRef]
  219. Puverel, C.; Abourachid, A.; Bohmer, C.; Leban, J.M.; Svoboda, M.; Paillet, Y. This is my spot: What are the characteristics of the trees excavated by the Black Woodpecker? A case study in two managed French forests. For. Ecol. Manag. 2019, 453, 117621. [Google Scholar] [CrossRef]
  220. Ratnayeke, S.; van Manen, F.T. Assessing sloth bears as surrogates for carnivore conservation in Sri Lanka. Ursus 2012, 23, 206–217. [Google Scholar] [CrossRef]
  221. Real, J.; Bosch, R.; Tinto, A.; Hernandez-Matias, A. Identifying key habitats for the conservation of Bonelli’s Eagle Aquila fasciata using radiotracking. Ibis 2016, 158, 556–568. [Google Scholar] [CrossRef]
  222. Reza, M.I.H.; Abdullah, S.A.; Nor, S.B.; Ismail, M.H. Integrating GIS and expert judgment in a multi-criteria analysis to map and develop a habitat suitability index: A case study of large mammalia on the Malayan Peninsula. Ecol. Indic. 2013, 34, 149–158. [Google Scholar] [CrossRef] [Green Version]
  223. Roberge, J.M.; Mikusinski, G.; Svensson, S. The white-backed woodpecker: Umbrella species for forest conservation planning? Biodivers. Conserv. 2008, 17, 2479–2494. [Google Scholar] [CrossRef]
  224. Roberts, S.B.; Jordan, J.D.; Bettinger, P.; Warren, R.J. Using Bobcat Habitat Suitability to Prioritize Habitat Preservation on a Suburbanizing Barrier Island. J. Wildl. Manag. 2010, 74, 386–394. [Google Scholar] [CrossRef]
  225. Rose, P.K.; Brigham, R.M.; Davis, S.K. Conservation of Sage-grouse Critical Habitat and Implications for Prairie Songbirds. Wildl. Soc. Bull. 2021, 45, 258–266. [Google Scholar] [CrossRef]
  226. Rosenblatt, C.J.; Matthews, S.N.; Gates, R.J.; Peterman, W.E.; Shumar, M.B. Are northern bobwhites an umbrella species for open-land birds in Ohio? J. Wildl. Manag. 2022, 86, e22141. [Google Scholar] [CrossRef]
  227. Rosner, S.; Mussard-Forster, E.; Lorenc, T.; Muller, J. Recreation shapes a “landscape of fear” for a threatened forest bird species in Central Europe. Landsc. Ecol. 2014, 29, 55–66. [Google Scholar] [CrossRef]
  228. Rowland, M.M.; Wisdom, M.J.; Suring, L.H.; Meinke, C.W. Greater sage-grouse as an umbrella species for sagebrush-associated vertebrates. Biol. Conserv. 2006, 129, 323–335. [Google Scholar] [CrossRef]
  229. Rozylowicz, L.; Popescu, V.D.; Patroescu, M.; Chisamera, G. The potential of large carnivores as conservation surrogates in the Romanian Carpathians. Biodivers. Conserv. 2011, 20, 561–579. [Google Scholar] [CrossRef]
  230. Rubino, M.J.; Hess, G.R. Planning open spaces for wildlife 2, Modeling and verifying focal species habitat. Landsc. Urban Plan. 2003, 64, 89–104. [Google Scholar] [CrossRef]
  231. Rubinoff, D. Evaluating the California gnatcatcher as an umbrella species for conservation of southern California coastal sage scrub. Conserv. Biol. 2001, 15, 1374–1383. [Google Scholar] [CrossRef]
  232. Ruiz-Garcia, M.; Castellanos, A.; Arias-Vasquez, J.Y.; Shostell, J.M. Genetics of the Andean bear (Tremarctos ornatus; Ursidae, Carnivora) in Ecuador: When the Andean Cordilleras are not an Obstacle. Mitochondrial DNA Part A 2020, 31, 190–208. [Google Scholar] [CrossRef] [PubMed]
  233. Runge, C.A.; Withey, J.C.; Naugle, D.E.; Fargione, J.E.; Helmstedt, K.J.; Larsen, A.E.; Martinuzzi, S.; Tack, J.D. Single species conservation as an umbrella for management of landscape threats. PLoS ONE 2019, 14, e0209619. [Google Scholar] [CrossRef] [Green Version]
  234. Santangeli, A.; Kunttu, P.; Laaksonen, T. The surrogacy potential of white-tailed sea eagle nesting habitat on islands of the Baltic Sea. Ecol. Indic. 2015, 57, 215–218. [Google Scholar] [CrossRef]
  235. Savignac, C.; Desrochers, A.; Huot, J. Habitat use by Pileated Woodpeckers at two spatial scales in eastern Canada. Can. J. Zool.-Rev. Can. Zool. 2000, 78, 219–225. [Google Scholar] [CrossRef]
  236. Schlegel, J.; Rupf, R. Attitudes towards potential animal flagship species in nature conservation: A survey among students of different educational institutions. J. Nat. Conserv. 2010, 18, 278–290. [Google Scholar] [CrossRef]
  237. Sergio, F.; Newton, I.; Marchesi, L.; Pedrini, P. Ecologically justified charisma: Preservation of top predators delivers biodiversity conservation. J. Appl. Ecol. 2006, 43, 1049–1055. [Google Scholar] [CrossRef] [Green Version]
  238. Shardlow, T.F.; Hyatt, K.D. Quantifying associations of large vertebrates with salmon in riparian areas of British Columbia streams by means of camera-traps, bait stations, and hair samples. Ecol. Indic. 2013, 27, 97–107. [Google Scholar] [CrossRef]
  239. Shen, X.L.; Li, S.; McShea, W.J.; Wang, D.J.; Yu, J.P.; Shi, X.G.; Dong, W.; Mi, X.C.; Ma, K.P. Effectiveness of management zoning designed for flagship species in protecting sympatric species. Conserv. Biol. 2020, 34, 158–167. [Google Scholar] [CrossRef] [PubMed]
  240. Sibarani, M.C.; Di Marco, M.; Rondinini, C.; Kark, S. Measuring the surrogacy potential of charismatic megafauna species across taxonomic, phylogenetic and functional diversity on a megadiverse island. J. Appl. Ecol. 2019, 56, 1220–1231. [Google Scholar] [CrossRef] [Green Version]
  241. Singer, D.; Hondong, H.; Dietz, M. Habitat use of Bechstein’s Bat (Myotis bechsteinii) and woodpeckers reveals the importance of old-growth features in European beech forests. For. Ecol. Manag. 2021, 498, 119547. [Google Scholar] [CrossRef]
  242. Singh, M.; Singh, M.; Kumara, H.N.; Kumar, M.A.; Dsouza, L. Inter- and intra-specific associations of non-human primates in Anaimalai Hills, South India. Mammalia 1997, 61, 17–28. [Google Scholar] [CrossRef]
  243. Sinsch, U.; Greenbaum, E.; Kusamba, C.; Lehr, E. Rapid assessment of montane anuran communities in the Albertine Rift: Hyperolius castaneus Ahl, 1931 as an umbrella species for conservation. Afr. Zool. 2011, 46, 320–333. [Google Scholar] [CrossRef]
  244. Sitzia, T.; Campagnaro, T.; Dainese, M.; Dallabrida, F.; Mattedi, S.M.; Portaccio, A. Altitudinal Shift of Tetrao urogallus in an Alpine Natura 2000 Site: Implications for Habitat Restoration. Appl. Sci. 2019, 9, 1164. [Google Scholar] [CrossRef] [Green Version]
  245. Smith, I.T.; Knetter, S.J.; Svancara, L.K.; Karl, J.W.; Johnson, T.R.; Rachlow, J.L. Overlap Between Sagebrush Habitat Specialists Differs Among Seasons: Implications for Umbrella Species Conservation. Rangel. Ecol. Manag. 2021, 78, 142–154. [Google Scholar] [CrossRef]
  246. Smith, I.T.; Rachlow, J.L.; Svancara, L.K.; McMahon, L.A.; Knetter, S.J. Habitat specialists as conservation umbrellas: Do areas managed for greater sage-grouse also protect pygmy rabbits? Ecosphere 2019, 10, e02827. [Google Scholar] [CrossRef] [Green Version]
  247. Smith, M.J.; Forbes, G.J.; Betts, M.G. Landscape configuration influences gap-crossing decisions of northern flying squirrel (Glaucomys sabrinus). Biol. Conserv. 2013, 168, 176–183. [Google Scholar] [CrossRef]
  248. Snaith, T.V.; Beazley, K.F. Moose (Alces alces americana Gray Linnaeus Clinton Peterson) as a focal species for reserve design in Nova Scotia, Canada. Nat. Areas J. 2002, 22, 235–240. [Google Scholar]
  249. Stermin, A.N.; David, A.; Sevianu, E. An Evaluation of Acoustic Monitoring Methods for a Water Rail (Rallus aquaticus) Population in a Large Reed Bed. Waterbirds 2013, 36, 463–469. [Google Scholar] [CrossRef]
  250. Stewart, J.A.E.; Butterfield, H.S.; Richmond, J.Q.; Germano, D.J.; Westphal, M.F.; Tennant, E.N.; Sinervo, B. Habitat restoration opportunities, climatic niche contraction, and conservation biogeography in California’s San Joaquin Desert. PLoS ONE 2019, 14, e0210766. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  251. Stighall, K.; Roberge, J.M.; Andersson, K.; Angelstam, P. Usefulness of biophysical proxy data for modelling habitat of an endangered forest species: The white-backed woodpecker Dendrocopos leucotos. Scand. J. For. Res. 2011, 26, 576–585. [Google Scholar] [CrossRef]
  252. Stoffyn-Egli, P.; Willison, J.H.M. Including wildlife habitat in the definition of riparian areas: The beaver (Castor canadensis) as an umbrella species for riparian obligate animals. Environ. Rev. 2011, 19, 479–493. [Google Scholar] [CrossRef]
  253. Suazo, A.A.; Fauth, J.E.; Roth, J.D.; Parkinson, C.L.; Stout, I.J. Responses of small rodents to habitat restoration and management for the imperiled Florida Scrub-Jay. Biol. Conserv. 2009, 142, 2322–2328. [Google Scholar] [CrossRef]
  254. Suorsa, P.; Huhta, E.; Jantti, A.; Nikula, A.; Helle, H.; Kuitunen, M.; Koivunen, V.; Hakkarainen, H. Thresholds in selection of breeding habitat by the Eurasian treecreeper (Certhia familiaris). Biol. Conserv. 2005, 121, 443–452. [Google Scholar] [CrossRef]
  255. Tanneberger, F.; Flade, M.; Preiksa, Z.; Schroder, B. Habitat selection of the globally threatened Aquatic Warbler Acrocephalus paludicola at the western margin of its breeding range and implications for management. Ibis 2010, 152, 347–358. [Google Scholar] [CrossRef]
  256. Tarjuelo, R.; Morales, M.B.; Traba, J.; Delgado, M.P. Are Species Coexistence Areas a Good Option for Conservation Management? Applications from Fine Scale Modelling in Two Steppe Birds. PLoS ONE 2014, 9, e87847. [Google Scholar] [CrossRef] [Green Version]
  257. Thorne, J.H.; Cameron, D.; Quinn, J.F. A conservation design for the central coast of California and the evaluation of mountain lion as an umbrella species. Nat. Areas J. 2006, 26, 137–148. [Google Scholar] [CrossRef]
  258. Thornton, D.; Zeller, K.; Rondinini, C.; Boitani, L.; Crooks, K.; Burdett, C.; Rabinowitz, A.; Quigley, H. Assessing the umbrella value of a range-wide conservation network for jaguars (Panthera onca). Ecol. Appl. 2016, 26, 1112–1124. [Google Scholar] [CrossRef] [Green Version]
  259. Timmer, J.M.; Aldridge, C.L.; Fernandez-Gimenez, M.E. Managing for multiple species: Greater sage-grouse and sagebrush songbirds. J. Wildl. Manag. 2019, 83, 1043–1056. [Google Scholar] [CrossRef]
  260. Tomecek, J.M.; Pierce, B.L.; Reyna, K.S.; Peterson, M.J. Inadequate thermal refuge constrains landscape habitability for a grassland bird species. Peerj 2017, 5, e3709. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  261. Ucarli, Y. Usability of large carnivore as a keystone species in Eastern Black Sea Region, Turkey. Afr. J. Biotechnol. 2011, 10, 2032–2036. [Google Scholar]
  262. van Langevelde, F.; Schotman, A.; Claassen, F.; Sparenburg, G. Competing land use in the reserve site selection problem. Landsc. Ecol. 2000, 15, 243–256. [Google Scholar] [CrossRef]
  263. Velo-Anton, G.; Godinho, R.; Campos, J.C.; Brito, J.C. Should I Stay or Should I Go? Dispersal and Population Structure in Small, Isolated Desert Populations of West African Crocodiles. PLoS ONE 2014, 9, e94626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  264. Vieira, B.P.; Furness, R.W.; Nager, R.G. What do we know about Black Skimmers? A review on its annual-cycle and life-history main events. Ardea 2018, 106, 119–130. [Google Scholar] [CrossRef]
  265. Viterbi, R.; Imperio, S.; Alpe, D.; Bosser-peverelli, V.; Provenzale, A. Climatic Control and Population Dynamics of Black Grouse (Tetrao tetrix) in the Western Italian Alps. J. Wildl. Manag. 2015, 79, 156–166. [Google Scholar] [CrossRef]
  266. Wang, B.; Xu, Y.; Ran, J.H. Predicting suitable habitat of the Chinese monal (Lophophorus lhuysii) using ecological niche modeling in the Qionglai Mountains, China. Peerj 2017, 5, e3477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  267. Wang, F.; McShea, W.J.; Li, S.; Wang, D.J. Does one size fit all? A multispecies approach to regional landscape corridor planning. Divers. Distrib. 2018, 24, 415–425. [Google Scholar] [CrossRef] [Green Version]
  268. Wang, F.; Winkler, J.; Viña, A.; McShea, W.J.; Li, S.; Connor, T.; Zhao, Z.; Wang, D.; Yang, H.; Tang, Y.; et al. The hidden risk of using umbrella species as conservation surrogates: A spatio-temporal approach. Biol. Conserv. 2021, 253, 108913. [Google Scholar] [CrossRef]
  269. Westekemper, K.; Tiesmeyer, A.; Steyer, K.; Nowak, C.; Signer, J.; Balkenhol, N. Do all roads lead to resistance? State road density is the main impediment to gene flow in a flagship species inhabiting a severely fragmented anthropogenic landscape. Ecol. Evol. 2021, 11, 8528–8541. [Google Scholar] [CrossRef] [PubMed]
  270. Wiersma, Y.F.; Sleep, D.J.H. The effect of target setting on conservation in Canada’s boreal: What is the right amount of area to protect? Biodivers. Conserv. 2018, 27, 733–748. [Google Scholar] [CrossRef]
  271. Winchell, C.S.; Doherty, P.F. Using california gnatcatcher to test underlying models in habitat conservation plans. J. Wildl. Manag. 2008, 72, 1322–1327. [Google Scholar] [CrossRef]
  272. Winchell, C.S.; Doherty, P.F. Effects of habitat quality and wildfire on occupancy dynamics of Coastal California Gnatcatcher (Polioptila californica californica). Condor 2014, 116, 538–545. [Google Scholar] [CrossRef]
  273. Winder, V.L.; Carrlson, K.M.; Gregory, A.J.; Hagen, C.A.; Haukos, D.A.; Kesler, D.C.; Larsson, L.C.; Matthews, T.W.; McNew, L.B.; Patten, M.A.; et al. Factors affecting female space use in ten populations of prairie chickens. Ecosphere 2015, 6, 1–17. [Google Scholar] [CrossRef]
  274. Winder, V.L.; McNew, L.B.; Pitman, J.C.; Sandercock, B.K. Space Use of Female Greater Prairie-Chickens in Response to Fire and Grazing Interactions. Rangel. Ecol. Manag. 2017, 70, 165–174. [Google Scholar] [CrossRef]
  275. Xu, Y.; Wang, B.; Zhong, X.; Yang, B.; Zhang, J.D.; Zhao, C.; He, X.C.; Li, J.G.; Ran, J.H.; Zhou, C.Q. Predicting range shifts of the Chinese monal (Lophophorus lhuysii) under climate change: Implications for long-term conservation. Glob. Ecol. Conserv. 2020, 22, e01018. [Google Scholar] [CrossRef]
  276. Xu, W.Y.; Wang, L.; Gong, Y.; Wang, H.T. The indicator roles of endangered scaly sided merganser (Mergus squamatus) in submontane rivers of Changbai Mountains, China. Ecol. Indic. 2021, 129, 107966. [Google Scholar] [CrossRef]
  277. Zhao, N.; Zhang, X.; Shan, G.; Ye, X. Evaluating the Effects of Climate Change on Spatial Aggregation of Giant Pandas and Sympatric Species in a Mountainous Landscape. Animals 2021, 11, 3332. [Google Scholar] [CrossRef]
Biology 12 00509 g001 550
Figure 1. The yearly number of published articles with umbrella species as study species indexed by Science Citation Index Expanded, as well as the yearly number of total and newly (excluding umbrella species that had been proposed before) recommended umbrella species since 1984 to 2021 (A), the proportions of 213 recommended umbrella species across different taxa (B), the proportions of recommended umbrella species that use varying types of habitat (C), and the number of species for each type of habitat (D).
Figure 1. The yearly number of published articles with umbrella species as study species indexed by Science Citation Index Expanded, as well as the yearly number of total and newly (excluding umbrella species that had been proposed before) recommended umbrella species since 1984 to 2021 (A), the proportions of 213 recommended umbrella species across different taxa (B), the proportions of recommended umbrella species that use varying types of habitat (C), and the number of species for each type of habitat (D).
Biology 12 00509 g001
Biology 12 00509 g002 550
Figure 2. Distribution of study efforts and recommended umbrella species across continents, and the most studied representatives for each continent, with the number of articles on each representative in parentheses.
Figure 2. Distribution of study efforts and recommended umbrella species across continents, and the most studied representatives for each continent, with the number of articles on each representative in parentheses.
Biology 12 00509 g002
Biology 12 00509 g003 550
Figure 3. The threat statuses of 213 recommended umbrella species: (A) the proportions of recommended umbrella species that are impacted by varying types of threats and (B) the number of species that are impacted by each type of threat; (C) the proportions of recommended umbrella species that are harvested by humans (whole individuals, parts, or products from individuals) for varying types of end uses, and (D) the number of species that are used for each type of end use.
Figure 3. The threat statuses of 213 recommended umbrella species: (A) the proportions of recommended umbrella species that are impacted by varying types of threats and (B) the number of species that are impacted by each type of threat; (C) the proportions of recommended umbrella species that are harvested by humans (whole individuals, parts, or products from individuals) for varying types of end uses, and (D) the number of species that are used for each type of end use.
Biology 12 00509 g003
Biology 12 00509 g004 550
Figure 4. Proportions of the 213 recommended umbrella species across different threatened categories assessed at the year closest to the first recommendation of each umbrella species (blue bars), and assessed in the latest version of the IUCN Red List of threatened species (2022-2; orange bars). Any categories assigned as unknown, not recognized, and data deficient were grouped as unknown.
Figure 4. Proportions of the 213 recommended umbrella species across different threatened categories assessed at the year closest to the first recommendation of each umbrella species (blue bars), and assessed in the latest version of the IUCN Red List of threatened species (2022-2; orange bars). Any categories assigned as unknown, not recognized, and data deficient were grouped as unknown.
Biology 12 00509 g004
Biology 12 00509 g005 550
Figure 5. Conservation statuses of the 213 recommended umbrella species: (A) the proportions of recommended umbrella species that are currently protected by varying types of conservation actions, and (B) the number of species that are under protection for each type of conservation action; (C) the proportions of recommended umbrella species that need varying types of conservation actions, and (D) the number of species that need each type of conservation action.
Figure 5. Conservation statuses of the 213 recommended umbrella species: (A) the proportions of recommended umbrella species that are currently protected by varying types of conservation actions, and (B) the number of species that are under protection for each type of conservation action; (C) the proportions of recommended umbrella species that need varying types of conservation actions, and (D) the number of species that need each type of conservation action.
Biology 12 00509 g005
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yang, N.; Price, M.; Xu, Y.; Zhu, Y.; Zhong, X.; Cheng, Y.; Wang, B. Assessing Global Efforts in the Selection of Vertebrates as Umbrella Species for Conservation. Biology 2023, 12, 509. https://doi.org/10.3390/biology12040509

AMA Style

Yang N, Price M, Xu Y, Zhu Y, Zhong X, Cheng Y, Wang B. Assessing Global Efforts in the Selection of Vertebrates as Umbrella Species for Conservation. Biology. 2023; 12(4):509. https://doi.org/10.3390/biology12040509

Chicago/Turabian Style

Yang, Nan, Megan Price, Yu Xu, Yun Zhu, Xue Zhong, Yuehong Cheng, and Bin Wang. 2023. "Assessing Global Efforts in the Selection of Vertebrates as Umbrella Species for Conservation" Biology 12, no. 4: 509. https://doi.org/10.3390/biology12040509

APA Style

Yang, N., Price, M., Xu, Y., Zhu, Y., Zhong, X., Cheng, Y., & Wang, B. (2023). Assessing Global Efforts in the Selection of Vertebrates as Umbrella Species for Conservation. Biology, 12(4), 509. https://doi.org/10.3390/biology12040509

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop