sign in sign up
<<
Home , Assiniboine Park Zoo, Catalogue of Life, Chahinkapa Zoo, Charles Paddock Zoo, Crested coua, Dartmoor Zoological Park

Data Science for the One Plan Approach: Exploring the potential of Species360 in synergy with other biodiversity databases

CONVENORS: Dalia A. Conde, Jim Gunter & Lionel Jouvet AIM: The goal of this working group is to find the best ways to leverage data on more than 21 000 from our members for conservation planning. INTRODUCTION: Data on species life history traits, such as fertility and reproduction are essential for conservation planning. However, the lack of such data for most of the described species is overwhelming. In this workshop we want to explore how can we maximize the use of Species360’s global data on more than 21 000 species, 10 million individuals, and 170 million medical and husbandry records. Species360 is a global, non-profit, organization dedicated to gathering, sharing, and standardizing information of the under more our members care. Data from Species360's members have been used to answer the different question in species life history and evolution (Tidere et al. 2016). Furthermore, there is example of the utilization of the data for species conservation planning. These range from estimating the potential of threatened species in to act as insurance populations or as a source of information for species when there is no data (Conde et al. 2011). For example, we have been able to estimate opportunities and costs to protect species either in the wild and captivity by merging Species360 with other databases, such as World Bank social indicators, urbanization projections, and the IUCN Red List Projects to fight the illegal species trade are being developed by using more detail data from Species360 (Conde et al. 2015, Funk et al. 2017). A notable example is the use of our member's data to unveil the laundering of individuals as “captive bred” in the international markets. Wild Life Reserves of Singapore (WRS), with the aim to stop the laundering of pangolins as “captive bred” used Species360 member’s Pangolin data on reproduction. With this information, they were able to prove the challenges of obtaining the reported number of individuals from "captive breeding." Together with WRS, Chris Shepherd and the Asian Species Action Partnership (ASAP) we are pursuing a similar project with 40 species of turtles and tortoises which are being laundered as “captive bred.” Data, such as maximum reported lifespan, or age at first reproduction has already been used to fill knowledge gaps in widely accessed databases such as the and Longevity Database (AnAge). Furthermore, we believe data from Species360 can serve to improve, in some cases, generation length estimates. Generation length, a measure of the time for a population to renew itself, it is widely used for the development of IUCN Red List assessments. However, measures from closely related species or imputation analyses are applied to fill the data gaps for a high percentage of the species. Species360 has data on medical records, such as anesthesia, and husbandry records that can have applications as well for conservation. Since the inception of Species360, 43 years ago, is the idea of integrating data from wild and populations under human care has existed. We think that by working with IUCN Specialist Groups (SGs) and Taxon Advisory Groups (TAGs), is an essential step to be able to find opportunities to start such project, with the aim to support with data the One Plan Approach of Conservation Planning (OPA) from CPSG. PROCESS: For each Specialist Group (SG) attending the workshop, we will send the species reports that our members use to manage their populations (see a sample in annexed materials). During this workshop, when possible, we will have for each Specialist Group a matching TAG representative. With the aim of exploring synergies for data and knowledge exchange between both groups and find possibilities for Species360 to facilitate this process, with both data, analytics, visualization, and technology. To have a baseline of the data needs, the SGs and TAGs that have confirmed their attendance will receive a short survey. During the working group session, we will do a very brief introduction to the wealth of biodiversity databases and how we are already making standards to merge it with primary Species360 data. Following, we will give a short introduction to the expanding possibilities of data-analytics for high volumes, variety, velocity and veracity of information. We would like to discuss how these can affect or support SGs and TAGs decision-making processes. After the short introduction, we will work together to find ways to leverage data from Species360’s members, with the new analytics and other databases to support species conservation. OUTCOMES:

• To assess which are the main challenges and opportunities to leverage the wealth of data in Species360 for conservation under the One Plan approach. • To find ways in which Species360 can play a role in facilitating the exchange of data between SGs and TAGs. • To identify possible ways to obtain funds to make data transfer in the necessary format and standardized with other databases such as GenBank, IUCN (databases), EDGE, LPI. PREPARATION: • We will tackle the working group based on the DIET approach concept. Which provides four steps to help convert data into knowledge: Define, Integrate, Explore and Test. • The briefing materials contain an example of a the Species360 data available in the form of a ZIMS report that will help participants to have a better understanding of the wealth of data managed in Species360. • We ask that SG and TAG representatives answer a questionnaire, referent to the Species360 reports, that will be sent one week before the CPSG Annual Meeting. • If you attend the working group titled “Getting most out of ICAPS” please bring as many perspectives derived from that session. We believe that ideas on data needs for Conservation Planning discussed there would be highly valuable for this working group. ABOUT THE CONVENORS: Jim Gunter is the CEO of Species360; he has extensive experience in the development of technology with primary focus on databases. Since his beginning at Species360, he has developed a passion for conservation, in particular on how to apply data and computational technology to slow down the current trends. Dalia A. Conde is the Director of Science of Species360, a conservation biologist passionate about working and standardizing multiple databases for conservation planning. Her primary research focus of her team is on finding new ways to leverage Zoos and Aquarium data for conservation. Lionel Jouvet is a Researcher at Max Planck Odense and a member of the Species360 Science team. He is a marine conservation biologist, previously working in the laboratory now he is higly driven on applying data curation, analytics and visualization for conservation. REFERENCES:

Conde, Dalia A., Fernando Colchero, Burak Güneralp, Markus Gusset, Ben Skolnik, Michael Parr, Onnie Byers et al. "Opportunities and costs for preventing vertebrate ." Current Biology 25, no. 6 (2015): R219-R221.

Conde, Dalia A., Nate Flesness, Fernando Colchero, Owen R. Jones, and Alexander Scheuerlein. "An emerging role of zoos to conserve biodiversity." Science 331, no. 6023 (2011): 1390-1391.

Funk, Stephan M., Dalia A. Conde, John Lamoreux, and John E. Fa. "Meeting the Aichi targets: Pushing for zero extinction conservation." Ambio (2017): 1-13.

Tidière, Morgane, Jean-Michel Gaillard, Vérane Berger, Dennis WH Müller, Laurie Bingaman Lackey, Olivier Gimenez, Marcus Clauss, and Jean-François Lemaître. "Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals." Scientific reports 6 (2016): 36361.

BRIEFING MATERIALS:

1. The DIET approach to data: How to make Better Decisions with Less Data 2. How the Big Data Explosion Has Changed Decision Making 3. A sample of some Species360’s ZIMS data reports: i) Species Holdings, ii) Population Overview, iii) Age Distribution, iv) Animal Weight Report, v) Drug Usage, vi) Species360 Physiological Reference Intervals for Captive Wildlife

How to Make Better Decisions with Less Data 25/07/2017, 14.39

DATA How to Make Better Decisions with Less Data by Tanya Menon and Leigh Thompson

NOVEMBER 07, 2016

Maria, an executive in financial services, stared at another calendar invite in Outlook that would surely kill three hours of her day. Whenever a tough problem presented itself, her boss’s knee-jerk response was, “Collect more data!” Maria appreciated her boss’s analytical approach, but as the surveys, reports, and stats began to pile up, it was clear

https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 1 of 6 How to Make Better Decisions with Less Data 25/07/2017, 14.39

that the team was stuck in analysis paralysis. And despite the many meetings, task forces, brainstorming sessions, and workshops created to solve any given issue, the team tended to offer the same solutions — often ones that were recycled from prior problems.

As part of our research for our book, Stop Spending, Start Managing, we asked 83 executives how much they estimated that their companies wasted on relentless analytics on a daily basis. They reported a whopping $7,731 per day — $2,822,117 per year! Yet despite all of the data available, people often struggle to convert it into effective solutions to problems. Instead, they fall prey to what Jim March and his coauthors describe as “garbage can” decision making: a process whereby actors, problems, and possible solutions swirl about in a metaphorical garbage can and people end up agreeing on whatever solution rises to the top. The problem isn’t lack of data inside the garbage can; the vast amount of data means managers struggle to prioritize what’s important. In the end, they end up applying arbitrary data toward new problems, reaching a subpar solution.

YOU AND YOUR TEAM SERIES To curb garbage-can decision making, Thinking Strategically managers and their teams should think more carefully about the information they need to solve a problem and think more strategically about how to apply it to their decision making and actions. We recommend the data DIET approach, which provides four steps of intentional thought to help convert data into knowledge and How to Create an Exponential Mindset wisdom. by Mark Bonchek 5 Strategy Questions Every Leader Should Make Time For Step 1: Define by Freek Vermeulen Games Can Make You a Better Strategist by Martin Reeves and Georg Wittenburg https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 2 of 6 How to Make Better Decisions with Less Data 25/07/2017, 14.39

When teams and individuals think about a problem, they likely jump right into suggesting possible solutions. It’s the basis of many brainstorming sessions. But while the prospect of problem solving sounds positive, people tend to fixate on familiar approaches rather than stepping back to understand the contours of the problem.

Start with a problem-finding mindset, where you loosen the definitions around the problem and allow people to see it from different angles, thereby exposing hidden assumptions and revealing new questions before the hunt for data begins. With your team, think of critical questions about the problem in order to fully understand its complexity: How do you understand the problem? What are its causes? What assumptions does your team have? Alternately, write about the problem (without proposing solutions) from different perspectives — the customer, the supplier, and the competitor, for example — to see the situation in new ways.

Once you have a better view of the problem, you can move forward with a disciplined data search. Avoid decision-making delays by holding data requests accountable to if- then statements. Ask yourself a simple question: If I collect the data, then how would my decision change? If the data won’t change your decision, you don’t need to track down the additional information.

Step 2: Integrate Once you’ve defined the problem and the data you need, you must use that information effectively. In the example above, Maria felt frustrated because as the team collected more and more pieces of the jigsaw puzzle, they weren’t investing the same amount of time to see how the pieces fit together. Their subconscious beliefs or assumptions about problems guided their behavior, causing them to follow the same tired routine time and time again: collect data, hold meetings, create strategy moving forward. But this is garbage-can decision making. In order to keep the pieces from coming together in an arbitrary fashion, you need to look at the data differently.

https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 3 of 6 How to Make Better Decisions with Less Data 25/07/2017, 14.39

Integration lets you analyze how your problem and data fit together, which then lets you break down your hidden assumptions. With your team, create a KJ diagram (named after author Kawakita Jiro) to sort facts into causal relationships. Write the facts on notecards and then sort them into piles based on observable relationships — for example, an increase in clients after a successful initiative, a drop in sales caused by a delayed project, or any other data points that may indicate correlated items or causal relationships. In doing this, you can create a visual model of the patterns that emerge and make connections in the data.

Step 3: Explore At this point in the process, you may have some initial ideas or solutions based on your KJ diagrams. Now’s the time to develop them. To facilitate collaborative exploration, one of our favorite exercises (often used in art schools) is what we call the passing game. Assign distinct ideas to each team member and give each individual five minutes to develop it by drawing or writing in silence. Then have them pass their work to a teammate, who continues drafting the idea while they take over a teammate’s creation.

Discuss the collaborative output. Teammates recognize how it feels to give up “ownership” of an idea and how it feels to both edit and be edited; they also recognize their implicit assumptions about collaboration. The new perspective forces them to confront directions that they didn’t choose or never would have considered. Indeed, you can add multiple sequential passes (like a telephone game) to demonstrate the idea’s unpredictable evolution as three or four teammates play with the initial ideas. After allowing people this space for exploration, discuss the directions that are most fruitful.

Step 4: Test The last dimension requires team members to use their powers of critical thinking to consider feasibility and correct for overreach. Design tests to see if your plan forward will work. Under which types of situations will the solution fail? Select a few critical tests and

https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 4 of 6 How to Make Better Decisions with Less Data 25/07/2017, 14.39

run them. While people often over-collect data that supports their priors, people under- collect disconfirming data. By running even a single test that fights confirmation biases, you can see what you need to see, even if you don’t want to.

The solution to garbage-can decisions isn’t cutting out data entirely. Thinking strategically about your data needs pushes you to do more with less — widening, deepening, integrating, extending, and testing the data you do have to convert it into knowledge and wisdom. In practicing the mental exercises above with your team, you can curb your appetite for data while getting better at digesting the data you have.

Tanya Menon ([email protected]) is an associate professor of Management and Human Resources at the Ohio State University’s Fisher College of Business. She is the coauthor of Stop Spending, Start Managing: Strategies to Transform Wasteful Habits (Harvard Business Review Press, 2016).

Leigh Thompson is the J. Jay Gerber Professor of Dispute Resolution and Organizations at the Kellogg School of Management. She is the author of Creative Conspiracy: The New Rules of Breakthrough Collaboration (HBR Press, 2013) and coauthor of Stop Spending, Start Managing: Strategies to Transform Wasteful Habits (HBR Press, 2016).

This article is about DATA

 FOLLOW THIS TOPIC

Related Topics: DECISION MAKING | STRATEGIC THINKING

https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 5 of 6 How to Make Better Decisions with Less Data 25/07/2017, 14.39 Comments

Leave a Comment

POST

8 COMMENTS

ruben gellibert 2 months ago "Analysis paralysis" = terrible

REPLY 0  0 

 JOIN THE CONVERSATION

POSTING GUIDELINES We hope the conversations that take place on HBR.org will be energetic, constructive, and thought-provoking. To comment, readers must sign in or register. And to ensure the quality of the discussion, our moderating team will review all comments and may edit them for clarity, length, and relevance. Comments that are overly promotional, mean-spirited, or off-topic may be deleted per the moderators' judgment. All postings become the property of Harvard Business Publishing.

https://hbr.org/2016/11/how-to-make-better-decisions-with-less-data?referral=03759&cm_vc=rr_item_page.bottom Page 6 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

MANAGING ORGANIZATIONS How the Big Data Explosion Has Changed Decision Making by Michael Schrage

AUGUST 25, 2016

Organizations I work with increasingly struggle to straddle two painfully polarizing operating principles. On the one hand, they desperately seek greater agility; on the other, they genuinely want to include all the right stakeholders in their processes. This conflict

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 1 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

uncomfortably transcends traditional “centralization/decentralization” debates. Customers and clients demand greater agility, and employees and partners expect greater empowerment. So the companies push hard to provide both.

Including more people, alas, typically increases coordination costs and response times. But, almost paradoxically, greater organizational agility requires greater responsiveness and improved coordination. The more stakeholders involved, the more likely that decisions are delayed. But effective agility frequently demands inclusive stakeholder involvement.

In other words, more people want to make more-agile decisions more often. This tension drives my clients mad. At one Fortune 1000 company, for example, “flame wars” broke out between customer support units, desperate to respond faster to customer complaints, and the technical design group, equally desperate to avoid ad hoc fixes. Neither group could effectively solve the problems without the other, but their overlaps quickly became sources of conflict rather than collaboration. That pathology isn’t uncommon.

The digitally networked enterprise — whether Slacked, Chattered, Skyped, Google Doc-ed — sharply exacerbates tensions and pain points: More stakeholders can instantly access, and share, actionable information. Technology facilitates greater transparency and visibility throughout enterprise ecosystems. Real-time situational awareness dramatically increases. But the managerial and operational ability to act on that data- driven information may not.

By far the best and most useful approach for managing those tensions is Michael Jensen’s -breaking work in decision rights a quarter-century ago. Simply put, decision rights clarify authority and accountability for decisions and decision making. Decision rights are about how organizations “decide how to decide” who is empowered to make decisions. Think of it as a governance model for enterprise decision.

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 2 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

Jensen’s subtle and brilliant insight was that the right to make decisions — not just the ability to perform or be responsible for tasks — is essential to organizational efficiency and effectiveness. Consequently, assigning and allocating decision rights is every bit as organizationally important as defining jobs, roles, and tasks. In that light, decision rights can and should be seen as a managerial mechanism for empowerment. The greater your or your team’s decision rights, the more empowered and accountable you are.

The RACI framework offers an excellent real-world instantiation of Jensen’s decision rights approach:

Responsible. Who is completing the task? Accountable. Who is making decisions and taking actions on the task? Consulted. Who will be communicated with regarding decisions and tasks? Informed. Who will be updated on decisions and actions during the project/process?

These questions are uncomplicated and relatively easy to map. That is, digitally linking the relevant individuals and teams identified in a RACI review should be straightforward. An increasing number of organizations I work with use RACI (or some variant) to create auditable accountability networks for project and process management.

These networks simultaneously become platforms for both inclusion and agility. Individuals and teams who want to be consulted or informed can ask to opt in to the network; conversely, when accountable or responsible managers need more agility in response to customer needs, they can tap their RACI network for a “just-in-time” response. Mapping these networks creates visibility and clarity for stakeholders and top management alike. They provide essential windows and lenses into the firm’s decision hierarchies.

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 3 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

Intriguingly, ironically, and importantly, the fastest-growing application of decision rights I see emphasizes digitalization, data, and analytics. Who has the right to access, process, and share data has become the greatest source of opportunity and contention in the enterprise. This structural shift goes well beyond what Jensen originally envisioned and described 25 years ago because the rise of Big Data – and its associated analytics – changes contemporary debates and arguments around decision rights.

Decision rights around data increasingly require data around decision rights. In other words, if your organization has ready access to process and share 10x to 100x more data, chances are your existing decision rights mechanisms are woefully out of date. To wit, would any serious brand manager run a marketing campaign today without a capability for incorporating analytics? But brand managers need the computational competence of data scientists and analytic tools to get greater value from that data. Decision rights are needed to determine and define how brand management and data management collaborate.

At one company I’ve worked with, the big data explosion completely reframed the decision rights and RACI discussion. The company had traditionally focused its design and development efforts on new products. But with the rise of mobile apps, the firm’s innovation priorities shifted away from building better products to facilitating better user experiences. That transformed the RACI decision rights template. Accountability for UX required different data and analytics than for products; a UX emphasis meant different teams and individuals needed to be consulted and informed. In essence, UX-driven data and analytics rebalanced the decision rights relationships between agility and inclusion.

The company wrapped its people, process, and technologies around UX decision rights — and the results proved measurably stupendous. The company received 10x more usable feedback via all forms of social media and use case monitoring, and it developed a better next version in three months, as opposed to the typical one-year timeframe, for previous product development efforts and for half of the usual product development cost.

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 4 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

As organizational decisions increasingly become more data driven, top managers need to assure decision rights are data driven as well. That explains why so many organizations have made data governance a strategic and organizational priority. Instead of more traditional IT governance, which seeks to create greater accountability for IT systems management, data governance recognizes that data is the mission-critical asset to manage.

How does that data get shared (inclusiveness)? And how does the organization effectively take advantage of that data (agility)? The answer to those data governance questions will be found in the innovative application of data-driven decision rights. The future of data governance depends on the future of decision rights, and the future of decision rights depends on the future of data governance.

Michael Schrage, a research fellow at MIT Sloan School’s Center for Digital Business, is the author of the books Serious Play (HBR Press), Who Do You Want Your Customers to Become? (HBR Press) and The Innovator’s Hypothesis (MIT Press).

This article is about MANAGING ORGANIZATIONS

 FOLLOW THIS TOPIC

Related Topics: DATA | DECISION MAKING

Comments

Leave a Comment

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 5 of 6 How the Big Data Explosion Has Changed Decision Making 25/07/2017, 14.35

POST

5 COMMENTS

Gus Amaral 10 months ago Nice piece of big data into decision making. I love decision making and valuations. We provide valuation services to help people make the right project investment decisions with supporting financial facts. Please visit our website www.projectsworth.com

REPLY 0  0 

 JOIN THE CONVERSATION

POSTING GUIDELINES We hope the conversations that take place on HBR.org will be energetic, constructive, and thought-provoking. To comment, readers must sign in or register. And to ensure the quality of the discussion, our moderating team will review all comments and may edit them for clarity, length, and relevance. Comments that are overly promotional, mean-spirited, or off-topic may be deleted per the moderators' judgment. All postings become the property of Harvard Business Publishing.

https://hbr.org/2016/08/how-the-big-data-explosion-has-changed-decision-making?referral=03759&cm_vc=rr_item_page.bottom Page 6 of 6 Species holding report for: Panthera tigris /

Birth (last Institution Male Female Other Group M. Group F. Group O. Total 12 month) All 443 Institutions, 6 Regions 867 956 6 107 2 4 0 1835 Species: Panthera tigris / Tiger All 143 Institutions, 6 Regions 248 280 0 23 0 0 0 528

Region: 3 Institutions, Male: 6 , Female: 7, Other: 0

CAIRO / Giza Zoological Garden 1 1 0 0 0 0 0 2 OUDTSHORN / Cango Wildlife Ranch 3 5 0 0 0 0 0 8 PRETORIA / Nat'l Zoological Gardens of S. Africa 2 1 0 0 0 0 0 3 Region: Asia 20 Institutions, Male: 80 , Female: 95, Other: 0

ALMAYYA / Al Mayya Sanctuary 2 2 0 0 0 0 0 4 ASSAM / Assam State Zoo and 6 5 0 0 0 0 0 11 AURANGABA / Aurangabad Municipal Zoo 3 3 0 0 0 0 0 6 BANNERGHA / Bannerghatta Zool Garden National Park 13 12 0 2 0 0 0 25 BATUSECRE / Batu Secret Zoo 3 6 0 0 0 0 0 9 CHATBIR Z / Mahendra Chaudhary Zoological Park 2 1 0 0 0 0 0 3 KANPUR / Kanpur Zoological Park 1 0 0 0 0 0 0 1 KHAOKHEOW / Khao Kheow Open Zoo 3 2 0 0 0 0 0 5 KHORAT / Nakhon Ratchasema Zoological Park 4 4 0 3 0 0 0 8 LAMONGAN / Maharani Zoo & Goa 2 4 0 0 0 0 0 6 MADRAS / Arignar Anna Zool. Park, Chennai 2 3 0 0 0 0 0 5 MYSORE / Sri Chamarajendra Zoo (Mysore Zoo) 0 1 0 0 0 0 0 1 NANDANKAN / Nandankanan Biological Park 9 11 0 2 0 0 0 20 NIGHTSAF / Chiangmai Night Safari (DASTA) 19 30 0 2 0 0 0 49 SAIGON / Saigon Zoo & Botanical Gardens 3 2 0 2 0 0 0 5 SONGKHLAZ / Songkhla Zoo 0 1 0 0 0 0 0 1 SURAT / Dr. Shyama Prasad Mukharjee Zoo 2 1 0 0 0 0 0 3 TATA / Tata Steel Zoological Park 2 3 0 0 0 0 0 5 UBON ZOO / Ubon Ratchathani Zoo 2 1 0 0 0 0 0 3 VISAKAPAT / Indira Gandhi Zoological Park 2 3 0 0 0 0 0 5 Region: Australia (Oceania) 5 Institutions, Male: 9 , Female: 8, Other: 0

BEERWAH / Australia Zoo 1 2 0 0 0 0 0 3 COOMERA / Dreamworld Pty Ltd 4 6 0 0 0 0 0 10 HELLINSBU / Symbio Wildlife Gardens 1 0 0 0 0 0 0 1 MOGO / Mogo Zoo P/L 1 0 0 0 0 0 0 1 YARRALUML / National Zoo & Aquarium 2 0 0 0 0 0 0 2 Region: 69 Institutions, Male: 84 , Female: 101, Other: 0

AAPALMERE / AAP Rescue centre for Exotic Animals 0 1 0 0 0 0 0 1 AMERSFOOR / Dierenpark Amersfoort 1 1 0 0 0 0 0 2 APHOLLAND / Stichting Landgoed Hoenderdaell 2 1 0 0 0 0 0 3 AUVERGNE / Parc Animalier d'Auvergne 1 1 0 0 0 0 0 2 AYWAILLE / Monde Sauvage Safari SPRL 1 1 0 0 0 0 0 2 BADOCA PK / Badoca 1 2 0 0 0 0 0 3 BEAUVAL / Zoo Parc de Beauval 1 1 0 4 0 0 0 2 BLAIRDRUM / Blair Drummond Safari Park 1 0 0 0 0 0 0 1 BOUILLON / Parc Animalier de Bouillon 2 0 0 0 0 0 0 2 BRATISLAV / Zoologicka Zahrada Bratislava 1 1 0 0 0 0 0 2 BROXBOURN / 2 0 0 0 0 0 0 2 BUCURESTI / Gradina Zoologica Bucuresti 2 2 0 0 0 0 0 4 CABARCENO / Parque de la Naturaleza de Cabarceno 1 2 0 0 0 0 0 3 CAMBRON / Pairi Daiza 1 1 0 0 0 0 0 2 COLCHESTR / 0 1 0 0 0 0 0 1 CORDOBA / Parque Zoologico de Cordoba 1 1 0 0 0 0 0 2 COULANGE / Parc Zoologique d'Amneville 8 8 0 3 0 0 0 16 FALCONARA / Parco Zoo di Falconara 2 0 0 0 0 0 0 2 HAMERTON / Hamerton Zoological Park 2 2 0 0 0 0 0 4 HEADCORN / Wildlife Heritage Foundation 1 1 0 0 0 0 0 2 HODENHAGN / -Park Hodenhagen 7 9 0 0 0 0 0 16 IEPER / 1 3 0 0 0 0 0 4 IVANOVO Z / Ivanovo Zoo 1 0 0 0 0 0 0 1 JEREZ / ZooBotánico de Jerez 1 1 0 0 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 1 of 10 KATOWICE / Silesian Zoological Garden 0 2 0 0 0 0 0 2 KAZAN / Kazan Zoological & Botanical Garden 0 1 0 0 0 0 0 1 KISHINEV / Kishinev Zoopark 1 1 0 0 0 0 0 2 KISKUTLIG / Xantus János Állatkert Kht. 2 2 0 0 0 0 0 4 KOSICE / Zoologicka Zahrada Kosice 1 0 0 0 0 0 0 1 ZOO / Kiev Zoological Park 2 2 0 0 0 0 0 4 LA FLECHE / Parc Zoologique de La Fleche 1 2 0 0 0 0 0 3 LA PALMYR / Parc Zoologique de La Palmyre 1 1 0 0 0 0 0 2 LA PLAINE / Espace Zoolog de St-Martin-la-Plaine 0 2 0 0 0 0 0 2 LA TESTE / Zooland-Park 1 1 0 0 0 0 0 2 LIBEREC / Zoologicka zahrada Liberec 1 1 0 0 0 0 0 2 LISBON / Jardim Zoologico / Lisbon Zoo 1 1 0 0 0 0 0 2 LISIEUX Z / CERZA Centre d'Etude et de Recherche Zoologique Augeron 1 5 0 0 0 0 0 6 Z / (GRPR) 1 1 0 0 0 0 0 2 MAUBEUGE / Zoo de Maubeuge 1 1 0 0 0 0 0 2 MINSK ZOO / Minskiij Zoopark (Minsk Zoo) 1 0 0 0 0 0 0 1 MISKOLCZO / Miskolci Városgazda Nonprofit Kft. 1 0 0 0 0 0 0 1 NESLES / Le Parc des Felins 4 7 0 2 0 0 0 11 NEWBALL / Woodside Wildlife and Falconry Park 0 1 0 0 0 0 0 1 NYIREGYHA / Nyíregyházi Állatpark Nonprofit KFT (Sosto Zoo) 2 2 0 0 0 0 0 4 OLMENSE / Olmense Zoo 0 2 0 0 0 0 0 2 ORADEA / Zoo Oradea 1 0 0 0 0 0 0 1 OVERLOON / Zoo Parc Overloon 1 1 0 0 0 0 0 2 PECS / Zoo and Aqua­Terrarium Ltd. Pécs 0 2 0 0 0 0 0 2 PESSAC / Parc Zool. De Bordeaux-Pessac 1 1 0 0 0 0 0 2 PISTOIA / Societa Zoologica Di Pistoia S.R.L 1 1 0 0 0 0 0 2 POZNAN / Ogrod Zoologiczny w Poznaniu 1 0 0 0 0 0 0 1 PT ST PER / Planete Sauvage 1 0 0 0 0 0 0 1 RIVNE / Rivne Zoopark 0 1 0 0 0 0 0 1 ROMA / Rome Zoo-Fondazione 0 1 0 0 0 0 0 1 SANTILLAN / Zoo de Santillana y Parque Cuaternario 0 2 0 0 0 0 0 2 SHEPRETH / Shepreth Wildlife Park 1 1 0 0 0 0 0 2 SOFIAZOO / Sofia Zoological Gardens 0 1 0 0 0 0 0 1 TABERNAS / Oasys Parque del Desierto de Tabernas 1 0 0 0 0 0 0 1 / Zoo 2 1 0 0 0 0 0 3 TERRA NAT / S.A. 2 1 0 0 0 0 0 3 THOIRY / Thoiry Zoological Park 1 1 0 0 0 0 0 2 TOUROPARC / Touroparc 1 1 0 0 0 0 0 2 TREGOMZOO / Parc Zoologique de Tregomeur 0 2 0 0 0 0 0 2 VALBREMBO / Parco Faunistico 2 4 0 0 0 0 0 6 WIGHT ZOO / Isle of Wight Zoo 0 1 0 0 0 0 0 1 WINGHAMBP / 2 0 0 0 0 0 0 2 WINGST ZO / Zoo in der Wingst 0 1 0 0 0 0 0 1 WRAXALL / Noah's Ark Zoo Farm 1 1 0 0 0 0 0 2 ZOOPARKSY / Zoopark Sydsjælland (Zoopark Aps) 2 2 0 2 0 0 0 4 Region: 36 Institutions, Male: 63 , Female: 55, Other: 0

ABILENE / Abilene Zoological Gardens 1 0 0 0 0 0 0 1 ALEXANDRI / Alexandria Zoological Park 1 1 0 0 0 0 0 2 AMARILLO / Amarillo Zoo 0 1 0 0 0 0 0 1 AUDUBON / Audubon Zoo 1 0 0 0 0 0 0 1 BISMARCK / 1 2 0 0 0 0 0 3 BLACKBEAU / Fund for Animals' Black Beauty Ranch 3 0 0 0 0 0 0 3 BROWNSVIL / Gladys Porter Zoo 2 1 0 0 0 0 0 3 CALDWELL / Caldwell Zoo 1 1 0 0 0 0 0 2 CAPE MAY / Cape May County Park Zoo 1 0 0 0 0 0 0 1 CINCINNAT / Cincinnati Zoo & Botanical Garden 1 1 0 0 0 0 0 2 DUNLAP / Project Survival Cat Haven 2 0 0 0 0 0 0 2 FRANKLINP / Zoo New England, Franklin Park Zoo 1 1 0 0 0 0 0 2 GREATBEND / Great Bend Zoo and Raptor Center 1 0 0 0 0 0 0 1 GREEN NSC / Greensboro Science Center 1 0 0 0 0 0 0 1 GUADALJR / Guadalajara Zoo 1 1 0 0 0 0 0 2 GUAT CITY / Zoologico Nacional La Aurora 2 3 0 0 0 0 0 5 HEMMINGFD / / Fondation les Amis Parc Sauvage 1 1 0 0 0 0 0 2 HOLLYWILD / Hollywild Animal Park 2 1 0 0 0 0 0 3 ISSAQUAH / Mountain Zoological Park 4 0 0 0 0 0 0 4 KNOXVILLE / Knoxville Zoological Gardens 0 1 0 0 0 0 0 1 MEXICOCTY / Zoologico de Chapultepec 2 2 0 0 0 0 0 4 OMAHA / Omaha's Henry Doorly Zoo 0 1 0 0 0 0 0 1 ORONO / Jungle Cat World Wildlife Park Inc. 1 0 0 0 0 0 0 1

Copyright, Species360, 2017. All rights reserved. Page 2 of 10 PANAEWA / Pana'ewa Rainforest Zoo & Gardens 1 0 0 0 0 0 0 1 PUEBLA / (Africam, S. A. de C.V.) 4 3 0 0 0 0 0 7 REDWOOD / Six Flags Discovery 5 5 0 0 0 0 0 10 ROCKWELL / Tiger World 9 7 0 0 0 0 0 16 ROSAMOND / Exotic Feline Breeding Compound Inc. 2 1 0 0 0 0 0 3 S DOMINGO / Parque Zoologico Nacional, ZOODOM 1 2 0 0 0 0 0 3 TALLAHASE / Tallahassee Museum of History and Natural Science 0 3 0 0 0 0 0 3 VA SAFARI / Virginia Safari Park & Preserv Ctr,Inc 1 1 0 0 0 0 0 2 VALLEYZOO / Valley Zoo & John Janzen Nature Center 0 2 0 0 0 0 0 2 VICTOR TX / Texas Zoo 0 1 0 0 0 0 0 1 WILDLIFE / Big Cat Rescue-Carole Baskin 7 6 0 0 0 0 0 13 YULEE / White Oak Conservation Center 0 3 0 0 0 0 0 3 ZOOFARI / Zoofari 3 3 0 0 0 0 0 6 Region: 10 Institutions, Male: 6 , Female: 14, Other: 0

BARRANQUL / Barranquilla Zoo 1 1 0 0 0 0 0 2 BOGOTA / Parque Zoologico Jaime Duque - Bogota 1 2 0 0 0 0 0 3 BUIN ZOO / Parque Zoológico Buin Zoo 0 2 0 0 0 0 0 2 CALI / Fundacion Zoologica de Cali 1 1 0 1 0 0 0 2 COLOMSANT / Fundacion Zoologico Santacruz 1 1 0 0 0 0 0 2 MEDELLIN / Parque Zoologico Santa Fe 1 1 0 0 0 0 0 2 PEREIRABP / Bioparque Ukumarí 0 1 0 0 0 0 0 1 PISCILAGO / Parque Recreativo y Zool. Piscilago 1 1 0 0 0 0 0 2 SANTIAGOZ / Zool.Nacional Parque Metro De Santiago 0 3 0 0 0 0 0 3 TEMAIKEN / Parque De Animales Silvestres Temaikèn 0 1 0 0 0 0 0 1 Subspecies: Panthera tigris tigris / All 72 Institutions, 5 Regions 185 186 0 16 2 3 0 376

Region: Africa 4 Institutions, Male: 9 , Female: 8, Other: 0

BLOEMFNTN / Bloemfontein Zoological Gardens 2 0 0 0 0 0 0 2 CASELA / Casela World of Adventures 2 3 0 0 2 3 0 10 ENDOFNZOO / EndoFaun Zoological Park & 2 1 0 0 0 0 0 3 LORY PARK / Lory Park Zoo & Sanctuary 1 1 0 0 0 0 0 2 Region: Asia 38 Institutions, Male: 136 , Female: 126, Other: 0

AHMEDABAD / Kamla Nehru Zoological Garden 1 1 0 0 0 0 0 2 AL AIN / Al Ain Zoo 2 0 0 0 0 0 0 2 ALBUSTAN / Al Bustan Zoological Center 2 1 0 0 0 0 0 3 ASSAM / Assam State Zoo and Botanical Garden 1 3 0 0 0 0 0 4 BANGKOK / Dusit (Bangkok) Zoological Park 2 2 0 0 0 0 0 4 BANNERGHA / Bannerghatta Zool Garden National Park 4 0 0 0 0 0 0 4 BAYRAMOGL / Faruk Yalcin Zoo (Hayvanlar Alemi & Botanik Bahcesi) 1 1 0 0 0 0 0 2 CHATBIR Z / Mahendra Chaudhary Zoological Park 7 5 0 0 0 0 0 12 CHIANGMAI / Chiangmai Zoological Garden 1 0 0 0 0 0 0 1 COLOMBO / Department of National Zoological Gardens 4 5 0 5 0 0 0 9 DARJEELIN / Padmaja Naidu Himalayan Zoological Park 1 2 0 0 0 0 0 3 DELHI / National Zoological Park, New Delhi 5 7 0 0 0 0 0 12 HYDERABAD / Nehru Zoological Park 10 4 0 0 0 0 0 14 INDORE / Kamala Nehru Prani Sanghrahalay Zoo 3 3 0 0 0 0 0 6 ITANAGAR / Biological Park Itanagar 4 3 0 0 0 0 0 7 IZMIR ZOO / Izmir Zoo / Izmir Dogal Yasam Parki 0 3 0 0 0 0 0 3 JUNAGADH / Sakkarbaugh Zoo, Junagadh 3 4 0 0 0 0 0 7 KANPUR / Kanpur Zoological Park 4 3 0 0 0 0 0 7 KATHMANDU / National Trust for Nature Conservation 3 0 0 0 0 0 0 3 KHON KAEN / Khao Suan Kwang Zoo 0 1 0 0 0 0 0 1 LUCKNOW / Lucknow Zoological Park 4 3 0 0 0 0 0 7 MADRAS / Arignar Anna Zool. Park, Chennai 8 14 0 0 0 0 0 22 MANGALORE / Dr. Shivarama Karanth Pilikula Biol.Pk 10 1 0 4 0 0 0 11 MYSORE / Sri Chamarajendra Zoo (Mysore Zoo) 10 3 0 0 0 0 0 13 NAINITAL / Bharat Ratna Pt. Govind Ballabh Pant High Altitude Zoo Nainital 0 1 0 0 0 0 0 1 NANDANKAN / Nandankanan Biological Park 3 3 0 3 0 0 0 6 PATNA / Sanjay Gandhi Biological Park 2 3 0 0 0 0 0 5 PUNE / Rajiv Gandhi Zoological Park and Wildlife Research Centre 4 3 0 0 0 0 0 7 RAJKOT / Rajkot Municipal Corporation Zoo 2 9 0 0 0 0 0 11 RANCHI / Bhagwan Birsa Munda Biological Park 2 1 0 0 0 0 0 3 SAIGON / Saigon Zoo & Botanical Gardens 2 1 0 0 0 0 0 3 SEPAHIJAL / Sepahijala Zoological Park 1 1 0 0 0 0 0 2 SINGAPORE / Singapore Zoological Gardens 2 1 0 0 0 0 0 3 TAIPEI / Taipei Zoo 4 5 0 0 0 0 0 9

Copyright, Species360, 2017. All rights reserved. Page 3 of 10 TIGRKNGCM / Tiger Kingdom - Chiang Mai Maerim 18 20 0 0 0 0 0 38 VANVIHAR / Van Vihar National Park, Bhopal 5 6 0 0 0 0 0 11 VEERMATA / Veermata Jijabai Bhosle Udyan & Zoo 1 1 0 0 0 0 0 2 VISAKAPAT / Indira Gandhi Zoological Park 0 2 0 0 0 0 0 2 Region: Europe 9 Institutions, Male: 11 , Female: 21, Other: 0

APHOLLAND / Stichting Landgoed Hoenderdaell 2 2 0 0 0 0 0 4 BEKESBRNE / Howletts Wild Animal Park 0 1 0 0 0 0 0 1 BEWDLEY / West Midland Safari & Leisure Park Ltd 3 2 0 0 0 0 0 5 KISHINEV / Kishinev Zoopark 1 0 0 0 0 0 0 1 LYMPNE / Port Lympne Wild Animal Park 2 0 0 0 0 0 0 2 MINSK ZOO / Minskiij Zoopark (Minsk Zoo) 0 2 0 0 0 0 0 2 PALIC ZOO / Palic Zoo 0 2 0 0 0 0 0 2 PARROTZOO / Lincolnshire Wildlife Park 3 8 0 0 0 0 0 11 WIGHT ZOO / Isle of Wight Zoo 0 4 0 0 0 0 0 4 Region: North America 17 Institutions, Male: 26 , Female: 29, Other: 0

AUSTIN ZO / Austin Zoo 4 0 0 0 0 0 0 4 BLACKBEAU / Fund for Animals' Black Beauty Ranch 0 1 0 0 0 0 0 1 BOWMANVIL / Bowmanville Zoological Park 2 0 0 0 0 0 0 2 DUNLAP / Project Survival Cat Haven 0 1 0 0 0 0 0 1 ECWRZOO / Emerald Coast Wildlife Refuge Zoo 1 1 0 0 0 0 0 2 FRESNO / 0 2 0 0 0 0 0 2 GUADALJR / Guadalajara Zoo 2 2 0 0 0 0 0 4 GULF SHOR / Alabama Gulf Coast Zoo 4 2 0 0 0 0 0 6 JU ARAGON / Zoologico De San Juan De Aragon 1 1 0 0 0 0 0 2 LANDRYSAQ / Landry's (Houston) Downtown Aquarium 2 2 0 0 0 0 0 4 LANSING / Potter Park Zoological Gardens 0 1 0 0 0 0 0 1 MONTGOMRY / Montgomery Zoo 1 1 0 0 0 0 0 2 ROCKWELL / Tiger World 3 4 0 4 0 0 0 7 S DOMINGO / Parque Zoologico Nacional, ZOODOM 2 2 0 0 0 0 0 4 SOUTHWICK / Southwicks Zoo 0 2 0 0 0 0 0 2 WAHPETON / Chahinkapa Zoo 1 1 0 0 0 0 0 2 WILD WRLD / Wildlife World Zoo 3 6 0 0 0 0 0 9 Region: South America 4 Institutions, Male: 5 , Female: 5, Other: 0

BARRANQUL / Barranquilla Zoo 0 1 0 0 0 0 0 1 PERU CERH / Parque Zoologico Huachipa 1 0 0 0 0 0 0 1 SAO PAULO / Fundacao Parque Zoologico de Sao Paulo 3 1 0 0 0 0 0 4 TEMAIKEN / Parque De Animales Silvestres Temaikèn 1 3 0 0 0 0 0 4 Subspecies: Panthera tigris altaica / Amur tiger All 187 Institutions, 5 Regions 227 289 2 46 0 1 0 519

Region: Africa 2 Institutions, Male: 3 , Female: 8, Other: 0

JOHANSBRG / Johannesburg Zoological Gardens 2 5 0 4 0 0 0 7 LORY PARK / Lory Park Zoo & Owl Sanctuary 1 3 0 2 0 0 0 4 Region: Asia 14 Institutions, Male: 21 , Female: 34, Other: 2

ALMA-ATA / Almaty State Zoo of Kazakhstan 5 3 0 0 0 0 0 8 BATUSECRE / Batu Secret Zoo 0 1 0 0 0 0 0 1 BAYRAMOGL / Faruk Yalcin Zoo (Hayvanlar Alemi & Botanik Bahcesi) 1 1 0 0 0 0 0 2 BURSA ZOO / Bursa Zoo (Bursa Hayvanat Bahcesi) 1 1 0 0 0 0 0 2 KHAOKHEOW / Khao Kheow Open Zoo 1 3 0 0 0 0 0 4 KHORAT / Nakhon Ratchasema Zoological Park 0 1 0 0 0 0 0 1 KOBE PARK / Kobe Oji Zoo 1 2 0 0 0 0 0 3 NIGHTSAF / Chiangmai Night Safari (DASTA) 1 0 0 0 0 0 0 1 OSAKA / Osaka Municipal Tennoji Zool. Gdns. 2 0 0 0 0 0 0 2 PAPHOS BP / Pafos Zoo 1 5 0 0 0 0 0 6 SAPPORO / Sapporo Maruyama Zoo 1 1 0 0 0 0 0 2 SEOUL / Seoul Zoo 6 14 2 0 0 0 0 22 TOKYOTAMA / Tama Zoological Park 0 2 0 0 0 0 0 2 UBON ZOO / Ubon Ratchathani Zoo 1 0 0 0 0 0 0 1 Region: Europe 115 Institutions, Male: 144 , Female: 160, Other: 0

AGRATE / Parco Faunistico 0 1 0 0 0 0 0 1 AMERSFOOR / Dierenpark Amersfoort 1 1 0 0 0 0 0 2 APHOLLAND / Stichting Landgoed Hoenderdaell 2 3 0 0 0 0 0 5 ASHBOURNE / Tayto Park 1 1 0 0 0 0 0 2 / Safaripark 3 3 0 1 0 0 0 6 BANHAM / ZSEA Ltd. 1 1 0 0 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 4 of 10 BEKESBRNE / Howletts Wild Animal Park 0 2 0 0 0 0 0 2 BERLIN TP / -Friedrichsfelde GmbH 2 4 0 0 0 0 0 6 BESANCON / Museum de Besancon 3 2 0 4 0 0 0 5 BLACKPOOL / 1 1 0 0 0 0 0 2 BLAIRDRUM / Blair Drummond Safari Park 0 1 0 0 0 0 0 1 BORAS / Boras Djurpark Zoo 1 1 0 0 0 0 0 2 BRANTON / 3 3 0 0 0 0 0 6 BROXBOURN / Paradise Wildlife Park 0 2 0 0 0 0 0 2 BUDAPEST / Budapest Zool.& Botanical Garden 1 3 0 0 0 0 0 4 BUSSOLENG / 1 1 0 0 0 0 0 2 CHELYABIN / Chelyabinsk Zoo 1 1 0 3 0 0 0 2 CHEMNITZ / Tierpark Chemnitz 1 0 0 0 0 0 0 1 CHERKASY / Cherkasky Zoo 0 1 0 0 0 0 0 1 COLCHESTR / Colchester Zoo 1 0 0 0 0 0 0 1 COPENHAGE / 0 3 0 0 0 0 0 3 COULANGE / Parc Zoologique d'Amneville 0 1 0 0 0 0 0 1 DARTMOOR / 2 1 0 0 0 0 0 3 DEBRECEN / Nagyerdei Kultúrpark Nonprofit Kft 1 1 0 0 0 0 0 2 DROGOBYCH / Limpopo Zoo 0 1 0 0 0 0 0 1 DUBLIN / Dublin Zoo - of Ireland 1 1 0 0 0 0 0 2 DUISBURG / Zoo Duisburg AG 2 2 0 2 0 0 0 4 EUROPA / Dierenrijk 1 1 0 0 0 0 0 2 FARJESTAD / Olands Djurpark 1 2 0 0 0 0 0 3 FOLKEPARK / Zoo & Botanical Garden 0 1 0 0 0 0 0 1 FROSON / Froson-Djurpark 3 0 0 0 0 0 0 3 GDANSK / Miejski Ogrod Zoologiczny Wybrzeza 1 1 0 0 0 0 0 2 GELSNKRKN / ZOOM Erlebniswelt Gelsenkirchen 2 0 0 0 0 0 0 2 HAMBURG / GmbH 1 1 0 0 0 0 0 2 HANNOVER / Zoo Hannover GmbH 1 0 0 0 0 0 0 1 HEADCORN / Wildlife Heritage Foundation 1 1 0 0 0 0 0 2 HELSINKI / Helsinki Zoo 1 4 0 3 0 0 0 5 HILVARENB / 2 2 0 0 0 0 0 4 HLUBOKA / Zoologicka Zahrada Ohrada 1 1 0 0 0 0 0 2 HODONIN Z / Zoologická zahrada Hodonín 3 1 0 0 0 0 0 4 HUNBSTRND / Nordens Ark 2 2 0 0 0 0 0 4 IVANOVO Z / Ivanovo Zoo 0 1 0 0 0 0 0 1 JURQUES / Parc Zoologique de Jurques 1 1 0 0 0 0 0 2 KALININGR / Kaliningrad Zoo 1 1 0 0 0 0 0 2 KAUNAS / Lietuvos Zoologijos Sodas 2 1 0 0 0 0 0 3 KAZAN / Kazan Zoological & Botanical Garden 1 0 0 0 0 0 0 1 KINGUSSIE / 1 1 0 0 0 0 0 2 KNOWSLEY / 0 2 0 0 0 0 0 2 KOLMARDEN / Kolmardens Djurpark AB 3 3 0 0 0 0 0 6 KOLN / Cologne Zoo 1 1 0 0 0 0 0 2 KRAKOW / Park i Ogrod Zoologiczny w Krakowie 1 2 0 1 0 0 0 3 KRISTIANS / Kristiansand Dyrepark ASA 3 4 0 0 0 0 0 7 LA PLAINE / Espace Zoolog de St-Martin-la-Plaine 1 0 0 0 0 0 0 1 / Zoo Landau in der Pfalz 1 1 0 0 0 0 0 2 LEIPZIG / Zoo Leipzig 1 1 0 0 0 0 0 2 LESNA / Zoologicka Garden & Chateau Zlin-Lesna 3 1 0 0 0 0 0 4 LINTON / Linton Zoological Gardens 1 1 0 0 0 0 0 2 LISBON / Jardim Zoologico / Lisbon Zoo 1 1 0 0 0 0 0 2 LJUBLJANA / Zivalski vrt Ljubljana 1 1 0 0 0 0 0 2 LODZ / Miejski Ogród Zoologiczny w Lodzi Sp. z o.o. 0 3 0 0 0 0 0 3 LONGLEAT / Longleat Safari & Adventure Park 0 2 0 0 0 0 0 2 LYMPNE / Port Lympne Wild Animal Park 1 1 0 0 0 0 0 2 MAGDEBURG / Zoologischer Garten Magdeburg 1 1 0 0 0 0 0 2 MARWELL / Marwell Wildlife 2 3 0 3 0 0 0 5 MOSCOW / Moscow Zoological Park 5 3 0 0 0 0 0 8 MULHOUSE / Parc Zoologique Et Botanique Mulhouse 2 0 0 0 0 0 0 2 MUNICH / Münchener Tierpark Hellabrunn 1 1 0 0 0 0 0 2 MURES ZOO / Gradina Zoologica Tirgu-Mures 2 3 0 0 0 1 0 6 NESLES / Le Parc des Felins 3 3 0 0 0 0 0 6 NEUWIED / Zoo Neuwied 1 0 0 0 0 0 0 1 NIKOLAEV / Nikolaev Zoo of Nikolaev-City Council 1 2 0 4 0 0 0 3 NOVOSIBRK / Novosibirsk Zoological Park 1 1 0 0 0 0 0 2 NURNBERG / Tiergarten der Stadt Nürnberg 2 1 0 0 0 0 0 3 NYIREGYHA / Nyíregyházi Állatpark Nonprofit KFT (Sosto Zoo) 2 3 0 0 0 0 0 5 ODENSE / Odense Zoologiske Have 1 3 0 0 0 0 0 4 OLOMOUC / Zoologicka zahrada Olomouc 1 2 0 0 0 0 0 3

Copyright, Species360, 2017. All rights reserved. Page 5 of 10 ORADEA / Zoo Oradea 1 0 0 0 0 0 0 1 ORSA / Orsa Grönklitt Bjornpark (Orsa Pk) 2 4 0 0 0 0 0 6 OSIJEK / Zoo Osijek/UNIKOMza Komun Gospodarstvo 1 0 0 0 0 0 0 1 OVERLOON / Zoo Parc Overloon 1 1 0 0 0 0 0 2 PEAUGRES / Safari de Peaugres 1 2 0 0 0 0 0 3 PELISSANE / Parc Zoologique de la Barben 2 0 0 0 0 0 0 2 PERM ZOO / Mauk "Permskii Zoopark" 1 1 0 0 0 0 0 2 PLAISANCE / African Safari 1 1 0 0 0 0 0 2 PLEUGUEN / Château et Parc Zoologique de la Bourbansais 1 1 0 0 0 0 0 2 PLOCK / Miejski Ogrod Zoologiczny, Plock 1 1 0 0 0 0 0 2 PLZEN / Zoologická a botanická zahrada Plzen 1 1 0 0 0 0 0 2 PRAHA / The Prague Zoological Garden 1 2 0 0 0 0 0 3 PUNTAVERD / Parco Zoo Punta Verde 1 1 0 0 0 0 0 2 QUINTASI / Zoo de Gaia ­­ Zoo Sánto Inacio 1 1 0 0 0 0 0 2 RHENEN / Ouwehand Zoo 1 1 0 0 0 0 0 2 RIGA / Riga Zoo 2 1 0 0 0 0 0 3 RIVNE / Rivne Zoopark 1 0 0 0 0 0 0 1 ROEVRUCHI / Municipal Independent Org."Roev Ruchei 3 2 0 0 0 0 0 5 SAKHALIN / Sakhalin Zoo Botanical Park 1 0 0 0 0 0 0 1 SCHMIDING / Zoologischer Garten Schmiding 0 2 0 0 0 0 0 2 SCHWERIN / Zoologischer Garten Schwerin 1 2 0 0 0 0 0 3 SERVION / Zoo De Servion 1 1 0 0 0 0 0 2 SOFIAZOO / Sofia Zoological Gardens 1 1 0 0 0 0 0 2 ST PETERS / Leningrad Zoo - St. Petersburg 1 1 0 0 0 0 0 2 STRAUBING / Tiergarten Straubing 2 2 0 2 0 0 0 4 SZEGED / Szeged Zoo 2 0 0 0 0 0 0 2 TABERNAS / Oasys Parque del Desierto de Tabernas 0 1 0 0 0 0 0 1 TABOR / Zoologicka Zahrada Tabor 1 1 0 0 0 0 0 2 TALLIN / Tallinn Zoo 1 1 0 0 0 0 0 2 VALCORBA / Parco Faunistico Valcorba 0 1 0 0 0 0 0 1 VESZPREM / Kittenberger Kálmán Nonprofit Kft. 2 3 0 2 0 0 0 5 VIENNA / Schönbrunner Tiergarten GmbH 0 2 0 0 0 0 0 2 WALTER / Abenteuerland Walter Zoo 1 1 0 0 0 0 0 2 WHIPSNADE / ZSL 1 1 0 0 0 0 0 2 WOBURNLTD / 1 3 0 0 0 0 0 4 WUPPERTAL / Zoologischer Garten Wuppertal 2 1 0 0 0 0 0 3 ZAMOSCZSM / Ogrod Zoologiczny im. Stefana Milera 1 0 0 0 0 0 0 1 ZOOMTORIN / Spa 3 0 0 0 0 0 0 3 ZURICH / Zoo Zürich 1 1 0 0 0 0 0 2 Region: North America 53 Institutions, Male: 55 , Female: 87, Other: 0

ALDERGROV / 0 1 0 0 0 0 0 1 BILLINGS / ZooMontana 0 2 0 0 0 0 0 2 BOISE / Zoo Boise 0 1 0 0 0 0 0 1 BRIDGEPRT / Connecticut's Beardsley Zoo 1 1 0 0 0 0 0 2 BUFFALO / Buffalo Zoo 0 1 0 0 0 0 0 1 CALGARY / , Garden & 1 2 0 0 0 0 0 3 CHICAGOBR / Chicago Zoological Park / Brookfield Zoo 1 1 0 0 0 0 0 2 CLEVELAND / Cleveland Metroparks Zoo 1 1 0 0 0 0 0 2 COLO SPRG / Cheyenne Mtn Zoological Park 2 0 0 0 0 0 0 2 COLUMBIA / Riverbanks Zoo and Garden 1 2 0 0 0 0 0 3 COLUMBUS / Columbus Zoo and Aquarium 2 4 0 3 0 0 0 6 DES MOINE / Blank Park Zoo of Des Moines 1 1 0 0 0 0 0 2 DETROIT / Detroit Zoological Society 0 1 0 0 0 0 0 1 DULUTH / Lake Superior Zoological Gardens 0 1 0 0 0 0 0 1 ERIE / Erie Zoological Gardens 1 2 0 0 0 0 0 3 EVANSVLLE / Mesker Park Zoo 0 2 0 0 0 0 0 2 GLEN OAK / Peoria Zoo in Glen Oak Park 0 2 0 0 0 0 0 2 GRANBY / Zoo de Granby 3 3 0 0 0 0 0 6 GULF SHOR / Alabama Gulf Coast Zoo 0 1 0 0 0 0 0 1 HOGLE / Utah's 1 1 0 0 0 0 0 2 INDIANAPL / Indianapolis Zoo 2 1 0 0 0 0 0 3 JOHN BALL / John Ball Zoo 2 1 0 0 0 0 0 3 LANSING / Potter Park Zoological Gardens 1 1 0 0 0 0 0 2 LOUISVILL / Louisville Zoological Garden 1 1 0 1 0 0 0 2 MADISON / Henry Vilas Zoo 1 1 0 0 0 0 0 2 MILWAUKEE / Milwaukee County Zoological Gardens 2 4 0 4 0 0 0 6 MINNESOTA / Minnesota Zoological Garden 1 2 0 0 0 0 0 3 MINOT / 1 1 0 0 0 0 0 2 / Zoo 1 1 0 3 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 6 of 10 NY BRONX / /Wildlife Conservation Society 5 4 0 0 0 0 0 9 OMAHA / Omaha's Henry Doorly Zoo 3 3 0 3 0 0 0 6 ORONO / Jungle Cat World Wildlife Park Inc. 0 3 0 0 0 0 0 3 PHILADELP / Philadelphia Zoo 3 1 0 0 0 0 0 4 PITTSBURG / Pittsburgh Zoo & PPG Aquarium 2 2 0 0 0 0 0 4 PORTLAND / Oregon Zoo 1 0 0 0 0 0 0 1 RACINE / Racine Zoological Gardens 0 2 0 0 0 0 0 2 ROCHESTER / Seneca Park Zoo 0 2 0 0 0 0 0 2 ROCKWELL / Tiger World 3 3 0 0 0 0 0 6 ROLLING H / Rolling Hills Zoo 1 0 0 0 0 0 0 1 SAN FRAN / San Francisco Zoological Gardens 1 0 0 0 0 0 0 1 SCOTTSBLU / Riverside Discovery Center 1 1 0 0 0 0 0 2 SEDGWICK / Sedgwick County Zoo 1 3 0 0 0 0 0 4 SIOUX FAL / Great Plains Zoo 0 4 0 0 0 0 0 4 SOUTHBEND / Potawatomi Zoo 0 4 0 0 0 0 0 4 ST FELICI / Zoo Sauvage de St­Félicien 2 2 0 0 0 0 0 4 ST LOUIS / Saint Louis Zoological Park 1 1 0 0 0 0 0 2 ST PAUL / Como Park Zoo and Conservatory 1 1 0 0 0 0 0 2 SYRACUSE / Rosamond Gifford Zoo at Burnet Park 1 1 0 0 0 0 0 2 TAUTPHAUS / Idaho Falls Zoo at Tautphaus Park 0 1 0 0 0 0 0 1 TOLEDO / Toledo Zoological Gardens 0 2 0 0 0 0 0 2 TORONTO / 0 0 0 1 0 0 0 0 WATERTNSD / Bramble Park Zoo 0 2 0 0 0 0 0 2 / Zoo 2 2 0 0 0 0 0 4 Region: South America 3 Institutions, Male: 4 , Female: 1, Other: 0

HORIZONTE / Fundacao Zoo-Botan. de Belo Horizonte 0 1 0 0 0 0 0 1 POMERODE / Zoologico de Pomerode 3 0 0 0 0 0 0 3 SAO PAULO / Fundacao Parque Zoologico de Sao Paulo 1 0 0 0 0 0 0 1 Subspecies: Panthera tigris corbetti / North Indochinese tiger All 11 Institutions, 3 Regions 23 30 0 0 0 0 0 53

Region: Asia 8 Institutions, Male: 21 , Female: 27, Other: 0

KHAOKHEOW / Khao Kheow Open Zoo 5 7 0 0 0 0 0 12 KHON KAEN / Khao Suan Kwang Zoo 2 1 0 0 0 0 0 3 KHORAT / Nakhon Ratchasema Zoological Park 0 1 0 0 0 0 0 1 NIGHTSAF / Chiangmai Night Safari (DASTA) 3 3 0 0 0 0 0 6 SAIGON / Saigon Zoo & Botanical Gardens 1 2 0 0 0 0 0 3 SONGKHLAZ / Songkhla Zoo 5 5 0 0 0 0 0 10 TAIPING / Zoo Taiping & Night Safari 5 7 0 0 0 0 0 12 UBON ZOO / Ubon Ratchathani Zoo 0 1 0 0 0 0 0 1 Region: Europe 2 Institutions, Male: 2 , Female: 2, Other: 0

BERLIN TP / Tierpark Berlin-Friedrichsfelde GmbH 1 1 0 0 0 0 0 2 NYIREGYHA / Nyíregyházi Állatpark Nonprofit KFT (Sosto Zoo) 1 1 0 0 0 0 0 2 Region: North America 1 Institutions, Male: 0 , Female: 1, Other: 0

ROCKWELL / Tiger World 0 1 0 0 0 0 0 1 Subspecies: Panthera tigris jacksoni / Malayan tiger All 34 Institutions, 3 Regions 48 32 0 2 0 0 0 80

Region: Asia 2 Institutions, Male: 4 , Female: 5, Other: 0

SINGAPORE / Singapore Zoological Gardens 3 2 0 0 0 0 0 5 TAIPING / Zoo Taiping & Night Safari 1 3 0 0 0 0 0 4 Region: Europe 7 Institutions, Male: 7 , Female: 6, Other: 0

HALLE / Zoologischer Garten Halle GmbH 1 1 0 0 0 0 0 2 HAMERTON / Hamerton Zoological Park 1 1 0 0 0 0 0 2 NAMERVENT / Natur'Zoo de Mervent 2 0 0 0 0 0 0 2 NESLES / Le Parc des Felins 1 1 0 1 0 0 0 2 PRAHA / The Prague Zoological Garden 1 1 0 0 0 0 0 2 PT ST PER / Planete Sauvage 1 1 0 0 0 0 0 2 USTI / Usti nad Labem Zoo 0 1 0 0 0 0 0 1 Region: North America 25 Institutions, Male: 37 , Female: 21, Other: 0

ALEXANDRI / Alexandria Zoological Park 1 1 0 0 0 0 0 2 ATASCADER / Charles Paddock Zoo 1 0 0 0 0 0 0 1 AUDUBON / Audubon Zoo 1 0 0 0 0 0 0 1 BATONROUG / BREC's Baton Rouge Zoo 1 1 0 0 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 7 of 10 BIRMINGHM / Birmingham Zoo 1 0 0 0 0 0 0 1 CINCINNAT / Cincinnati Zoo & Botanical Garden 1 1 0 0 0 0 0 2 DICKERSON / Dickerson Park Zoo 1 1 0 0 0 0 0 2 DREHER PA / Palm Beach Zoo at Dreher Park 3 1 0 0 0 0 0 4 EL PASO / El Paso Zoo 1 2 0 0 0 0 0 3 FRESNO / Fresno Chaffee Zoo 1 2 0 0 0 0 0 3 JACKSONVL / Jacksonville Zoo and Gardens 2 0 0 0 0 0 0 2 JNGLARY F / The Naples Zoo 2 0 0 0 0 0 0 2 KNOXVILLE / Knoxville Zoological Gardens 2 0 0 0 0 0 0 2 LITTLEROC / Little Rock Zoological Gardens 1 1 0 0 0 0 0 2 LOWRY / Tampa's Lowry Park Zoo 1 2 0 1 0 0 0 3 LUFKIN / Ellen Trout Zoo 1 1 0 0 0 0 0 2 MANHATTAN / Sunset Zoo 2 0 0 0 0 0 0 2 NORFOLK / Virginia Zoological Park 3 0 0 0 0 0 0 3 NY BRONX / Bronx Zoo/Wildlife Conservation Society 1 3 0 0 0 0 0 4 OMAHA / Omaha's Henry Doorly Zoo 0 1 0 0 0 0 0 1 ROSAMOND / Exotic Feline Breeding Compound Inc. 2 1 0 0 0 0 0 3 SANDIEGOZ / 3 0 0 0 0 0 0 3 SEATTLE / Woodland Park Zoo 3 0 0 0 0 0 0 3 TUCSON / Reid Park Zoo 1 1 0 0 0 0 0 2 TULSA / Tulsa Zoo 1 2 0 0 0 0 0 3 Subspecies: Panthera tigris sumatrae / All 102 Institutions, 5 Regions 132 135 4 19 0 0 0 271

Region: Asia 10 Institutions, Male: 15 , Female: 16, Other: 2

ALMAYYA / Al Mayya Sanctuary 1 1 0 0 0 0 0 2 BANNERGHA / Bannerghatta Zool Garden National Park 1 0 0 0 0 0 0 1 BATUSECRE / Batu Secret Zoo 2 2 0 0 0 0 0 4 JERUSALEM / The Tisch Family Zoological Gardens 1 1 0 0 0 0 0 2 LAMONGAN / Maharani Zoo & Goa 3 2 0 0 0 0 0 5 PASURUAN / PT Taman Safari II Prigen 0 2 0 0 0 0 0 2 RAMAT GAN / Zoological Center Tel Aviv - Ramat Gan 2 0 0 0 0 0 0 2 SENDAISHI / Yagiyama Zoological Park Sendai 3 3 0 0 0 0 0 6 TOKYOUENO / Ueno Zoological Gardens 1 2 0 0 0 0 0 3 ZOORASIA / Yokohama Zool. Gardens (ZOORASIA) 1 3 2 3 0 0 0 6 Region: Australia (Oceania) 13 Institutions, Male: 26 , Female: 22, Other: 0

ADELAIDE / 1 2 0 0 0 0 0 3 AUCKLAND / Auckland Zoological Park 2 1 0 0 0 0 0 3 BEERWAH / Australia Zoo 7 4 0 3 0 0 0 11 COOMERA / Dreamworld Pty Ltd 1 2 0 0 0 0 0 3 DUBBO / Taronga Western Plains Zoo 3 3 0 0 0 0 0 6 HAMILTON / Hamilton Zoo 2 3 0 0 0 0 0 5 HELLINSBU / Symbio Wildlife Gardens 1 1 0 0 0 0 0 2 MELBOURNE / Melbourne Zoo 1 2 0 0 0 0 0 3 MOGO / Mogo Zoo P/L 2 1 0 0 0 0 0 3 ORANA / Orana Wildlife Park 2 0 0 0 0 0 0 2 PERTH / Perth Zoological Parks Authority 2 0 0 0 0 0 0 2 WELLINGTN / Wellington Zoo Trust 1 1 0 0 0 0 0 2 YARRALUML / National Zoo & Aquarium 1 2 0 0 0 0 0 3 Region: Europe 52 Institutions, Male: 55 , Female: 60, Other: 2

AALBORG / 1 1 0 0 0 0 0 2 ARNHEM / Royal Burgers' Zoo 1 4 0 0 0 0 0 5 ATTICAZOO / Attica Zoological Park S.A. 1 1 0 0 0 0 0 2 AUGSBURG / Zoologischer Garten Augsburg GmbH 1 1 0 0 0 0 0 2 BARCELONA / Parc Zoologic de Barcelona 1 1 0 0 0 0 0 2 BEAUVAL / Zoo Parc de Beauval 3 1 0 0 0 0 0 4 BEKESBRNE / Howletts Wild Animal Park 1 1 0 0 0 0 0 2 BELFAST / Belfast Zoological Gardens 1 1 0 0 0 0 0 2 BERLIN TP / Tierpark Berlin-Friedrichsfelde GmbH 1 1 0 0 0 0 0 2 BEWDLEY / West Midland Safari & Leisure Park Ltd 1 1 0 0 0 0 0 2 BOISSIERE / Espace Zoologique la Boissiere du Dore 1 1 0 0 0 0 0 2 BRNO / Brno Zoo and Environmental Education Centre, Semi Budgetary 1 1 0 0 0 0 0 2 Organization CHAMPREP / Parc Zoologique de Champrépus 0 1 0 0 0 0 0 1 CHESINGTN / Chessington World of Adventures, Ltd. 0 2 0 0 0 0 0 2 CHESTER / North of England Zoological Society 0 2 0 0 0 0 0 2 COLWYNBAY / 1 1 0 0 0 0 0 2 DUDLEY / Dudley Zoological Gardens 1 1 0 0 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 8 of 10 EBELTOFT / Ree Park - Ebeltoft Safari 2 1 0 0 0 0 0 3 EDINBURGH / - Scottish National Zoo 1 1 0 0 0 0 0 2 ESKILSTUN / Parken Zoo i Eskilstuna AB 2 1 0 0 0 0 0 3 FONTAINE / BioParc de Doué 1 1 0 0 0 0 0 2 FOTA / Fota Wildlife Park 2 1 0 0 0 0 0 3 FRANKFURT / Zoologischer Garten Frankfurt 0 1 0 0 0 0 0 1 FUENGIROL / Bioparc Fuengirola (Rain Forest S.L.) 2 1 0 0 0 0 0 3 HEADCORN / Wildlife Heritage Foundation 2 1 0 0 0 0 0 3 HEIDELBRG / Tiergarten Heidelberg 1 0 0 0 0 0 0 1 JIHLAVA / Zoologicka Zahrada Jihlava 0 1 0 0 0 0 0 1 KREFELD / Zoo Krefeld GmbH 1 0 0 0 0 0 0 1 LA FLECHE / Parc Zoologique de La Fleche 1 1 0 0 0 0 0 2 LE PAL / Le Pal, Parc Animalier 2 1 0 0 0 0 0 3 LE VIGEN / Parc ZOO du Reynou 1 1 0 0 0 0 0 2 LINTON / Linton Zoological Gardens 0 1 0 0 0 0 0 1 LISBON / Jardim Zoologico / Lisbon Zoo 1 2 0 0 0 0 0 3 LISIEUX Z / CERZA Centre d'Etude et de Recherche Zoologique Augeron 1 1 0 0 0 0 0 2 LONDON RP / ZSL 2 2 0 2 0 0 0 4 MALTON / LTD 1 1 0 0 0 0 0 2 MANOR HS / Manor House Wildlife Park 1 1 0 0 0 0 0 2 NESLES / Le Parc des Felins 2 2 0 0 0 0 0 4 NYIREGYHA / Nyíregyházi Állatpark Nonprofit KFT (Sosto Zoo) 1 1 0 0 0 0 0 2 OBTERRE / Parc de la Haute Touche (MNHN) 1 1 2 3 0 0 0 4 OSNABRUCK / Zoo Osnabrück 1 1 0 0 0 0 0 2 PAIGNTON / Environmental Park 2 1 0 3 0 0 0 3 PRAHA / The Prague Zoological Garden 1 1 0 0 0 0 0 2 ROMA / Rome Zoo-Fondazione Bioparco di Roma 1 1 0 0 0 0 0 2 ROTTERDAM / Rotterdam Zoo 1 1 0 0 0 0 0 2 SO LAKES / Safari Zoo 1 3 0 0 0 0 0 4 STUTTGART / Zoo 0 1 0 0 0 0 0 1 TAMWORTH / Drayton Manor Park Zoo 1 1 0 0 0 0 0 2 TERRA NAT / Terra Natura S.A. 1 1 0 0 0 0 0 2 WARSAW / Miejski Ogrod Zoologiczny Warsaw 0 1 0 0 0 0 0 1 WROCLAW / ZOO Wroclaw Sp z o.o. 1 1 0 0 0 0 0 2 YARMOUTH / Thrigby Hall Wildlife Gardens 1 1 0 0 0 0 0 2 Region: North America 26 Institutions, Male: 36 , Female: 36, Other: 0

AKRON / Akron Zoological Park 2 0 0 0 0 0 0 2 BATONROUG / BREC's Baton Rouge Zoo 2 0 0 0 0 0 0 2 DALLAS / Dallas Zoo 2 3 0 0 0 0 0 5 DISNEY AK / Disney's Animal Kingdom 1 1 0 0 0 0 0 2 FT WAYNE / Fort Wayne Children's Zoo 1 1 0 0 0 0 0 2 HATTIESBG / Hattiesburg Zoo 2 0 0 0 0 0 0 2 HONOLULU / Honolulu Zoo 1 1 0 0 0 0 0 2 JACKSON / Jackson Zoological Park 2 1 0 0 0 0 0 3 JACKSONVL / Jacksonville Zoo and Gardens 1 2 0 0 0 0 0 3 KANSASCTY / Kansas City Zoo 2 0 0 0 0 0 0 2 LOSANGELE / & Botanical Gardens 1 1 0 0 0 0 0 2 LOUISVILL / Louisville Zoological Garden 1 1 0 0 0 0 0 2 METROZOO / Zoo Miami 2 1 0 0 0 0 0 3 MEXICOCTY / Zoologico de Chapultepec 1 0 0 0 0 0 0 1 NZP-WASH / Smithsonian National Zoological Park 2 1 0 0 0 0 0 3 OKLAHOMA / Oklahoma City Zoological Park 1 1 0 0 0 0 0 2 PHOENIX / Phoenix Zoo 1 1 0 2 0 0 0 2 SACRAMNTO / 1 0 0 0 0 0 0 1 SAN ANTON / San Antonio Zoological Gardens & Aquar 0 3 0 0 0 0 0 3 SAN FRAN / San Francisco Zoological Gardens 1 2 0 0 0 0 0 3 SD-WAP / San Diego Zoo Safari Park 4 5 0 3 0 0 0 9 TACOMA / Point Defiance Zoo & Aquarium 1 3 0 0 0 0 0 4 TOPEKA / Topeka Zoological Park 1 4 0 0 0 0 0 5 TORONTO / Toronto Zoo 1 1 0 0 0 0 0 2 WACO / Cameron Park Zoo 2 1 0 0 0 0 0 3 WINSTON / Wildlife Safari Inc 0 2 0 0 0 0 0 2 Region: South America 1 Institutions, Male: 0 , Female: 1, Other: 0

SAO PAULO / Fundacao Parque Zoologico de Sao Paulo 0 1 0 0 0 0 0 1 Variety: Panthera tigris color_mutation / Tiger (color mutation) All 4 Institutions, 2 Regions 4 4 0 1 0 0 0 8

Region: Asia 1 Institutions, Male: 1 , Female: 1, Other: 0

Copyright, Species360, 2017. All rights reserved. Page 9 of 10 HAIFA / Haifa Educ.Zoo & Biological Institute 1 1 0 0 0 0 0 2 Region: Europe 3 Institutions, Male: 3 , Female: 3, Other: 0

MOSCOW / Moscow Zoological Park 0 1 0 0 0 0 0 1 NOVOSIBRK / Novosibirsk Zoological Park 2 1 0 1 0 0 0 3 ROEVRUCHI / Municipal Independent Org."Roev Ruchei 1 1 0 0 0 0 0 2

Copyright, Species360, 2017. All rights reserved. Page 10 of 10 Population Overview Report for Panthera tigris / Tiger IUCN: Endangered (EN) CITES: I From: 26 Jan 1997 to 26 Jan 2017 | Population Subset: All ISIS Members (1017)

Acquisitions (A) and Dispositions (D) by Year Animal Age Graph / Live Animals 30 1 70 29 28 27 60 26 25 24 50 23 22 21 2 1 20 4 3 40 19 5 5 18 7 4 17 6 7 30 16 4 8 Number 15 12 4 14 7 6 20 13 6 5 12 10 16 11 10 11

Age (In years) 10 5 11 10 9 18 16 8 13 13 7 8 12 0 6 20 19

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 5 18 18 4 11 17 3 17 17 2 12 13 1 7 16 0 6 15

Year 20 10 0 10 20

Births A-Wild A-From Non-Species360 Count (Animals) A-From Species360, Outside Population Subset Deaths D-Wild D-To Non-Species360 D-To Species360, Outside Population Subset Unknown/Other Male Unknown/Other Female Population Data and Data Quality Indicators Population and Holders by Year Individuals 600 Living Individuals Contributing Founders (>=) 14.5.0 = 19 total Living Individuals 248.281.0 = 529 total 500 Living Descendants (from Founders) (>=)8.7.1 = 16 total Living Breeders 50.56.2 = 108 total 400 Living Captive Born 217.258.0 = 475 total Living Wild Born 5.3.0 = 8 total % Marked Hybrid 0% (0 of 0 total) 300 % Ancestry Includes Inconsistent 15% (79 of 529 total) % Pedigree Known 6.13% (Avg - 529 animals) Number % Pedigree Certain 6.13% (Avg - 529 animals) 200 Living and Historical Individuals % Estimated Birth Dates (> One Month) 6% (41 of 744 total) 100 % Unknown Date of Birth 2% (15 of 744 total) % Individually Identified Sires and Dams 75% (558 of 736 total - excludes Founders) % Individuals with Multiple Sires or Dams 0% (0 of 0 total - excludes Founders) 0 % MULT Parents without Identification 0% (0 of 0 total - excludes Founders) 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 % Animals without Recorded Birth or Capture 37% (276 of 744 total) % Animals Lost to Follow Up 9% (69 of 744 total) Groups Year Living Animals in Groups 0.0.0 = 0 total Current Founder Groups 0 Population Holders Number of Current Groups 0 % Pedigree Known 0% (Avg - 0 groups) % Pedigree Certain 0% (Avg - 0 groups) Disclaimer: These tables and figures are based on institutional data submitted to Species360, not studbook data. Copyright, Species360, 2017. All rights reserved.

Printed: Jan 26, 2017 11:28 Species360 Page: 1 of 1 Species360 ZIMS version 2.3.5.1 Age Distribution Panthera tigris/Tiger

Copyright, Species360, 2017. All rights reserved. Male Female

Include Taxonomy below selected level: True Global Scope: True Number of Animals of Unknown Age Excluded: 181

Printed: Jan 26, 2017 11:25 Species360 Page: 1 of 1 Species360 ZIMS version 2.3.5.1 Report Start Date Animal Weight Report Report End Date Jan 01, 1800 Panthera tigris/Tiger Jan 26, 2017 Copyright, Species360, 2017. All rights reserved.

Type: Global Data Only Units: kilogram Starting Age: 0 years Ending Age: 200 years Number of Animals: 2245 Number of Weight Records: 44248

Printed: Jan 26, 2017 11:27 Species360 Page: 1 of 2 Species360 ZIMS version 2.3.5.1 Report Start Date Animal Weight Report Report End Date Jan 01, 1800 Panthera tigris/Tiger Jan 26, 2017 Copyright, Species360, 2017. All rights reserved.

Note: Outlier values have been removed. Box is +/- (One Standard Deviation) from median. Whiskers are based on Min and Max of remaining full range.

Printed: Jan 26, 2017 11:27 Species360 Page: 2 of 2 Species360 ZIMS version 2.3.5.1 Drug Usage Search

Active Ingredient(s) Species Level Summary Prescription Count Level Summary Prescription Count

Itraconazole Spheniscus humboldti / Humboldt 2024 Spheniscus / Penguin 3820 Itraconazole Spheniscus demersus / Jackass penguin 1462 Spheniscus / Penguin 3820 Itraconazole Atelopus zeteki / Panamanian golden frog 520 Atelopus / Painted frog 529 Itraconazole Eudyptes chrysocome / Southern rockhopper penguin 427 Eudyptes / Penguin 741 Itraconazole Pygoscelis papua / Gentoo penguin 362 Pygoscelis / Penguin 406 Terbinafine Spheniscus demersus / Jackass penguin 349 Spheniscus / Penguin 595 Itraconazole Spheniscus magellanicus / Magellanic penguin 312 Spheniscus / Penguin 3820 Fluconazole Spheniscus magellanicus / Magellanic penguin 303 Spheniscus / Penguin 327 Itraconazole Tursiops truncatus / Bottlenose 299 Tursiops / Bottlenose dolphin 305 Itraconazole Eudyptes chrysolophus / Macaroni penguin 241 Eudyptes / Penguin 741 Itraconazole Aptenodytes patagonicus / King penguin 206 Aptenodytes / Penguin 206 Voriconazole Spheniscus magellanicus / Magellanic penguin 194 Spheniscus / Penguin 361 Itraconazole Haliaeetus leucocephalus / 174 Haliaeetus / Eagle 186 Itraconazole Peltophryne lemur / Puerto Rican crested toad 167 Peltophryne / Toad 167 Itraconazole Somateria fischeri / Spectacled eider 165 Somateria / Eider 203 Terbinafine Spheniscus humboldti / Humboldt penguin 135 Spheniscus / Penguin 595 Voriconazole Spheniscus humboldti / Humboldt penguin 134 Spheniscus / Penguin 361 Amphotericin B Melopsittacus undulatus / Budgerigar 133 Melopsittacus / Budgerigar 133 Voriconazole Pogona vitticeps / Inland bearded dragon 124 Pogona / Bearded dragon 124 Flucytosine Spheniscus humboldti / Humboldt penguin 121 Spheniscus / Penguin 129 Terbinafine Tursiops truncatus / Bottlenose dolphin 113 Tursiops / Bottlenose dolphin 118 Terbinafine Pygoscelis papua / Gentoo penguin 112 Pygoscelis / Penguin 112 Itraconazole Rollulus rouloul / Crested wood partridge 108 Rollulus / Crested wood partridge 108 Terbinafine Somateria fischeri / Spectacled eider 102 Somateria / Eider 151 Miconazole Capra hircus / Goat 99 Capra / Goat/ibex/markhor 99 Itraconazole Anaxyrus baxteri / Wyoming toad 95 Anaxyrus / Toad 126 Itraconazole Eudyptula minor / Blue penguin 93 Eudyptula / Penguin 93 Terbinafine Spheniscus magellanicus / Magellanic penguin 91 Spheniscus / Penguin 595 Terbinafine Eudyptes chrysolophus / Macaroni penguin 87 Eudyptes / Penguin 140 Itraconazole Bubo scandiacus / 85 Bubo / Eagle owl 155 Itraconazole Phoenicopterus ruber / American flamingo 83 Phoenicopterus / Flamingo 159 Itraconazole Halichoerus grypus / Grey seal 79 Halichoerus / Grey seal 79 Itraconazole Buteo jamaicensis / Red-tailed hawk 77 Buteo / Hawk 113 Amphotericin B Spheniscus demersus / Jackass penguin 73 Spheniscus / Penguin 140 Itraconazole Grus americana / Whooping 71 Grus / Crane 85 Miconazole Ailurus fulgens / 69 Ailurus / Red panda 69 Itraconazole Eudyptes moseleyi / Northern rockhopper penguin 69 Eudyptes / Penguin 741 Fluconazole Pongo pygmaeus / Bornean 69 Pongo / Orangutan 87 Fluconazole Pithecia pithecia / White-faced saki 67 Pithecia / Saki 67 Itraconazole Hemignathus virens / Amakihi 66 Hemignathus / Akialoa 66 Fluconazole Mandrillus sphinx / Mandrill 66 Mandrillus / Drill/mandrill 66 Itraconazole Gallus gallus / 64 Gallus / Junglefowl 65 Itraconazole Phoenicopterus chilensis / Chilean flamingo 63 Phoenicopterus / Flamingo 159 Itraconazole Cygnus atratus / Black swan 62 Cygnus / Swan 181 Itraconazole Odobenus rosmarus / Walrus 62 Odobenus / Walrus 62 Fluconazole Lemur catta / Ring-tailed lemur 61 Lemur / Lemur 61 Fluconazole Phoca vitulina / 61 Phoca / Harbor seal 61 Fluconazole Zalophus californianus / California sealion 59 Zalophus / Sealion 59 Itraconazole Ambystoma tigrinum / Tiger salamander 58 Ambystoma / Mole salamander 95 Itraconazole Fratercula cirrhata / Tufted puffin 58 Fratercula / Puffin 83 Itraconazole Eudromia elegans / Elegant crested tinamou 56 Eudromia / Tinamou 56 Itraconazole Bubo virginianus / 55 Bubo / Eagle owl 155 Itraconazole Pauxi pauxi / Northern helmeted curassow 55 Pauxi / Helmeted curassow 55 Itraconazole Afropavo congensis / Congo peacock 54 Afropavo / Congo peacock 54 Itraconazole Larosterna inca / Inca tern 54 Larosterna / Inca tern 54 Fluconazole Hydrictis maculicollis / Spotted-necked otter 51 Hydrictis / Spotted-neck otter 51 Itraconazole Cochlearius cochlearius / Boat-billed heron 50 Cochlearius / Boat-billed heron 50 Amphotericin B Spheniscus humboldti / Humboldt penguin 49 Spheniscus / Penguin 140 Itraconazole Ailurus fulgens / Red panda 48 Ailurus / Red panda 48 Terbinafine Bubo scandiacus / Snowy owl 48 Bubo / Eagle owl 65 Terbinafine Eudyptula minor / Blue penguin 48 Eudyptula / Penguin 48 Terbinafine Somateria mollissima / Eider 47 Somateria / Eider 151 Itraconazole Calyptomena viridis / Lesser green broadbill 45 Calyptomena / Green broadbill 45 Itraconazole Cryptobranchus alleganiensis / Hellbender 45 Cryptobranchus / Hellbender 45 Itraconazole Falco peregrinus / Peregrine falcon 45 Falco / Kestrel/falcon 84 Terbinafine Haliaeetus leucocephalus / Bald eagle 45 Haliaeetus / Eagle 51 Itraconazole Trichoglossus haematodus / Coconut lorikeet 45 Trichoglossus / Lory 94 Itraconazole Aquila chrysaetos / Golden eagle 43 Aquila / Eagle 47 Terbinafine Fratercula cirrhata / Tufted puffin 43 Fratercula / Puffin 56 Itraconazole Phoca vitulina / Harbor seal 43 Phoca / Harbor seal 43 Itraconazole Trichoglossus moluccanus / Australian rainbow 40 Trichoglossus / Lory 94 lorikeet Enilconazole Capra hircus / Goat 39 Capra / Goat/ibex/markhor 39 Itraconazole Eudocimus ruber / Scarlet ibis 39 Eudocimus / Ibis 49 Itraconazole Gorilla gorilla / Western gorilla 39 Gorilla / Gorilla 39 Fluconazole Helarctos malayanus / Malayan 39 Helarctos / Malayan sun bear 39 Itraconazole Anodorhynchus hyacinthinus / Hyacinth 38 Anodorhynchus / Macaw 38 Terbinafine Bucephala islandica / Barrow's goldeneye 38 Bucephala / Goldeneye 40 Itraconazole Cygnus buccinator / Trumpeter swan 38 Cygnus / Swan 181 Fluconazole Macropus rufogriseus / Red-necked wallaby 37 Macropus / Wallaby/kangaroo/wallaroo 41 Itraconazole Megascops asio / Eastern screech owl 37 Megascops / Owl 38 Itraconazole Pelecanus occidentalis / Brown pelican 37 Pelecanus / Pelican 83 Itraconazole Tangara mexicana / Turquoise tanager 37 Tangara / Tanager 73 Itraconazole Tremarctos ornatus / Spectacled bear 37 Tremarctos / Spectacled bear 37 Itraconazole Macropus rufogriseus / Red-necked wallaby 36 Macropus / Wallaby/kangaroo/wallaroo 75 Itraconazole Anas platyrhynchos / 35 Anas / Black /wigeon/teal 103 Itraconazole Irena puella / Fairy bluebird 34 Irena / Fairy bluebird 34 Itraconazole Meleagris gallopavo / 34 Meleagris / Wild turkey 35 Itraconazole Tragopan caboti / Cabot's tragopan 34 Tragopan / Tragopan 69 Terbinafine Anas platyrhynchos / Mallard 33 Anas / Black duck/wigeon/teal 49 Terbinafine Aptenodytes patagonicus / King penguin 33 Aptenodytes / Penguin 33 Fluconazole Panthera leo / 33 Panthera / Lion///tiger 52 Itraconazole Dacelo novaeguineae / Laughing 32 Dacelo / Giant 34 Itraconazole Athene cunicularia / Burrowing owl 31 Athene / Little owl 34 Itraconazole Geronticus eremita / Waldrapp ibis 31 Geronticus / Ibis 31 Itraconazole Histrionicus histrionicus / Harlequin duck 31 Histrionicus / Harlequin duck 31 Itraconazole Nestor notabilis / Kea 31 Nestor / Kea/kaka 36 Itraconazole Pygoscelis adeliae / Adelie penguin 31 Pygoscelis / Penguin 406 Terbinafine Equus caballus / 30 Equus / Horse//ass/mule//burro 32 Itraconazole Podargus strigoides / Tawny frogmouth 30 Podargus / Frogmouth 30 Itraconazole Cygnus melanocoryphus / Black-necked swan 29 Cygnus / Swan 181 Fluconazole Haliaeetus leucocephalus / Bald eagle 29 Haliaeetus / Eagle 29 Itraconazole Lemur catta / Ring-tailed lemur 29 Lemur / Lemur 29 Itraconazole Leucopsar rothschildi / mynah 29 Leucopsar / mynah 29 Itraconazole Lophodytes cucullatus / Hooded merganser 29 Lophodytes / Hooded merganser 29 Salicylic acid Odobenus rosmarus / Walrus 29 Odobenus / Walrus 29 Itraconazole Papio hamadryas / Hamadryas baboon 29 Papio / Baboon 29 Itraconazole Pavo cristatus / Common peafowl 29 Pavo / Peacock 29 Itraconazole Erythrura gouldiae / Gouldian finch 28 Erythrura / finch 31 Itraconazole Macropus rufus / Red kangaroo 28 Macropus / Wallaby/kangaroo/wallaroo 75 Fluconazole Tremarctos ornatus / Spectacled bear 28 Tremarctos / Spectacled bear 28 Posaconazole Gorilla gorilla / Western gorilla 27 Gorilla / Gorilla 27 Itraconazole Goura victoria / Victoria crowned pigeon 27 Goura / Crowned pigeon 30 Itraconazole Ptilinopus pulchellus / Beautiful 27 Ptilinopus / Fruit dove 58 Voriconazole Spheniscus demersus / Jackass penguin 27 Spheniscus / Penguin 361 Itraconazole Argusianus argus / Great argus 26 Argusianus / Great argus 26 Terbinafine Eudyptes moseleyi / Northern rockhopper penguin 26 Eudyptes / Penguin 140 Fluconazole Myrmecophaga tridactyla / 26 Myrmecophaga / Giant anteater 26 Fluconazole Phascolarctos cinereus / 26 Phascolarctos / Koala 26 Itraconazole Somateria mollissima / Eider 26 Somateria / Eider 203 Itraconazole Zalophus californianus / California sealion 26 Zalophus / Sealion 26 Fluconazole Gallus gallus / Red junglefowl 25 Gallus / Junglefowl 25 Itraconazole Platalea ajaja / Roseate spoonbill 25 Platalea / Spoonbill 42 Itraconazole Pogona vitticeps / Inland bearded dragon 25 Pogona / Bearded dragon 33 Itraconazole Dendrocygna bicolor / Fulvous whistling duck 24 Dendrocygna / Whistling duck 62 Itraconazole Gopherus agassizii / Desert tortoise 24 Gopherus / Gopher tortoise 24 Itraconazole Parabuteo unicinctus / Harris' hawk/bay-winged hawk 24 Parabuteo / Harris' hawk/bay-winged hawk 24 Itraconazole Rhabdotorrhinus corrugatus / Wrinkled 24 Rhabdotorrhinus / Horbill 24 Ketoconazole Tremarctos ornatus / Spectacled bear 24 Tremarctos / Spectacled bear 24 Itraconazole Uncia uncia / leopard 24 Uncia / 24 Fluconazole Varecia rubra / Red ruffed lemur 24 Varecia / Ruffed lemur 40 Itraconazole Ardea herodias / Great blue heron 23 Ardea / Heron 31 Itraconazole Cosmopsarus regius / Golden-breasted starling 23 Cosmopsarus / Starling 23 Itraconazole Ephippiorhynchus senegalensis / Saddle-billed stork 23 Ephippiorhynchus / Stork 23 Fluconazole Lama glama / 23 Lama / Llama// 30 Terbinafine Milvus migrans / Black kite 23 Milvus / Kite 23 Itraconazole Mycteria americana / Wood stork 23 Mycteria / Stork 32 Itraconazole Ramphastos swainsonii / Chestnut-mandibled toucan 23 Ramphastos / Toucan 43 Itraconazole Saimiri boliviensis / Black-capped squirrel 23 Saimiri / Squirrel monkey 29 Fluconazole Alouatta caraya / Black howler 22 Alouatta / Howler 22 Flucytosine Aptenodytes patagonicus / King penguin 22 Aptenodytes / Penguin 22 Itraconazole Bucephala islandica / Barrow's goldeneye 22 Bucephala / Goldeneye 41 Ketoconazole Canis lupus / Gray 22 Canis / Wolf//jackal/dog 23 Itraconazole Paradisaea rubra / Red -of-paradise 22 Paradisaea / Bird-of-paradise 57 Itraconazole cinnamominus / Guam kingfisher 22 Todiramphus / Kingfisher 22 Itraconazole Eclectus roratus / Eclectus parrot 21 Eclectus / Eclectus parrot 21 Clotrimazole Equus caballus / Horse 21 Equus / Horse/zebra/ass/mule/donkey/burro 21 Fluconazole Halichoerus grypus / Grey seal 21 Halichoerus / Grey seal 21 Itraconazole Momotus momota / Blue-crowned motmot 21 Momotus / Crowned motmot 21 Itraconazole Vulpes zerda / Fennec fox 21 Vulpes / Fox 21 Itraconazole Aix sponsa / North American 20 Aix / Wood duck 29 Itraconazole Ara macao / 20 Ara / Macaw 78 Amphotericin B Ateles geoffroyi / Black-handed spider monkey 20 Ateles / Spider monkey 20 Itraconazole Chauna torquata / Southern screamer 20 Chauna / Screamer 20 Itraconazole Cygnus columbianus / Tundra Swan 20 Cygnus / Swan 181 Griseofulvin Gorilla gorilla / Western gorilla 20 Gorilla / Gorilla 20 Amphotericin B Milvus migrans / Black kite 20 Milvus / Kite 20 Itraconazole Notophthalmus viridescens / Eastern newt 20 Notophthalmus / Newt 36 Itraconazole Paradisaea minor / Lesser bird-of-paradise 20 Paradisaea / Bird-of-paradise 57 Fluconazole Phacochoerus africanus / Warthog 20 Phacochoerus / Warthog 20 Itraconazole Acinonyx jubatus / 19 Acinonyx / Cheetah 19 Itraconazole Ardeotis kori / Kori bustard 19 Ardeotis / Bustard 19 Itraconazole Caloenas nicobarica / Nicobar pigeon 19 Caloenas / Nicobar pigeon 19 Terbinafine Chrysolophus pictus / 19 Chrysolophus / Ruffed pheasant 19 Itraconazole Ciconia ciconia / 19 Ciconia / Old World stork 31 Itraconazole Corvus corax / Raven 19 Corvus / Crow/raven 33 Itraconazole Cygnus cygnus / Whooper swan 19 Cygnus / Swan 181 Voriconazole Eudyptes chrysolophus / Macaroni penguin 19 Eudyptes / Penguin 19 Itraconazole Euphonia violacea / Violaceous euphonia 19 Euphonia / Euphonia 19 Fluconazole Gorilla gorilla / Western gorilla 19 Gorilla / Gorilla 19 Amphotericin B Megascops asio / Eastern screech owl 19 Megascops / Owl 19 Itraconazole Phascolarctos cinereus / Koala 19 Phascolarctos / Koala 19 Itraconazole Strix varia / Barred owl 19 Strix / Owl 57 Itraconazole Tragopan temminckii / Temminck's tragopan 19 Tragopan / Tragopan 69 Itraconazole Ursus maritimus / 19 Ursus / Bear 24 Itraconazole Acryllium vulturinum / Vulturine guineafowl 18 Acryllium / Vulturine guineafowl 18 Terbinafine Aldabrachelys gigantea / Aldabra tortoise 18 Aldabrachelys / Tortoise 18 Amphotericin B Anas platyrhynchos / Mallard 18 Anas / Black duck/wigeon/teal 18 Itraconazole Ara ararauna / Blue-and-yellow macaw 18 Ara / Macaw 78 Terbinafine Bubo bubo / Eurasian eagle owl 18 Bubo / Eagle owl 65 Terbinafine Buceros bicornis / Great Indian hornbill 18 Buceros / Hornbill 18 Itraconazole Burhinus superciliaris / Peruvian thick-knee 18 Burhinus / Thick-knee 19 Griseofulvin Capra hircus / Goat 18 Capra / Goat/ibex/markhor 18 Itraconazole Chrysolophus pictus / Golden pheasant 18 Chrysolophus / Ruffed pheasant 20 Itraconazole Cyanerpes cyaneus / Red-legged honeycreeper 18 Cyanerpes / Honeycreeper 22 Itraconazole Dromaius novaehollandiae / Emu 18 Dromaius / Emu 18 Fluconazole Okapia johnstoni / Okapi 18 Okapia / Okapi 18 Itraconazole Oxyura jamaicensis / Ruddy duck 18 Oxyura / Duck 23 Itraconazole Pelecanus erythrorhynchos / American white pelican 18 Pelecanus / Pelican 83 Itraconazole Pelecanus rufescens / Pink-backed pelican 18 Pelecanus / Pelican 83 Itraconazole Tyto alba / Common 18 Tyto / Barn owl 22 Itraconazole Uria aalge / Common murre 18 Uria / Murre 21 Itraconazole Aythya americana / Redhead 17 Aythya / Scaup/pochard 57 Itraconazole Balearica regulorum / Grey crowned-crane 17 Balearica / African crowned crane 23 Itraconazole Callonetta leucophrys / Ringed teal 17 Callonetta / Ringed teal 17 Itraconazole Chalcophaps indica / Grey-capped emerald dove 17 Chalcophaps / Dove/pigeon 17 Itraconazole Fratercula corniculata / Horned puffin 17 Fratercula / Puffin 83 Itraconazole Lophura edwardsi / Edward's pheasant 17 Lophura / Gallopheasant 29 Itraconazole Polyplectron malacense / Malayan peacock pheasant 17 Polyplectron / Peacock pheasant 31 Itraconazole Psophia crepitans / Grey-winged trumpeter 17 Psophia / Trumpeter 17 Itraconazole Sarcoramphus papa / King vulture 17 Sarcoramphus / King vulture 17 Terbinafine Vultur gryphus / Andean condor 17 Vultur / Andean condor 17 Terbinafine Argusianus argus / Great argus 16 Argusianus / Great argus 16 Itraconazole Crax globulosa / Wattled curassow 16 Crax / Curassow 33 Itraconazole Dendrocygna autumnalis / Black-bellied whistling duck 16 Dendrocygna / Whistling duck 62 Terbinafine Eudyptes chrysocome / Southern rockhopper penguin 16 Eudyptes / Penguin 140 Amphotericin B Halichoerus grypus / Grey seal 16 Halichoerus / Grey seal 16 Itraconazole Nasua narica / White-nosed 16 Nasua / Coati 16 Fluconazole Nomascus gabriellae / Buff-cheeked gibbon 16 Nomascus / Gibbon 17 Itraconazole Numida meleagris / Helmeted guineafowl 16 Numida / Helmeted guineafowl 16 Itraconazole Pulsatrix perspicillata / Spectacled owl 16 Pulsatrix / Owl 16 Itraconazole Ramphiculus jambu / Jambu fruit-dove 16 Ramphiculus / Fruit dove 16 Miconazole Ambystoma tigrinum / Tiger salamander 15 Ambystoma / Mole salamander 15 Itraconazole Anser cygnoid / Swan goose 15 Anser / Goose 42 Itraconazole Cariama cristata / Red-legged seriema 15 Cariama / Red-legged seriema 15 Itraconazole Chelonoidis denticulata / Yellow-footed tortoise 15 Chelonoidis / Tortoise 19 Itraconazole Dendrocygna viduata / White-faced whistling duck 15 Dendrocygna / Whistling duck 62 Itraconazole Falco sparverius / American kestrel/sparrowhawk 15 Falco / Kestrel/falcon 84 Itraconazole Garrulax leucolophus / White-crested laughing thrush 15 Garrulax / Laughing thrush 37 Griseofulvin Lontra canadensis / North American river otter 15 Lontra / River otter 15 Miconazole Oryctolagus cuniculus / 15 Oryctolagus / European rabbit 15 Itraconazole Panthera tigris / Tiger 15 Panthera / Lion/leopard/jaguar/tiger 29 Itraconazole Pantherophis guttatus / Corn 15 Pantherophis / Rat snake 18 Itraconazole Phyllobates terribilis / Golden poison dart frog 15 Phyllobates / Poison dart frog 21 Itraconazole Platalea alba / African spoonbill 15 Platalea / Spoonbill 42 Itraconazole Anas acuta / Northern pintail 14 Anas / Black duck/wigeon/teal 103 Itraconazole Ara militaris / Military macaw 14 Ara / Macaw 78 Terbinafine Falco peregrinus / Peregrine falcon 14 Falco / Kestrel/falcon 21 Itraconazole Nerodia sipedon / Northern watersnake 14 Nerodia / Watersnake 25 Itraconazole Paradisaea raggiana / Raggiana bird-of-paradise 14 Paradisaea / Bird-of-paradise 57 Itraconazole Pitta sordida / Hooded pitta 14 Pitta / Pitta 14 Itraconazole Procavia capensis / Rock hyrax 14 Procavia / Rock hyrax 14 Itraconazole Pteronura brasiliensis / 14 Pteronura / Giant otter 14 Fluconazole Spheniscus humboldti / Humboldt penguin 14 Spheniscus / Penguin 327 Fluconazole Spheniscus demersus / Jackass penguin 14 Spheniscus / Penguin 327 Miconazole Actinemys marmorata / Pacific pond turtle 13 Actinemys / Pond turtle 13 Clotrimazole Ailurus fulgens / Red panda 13 Ailurus / Red panda 13 Itraconazole Alopochen aegyptiaca / Egyptian goose 13 Alopochen / Egyptian goose 13 Itraconazole Ampeliceps coronatus / Golden-crested mynah 13 Ampeliceps / Golden-crested mynah 13 Itraconazole Anaxyrus americanus / American toad 13 Anaxyrus / Toad 126 Itraconazole Antigone canadensis / 13 Antigone / Crane 29 Itraconazole Atelerix albiventris / Four-toed hedgehog 13 Atelerix / Hedgehog 13 Terbinafine Gallirallus owstoni / 13 Gallirallus / Weka 14 Itraconazole Haliaeetus pelagicus / Steller's Sea-eagle 13 Haliaeetus / Eagle 186 Itraconazole Hyla versicolor / Grey tree frog 13 Hyla / Tree frog 21 Fluconazole Lycaon pictus / African hunting dog 13 Lycaon / African hunting dog 13 Voriconazole Pygoscelis papua / Gentoo penguin 13 Pygoscelis / Penguin 13 Itraconazole Aegypius monachus / Cinereous vulture 12 Aegypius / Cinereous vulture 12 Itraconazole Ara chloropterus / Green-winged macaw 12 Ara / Macaw 78 Itraconazole Bubo bubo / Eurasian eagle owl 12 Bubo / Eagle owl 155 Itraconazole Bucephala clangula / Common goldeneye 12 Bucephala / Goldeneye 41 Itraconazole Buceros bicornis / Great Indian hornbill 12 Buceros / Hornbill 15 Fluconazole Callithrix geoffroyi / White-fronted marmoset 12 Callithrix / Short-tusked marmoset 12 Itraconazole Choloepus hoffmanni / Hoffmann's two-toed 12 Choloepus / Two-toed sloth 17 Itraconazole Dendrobates tinctorius / Dyeing poison frog 12 Dendrobates / Poison dart frog 23 Miconazole Elephas maximus / 12 Elephas / Asian elephant 12 Itraconazole Eudocimus albus / White ibis 12 Eudocimus / Ibis 49 Amphotericin B Eudyptes chrysocome / Southern rockhopper penguin 12 Eudyptes / Penguin 12 Miconazole Giraffa camelopardalis / 12 Giraffa / Giraffe 12 Itraconazole Litoria caerulea / White's tree frog 12 Litoria / Tree frog 12 Terbinafine Megascops asio / Eastern screech owl 12 Megascops / Owl 12 Itraconazole Pan troglodytes / 12 Pan / Chimpanzee 12 Itraconazole Phoeniconaias minor / Lesser flamingo 12 Phoeniconaias / Lesser flamingo 12 Itraconazole Polyplectron napoleonis / Palawan peacock pheasant 12 Polyplectron / Peacock pheasant 31 Itraconazole Rhinella marina / Cane toad 12 Rhinella / Toad 12 Itraconazole Strix nebulosa / Great grey owl 12 Strix / Owl 57 Ketoconazole Struthio camelus / 12 Struthio / Ostrich 12 Terbinafine Trichoglossus haematodus / Coconut lorikeet 12 Trichoglossus / Lory 18 Fluconazole Tursiops truncatus / Bottlenose dolphin 12 Tursiops / Bottlenose dolphin 12 Itraconazole Anas undulata / Yellow-billed duck 11 Anas / Black duck/wigeon/teal 103 Itraconazole Aythya baeri / Baer's pochard 11 Aythya / Scaup/pochard 57 Itraconazole Branta ruficollis / Red-breasted goose 11 Branta / Goose 33 Itraconazole Casuarius casuarius / Southern cassowary 11 Casuarius / Cassowary 11 Miconazole Cavia porcellus / Guinea 11 Cavia / Cavy/guinea pig 12 Itraconazole Cygnus olor / Mute swan 11 Cygnus / Swan 181 Miconazole Equus caballus / Horse 11 Equus / Horse/zebra/ass/mule/donkey/burro 19 Itraconazole Lamprotornis superbus / Superb starling 11 Lamprotornis / Glossy starling 19 Itraconazole Leptoptilos crumenifer / Marabou stork 11 Leptoptilos / Adjutant stork 21 Itraconazole Necrosyrtes monachus / Hooded vulture 11 Necrosyrtes / Hooded vulture 11 Itraconazole Neophema splendida / Scarlet-chested parrot 11 Neophema / Parrot 13 Terbinafine Pelecanus occidentalis / Brown pelican 11 Pelecanus / Pelican 30 Itraconazole Phoenicopterus roseus / 11 Phoenicopterus / Flamingo 159 Itraconazole Pongo pygmaeus / 11 Pongo / Orangutan 13 Itraconazole Ptilinopus roseicapilla / Pink-crowned fruit dove 11 Ptilinopus / Fruit dove 58 Amphotericin B Pygoscelis papua / Gentoo penguin 11 Pygoscelis / Penguin 11 Itraconazole Ramphastos toco / Toco toucan 11 Ramphastos / Toucan 43 Itraconazole Rana catesbeiana / American bullfrog 11 Rana / Frog 66 Itraconazole Rana pipiens / Northern leopard frog 11 Rana / Frog 66 Clotrimazole Spheniscus magellanicus / Magellanic penguin 11 Spheniscus / Penguin 32 Terbinafine Struthio camelus / Common ostrich 11 Struthio / Ostrich 11 Itraconazole Tangara gyrola / Bay-headed tanager 11 Tangara / Tanager 73 Itraconazole Tragopan satyra / Satyr tragopan 11 Tragopan / Tragopan 69 Terbinafine Tyto alba / Common barn owl 11 Tyto / Barn owl 11 Itraconazole Bambusicola fytchii / Bamboo partridge 10 Bambusicola / Bamboo partridge 12 Itraconazole Cathartes aura / Turkey vulture 10 Cathartes / Vulture 10 Itraconazole Coscoroba coscoroba / Coscoroba swan 10 Coscoroba / Coscoroba swan 10 Griseofulvin Equus asinus / Donkey 10 Equus / Horse/zebra/ass/mule/donkey/burro 16 Terbinafine Gallus gallus / Red junglefowl 10 Gallus / Junglefowl 10 Terbinafine Irena puella / Fairy bluebird 10 Irena / Fairy bluebird 10 Itraconazole Lophophorus impejanus / Himalayan impeyan 10 Lophophorus / Monal 10 pheasant Clotrimazole Phoca vitulina / Harbor seal 10 Phoca / Harbor seal 10 Terbinafine Phoenicopterus ruber / American flamingo 10 Phoenicopterus / Flamingo 20 Itraconazole Polihierax semitorquatus / African pygmy falcon 10 Polihierax / Pygmy falcon 10 Miconazole Pongo abelii / Sumatran orangutan 10 Pongo / Orangutan 11 Terbinafine Rollulus rouloul / Crested wood partridge 10 Rollulus / Crested wood partridge 10 Itraconazole Struthio camelus / Common ostrich 10 Struthio / Ostrich 10 Clotrimazole Tolypeutes matacus / Southern three-banded armadillo 10 Tolypeutes / Three-banded armadillo 10 Fluconazole Trichoglossus forsteni / Scaley-breasted lorikeet 10 Trichoglossus / Lory 17 Itraconazole natans / Aquatic 10 Typhlonectes / Caecilian 10 Itraconazole Varecia rubra / Red ruffed lemur 10 Varecia / Ruffed lemur 11 Itraconazole Vultur gryphus / Andean condor 10 Vultur / Andean condor 10 Itraconazole Aix galericulata / Mandarin duck 9 Aix / Wood duck 29 Itraconazole Ambystoma californiense / California tiger salamander 9 Ambystoma / Mole salamander 95 Terbinafine Anodorhynchus hyacinthinus / 9 Anodorhynchus / Macaw 9 Itraconazole Anser anser / Greylag goose 9 Anser / Goose 42 Fluconazole Arctocephalus pusillus / Afro-Australian fur seal 9 Arctocephalus / Southern fur seal 9 Itraconazole Ardea goliath / Goliath heron 9 Ardea / Heron 31 Itraconazole Atelopus varius / Painted frog 9 Atelopus / Painted frog 529 Itraconazole Aythya nyroca / Common white-eye 9 Aythya / Scaup/pochard 57 Itraconazole Balearica pavonina / Black crowned-crane 9 Balearica / African crowned crane 23 Itraconazole Butorides virescens / Green heron 9 Butorides / Green heron 9 Terbinafine Callonetta leucophrys / Ringed teal 9 Callonetta / Ringed teal 9 Itraconazole Copsychus malabaricus / Common shama thrush 9 Copsychus / Shama 16 Itraconazole Coragyps atratus / Black vulture 9 Coragyps / Black vulture 9 Terbinafine Corvus corax / Raven 9 Corvus / Crow/raven 9 Itraconazole Gallirallus philippensis / Buff-banded rail 9 Gallirallus / Weka 9 Terbinafine Geronticus eremita / Waldrapp ibis 9 Geronticus / Ibis 12 Itraconazole Gonocephalus chamaeleontinus / forest 9 Gonocephalus / Dragon 10 dragon Terbinafine Harpia harpyja / Harpy eagle 9 Harpia / Harpy eagle 9 Itraconazole Hypergerus atriceps / Oriole warbler 9 Hypergerus / Oriole warbler 9 Itraconazole Lepidochelys kempii / Atlantic Ridley turtle 9 Lepidochelys / Ridley turtle 11 Itraconazole Lophura ignita / Crested pheasant 9 Lophura / Gallopheasant 29 Griseofulvin Martes pennanti / Fisher 9 Martes / Marten/fisher 9 Itraconazole Musophaga rossae / Lady Ross' turaco 9 Musophaga / Plantain-eater 12 Itraconazole Mycteria ibis / Yellow-billed stork 9 Mycteria / Stork 32 Miconazole Panthera tigris / Tiger 9 Panthera / Lion/leopard/jaguar/tiger 14 Itraconazole Pluvianus aegyptius / -bird 9 Pluvianus / Egyptian plover 9 Itraconazole Pteroglossus viridis / Green aracari 9 Pteroglossus / Aracari 13 Itraconazole Pteropus giganteus / Indian flying fox 9 Pteropus / Flying fox 15 Itraconazole Rattus norvegicus / Norway rat 9 Rattus / Rat 9 Itraconazole Rhynchopsitta pachyrhyncha / Thick-billed parrot 9 Rhynchopsitta / Parrot 9 Itraconazole Somateria spectabilis / King eider 9 Somateria / Eider 203 Terbinafine Speothos venaticus / 9 Speothos / Bush dog 9 Itraconazole Sterna hirundo / Common tern 9 Sterna / Tern 10 Itraconazole Alligator sinensis / Chinese alligator 8 Alligator / Alligator 8 Itraconazole Amazona leucocephala / Cuban amazon 8 Amazona / Amazon 42 Itraconazole Anthropoides virgo / Demoiselle crane 8 Anthropoides / Crane 20 Itraconazole Aonyx cinereus / Asian small-clawed otter 8 Aonyx / Otter 8 Terbinafine Aquila chrysaetos / Golden eagle 8 Aquila / Eagle 8 Itraconazole Aratinga solstitialis / Sun conure 8 Aratinga / Conure 8 Itraconazole Bombina orientalis / Oriental fire-bellied toad 8 Bombina / Fire-bellied toad 8 Terbinafine Cariama cristata / Red-legged seriema 8 Cariama / Red-legged seriema 8 Terbinafine Cosmopsarus regius / Golden-breasted starling 8 Cosmopsarus / Starling 8 Itraconazole Didelphis virginiana / Virginia opossum 8 Didelphis / Large American opossum 8 Itraconazole Dryonastes courtoisi / Blue-crowned laughing thrush 8 Dryonastes / Laughing thrush 8 Flucytosine Eudyptes chrysocome / Southern rockhopper penguin 8 Eudyptes / Penguin 27 Itraconazole Fratercula arctica / Atlantic puffin 8 Fratercula / Puffin 83 Itraconazole Furcifer pardalis / panther chameleon 8 Furcifer / Chameleon 10 Terbinafine Gorilla gorilla / Western gorilla 8 Gorilla / Gorilla 8 Ketoconazole Halichoerus grypus / Grey seal 8 Halichoerus / Grey seal 8 Miconazole Loxodonta africana / African elephant 8 Loxodonta / African elephant 8 Terbinafine Macropus rufogriseus / Red-necked wallaby 8 Macropus / Wallaby/kangaroo/wallaroo 23 Clotrimazole Macropus eugenii / Tammar wallaby 8 Macropus / Wallaby/kangaroo/wallaroo 13 Itraconazole Melopsittacus undulatus / Budgerigar 8 Melopsittacus / Budgerigar 9 Itraconazole Mergellus albellus / Smew 8 Mergellus / Merganser 8 Itraconazole Otidiphaps nobilis / Pheasant pigeon 8 Otidiphaps / Pheasant pigeon 10 Itraconazole Podocnemis expansa / Arrau turtle 8 Podocnemis / South American side-necked river 10 turtle Itraconazole Psarisomus dalhousiae / Long-tailed broadbill 8 Psarisomus / Long-tailed broadbill 8 Itraconazole Psarocolius decumanus / Crested oropendola 8 Psarocolius / Oropendola 12 Itraconazole Pseudacris regilla / Pacific tree frog 8 Pseudacris / Chorus frog 16 Itraconazole Rana sylvatica / Wood frog 8 Rana / Frog 66 Itraconazole Suricata suricatta / Slender-tailed 8 Suricata / Slender-tailed meerkat 8 Itraconazole Taeniopygia bichenovii / Double-barred finch 8 Taeniopygia / Finch 12 Itraconazole Tiliqua rugosa / Shingleback skink 8 Tiliqua / Skink 19 Itraconazole Tiliqua scincoides / Blue-tongued skink 8 Tiliqua / Skink 19 Terbinafine Uria aalge / Common murre 8 Uria / Murre 15 Griseofulvin Ailurus fulgens / Red panda 7 Ailurus / Red panda 7 Fluconazole Ailurus fulgens / Red panda 7 Ailurus / Red panda 7 Itraconazole Anas bernieri / Madagascar teal 7 Anas / Black duck/wigeon/teal 103 Itraconazole Anaxyrus boreas / Boreal toad 7 Anaxyrus / Toad 126 Itraconazole Anseranas semipalmata / Magpie goose 7 Anseranas / Magpie goose 7 Itraconazole Antigone vipio / White-naped crane 7 Antigone / Crane 29 Terbinafine Aonyx cinereus / Asian small-clawed otter 7 Aonyx / Otter 7 Terbinafine Athene cunicularia / Burrowing owl 7 Athene / Little owl 7 Itraconazole Branta sandvicensis / Ne-ne 7 Branta / Goose 33 Itraconazole Bycanistes bucinator / Trumpeter hornbill 7 Bycanistes / Hornbill 15 Itraconazole Cacatua leadbeateri / Mitchell's 7 Cacatua / Cockatoo 26 Ketoconazole Capra hircus / Goat 7 Capra / Goat/ibex/markhor 7 Itraconazole Cavia porcellus / Guinea pig 7 Cavia / Cavy/guinea pig 8 Itraconazole Chamaeleo calyptratus / Veiled chameleon 7 Chamaeleo / Chameleon 8 Itraconazole Chelonia mydas / Green turtle 7 Chelonia / Green turtle 7 Itraconazole Cyanerpes caeruleus / Purple honeycreeper 7 Cyanerpes / Honeycreeper 22 Itraconazole Cyanoramphus unicolor / Antipodes green parakeet 7 Cyanoramphus / Parakeet 12 Miconazole Didelphis virginiana / Virginia opossum 7 Didelphis / Large American opossum 7 Itraconazole Eidolon helvum / African straw-coloured fruit bat 7 Eidolon / Straw-coloured fruit bat 7 Itraconazole Erethizon dorsatum / North American porcupine 7 Erethizon / North American porcupine 7 Itraconazole Eurypyga helias / Sunbittern 7 Eurypyga / Sunbittern 7 Terbinafine Fratercula corniculata / Horned puffin 7 Fratercula / Puffin 56 Itraconazole Geococcyx californianus / Roadrunner 7 Geococcyx / Roadrunner 7 Terbinafine Gopherus agassizii / Desert tortoise 7 Gopherus / Gopher tortoise 7 Voriconazole Haliaeetus leucocephalus / Bald eagle 7 Haliaeetus / Eagle 7 Ketoconazole Lemur catta / Ring-tailed lemur 7 Lemur / Lemur 7 Terbinafine Mandrillus sphinx / Mandrill 7 Mandrillus / Drill/mandrill 7 Itraconazole Necturus maculosus / Mudpuppy 7 Necturus / Waterdog 7 Itraconazole Neochen jubata / Orinoco goose 7 Neochen / Orinoco goose 7 Itraconazole Nerodia fasciata / Southern watersnake 7 Nerodia / Watersnake 25 Terbinafine Parabuteo unicinctus / Harris' hawk/bay-winged hawk 7 Parabuteo / Harris' hawk/bay-winged hawk 7 Itraconazole Ptilinopus porphyrea / Temminck's fruit dove 7 Ptilinopus / Fruit dove 58 Terbinafine Ramphastos sulfuratus / Keel-billed toucan 7 Ramphastos / Toucan 16 Terbinafine Terathopius ecaudatus / Bateleur eagle 7 Terathopius / Bateleur eagle 7 Itraconazole Theloderma corticale / Tonkin bug-eyed frog 7 Theloderma / Tree frog 7 Itraconazole Tockus deckeni / Von der Decken's hornbill 7 Tockus / Hornbill 18 Itraconazole Torgos tracheliotos / Lappet-faced vulture 7 Torgos / Lappet-faced vulture 7 Itraconazole Amazona oratrix / Yellow-headed amazon 6 Amazona / Amazon 42 Itraconazole Anas erythrorhyncha / Red-billed pintail 6 Anas / Black duck/wigeon/teal 103 Itraconazole Anser indicus / Bar-headed goose 6 Anser / Goose 42 Itraconazole Anthropoides paradiseus / Stanley crane 6 Anthropoides / Crane 20 Terbinafine Ara militaris / Military macaw 6 Ara / Macaw 18 Terbinafine Balearica regulorum / Grey crowned-crane 6 Balearica / African crowned crane 7 Griseofulvin Bos taurus / Cow/ox 6 Bos / Cow/// 6 Griseofulvin depressicornis / 6 Bubalus / Asiatic buffalo 6 Itraconazole Bucorvus leadbeateri / Southern ground hornbill 6 Bucorvus / Ground hornbill 9 Itraconazole Buteo platypterus / Broad-winged hawk 6 Buteo / Hawk 113 Itraconazole Buteo swainsonii / Swainson's hawk 6 Buteo / Hawk 113 Miconazole Canis lupus / Gray wolf 6 Canis / Wolf/coyote/jackal/dog 6 Clotrimazole Capra hircus / Goat 6 Capra / Goat/ibex/markhor 6 Griseofulvin Cavia porcellus / Guinea pig 6 Cavia / Cavy/guinea pig 6 Itraconazole Cinnyricinclus leucogaster / Violet-backed starling 6 Cinnyricinclus / Starling 6 Itraconazole Coracias cyanogaster / Blue-bellied roller 6 Coracias / Roller 12 Itraconazole Corvus brachyrhynchos / Common crow 6 Corvus / Crow/raven 33 Itraconazole Crocuta crocuta / 6 Crocuta / Spotted hyaena 6 Terbinafine Cygnus buccinator / Trumpeter swan 6 Cygnus / Swan 23 Itraconazole Dasypus novemcinctus / Nine-banded armadillo 6 Dasypus / Long-nosed armadillo 6 Itraconazole Dendrobates auratus / Green-and-black poison dart 6 Dendrobates / Poison dart frog 23 frog Terbinafine Eudocimus ruber / Scarlet ibis 6 Eudocimus / Ibis 6 Itraconazole Eupodotis senegalensis / White-bellied bustard 6 Eupodotis / Bustard 6 Itraconazole Guaruba guarouba / Golden conure 6 Guaruba / Conure 6 Itraconazole Gyps africanus / African white-backed vulture 6 Gyps / Vulture 14 Miconazole Halichoerus grypus / Grey seal 6 Halichoerus / Grey seal 6 Itraconazole Hyla cinerea / Green tree frog 6 Hyla / Tree frog 21 Itraconazole Iguana iguana / Green iguana 6 Iguana / Green iguana 6 Itraconazole Malaclemys terrapin / Diamondback terrapin 6 Malaclemys / Diamondback terrapin 6 Clotrimazole Mustela putorius / European polecat 6 Mustela / Weasel/stoat/mink/ermine 6 Miconazole Mustela putorius / European polecat 6 Mustela / Weasel/stoat/mink/ermine 6 Itraconazole Neofelis nebulosa / Clouded leopard 6 Neofelis / Clouded leopard 6 Itraconazole Nycticorax nycticorax / Black-crowned night heron 6 Nycticorax / Night heron 6 Terbinafine Oxyura vittata / Argentine ruddy duck 6 Oxyura / Duck 8 Griseofulvin Pan troglodytes / Chimpanzee 6 Pan / Chimpanzee 6 Itraconazole Pandion haliaetus / Osprey 6 Pandion / Osprey 6 Ketoconazole Panthera tigris / Tiger 6 Panthera / Lion/leopard/jaguar/tiger 11 Terbinafine Petrogale xanthopus / Yellow-footed rock wallaby 6 Petrogale / Rock wallaby 6 Itraconazole Phalacrocorax auritus / Double-crested cormorant 6 Phalacrocorax / Cormorant 13 Itraconazole Phyllobates vittatus / Golfodulcean poison dart frog 6 Phyllobates / Poison dart frog 21 Itraconazole Pipa pipa / Surinam toad 6 Pipa / Surinam toad 7 Itraconazole Poephila acuticauda / Long-tailed finch 6 Poephila / Finch 7 Itraconazole Probosciger aterrimus / 6 Probosciger / Palm cockatoo 6 Itraconazole Pyxicephalus adspersus / African bullfrog 6 Pyxicephalus / Bullfrog 6 Itraconazole Ramphocelus carbo / Silver-beaked tanager 6 Ramphocelus / Tanager 18 Itraconazole Rana pretiosa / Oregon spotted frog 6 Rana / Frog 66 Itraconazole Spatula clypeata / Northern shoveler 6 Spatula / Shoveler 26 Ketoconazole Spheniscus demersus / Jackass penguin 6 Spheniscus / Penguin 6 Itraconazole Strix uralensis / Ural owl 6 Strix / Owl 57 Terbinafine Vulpes zerda / Fennec fox 6 Vulpes / Fox 6 Itraconazole Acris crepitans / Northern cricket frog 5 Acris / Cricket frog 5 Itraconazole Agalychnis callidryas / Red-eyed tree frog 5 Agalychnis / Tree frog 5 Fluconazole Anthropoides paradiseus / Stanley crane 5 Anthropoides / Crane 5 Itraconazole Ara rubrogenys / Red-fronted macaw 5 Ara / Macaw 78 Miconazole Atelerix albiventris / Four-toed hedgehog 5 Atelerix / Hedgehog 5 Itraconazole Branta canadensis / goose 5 Branta / Goose 33 Fluconazole Buceros rhinoceros / Rhinoceros hornbill 5 Buceros / Hornbill 5 Itraconazole Cacatua haematuropygia / Red-vented cockatoo 5 Cacatua / Cockatoo 26 Itraconazole Caretta caretta / Loggerhead turtle 5 Caretta / Loggerhead turtle 5 Itraconazole Ceratobatrachus guentheri / Solomon Islands leaf frog 5 Ceratobatrachus / Frog 5 Itraconazole Charadrius melodus / Piping plover 5 Charadrius / Plover 9 Itraconazole Chelonoidis carbonaria / Red-footed tortoise 5 Chelonoidis / Tortoise 19 Itraconazole Choloepus didactylus / Linne's two-toed sloth 5 Choloepus / Two-toed sloth 17 Ketoconazole Chrysocyon brachyurus / 5 Chrysocyon / Maned wolf 5 Itraconazole Circus cyaneus / Northern harrier 5 Circus / Harrier 5 Itraconazole Colius striatus / Speckled mousebird 5 Colius / Mousebird 5 Itraconazole Copsychus saularis / Magpie robin 5 Copsychus / Shama 16 Clotrimazole Corucia zebrata / Prehensile-tailed skink 5 Corucia / Prehensile-tailed skink 5 Itraconazole cristata / Crested coua 5 Coua / Coua 5 Itraconazole Crax alberti / Blue-billed curassow 5 Crax / Curassow 33 Terbinafine Cygnus melanocoryphus / Black-necked swan 5 Cygnus / Swan 23 Ketoconazole Cygnus buccinator / Trumpeter swan 5 Cygnus / Swan 13 Terbinafine Cygnus atratus / Black swan 5 Cygnus / Swan 23 Terbinafine Dacelo novaeguineae / 5 Dacelo / Giant kingfisher 5 Itraconazole Diceros bicornis / Black rhinoceros 5 Diceros / Black rhinoceros 5 Itraconazole Ducula mullerii / Muller's imperial pigeon 5 Ducula / Imperial pigeon 20 Terbinafine Ephippiorhynchus senegalensis / Saddle-billed stork 5 Ephippiorhynchus / Stork 5 Miconazole Eunectes murinus / 5 Eunectes / Anaconda 5 Terbinafine Falco sparverius / American kestrel/sparrowhawk 5 Falco / Kestrel/falcon 21 Miconazole Furcifer pardalis / panther chameleon 5 Furcifer / Chameleon 5 Miconazole Gallus gallus / Red junglefowl 5 Gallus / Junglefowl 5 Itraconazole Garrulax bicolor / Sumatran laughing thrush 5 Garrulax / Laughing thrush 37 Itraconazole Gavia immer / Common loon 5 Gavia / Loon 10 Itraconazole Gavia stellata / Red-throated loon 5 Gavia / Loon 10 Miconazole Gorilla gorilla / Western gorilla 5 Gorilla / Gorilla 5 Itraconazole Guira guira / Guira 5 Guira / Guira cuckoo 5 Itraconazole Gyps rueppelli / Ruppell's griffon vulture 5 Gyps / Vulture 14 Terbinafine Halichoerus grypus / Grey seal 5 Halichoerus / Grey seal 5 Itraconazole Lampropeltis triangulum / Milksnake 5 Lampropeltis / Kingsnake 6 Terbinafine Lontra canadensis / North American river otter 5 Lontra / River otter 5 Itraconazole Merops bullockoides / White-fronted bee-eater 5 Merops / Bee-eater 5 Terbinafine Nasua narica / White-nosed coati 5 Nasua / Coati 5 Itraconazole Nectophrynoides asperginis / Kihansi spray toad 5 Nectophrynoides / Toad 5 Itraconazole Netta peposaca / Rosybill 5 Netta / Pochard 9 Itraconazole Oena capensis / Namaqua dove 5 Oena / Namaqua dove 5 Miconazole Okapia johnstoni / Okapi 5 Okapia / Okapi 5 Enilconazole Oryctolagus cuniculus / European rabbit 5 Oryctolagus / European rabbit 5 Clotrimazole Pan troglodytes / Chimpanzee 5 Pan / Chimpanzee 5 Miconazole Panthera leo / Lion 5 Panthera / Lion/leopard/jaguar/tiger 14 Terbinafine Phoca vitulina / Harbor seal 5 Phoca / Harbor seal 5 Miconazole Phoca vitulina / Harbor seal 5 Phoca / Harbor seal 5 Fluconazole Phoenicopterus chilensis / Chilean flamingo 5 Phoenicopterus / Flamingo 6 Terbinafine Psittacus erithacus / Grey parrot 5 Psittacus / Grey parrot 5 Itraconazole Ptilinopus melanospilus / Black-naped fruit-dove 5 Ptilinopus / Fruit dove 58 Clotrimazole Rattus norvegicus / Norway rat 5 Rattus / Rat 5 Terbinafine Rhinoceros unicornis / One-horned rhinoceros 5 Rhinoceros / Asian rhinoceros 5 Itraconazole Saimiri sciureus / Common squirrel monkey 5 Saimiri / Squirrel monkey 29 Terbinafine Scissirostrum dubium / Grosbeak starling 5 Scissirostrum / Grosbeak starling 5 Itraconazole Scissirostrum dubium / Grosbeak starling 5 Scissirostrum / Grosbeak starling 5 Flucytosine Spheniscus demersus / Jackass penguin 5 Spheniscus / Penguin 129 Itraconazole Symphalangus syndactylus / Siamang 5 Symphalangus / Siamang 5 Itraconazole Tauraco erythrolophus / Red-crested turaco 5 Tauraco / Turaco 26 Itraconazole Thraupis episcopus / Blue-grey tanager 5 Thraupis / Tanager 5 Itraconazole Tockus erythrorhynchus / Red-billed hornbill 5 Tockus / Hornbill 18 Fluconazole Trichoglossus moluccanus / Australian rainbow 5 Trichoglossus / Lory 17 lorikeet Itraconazole Trogon viridis / Green-backed Trogon 5 Trogon / Trogon 5 Itraconazole Varanus nebulosus / Clouded monitor 5 Varanus / Monitor 14 Fluconazole Vultur gryphus / Andean condor 5 Vultur / Andean condor 5 Species360 Physiological Reference Intervals for Captive Wildlife - 2013 Standard International Units. Switch Units edited by J. Andrew Teare, DVM

Back to Index of Species Tiger Sample Selection Criteria:

(Panthera tigris) • No selection by gender. • All ages combined Samples contributed by 109 • Animal was classified as healthy at the time of institutions. sample collection • Sample was not deteriorated © 2013 - Species360 (Citation Format)

Physiological Reference Intervals for Panthera tigris Referenc Low High Sampl Mea Media Animals Test Units e Sample Sample e n n d Interval a b Sizec White Blood Cell *10^9 5.62 - 10.6 10.17 1.70 24.90 2176 654 Count cells/L 18.66 7 *10^1 Red Blood Cell 4.50 - 2 6.88 6.92 2.16 11.80 2129 628 Count 8.95 cells/L Hemoglobin g/L 82 - 166 131 133 56 220 2175 635 0.245 - 0.39 Hematocrit L/L 0.400 0.117 0.690 2590 682 0.518 6 45.0 - MCV fL 57.7 57.8 35.5 80.5 2067 612 69.1 15.8 - MCH pg 19.2 19.3 13.5 25.0 2018 604 21.9 MCHC g/L 281 - 375 332 334 238 424 2116 622 Segmented *10^9 3.52 - 8.01 7.67 0.03 20.30 2174 654 Neutrophils cells/L 14.47 Neutrophilic *10^9 0.02 - 0.16 0.05 0.00 1.70 2024 646 Band Cells cells/L 1.31 *10^9 0.42 - Lymphocytes 1.65 1.43 0.03 5.33 2142 649 cells/L 4.05 *10^6 Monocytes 74 - 916 335 285 7 1242 1896 624 cells/L *10^6 Eosinophils 63 - 703 250 205 7 909 1705 598 cells/L *10^6 Basophils 6 - 251 92 87 2 321 267 190 cells/L *10^1 0.078 - 0.24 Platelet Count 2 0.235 0.000 0.595 1037 374 0.511 3 cells/L Nucleated Red /100 0 - 9 1 0 0 13 154 106 Blood Cells WBC Reticulocytes % 0.0 - 2.5 0.7 0.1 0.0 4.0 44 30 Referenc Low High Sampl Mea Media Animals Test Units e Sample Sample e n n d Interval a b Sizec mmol/ 4.15 - Glucose 7.87 7.44 0.61 19.03 2489 663 L 14.03 Blood Urea mmol/ 5.7 - 18.3 10.5 10.0 0.7 23.2 2464 662 Nitrogen L µmol/ Creatinine 55 - 370 222 225 0 566 2416 657 L BUN/Cr ratio 5.4 - 30.6 12.8 11.3 0.9 36.8 2308 627 µmol/ Uric Acid 0 - 60 18 12 0 95 414 182 L mmol/ 2.17 - Calcium 2.50 2.48 1.73 3.28 2390 650 L 2.97 mmol/ 1.19 - Phosphorus 1.92 1.83 0.03 3.75 2205 628 L 3.04 Ca/Phos ratio 1.2 - 2.6 1.8 1.7 0.8 3.4 2180 624 mmol/ Sodium 143 - 159 150 150 136 164 2236 627 L mmol/ Potassium 3.5 - 5.3 4.2 4.1 2.5 5.9 2240 630 L 26.8 - Na/K ratio 36.1 36.4 21.7 48.8 2222 625 43.1 mmol/ Chloride 110 - 128 119 119 102 137 2110 597 L Total Protein g/L 53 - 83 71 71 44 98 2079 614 Albumin g/L 25 - 44 36 37 19 52 1962 600 Globulin g/L 20 - 51 34 34 6 62 1968 603 Fibrinogen g/L * 2.18 2.00 0.00 8.00 35 16 Alkaline U/L 6 - 84 27 23 0 98 1992 566 Phosphatase Lactate U/L 37 - 717 237 202 1 950 958 302 Dehydrogenase Aspartate U/L 11 - 63 28 25 2 76 1996 602 Aminotransferase Alanine U/L 18 - 159 67 59 0 196 1838 604 Aminotransferase Creatine Kinase U/L 63 - 636 240 201 2 817 1026 437 Gamma- glutamyltransfera U/L 0 - 10 2 1 0 18 740 328 se 182 - Amylase U/L 1001 865 1 4320 912 384 2737 Lipase U/L 0 - 55 14 9 0 91 437 217 µmol/ Total Bilirubin 0.0 - 8.6 3.3 3.4 0.0 10.3 2099 627 L µmol/ Direct Bilirubin 0.0 - 1.7 0.6 0.0 0.0 1.7 334 175 L µmol/ Indirect Bilirubin 0.0 - 5.5 1.8 1.7 0.0 8.6 332 177 L mmol/ 3.59 - Cholesterol 6.39 6.16 1.81 13.65 2067 592 L 10.25 mmol/ 0.14 - Triglyceride 0.41 0.36 0.06 1.16 1161 376 L 0.96 mmol/ Bicarbonate 9.8 - 20.9 15.3 15.2 8.0 25.0 271 153 L mmol/ 0.462 - 0.88 Magnesium 0.882 0.321 1.549 336 174 L 1.218 4 µmol/ Iron 4.7 - 35.2 17.1 15.7 0.4 40.1 140 74 L mmol/ Carbon Dioxide 9.9 - 20.9 15.7 16.0 6.0 26.0 698 252 L nmol/ Thyroxine 7 - 55 23 18 4 58 159 98 L Referenc Low High Sampl Mea Media Animals Test Units e Sample Sample e n n d Interval a b Sizec Body 36.9 - C 38.8 38.7 34.6 42.7 1258 413 Temperature 41.1 a Lowest sample value used to calculate the reference interval. b Highest sample value used to calculate the reference interval. c Number of samples used to calculate the reference interval. d Number of different individuals contributing to the reference interval.

* Sample size is insufficient to produce a valid reference interval.

Species360 Suite 1040 7900 International Drive Bloomington, MN 55425 U.S.A. www.species360.org

Suggested citation format: Teare, J.A. (ed.): 2013, "Panthera_tigris_No_selection_by_gender__All_ages_ combined_Standard_International_Units__2013_CD.htm l" in ISIS Physiological Reference Intervals for Captive Wildlife: A CD-ROM Resource., Species360 , Bloomington, MN.

Magazine R219 the British Veterinary Zoological Society Opportunities and conservation of a species in its natural and Bat Conservation International. (COIh) and by establishing Acknowledgments to Tony Sainsbury, insurance populations in zoos (COIc). Michael Waters, Marcus Fritze and sample costs for preventing COIh considered costs of land contributors for their practical assistance, vertebrate acquisition and management in the and to Eric Petit and Serena Dool for species’ range country [4], likelihood comments. extinctions of political instability and/or politically motivated violence (including References Dalia A. Conde1,2,3,14,*, terrorism) affecting conservation 1. Fisher, M.C., Henk, D.A., Briggs, C.J., 2,4,14 Brownstein, J.S., Madoff, L.C., McCraw, S.L., Fernando Colchero , operations on the ground, as well as and Gurr, S.J. (2012). Emerging fungal threats Burak Güneralp5, Markus Gusset6, the latent impact of urban expansion to animal, and ecosystem health. Ben Skolnik7, Michael Parr7, on the species’ natural habitat Nature 484, 186–194. 8 9 2. Puechmaille, S.J., Frick, W., Kunz, T.H., Onnie Byers , Kevin Johnson , (Supplemental information). Global 10 11 Racey, P.A., Voigt, C.C., Wibbelt, G., and Glyn Young , Nate Flesness , distribution of the COIh for all AZE Teeling, E.C. (2011). White-Nose Syndrome: Hugh Possingham12, vertebrates is shown in Figure S1 is this emerging disease a threat to European 10,13,14, bats? Trends Ecol. Evol. 26, 570–576. and John E. Fa * (Supplemental information). COIc 3. Farrer, R.A., Weinert, L.A., Bielby, J., included costs of managing a zoo Garner, T.W.J., Balloux, F., Clare, F., Bosch, J., Cunningham, A.A., Weldon, population of at least 500 individuals C., du Preez, L.H., et al. (2011). Multiple Despite an increase in policy and of a species [5], together with a emergences of genetically diverse management responses to the global measure of breeding expertise -infecting chytrids include a globalized hypervirulent recombinant lineage. biodiversity crisis, implementation available for AZE vertebrates in zoos in Proc. Natl. Acad. Sci. USA 108, 18732–18736. of the 20 Aichi Biodiversity Targets the International Species Information 4. Ren, P., Haman, K.H., Last, L.A., still shows insufficient progress [1]. System [6] or, for , bred in Rajkumar, S.S., Keel, M.K., and Chaturvedi, V. (2012). Clonal spread of Geomyces These targets, strategic goals defined Amphibian Ark programs [7]. Although destructans among bats, midwestern and by the United Nations Convention on reintroduction costs are also important southern United States. Emerg. Infect. Dis. Biological Diversity (CBD), address to consider, we did not include these 18, 883–885. 5. Hewitt, G.M. (2000). The genetic legacy of the major causes of biodiversity loss in because of a lack of adequate data. Quaternary ice ages. Nature 405, 907–913. part by establishing protected areas Conservation opportunities for AZE 6. Puechmaille, S.J., Wibbelt, G., Korn, V., Fuller, H., Forget, F., Mühldorfer, K., Kurth, A., (Target 11) and preventing species vertebrates in their natural habitat Bogdanowicz, W., Borel, C., Bosch, T., extinctions (Target 12). To achieve this, were high, given that ~39% of species et al. (2011). Pan-European distribution of increased interventions will be required had high COIh (maximum = 10) values White-Nose Syndrome (Geomyces destructans) not associated with mass for a large number of sites and species. (Figure 1A). Mean (± SD) COIh for all mortality. PLoS One 6, e19167. The Alliance for Zero Extinction (AZE) species was 6.22 ± 1.80 (reptiles (6.89 ± 7. Khankhet, J., Vanderwolf, K.J., [2], a consortium of conservation- 1.64), mammals (6.46 ± 1.79), amphibians McAlpine, D.F., McBurney, S., Overy, D.P., Slavic, D., and Xu, J. (2014). Clonal oriented organisations that aims to (6.19 ± 1.70) and (6.03 ± 2.07)). expansion of the Pseudogymnoascus protect Critically Endangered and Opportunities for management in destructans genotype in North America restricted to single zoos were low for all taxonomic groups is accompanied by significant variation in phenotypic expression. PLoS One 9, sites, has identified 920 species of (Figure 1A). Mean COIc for all species e104684. mammals, birds, amphibians, reptiles, was 2.79 ± 2.88 (maximum = 10) 8. Wibbelt, G., Puechmaille, S.J., Ohlendorf, B., Mühldorfer, K., Bosch, T., Görföl, T., Passior, conifers and reef-building corals in 588 (reptiles (7.06 ± 4.70), birds (3.03 ± 3.01), K., Kurth, A., Lacremans, D., and Forget, F. ‘trigger’ sites [3]. These are arguably amphibians (2.69 ± 2.72) and mammals (2013). Skin lesions in European hibernating the most irreplaceable category of (2.39 ± 2.64)). Overall, 15 species had bats associated with Geomyces destructans, the etiologic agent of White-Nose Syndrome. important biodiversity conservation a high COIh and COIc, and another 15 PLoS One 8, e74105. sites. Protected area coverage of AZE a low COIh and COIc. 9. Warnecke, L., Turner, J.M., Bollinger, sites is a key indicator of progress Total annual costs for effectively T.K., Lorch, J.M., Misra, V., Cryan, P.M., Wibbelt, G., Blehert, D.S., and Willis, C.K.R. towards Target 11 [1]. Moreover, managing all AZE vertebrates in their (2012). Inoculation of bats with European effective conservation of AZE sites natural habitat were US$ 1.18 billion Geomyces destructans supports the novel is essential to achieve Target 12, as (Supplemental information). AZE site pathogen hypothesis for the origin of white- nose syndrome. Proc. Natl. Acad. Sci. USA the loss of any of these sites would costs (per species and year) were 109, 6999–7003. certainly result in the global extinction lowest for reptiles (US$0.59 ± 0.65 x 10. Palmer, J.M., Kubatova, A., Novakova, A., 6 Minnis, A.M., Kolarik, M., and Lindner, D.L. of at least one species [2]. However, 10 ), followed by mammals (US$0.95 ± 6 (2014). Molecular characterization averting human-induced species 1.52 x 10 ), amphibians (US$1.20 ± of a heterothallic mating system in extinctions within AZE sites requires 1.91 x 106) and birds (US$2.53 ± 4.74 x Pseudogymnoascus destructans, the fungus 6 causing White-Nose Syndrome of bats. G3: enhanced planning tools to increase 10 ). These differences were largely Genes|Genomes|Genetics 4. the chances of success [3]. Here, due to variations in total annual costs we assess the potential for ensuring of managing existing protected areas 1Pathology and Pathogen Biology, Royal the long-term conservation of AZE in the more expensive developed Veterinary College, London NW1 0TU, UK. vertebrate species (157 mammals, 165 countries than in developing nations 2Zoological Society of London, London birds, 17 reptiles and 502 amphibians) [4]. By region, estimated AZE site costs NW1 4RY, UK. 3Zoology Institute, Ernst- by calculating a conservation were highest for South America and Moritz-Arndt University, Greifswald opportunity index (COI) for each lowest for northern Africa (Figure 1B). D – 17489, . 4School of Biology & Environmental Science, University College species. The COI encompasses a set Total annual costs for effectively Dublin, Dublin 4, Ireland. of measurable indicators that quantify managing all AZE vertebrates in zoos *E-mail: [email protected] the possibility of achieving successful were US$0.16 billion (Supplemental Current Biology Vol 25 No 6 R220

ABCOI zoo 250 Habitat costs complementary action. This is Zoo costs N = 157 especially crucial for many AZE

55% /year) amphibians, since any neglect 42% 6 3% 10

0 200 400 of investment in insurance zoo 25 populations will likely be insufficient 37 30 0 43% to protect many species from the COI habitat major driver of amphibian declines Mammals 47 35 3 54% 2.5

Total cost ($ Total worldwide — the fungal disease chytridiomycosis [7]. Hence, dedicated 3 1 1 3% 0 resources on a global scale must be Low Mid High

Asia made available in zoological and Europe Oceania E. Africa M. Africa W. Africa N. Africa S. Africa other institutions for developing Caribbean C. America N. AmericaS. America expertise to breed threatened

COI zoo 250 species and for emergency response N = 165 to population declines. However,

48% /year) even if conservation opportunities

45% 6 6%

10 are high for a species, as we show, 0 200 400 25 a lack of timely action will result in 30 31 5 40% failure. A salient example of this COI habitat is the Christmas Island pipistrelle Birds 39 43 5 53% 2.5 (Pipistrellus murrayi), an AZE bat Total cost ($ Total species, which despite possessing one

6 6 0 7% 0 of the highest COIh (9.5) and a COIc of Low Mid High 5.0 became extinct [8]. Successes are Asia

Europe Oceania nonetheless possible, as exemplified E. Africa W. Africa M. Africa N. Africa S. Africa Caribbean N. America S. America C. America by AZE species such as the Mauritius kestrel (Falco punctatus), whooping 250 COI zoo crane (Grus americana), pygmy hog N = 17 (Porcula salvania) and ploughshare /year) 29% 0% 71% 6 tortoise (Astrochelys yniphora) [5]. 10 0 200 400 25 We estimated that for protecting

2 0 7 53% AZE vertebrates around US$1.3

COI habitat million per species is required, a figure

3 0 5 47% tal cost ($ 2.5 that compares well with McCarthy To Reptiles et al.’s [9] modeled median annual costs per species (US$0.85 million, 0 0 0 0% 0 Low Mid High range: US$0.04–8.96 million) to Asia Europe achieve downlisting within 10 years. E. Africa Oceania M. Africa N. Africa S. Africa W. Africa Caribbean C. America S. America N. America Such investment for protecting high- biodiversity value sites and threatened COI zoo 250 species within them is trivial when 49% N = 502 compared to what governments spend

49% /year) 2% 6 globally each year on other sectors. 10 0 200 400 25 There is probably time to protect a large number of AZE vertebrates from 83 99 3 37%

COI habitat extinction. However, at least 15 AZE

tal cost ($ species are in imminent danger given 155 138 8 60% 2.5 To their low COI. Innovative strategies,

Amphibians such as the One Plan approach [10], 6 9 1 3% 0 Low Mid High which combines conservation actions Asia inside and outside a species’ natural Europe Low Mid High 0 200 400 E. Africa M. Africa Oceania W. Africa S. Africa N. Africa Caribbean S. America C. America N. America habitat, must be rapidly implemented. Current Biology Worryingly, however, with less than five years to 2020 to achieve significant Figure 1. Conservation opportunity index (COI) and costs for protecting mammals, birds, rep- protection of these ‘worst-off’ species, tiles and amphibians included in the Alliance for Zero Extinction (AZE). (A) Number of species with a low (0 < COI ≤ 3.33), medium (3.33 < COI ≤ 6.67) or high (6.67 < COI ≤ conservation opportunity evaluations like ours need to be adopted and used 10) COI in zoos (COIc, horizontal barplot) and in their natural habitat (COIh, vertical barplot). (B) Total annual costs for conserving species in their natural habitat and in zoos per region. rapidly to help achieve immediate conservation benefits. information). Costs (per species and Although conservation success is year) were lowest for amphibians and more likely to be achieved through Supplemental Information reptiles (US$0.01 ± 0.00 x 106), followed the protection of the species’ natural Supplemental information including ex- by birds (US$0.35 ± 0.01 x 106) and habitat, safeguarding species in perimental procedures, one figure, three mammals (US$0.62 ± 0.94 x 106). zoos should be considered as a tables, and acknowledgements can be Magazine R221 found with this article online at http://dx.doi. surface orientation could potentially org/10.1016/j.cub.2015.01.048. Coupled provide information about a surface’s material properties. However, identical References computations of 1. Tittensor, D.P., Walpole, M., Hill, S.L., Boyce, luminance gradients can sometimes D.G., Britten, G.L., Burgess, N.D., Butchart, S.H., three-dimensional be generated by surfaces with Leadley, P.W., Regan, E.C., Alkemade, R. et al. different reflectance functions if three- (2014). A mid-term analysis of progress toward international biodiversity targets. Science 346, shape and material dimensional shape and the light field 241–244. are chosen appropriately. For example, 2. Ricketts, T.H., Dinerstein, E., Boucher, T., 1 2 Brooks, T.M., Butchart, S.H., Hoffmann, M., Phillip J. Marlow , Dejan Todorovic´ , a matte surface can generate the Lamoreux, J.F., Morrison, J., Parr, M., Pilgrim, and Barton L. Anderson1 same gradient as the specular surface J.D., et al. (2005). Pinpointing and preventing in Figure 1A if its three-dimensional imminent extinctions. Proc. Natl. Acad. Sci. USA 102, 18497–18501. Retinal image structure arises from surface orientation varies more 3. Alliance for Zero Extinction (2014). AZE the interaction between a surface’s rapidly than the specular surface. If overview. www.zeroextinction.org. 4. Wilson, K.A., Evans, M.C., Di Marco, M., three-dimensional shape, its reflectance the visual system exploits constraints Green, D.C., Boitani, L., Possingham, H.P., and transmittance properties, and imposed by three-dimensional shape Chiozza, F., and Rondinini, C. (2011). Prioritizing the surrounding light field. Any local to derive material properties, then it conservation investments for mammal species globally. Phil. Trans. R. Soc. B. 366, 2670–2680. image structure can be generated should be possible for an identical 5. Fa, J.E., Funk, S.M., and O’Connell, D.M. by an infinite number of different luminance gradient to appear as (2011). Zoo Conservation Biology. (Cambridge: Cambridge University Press). combinations of surface properties, either a matte or specular material by 6. Conde, D.A., Flesness, N., Colchero, F., which suggests that the visual system simply changing the perceived three- Jones, O.R., and Scheuerlein, A. (2011). An must somehow constrain the possible dimensional shape. Previous work has emerging role of zoos to conserve biodiversity. Science 331, 1390–1391. scene interpretations. The research on suggested that specular reflectance 7. Amphibian Ark (2014). Amphibian Ark: Keeping this has searched for such constraints can be derived directly from the two- Threatened Amphibian Species Afloat. http:// www.amphibianark.org. in statistical regularities of two- dimensional images, which implies 8. Martin, T.G., Nally, S., Burbidge, A.A., Arnall, dimensional image structure [1,2]. Here, that the perception of specularity S., Garnett, S.T., Hayward, M.W., Lumsden, we present a new class of displays could be derived prior to any explicit L.F., Menkhorst, P., McDonald-Madden, E., and Possingham, H.P. (2012). Acting fast helps avoid in which the perception of material representation of three-dimensional extinction. Conservation Lett. 5, 274–280. properties cannot be explained with structure [1–7]. 9. McCarthy, D.P., Donald, P.F., Scharlemann, J.P.W., Buchanan, G.M., Balmford, A., Green, J.M.H., two-dimensional image properties. To assess whether the visual Bennun, L.A., Burgess, N.D., Fishpool, L.D.C., The displays manipulate the perceived system exploits three-dimensional Garnett, S.T. et al. (2012). Financial costs three-dimensional shape of identical geometric constraints to derive material of meeting conservation targets: current spending and unmet needs. luminance gratings, and demonstrate properties, we exploited previous Science 338, 946–949. that perceived three-dimensional shape work which showed that perceived 10. Byers, O., Lees, C., Wilcken, J., and Schwitzer, C. (2013). The One Plan approach: the can alter perceived surface reflectance. three-dimensional shape [8–10] and philosophy and implementation of CBSG’s The material properties of a illumination direction [8,10] can be approach to integrated species conservation surface physically constrain the rate altered by manipulating the shape of planning. WAZA Magazine 14, 2–5. that luminance varies with its three- bounding contours. Figure 1B depicts a 1Department of Biology, University of Southern dimensional surface orientation. For pair of identical luminance gratings. The , 5230 Odense M, Denmark. 2Max- simplicity, we restrict attention to only physical difference between the Planck Odense Center on the Biodemography singly-curved surfaces, which project left and right images is the shape of the of Aging, University of Southern Denmark, luminance gradients that only vary bounding contours that flank the grating 5230 Odense M, Denmark. 3Centre for along the direction of the surface along its left and right sides. The shape Research and Conservation, Royal Zoological curves. The steepness of the luminance information provided by the contours Society of Antwerp, 2018 Antwerp, Belgium. 4Department of Mathematics and Computer gradients depends on the surface’s transforms the perceived three- Science, University of Southern Denmark, three-dimensional shape, surrounding dimensional shape and the illumination 5230 Odense M, Denmark. 5Department light field, and reflectance function. The direction of the two surfaces, as has of Geography, Texas A&M University, left side of Figure 1A depicts a matte been shown previously [8–10]. Note, College Station, TX 77843, USA. 6World (Lambertian) surface that projects however, that there is also a clear Association of Zoos and Aquariums (WAZA), a luminance gradient that varies as change in perceived material properties IUCN Conservation Centre, 1196 Gland, Switzerland. 7American Bird Conservancy a cosine of the angle between the of the two surfaces: the left image (ABC), The Plains, VA 20198, USA. 8IUCN surface normal and the direction of the appears matte, whereas the right image SSC Conservation Breeding Specialist incident illumination. The steepness of appears metallic. Group (CBSG), Apple Valley, MN 55124, USA. luminance gradients generated by a To experimentally document these 9Amphibian Ark, c/o IUCN SSC Conservation specular surface depends on a surface percepts, observers selected the Breeding Specialist Group (CBSG), Apple roughness parameter, which modulates surface that appeared more metallic Valley, MN 55124, USA. 10Durrell Wildlife Conservation Trust, Les Augrès Manor, the ‘spread’ of the specular lobe. For a from a pair of images. We tested all Jersey JE3 5BP, UK. 11International Species fixed surface geometry and moderate possible combinations of the two three- Information System (ISIS), Bloomington, amounts of surface roughness, specular dimensional shapes with six different MN 55425, USA. 12Centre of Excellence surfaces will typically generate steeper luminance gradients parametrically for Environmental Decisions, University of luminance gradients than Lambertian varying in steepness (see Figure S1 in 13 Queensland, St. Lucia 4072, Australia. ICCS, surfaces (Figure 1A). the Supplemental Information). Figure 1B Imperial College London, Ascot SL5 7PY, UK. 14Co-first author. Thus, for a fixed surface geometry, plots the proportion of times that each *E-mail: [email protected], the rate that luminance varies as a three-dimensional shape appeared [email protected] function of local three-dimensional more specular than the comparison POLICYFORUM

CONSERVATION

Roughly one in seven threatened terrestrial An Emerging Role of Zoos vertebrate species are held in captivity, to Conserve Biodiversity a resource for ex situ conservation efforts.

D. A. Conde, 1* N. Flesness,2 F. Colchero,1 O. R. Jones,1 A. Scheuerlein 1

t the October 2010 meeting of the global amphibian population declines (11 ). resented and 4% of amphibians. Our primary Convention on Biological Diversity Captive breeding for reintroduction has focus is on species of conservation concern; A(CBD) in Nagoya, Japan, delegates downsides. Sociopolitical factors can deter- for mammals, roughly one-fi fth to one-quar- discussed a plan to reduce pressures on the mine the success of programs. For example, ter of threatened ( 19) and Near-Threatened planet’s biodiversity. Key targets include reintroduction of Arabian (Oryx leu- species are represented in ISIS zoos (see expanding coverage of protected areas, halv- coryx) in central Oman was hampered by the fi gure) (table S1). With the exception of ing the rate of loss of natural , and poaching, partly because local communities Critically Endangered species, which only preventing extinction of threatened species were insuffi ciently involved in conservation have a 9% representation (tables S1 and S2), ( 1). For species whose habitat is severely efforts (12 , 13 ). Furthermore, captive breed- the picture is similar for birds. For amphib- threatened, however, the outlook is so bleak ing is costly, and technical diffi culties can ians, the representation of threatened spe- that the International Union for Conservation arise such as hybridization [breeding among cies is much lower (~3%); this is a concern of Nature (IUCN), the U.S. Endangered Spe- different species (14 ), e.g., if current cryp- because amphibians are a highly threatened cies Act, and the CBD (Article 9) recognize tic species are managed as one species, but group, with 41% of described species listed that in situ conservation actions (i.e., in the are later split into several species according as threatened or (EW) ( 5).

species’ natural habitat) will need to be com- to new taxonomic information]. The abil- The IUCN threat-level assessment for rep- on May 1, 2013 bined with ex situ approaches, such as captive ity of individuals to learn crucial skills that tiles has not been completed, so our results breeding in zoos, aquariums, and so on (2 , 3 ). allow them to survive in the wild (e.g., fear should be interpreted with caution, but of the Captive breeding may be the only short- of humans or predators) may be compro- 1672 species already evaluated, zoos hold term practical conservation option for species mised. In many cases, these diffi culties have 37% of threatened and 18% of Near-Threat- confi ned to dwindling habitats ( 4). However, been overcome by creative and species-spe- ened species. captive breeding is absent or plays a minor cifi c measures. For example, it was feared Overall, zoos and aquariums hold roughly role in the policies of most governments, con- that Puerto Rican (Amazona vittata) one in seven threatened species (15%), but it servation organizations, and multilateral insti- would be unable to escape predators in the is important to consider also the number of

tutions. To shed light on the state of captive wild, but this problem was solved with a pre- individuals held. Although individual zoos www.sciencemag.org breeding and its potential to contribute to con- release -based stimulation and exercise might not have large populations of a par- servation goals, we estimate the number of program (15 ). Because ex situ conservation ticular species, collectively, zoos hold siz- threatened species already held in captivity. programs can be challenged when called into able populations of certain species, including action at the last possible moment with only a highly threatened ones (see the fi gure). Zoos, Captive Breeding few remaining individuals of a species, cap- as a global network, should strive to ensure Although ecosystem health should be a con- tive breeding should not simply be seen as that their populations of threatened species

servation priority, a recent evaluation of the “emergency-room treatment.” It is a tool that can survive in the long term. However, each Downloaded from status of the world’s vertebrates ( 5) noted that should be considered before the species has zoo may make a larger conservation contri- captive breeding played a major role in the reached the point of no return. bution by specializing in breeding a few at- recovery of 17 of the 68 species whose threat risk targeted species, rather than aiming to level was reduced [e.g., Przewalski’s wild Counting Threatened Species in Captivity increase its species diversity, as specialization horse (Equus ferus przewalskii) ( 6), black- We used the International Species Informa- increases breeding success (4 ). footed ferret (Mustela nigripes) (7 ), and Cal- tion System (ISIS) database to estimate the Ultimately, success of conservation ifornia condor (Gymnogyps californianus) number of threatened species already held in actions depends on the extent to which birth ( 8)]. Captive breeding has the potential to captivity. ISIS is an organization that holds and death rates permit populations to survive maintain targeted populations as an “insur- the most comprehensive information on in the wild (8 ). Population viability analyses ance policy” against threats like disease or animals held in zoos and aquariums world- (PVAs) are used to forecast the probability of pressure from nonnative species [e.g., egg wide, with records of ~2.6 million individu- population extinction for conservation pro- predators on islands ( 9)] until reintroduction als shared among ~800 member institutions grams (20 ), but these require parameteriza- into the wild is possible. A striking example ( 16). From the IUCN Red List of Threatened tion with data on age-specifi c birth and death is the increase of amphibian collections in Species (17 ), we obtained the threat category rates (21 ). Adequate data from natural envi- zoos (10 ) as a response to chytridiomycosis, of each terrestrial vertebrate species repre- ronments are often unavailable, especially for a fungal infection responsible for precipitous sented in ISIS ( 18). [See supporting online threatened species ( 20). The zoo network has materials (SOM) for details.] large long-term data sets, including data such One-quarter of the world’s described bird as average litter size, interval between succes- 1Max Planck Institute for Demographic Research, Rostock 18057, Germany. 2International Species Information Sys- species and almost 20% of the mammal spe- sive litters, and age at maturity, which could tem, Eagan, MN 55121, USA. cies are held in ISIS zoos (table S1). Only be used to fi ll these gaps. Of course, zoo data *Author for correspondence: [email protected] 12% of the described reptile species are rep- should be used with caution because they

1390 18 MARCH 2011 VOL 331 SCIENCE www.sciencemag.org Published by AAAS POLICYFORUM

Mammals Birds Reptiles Amphibians 800 Described In zoos 600

400

200 18% Number of species 24% 25% 23% 17% 17% 37% 19% 28% 51% 100% 9% 100% 18% 0% 6% 4% 2% 3% 50% 0 NT VU EN CR EW NT VU EN CR EW NT VU EN CR EW NT VU EN CR EW 5000

250 250 250 250 500 50 50 50 50

50 10 10 10 10

5 Number of individuals

1 Percentage of 21 27 25 27 8 40 29 23 6 40 32 22 24 10 18 48 species per interval

Species (ranked by number of individuals) on May 1, 2013

NT: Near threatened VU: Vulnerable EN: Endangered CR: Critically endangered EW: Extinct in the wild

Threatened

Endangered species in zoos. (Top) The number of able for design of conservation programs, 7. J. Belant, P. Gober, D. Biggins, in IUCN Red List of Threat- species with IUCN status, globally described (color policy-makers must encourage and facilitate ened Species, Version 2010.4 (IUCN, Gland, Switzerland, bars) and in ISIS zoos (black bars). (Bottom) The the participation of zoos from regions with 2010). 8. V. J. Meretsky, N. F. R. Snyder, S. R. Beissinger, D. A. Clen- number of individuals in ISIS zoos for species listed high levels of biodiversity threat in global denen, J. W. Wiley, Conserv. Biol. 14, 957 (2000). www.sciencemag.org by IUCN—for mammals (142 species), birds (83 spe- networks, such as ISIS and the World Asso- 9. J.-C. Thibault, J.-Y. Meyer, Oryx 35, 73 (2001). cies), reptiles (90 species), and amphibians (29 spe- ciation of Zoos and Aquariums (WAZA). 10. Amphibian Ark, www.amphibianark.org. 11. L. F. Skerratt et al., EcoHealth 4, 125 (2007). cies). The vertical broken lines show the boundaries The potential for zoos to contribute to by 250, 50, and 10 individuals. The large numbers of 12. J. A. Spalton, M. W. Lawerence, S. A. Brend, Oryx 33, 168 conservation is not a new concept for the zoo (1999). individuals classifi ed as Vulnerable and Near Threat- community. Zoos and aquariums have devel- 13. V. Morell, Science 320, 742 (2008). ened are omitted for clarity. See SOM for details. 14. R. Barnett, N. Yamaguchi, I. Barnes, A. Cooper, Conserv. oped conservation projects in the wild, along- Genet. 7, 507 (2006). 15. T. H. White, J. A. Collazo, F. J. Vilella, Condor 107, 424 side research and education programs ( 23). Downloaded from do not necessarily refl ect the situation in the For example, members of WAZA collectively (2005). 16. International Species Information System, www.isis.org. wild, such as population fl exibility in the face spend ~U.S. $350 million per year on conser- 17. IUCN, IUCN Red List of Threatened Species, Version 3.1 of changing conditions. vation actions in the wild, which makes them (IUCN, Gland, Switzerland, 2009); www.iucnredlist.org. Despite their current and potential contri- the third major contributor to conservation 18. ISIS and IUCN information were matched on the species level using the Catalogue of Life (F. A. Bisby et al., Eds.); butions to species conservation, ISIS zoos are worldwide after the Nature Conservancy and www.catalogueofl ife.org. concentrated in temperate regions, whereas the World Wildlife Fund global network ( 24). 19. Threatened species are those listed as Critically Endan- most threatened species are tropical ( 5, 22) Given the scale of the biodiversity challenge, gered (CR), Endangered (EN), or Vulnerable (VU) by IUCN. 20. T. Coulson, G. M. Mace, E. Hudson, H. Possingham, (fi g. S1). This mismatch between the areas it is vital that conservation bodies and policy- Trends Ecol. Evol. 16, 219 (2001). where captive populations are held and their makers consider the potential that zoos as a 21. J. M. Reed et al., Conserv. Biol. 16, 7 (2002). native range poses a challenge for imple- global network can provide. 22. R. Grenyer et al., Nature 444, 93 (2006). 23. WAZA, Building a Future for Wildlife: The World Zoo and mentation of effective conservation actions. Aquarium Conservation Strategy (WAZA, Berne, Switzer- Acclimatization to a new home is likely to be References and Notes land, 2005). faster for animals raised in conditions similar 1. D. Normile, Science Insider, 29 October 2010; http:// 24. M. Gusset, G. Dick, Zoo Biol., 6 December 2010 (http:// news.sciencemag.org/scienceinsider/2010/10/negotia- onlinelibrary.wiley.com/doi/10.1002/zoo.20369/ to those where they are to be released. This tors-agree-on-biodiversity.html. abstract). is one reason that it is suggested that captive 2. Convention on Biological Diversity, Article 9, United 25. We thank J. Vaupel, M. Gusset, C. D. L. Orme, D. Levitis, breeding be done in the country of the spe- Nations—Treaty Series, pp. 149 and 150 (1993). D. de Man, W. van Lint, K. Zippel, S. Möller, J. Runge, E. cies’ origin ( 2). 3. IUCN, IUCN Technical Guidelines on the Management of Brinks, G. Fiedler, P. Kutter, and F. Quade. We also thank Ex Situ Populations for Conservation (IUCN, Gland, Swit- three anonymous referees. There are large parts of the world with high zerland, 2002), p. 4. biodiversity value, yet whose zoos are not 4. W. G. Conway, Zoo Biol. 30, 1 (2011). Supporting Online Material well represented in a global network (fi g. S1). 5. M. Hoffmann et al., Science 330, 1503 (2010). www.sciencemag.org/cgi/content/full/331/6023/1390/DC1 6. M. C. Van Dierendonck, M. F. Wallis de Vries, Conserv. Given the importance of having data avail- Biol. 10, 728 (1996). 10.1126/science.1200674

www.sciencemag.org SCIENCE VOL 331 18 MARCH 2011 1391 Published by AAAS Ambio 2017, 46:443–455 DOI 10.1007/s13280-016-0892-4

REVIEW

Meeting the Aichi targets: Pushing for zero extinction conservation

Stephan M. Funk, Dalia Conde, John Lamoreux, John E. Fa

Received: 4 November 2016 / Revised: 23 December 2016 / Accepted: 26 December 2016 / Published online: 31 January 2017

Abstract Effective protection of the *19 000 IUCN- (Crutzen 2002; Steffen et al. 2007) at least three of nine listed threatened species has never been more pressing. planetary boundaries have exceeded safe levels: climate Ensuring the survival of the most vulnerable and change, global nitrogen cycle and integrity of biodiversity irreplaceable taxa and places, such as those identified by (Rockstro¨m et al. 2009; Newbold et al. 2016). the Alliance for Zero Extinction (AZE) species and their Based on a conservative estimate, a total of 477 verte- associated sites (AZEs&s), is an excellent opportunity to brates have vanished since 1900, over three-quarters of the achieve the Aichi 2020 Targets T11 (protected areas) and 617 vertebrates that have become extinct since 1500 (Ce- T12 (preventing species extinctions). AZE taxa have small, ballos et al. 2015). Nonetheless, according to the most single-site populations that are especially vulnerable to recent IUCN Red List of Threatened Species more than human-induced extinctions, particularly for the many 7978 species of fishes, amphibians, reptiles, birds and amphibians. We show that AZEs&s can be protected mammals are globally threatened (IUCN 2016). Given feasibly and cost-effectively, but action is urgent. We argue these numbers, distinguishing which of these taxa to attend that the Alliance, whose initial main aim was to identify to first, and what resources to mobilize to ensure their AZEs&s, must be followed up by a second-generation survival, has never been so pressing (Wilson et al. initiative that directs and co-ordinates AZE conservation 2011, 2016). Despite this urgency, progress has been slow. activities on the ground. The prominent role of zoos, During the last two decades global strategies focussing on conservation NGOs, and governmental institutions biodiversity and species conservation have concentrated on provides a combination of all-encompassing knowhow large-scale prioritization approaches (Redford et al. 2003; that can, if properly steered, maximize the long-term Brooks et al. 2015). But, these exercises have done little in survival of AZEs&s. terms of identifying the actual sites where conservation needs to occur (Brooks et al. 2006; Howes et al. 2009; Keywords AZE Á Endangered species Á IUCN Red List Á Funk and Fa 2010). Likewise, high-level declarations of Protected areas intent, epitomized by nation states signing international conventions, routinely confirm the need to ensure the long- term survival of the world’s biological diversity, while the INTRODUCTION biodiversity crisis continues. Since the early 1990’s, a number of worldwide treaties Human impact on the environment has reached unprece- have been signed. Major international agreements such as dented levels. The planet’s biological–ecological, physical the Kyoto Protocol linked to the United Nations Frame- and chemical systems are threatened and with it our work Convention on Climate Change committed its Parties livelihoods (Stern and Treasury 2006; Rockstro¨m et al. by setting internationally binding emission reduction tar- 2009; Watson et al. 2016). On entering the Anthropocene gets. The detailed rules for the implementation of the Protocol were adopted in Marrakesh, Morocco, in 2001. However, international initiatives promoting the conser- Stephan M. Funk and John E. Fa are co-first authors. vation of biodiversity at the highest level, in particular the

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 444 Ambio 2017, 46:443–455

COP-6’s (the sixth Conference of the Parties to the Con- improving the of threatened species and vention on Biological Diversity) declaration have fallen preventing their extinction, as designated in T12a, will short of their intended targets. COP-6 committed countries likely not be achieved (Table 1). Given this dire prognosis, ‘‘to achieve by 2010 a significant reduction of the current finding ways to maximize the conservation of a significant rate of biodiversity loss’’ but because of a lack of signifi- number of highly threatened species is urgently required. cant improvements in the state of biodiversity By focussing on species that are most at risk of (Butchart et al. 2010; Adenle et al. 2015), new targets were extinction, it will be possible to improve the prospects of developed during COP-10 in Nagoya, Aichi Prefecture, achieving the aspirations set out in T11 and T12. More Japan. These, referred to as the Aichi Biodiversity Targets, particularly, in this review we make a case that species and are a set of 20 objectives (subsequently abbreviated as T1, sites listed by the Alliance for Zero Extinction (AZE) T2, …, T20), to be achieved by 2020 (SCBD 2010). There already provide the global conservation community with a are three targets of direct relevance for the conservation of realistic opportunity to contribute to the Aichi targets to biodiversity: T11 (protected areas), T12 (species) and T13 support countries to comply with these targets and to (genetic diversity of plant and animal domesticates) achieve the spirit of Aichi by directly reducing biodiversity (Table 1). For this review, we excluded T13 as it focuses loss. AZE, an alliance of conservation groups, aims to on domesticated and cultivated and animals. identify and promote the protection of taxa that are highly A mid-term assessment of the Aichi Targets, indicates vulnerable to human-induced extinctions and are restricted that current efforts will be insufficient not only to achieve to single locations (Table 2). Habitat conservation within most targets by 2020, but also that pressures on biodiver- AZE sites and/or the in situ and ex situ augmentation of sity will continue to rise over this period (SCBD 2014). population numbers of AZE species may require relatively According to this assessment, only one sub-target, T11a straightforward interventions. However, this potential has ‘conserving at least 17 per cent of terrestrial and inland only been partially realized (Butchart et al. 2012; Hsu et al. water areas’ may be met (Table 1). All others are likely to 2014; SCBD 2014; Butchart et al. 2015). AZE species and fail. It is doubtful that T11a on its own will be enough to sites, henceforth AZEs&s, constitute a first line of defence maintain biodiversity and ecosystem services in the long against predictable and preventable imminent species los- term. This is because T11 does not account for insufficient ses (Ricketts et al. 2005). As stated by Butchart et al. protected area (PA) management, lack of representative- (2012), the effective conservation of all AZE sites is ‘‘by ness, degazetting or degradation (Mascia et al. 2014; definition essential to achieve the CBD target of preventing Watson et al. 2014; Butchart et al. 2015). Likewise, extinctions of known threatened species’’. The protection

Table 1 Aichi Targets directly linked with the conservation of terrestrial species and ecosystems and prognosis for 2020 During the tenth meeting of the Conference of the Parties (COP 10) in Nagoya, Aichi Prefecture, Japan, the Convention on Biological Diversity (CBD) adopted a Strategic Plan for Biodiversity 2011–2020 with the mission to ‘‘take effective and urgent action to halt the loss of biodiversity in order to ensure that by 2020 ecosystems are resilient and continue to provide essential services, thereby securing the planets‘ variety of life, and contributing to human well-being, and poverty eradication’’ (SCBD 2010). CBD parties include 196 Parties of which 168 are signing parties (SCBD 2016). The Strategic Plan includes a set of 20 Aichi Biodiversity Targets, subsequently abbreviated as T1, T2, …, T20. The targets are clustered into strategic goals, whereby each target contains several sub-targets. For applied conservation of terrestrial species and ecosystems, T11 and T12 are the key targets. T11 and T12 are bundled in Strategic Goal C, which aims at ‘‘improving the status of biodiversity by safeguarding ecosystems, species and genetic diversity’’. The following list only includes those sub-targets that apply to non-domestic terrestrial species and protected areas, PAs T11: Increased global coverage of ecologically representative protected areas, PAs a: Conserving at least 17 per cent of terrestrial and inland water areas: A b: Conserving at least 17 per cent of coastal and marine areas: B c: areas of particular importance for biodiversity and ecosystem services conserved: B d: PAs are ecologically representative: B e: PAs are effectively and equitably managed: B f: PAs are well connected and integrated into the wider landscape/seascape: B T12: Reducing risk of extinction a: Extinction of known threatened species has been prevented: N b: The conservation status of those species most in decline has been improved and sustained: R The prognosticated progress (A: likely achieved; B: positive, but insufficient progress; N: no progress; R: regress) towards the implementation of the Strategic Plan for Biodiversity 2011–2020 follows the assessment by the CBD Secretariat (SCBD 2014)

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 445

Table 2 Alliance for Zero Extinction, AZE, species and sites Presented to the academic community in 2005 (Ricketts et al. 2005), the Alliance for Zero Extinction, AZE, is a worldwide consortium of currently 98 global biodiversity conservation organizations and an increasing number of regional partnerships, currently in , Columbia, Mexico, India and Peru (AZE 2013a). Membership is open for all NGOs with a focus on the conservation of biodiversity. AZE collaboration focuses on three principles (AZE 2011): • Development of site map and site list • Identification of conservation needs and implementing agencies • Develop and raise funds for conservation programmes There are no minimum requirements for the level of contribution and there is no obligation to make financial commitments. All members can also work independently without co-ordination of their priorities with AZE. No lead organization exists, but the AZE’s Secretary, currently the American Bird Conservancy, co-ordinates the activities, including the web presentation AZE’s main focus is to identify ‘trigger’ species, which are threatened by immediate extinction, and their associated sites (American Bird Conservancy 2005; Ricketts et al. 2005). The criteria for choosing AZE species are straightforward: • Species must be listed in the IUCN Red List of Threatened Species as either Critically Endangered or Endangered • More than 95% of the species’ population must be restricted to a single and thus irreplaceable site • The species’ site must have a definable boundary within ecological conditions different from adjacent sites AZE sites are those, which contain at least one AZE species. Because species extinctions are likely in these sites, protection is essential. AZE species have been identified so far for mammals, birds, amphibians, some reptiles, conifers and, in the recent update, reef-building corals. Originally, 794 species were identified in 595 sites, but the numbers have now changed to 920 species in 588 sites (AZE 2013b). AZE vertebrates currently include 502 amphibians, 165 birds, 157 mammals and 17 reptiles. Reptiles are underrepresented in this list because of the absence of an IUCN global species assessment for this group at the time of the launch of the new AZE website in 2014 of AZEs&s has been included as a critical piece of the species, pollution and human-induced land use changes. Convention for Biological Diversity (CBD), and confirmed Available data indicate that 25% of all AZE species will be by the signing of mutual collaboration agreements in 2010 affected by urban expansion and encroachment in the next and 2011. AZE sites are considered a crucial component of two decades (Seto et al. 2012). The highest impact is the Key Biodiversity Areas framework (Brooks et al. 2016; expected in Central and South America; a worrisome fact Juffe-Bignoli et al. 2016). Additionally, AZE sites have since the majority of AZE sites occur in the New World. also been included as part of the Critical Habitat Protection Global species diversity is currently underrepresented indicator in the Environmental Performance Index (EPI). within the existing network of PAs (Rodrigues et al. 2004; The EPI provides a gauge at a national government scale of Jenkins and Joppa 2009;Butchartetal.2012). This is also true how close countries are to established environmental pol- of AZE sites since only half are legally protected, with just icy goals. This proximity-to-target methodology facilitates over a third fully contained within a gazetted PA cross-country comparisons as well as an analysis of how (Butchart et al. 2012). Even within protected AZE sites, the global community performs collectively on each par- measures to conserve threatened species in them may be absent ticular policy issue (Emerson et al. 2010). or inadequate (Hsu et al. 2014). To date, only Brazil, Colombia In this review, we provide a summary of the available and Mexico have included AZE sites into their national bio- evidence on the nature of AZEs&s and evaluate the existing diversity protection strategies (Lamoreux et al. 2015). gap between the desired and realized efforts for the con- Additionally, the increase of the proportion of PAs that servation of AZEs&s. We then provide practical guidance cover AZE sites has declined over time with their coverage on how the protection of AZEs&s can contribute to stem- expected to be only about 24% by 2020, an increase of no ming the loss of biodiversity, in support of T11 and T12. more than 1% since 2010 (SCBD 2014). A sobering statistic is that there are three times as many AZE taxa at the risk of extinction as are species known to have been lost CURRENT PROTECTION STATUS OF AZE SITES within the same taxonomic groups in the last 500 years AND SPECIES (Ricketts et al. 2005).

AZEs&s are interlinked. On their own, AZE species rep- resent extremes of threat and irreplaceability; two widely WHAT DOES A CONSERVATION FOCUS ON AZE used metrics to denote species that are highly vulnerable to SPECIES MEAN? extinction (Brooks et al. 2006). Because AZE sites cover relatively small land areas, they are particularly vulnerable Almost one-fifth of extant vertebrate species are classified to biodiversity loss drivers such as climate change, invasive as threatened, ranging from 13% of birds to 41% of

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 446 Ambio 2017, 46:443–455 amphibians; a figure that is increasing (Hoffmann et al. murrayi) (Martin et al. 2012). Nonetheless, the remaining 2010; Ceballos et al. 2015). This bias towards amphibians challenge is to protect and effectively manage AZEs&s, is reflected in the AZE species list where 63% of the 841 often in demanding geographical (rough terrain, remote AZE vertebrates are frogs, toads and salamanders sites) conditions, and restrictive geopolitical circumstances (Table 2). This presents a significant challenge since (corruption, insurgency, war) (Conde et al. 2015). How- amphibians are not just affected by habitat destruction; ever, AZE sites are relatively small (median size there are numerous cases where habitat is protected but *121 km2) compared to existing national parks and other amphibians are still disappearing. The causes of these protected areas (Ricketts et al. 2005; UNEP-WCMC 2016). declines are complex, but chytridiomycosis, a disease This statistic, alongside the fact that most AZE species are caused by fungal pathogens, together with habitat loss are relatively small-bodied animals (Fig. 2), may mean that the most significant threats. Chytrid disease is associated despite the small area size of AZE sites, success is possible with the loss of hundreds of amphibian species at global due to the universal relation of body size and landscape scale, currently representing the ‘‘greatest species conser- requirements (Thornton and Fletcher 2013). AZE species, vation challenge in the history of humanity’’ (Gascon et al. being narrow-range endemics, generally inhabit reduced 2007). This means that the protection of amphibians from habitat , and are thus less reliant on interconnected extinction requires not just the conservation of landscapes landscapes; management of wide-ranging species is much but direct actions, including ex situ conservation more difficult to achieve. Conservation of AZE species interventions. requires the protection of their sites, which we argue is The main justification for pursuing AZE species con- relatively cheap if the political will at an international, servation is an ecocentric approach, in which nature’s national and local level exists. To this end, awareness intrinsic value is central (Butler and Acott 2007). However, building and a unified policy strategy by currently involved it is possible to invoke additional arguments. In a com- and to-be-involved organizations is crucial. parison between ecosystem services in AZE sites and The conservation opportunity index (COI) was devel- randomly selected sites, Larsen et al. (2012) found that the oped by Conde et al. (2015) to assess probability of success protection of AZE sites would result in the maintenance of of in situ conservation of AZE species. The COI quantifies ecosystem services, in turn generating direct human well- those factors that are likely to affect the likelihood of being benefits. Additionally, there are potential economic success: costs of land acquisition and management in the benefits from climate change mitigation at these sites. species’ range country, governance impediments to con- These benefits exceed the management cost of conserving servation including likelihood of political instability and AZE sites, delivering a disproportionate value for at least politically motivated violence (including terrorism), and one ecosystem service in 89% of the sites (Larsen et al. the impact of urban expansion on AZE sites. According to 2012). Likewise, AZE species may contribute to the pro- Conde et al. (2015), a total of 39% of AZE species have vision of potential future services e.g. new pharmaceuticals maximum COI with 80% being in the upper half and 3% in and other products (Gascon et al. 2015). Thus, if AZE the lower quartile of the possible COI range. Therefore, a species become extinct, this potential vanishes. Not only prioritization approach might be more effective by focus- are the AZE species unique by definition, but a substantial ing on the species with higher conservation opportunities number of AZE species are also listed as Evolutionarily showed by the index. Distinct and Globally Endangered (EDGE) species (Isaac et al. 2007). A total 35% of all AZE species (amphibians 25%, birds 13%, mammals 90%) are also EDGE species COSTS AND FUNDING (Fig. 1). EDGE identifies species that have a dispropor- tionate amount of unique evolutionary history. They have Annual costs for down-listing a threatened species on the few close relatives, who are often the only surviving IUCN Red List by at least one threat category have been member of their genus, and sometimes the last surviving estimated as ranging between $3.41 and $4.76 billion with genus of their evolutionary family. or without considering shared expenditure between species (McCarthy et al. 2012). Based on the estimates of land purchase, area and habitat management, foregone monetary CAN WE SAVE AZE SPECIES returns and transaction costs over a 20-year period, in situ FROM EXTINCTION? protection for AZE species would require annual expen- ditures of between *6000 and *30 000 000 US$ (Wilson It is clear that the AZE is an evolving project as species are et al. 2011; Conde et al. 2015). Annual costs are highly added and some are lost to the list as they are declared skewed with the respective majorities at the lower end of extinct e.g. the Christmas Island pipistrelle (Pipistrellus cost and the minorities at the higher end (Fig. 3). Median

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 447

Fig. 1 EDGE species amongst AZE mammal, bird and amphibian taxa. The EDGE score estimates evolutionary distinctiveness, thus irreplaceability, jointly with conservation status (Isaac et al. 2007). It increases with the degree of irreplaceability and conservation threat. EDGE species are the 100 highest-ranking amphibians, birds and mammals, respectively. Amongst AZE animals, mammals have the highest proportion of EDGE species (orange) and birds the highest proportion of non-EDGE species (green). EDGE data from Isaac et al. (2007) and the Zoological Society of London (2016)

Fig. 2 Body size distribution of AZE mammals and birds. Sizes are biased towards small and light birds, mammals with 92 and 79%, respectively, lighter than 1 kg, 65, and 56%, respectively, lighter than 100 g. All AZE amphibians and reptiles are lighter than 1 kg and are not shown here

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 448 Ambio 2017, 46:443–455 costs for down-listing a species would be 0.94, 0.98, 0.58 and sites are low, from a minimum of 0.0016% to a and 0.3 million US$ for amphibians, birds, mammals and maximum of 0.0024%. Management costs include both the reptiles, respectively. These values are within the range of establishment of protected areas and subsequent manage- median annual cost values (0.04–8.96 million US$, average ment of these sites, including those already under protec- 0.85 million US$) estimated by McCarthy et al.’s (2012)to tion (Conde et al. 2015). Conservation costs vary according down-list threatened bird species by one threat category. to the development status of a country. AZE sites in non- Costs for managing AZE sites are the same regardless of OECD countries, which contain *60% of the AZE spe- whether one or more AZE species are present (23% of AZE cies, can be protected for less than in OECD countries sites contain between 2 and 22 AZE species). It would cost (Fig. 3). As many as 65% of sites within non-OECD around 791 million US$ per annum to manage all sites countries and 45% in OECD countries require less than one (Conde et al. 2015). As a proportion of a country’s GDP million US$ annually. The estimated median annual man- (estimated GDP for 2015 for OECD countries combined; agement expenditure per site in developing countries is 220 (OECD 2016) the required annual expenditure for species 000 US$ (Conde et al. 2015).

Fig. 3 Total annual costs for conserving AZEs&s for sites where estimates are available (Conde et al. 2015). A Median cost for amphibians (N = 502), birds (N = 165), mammals (N = 157), reptiles (N = 17) and sites (N = 533) stratified whether sites are inside or outside OECD countries except for reptiles because of low N. B Site costs, ordered according to the values, for OECD and non-OECD sites

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 449

THE NEED TO INCORPORATE AZE SITES THE ROLE OF ZOOS INTO THE PROTECTED AREAS NETWORK The majority of institutions that compose the AZE con- The current global PA network performs poorly in pro- sortium are zoos (AZE 2013a). Zoos work in the interface moting the persistence of species, ecosystems, ecoregions between ex situ and in situ conservation actions, now or overall biodiversity (Rodrigues et al. 2004; Jenkins and defined as the One Plan Approach, in which species are Joppa 2009; Abella´n and Sa´nchez-Ferna´ndez 2015). Cru- managed across different levels of human intervention cially for AZE species, PA networks often do not ade- from highly managed populations in zoos up to populations quately cover narrow-range endemics (Abella´n and that are non-managed at all in the wild (Byers et al. 2013). Sa´nchez-Ferna´ndez 2015). Zoos are arguably the main institutions at a global level Protecting AZE sites as government-protected areas is that have the knowhow and the experience for imple- one strategy, but other forms of site protection should menting scientific management programmes for the not be overlooked (Butchart et al. 2015). In many recovery of small animal populations and of rare species countries, lack of trust of public institutions is a strong across this management continuum. This interface of barrier. Communities often do not have confidence in population management is an integral part of the new their own governments and, consequently, do not actively Conservation Management Strategy of the World Associ- support legal protection; in some cases, they even boy- ation of Zoos and Aquaria (Barongi et al. 2015). Numerous cott actions that come with the legal protection. AZE examples where zoos have contributed successfully to the sites are, due to their generally small size, often easier to recovery of highly threatened animal taxa have been doc- implement as community PAs compared to state PAs. umented (see Fa et al. 2011). A number of zoos have singly Similarly, private ownership can significantly contribute or as part of conservation consortia made substantial to conservation, in particular as they can be efficiently advances in protecting AZE species. In a few cases, managed, have high security, can quickly react to organizations such as the Durrell Wildlife Conservation emerging threats and many have been shown to suc- Trust (Durrell), have worked on multiple AZE species, cessfully achieve area protection, e.g. the Douglas improving the protection of as many as 14 of them (two Tompkins’ Pumalı´n Park in Chile. Community and pri- mammals, seven birds and five reptiles) as well as five vate parks are, however, also exposed to risks such as a other single-site taxa (Fa et al. 2011). For this organization, change of ownership, social-environmental conflicts and ex situ and in situ activities (albeit for a period of more issues inherent to the tragedy of the commons (Holmes than 50 years) have directly prevented the extinction of 2014, 2015). A recent analysis has shown that all types species such as the Mauritius kestrel (Falco punctatus). of area protection are powerful when applied in a The conservation status of other taxa has been improved regional mix of approaches (Leme´nager et al. 2014). through the application of a suite of interventions such as Here, AZE sites offer opportunities to strengthen the mix fostering education, disseminating conservation science, and consequently achieve a stronger and more resilient raising countrywide attention to species in danger, and PA system, provided that those potential risks arising training local researchers, educators and managers (Aichi from non-public ownership can be successfully addres- T1) as well as mobilizing funding resources (Aichi T1 and sed. The relative small size of AZE sites, flexible T20, respectively, Moss et al. 2015). Young et al. (2014) administrations and monitoring by third parties can turn suggest that out of 17 target amphibian, bird and mammal formal protection into actual measures of conserving species, eight underwent improvements in Red List cate- threatened species, a large problem for many formally gory (reductions in extinction risk) owing to the conser- protected large PAs (Hsu et al. 2014). AZE conservation vation activities led by Durrell; a 67% increase in the value must aim to have private and community sites embedded of the between 1988 and 2012. This con- into the Alliance with adequate safeguards because the trasts with a 23% decline in a counterfactual RLI showing risks, such as change of ownership or economic use, can projected trends if conservation had been withdrawn in be severe and could obliterate the site and its species. 1988. Communal or privately managed or owned sites will not Despite a number of examples of success, zoological necessarily lead to the level of legal protection as institutions need to step up their game if they are to remain required under T11a, but they can significantly contribute relevant (Fa et al. 2014). Overall, most successful projects to several other sub-targets and overall strategic goal for have resulted in the creation or management support of which T11 stands. Whether or not communal- or private- AZE sites by playing a crucial part in enhancing human protected sites contribute to T11, they directly contribute livelihoods, which is an integral component of CBD’s to T12 and these administrative models of AZE sites are vision to deliver benefits for all people by 2050 (Table 1). a major opportunity. Thus, if one zoo-based organization has been able to

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 450 Ambio 2017, 46:443–455 improve the fate of a substantial number of AZE species, inadequate and undermine any efforts to meet the biodi- more involvement by zoos alongside other organizations versity targets (McCarthy et al. 2012; Waldron et al. 2013; could no doubt create a greater wave of direct and imme- Butchart et al. 2015). Major funding gaps for conservation diate conservation of AZEs&s. Although the role of zoos, are not limited to low-income countries but also extend to and often their very existence, is still debated, they can OECD nations, which have the highest incomes worldwide play a vital role as emergency centres for species on the in terms of GDP (OECD 2016). For example, Chile is the brink of extinction including amphibians. For the latter ninth most underfunded country for biodiversity conser- groups, zoos can actively engage in the ex situ breeding of vation worldwide and the lowest performing OECD rescued animals (in some cases the last of the species) for member (Waldron et al. 2013), despite its outstanding subsequent re-introductions if and when the conditions in biodiversity (Funk and Fa 2010). In general, however the wild are adequate. Zoos and affiliated research centres directing funds from high-income to low-income countries can also generate the knowledge necessary to allow the is a strategy that can bridge this financing gap (Waldron treatment of the disease, raise awareness and engage in et al. 2013). For AZEs, zoos are especially well suited to capacity building (Tapley et al. 2015). achieve this goal due to their fundraising capacity and In those cases, where AZE species require direct man- relatively straightforward administration. Thus, they are agement by captive breeding as a safety net or a life-sup- well placed to lead the Alliance’s fundraising activities port system, costs for this would be relatively low; about towards AZEs&s. A major challenge is the expected 159 million US$ for all listed AZE vertebrates. AZE spe- increase in funding requirements of at least an order of cies are generally small-bodied animals (Fig. 2), and magnitude to fulfil the world´s commitment to safeguard because of the positive correlation between ex situ cost to species and ecosystems by 2020 and beyond. New body weight (Fa et al. 2011) delivering effective captive approaches such as crowd funding are starting to generate breeding programmes, where needed, would be inexpen- promising results and might bring new opportunities. sive. The estimated cost for amphibians and reptiles, are Indeed, zoos support in situ conservation by fundraising constant at *10 000 US$ (Conde et al. 2015). Cost for and they already contribute 350 million US$ on conser- birds vary moderately between 0.33 and 0.42 million US$ vation projects per year (Gusset and Dick 2011). Yet, much (median: 0.34) but much more for mammals, 0.66–10.27 of the funds collected by zoos are directed not to AZE million US$ (median: 0.38), reflecting the large size dif- species but to high-profile threatened species and habitats ferences ranging from small rodents and insectivores to the and primarily mammals, in particular charismatic non-AZE Javan rhinoceros (Rhinoceros sondaicus). Although ex situ primates and carnivores. Consequently, amphibians are costs are relatively low, the decision to take this option significantly underrepresented (Gusset and Dick 2010). must be based on a rigorous cost–benefit assessment and Finances in zoos are scarce, but much of these resources go adaptive planning to maximize the chances of success (Fa to expensive species, which are less likely to face near- et al. 2011; Tapley et al. 2015). In particular, the cost for term extinction (Fa et al. 2011). Therefore, zoos must re-introductions can be exceedingly high because this assess their commitment to AZE conservation and make an process and subsequent active management is lengthy and even stronger contribution to support their own AZE-re- because achieving the optimal demographic and genetic lated aims. structure of the new populations require well-planned long- The priority setting approach by zoos, as best placed for term monitoring schemes. mobilizing funds and conservation action for AZEs&s, remains a concern. Despite the fact that there is no doubt that zoos can play a significant role in in situ and joint ex RECOMMENDATIONS FOR ZOOS situ conservation, support for AZE conservation is still rare (Fa et al. 2011). In our experience, zoo conservation Besides the general difficulties of conserving biodiversity actions are rarely used in a strategic, global and all-en- in the face of a sixth mass extinction (Ceballos et al. 2015), compassing framework for biodiversity conservation and including the chasm between the legal and actual safe- sustainable development. A recent horizon scan for zoos guarding of PAs (Watson et al. 2015), there are still several and aquaria identified the 10 most important emerging specific issues that affect AZEs. These include the need for issues for species conservation by 2020, but AZE does not a clear organizational setup, more targeted priority setting, feature (Gusset et al. 2014). Clearly, a refocus is urgently planning and active involvement in conservation pro- required. First, participating institutions should focus more grammes on the ground as well as the plugging of existing on keeping AZE species in their collections, based on financial gaps, and effective outreach and lobbying initia- critical assessments including priority setting, ex situ tives (Table 3). However, worldwide funding levels for suitability, effects on demography and genetics, in situ conservation in general, and for PAs in particular, remains conditions, and financials and logistic resources to

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 451

Table 3 Specific recommendations to transform AZE into AZE 2.0 Organizational infrastructure: AZE 2.0 • Create a second-generation Alliance, AZE 2.0, suitable for efficient directing and co-ordinating active and efficient conservation of AZEs&s • Establish the essential organizational infrastructure and funding of thereof • Attract additional members strengthening and complementing the mix of expertise • Create a web-based, open access platform for effective information dissemination to the public and as co-ordination tool between members. Priority setting, planning and active conservation • Joint development of a strategic, global and all-encompassing framework for the protection of AZEs&s • Utilization of the wide geographic and disciplinary spread and expertise within all current AZE members and possible members of AZE 2.0 • Refocus in the collection planning of the zoos committed to AZEs&s conservation • Joint priority setting for in situ and ex situ conservation • Critical analysis which species need and are suitable for ex situ breeding and which can be repatriated with a reasonable likelihood of success • Long-term strategic planning • Explore and support and monitor systems of protection and management that is most suitable for specific sites: private, community and state protection • Identify research gaps for applied conservation, and co-ordinate, commission and implement research swiftly • Proceed from academic and strategic planning to implementation swiftly Fill financial gaps • Utilizing the existing fundraising capacity of the AZE consortium, especially zoos, to support AZE-based conservation activities • Encourage international multilateral organizations (e.g. GEF, World Bank, EU etc.) to put resources to promoting the conservation of AZEss Outreach and lobbying • Using the political leverage of the consortium to address the importance of AZEs&s • Facilitate that AZEs&s are incorporated into national and regional conservation planning • Utilize the available expertise amongst consortium members to extend focus in education, outreach and capacity building for AZEs&s maximize the chances of success (Fa et al. 2011; Pritchard achieved (Fa et al. 2011). Only a unified system that can et al. 2012; Conde et al. 2013). Second, the current gap in operate over large scales by drawing on spatially dispersed strategic priority setting for AZE needs to be addressed. participants, e.g. across multiple conservation project sites, There are numerous approaches on how to identify prior- can result in an inter-communicated system of project sites ities for in situ conservation (Myers et al. 2000; Isaac et al. that together can achieve cumulative change for a multi- 2007; Funk and Fa 2010), ex situ strategies (e.g. Regional tude of species and landscapes. Third, zoos can expand on Collection Plans) and both combined (Fa et al. 2011; Byers their shift over the last decades from ex situ collections to et al. 2013; Conde et al. 2013), but a coherent prioritization in situ conservation and the new added pillar of education scheme jointly amongst AZE partners still needs develop- and outreach to underpin the societal value of zoos (Fa ing. It is difficult to encourage zoos to agree on a joint et al. 2011). This is a good foundation to focus efforts not approach for prioritization even within regional zoo asso- only to concentrate on AZE species in their education ciation species management programmes, let alone at an programmes, but also to raise awareness for the urgent international level (Fa et al. 2011; Pritchard et al. 2012). need of sustainable development and mobilize societal Within institutions, prioritization in most cases relies on organizations for more active participation. the preferences of directors, staff and visitors, but sys- tematic planning such as the EDGE programme (Zoologi- cal Society of London, ZSL 2016; Isaac et al. 2007) is rare. AZE 2.0 Between in situ and ex situ organizations there has been a deep chasm in strategies and co-ordination (Fa et al. 2011; In addition to the recommendations for the zoo member- Pritchard et al. 2012). In situ and ex situ conservation ship of AZE, we have several recommendations for the programmes are often designed in isolation, not just of Alliance itself. We put these under the banner of AZE 2.0. each other, but also of similar ones undertaken by others The current goals of the AZE focus on identifying (e.g. other regions); a piecemeal approach that ignores the AZEs&s, as well as their conservation needs and devel- potential for making sure that ‘snowballing’ effects can be oping and funding programmes to protect them (AZE

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 452 Ambio 2017, 46:443–455

2011). The first goal of identifying AZEs&s has been Alliance to pursue the conservation needs part of its orig- successfully accomplished (Ricketts et al. 2005) and fully inal vision. revised (AZE 2010). However, it has become increasingly Compiling the conservation needs of each site is a dif- clear that the list of AZEs&s requires more frequent ferent task from site identification. It requires ascertaining updates. Furthermore, the organizational structure of AZE trends for a site, including its ownership, use and projected should be modified if it is to achieve the identification of vulnerability to human disturbance, invasive species and conservation needs portion of the vision. Perhaps most climate change. It can also include a community profile and importantly, for AZE to reach its full potential as a widely the identification of local partners who, if supported, would recognized requirement for accomplishing Aichi T12, have the capacity and desire to conserve the site. Only such members will have to communicate and collaborate more information will allow interested partners to judge which closely, leveraging both money and expertise. projects to launch, support or fund. Such an exercise is The AZE species list draws from the IUCN Red List of possible. BirdLife International has completed numerous Threatened Species, which is constantly undergoing revi- detailed site profiles for their Important Bird and Biodi- sion. Red List species accounts are updated to accommo- versity Areas Programme (Brooks et al. 2016). An in-depth date changes in our knowledge of species (e.g. distribution, study on the assessment of AZEs&s conservation needs taxonomy, population size, threats faced), to correct past was recently completed for southern Mexico (Lamoreux errors, and to reflect genuine changes in conservation sta- et al. 2015). The membership of AZE should support these tus. Correspondingly, the AZE list remains incomplete for types of data gathering, both financially and with their vast, terrestrial vertebrates because no global assessment for collective expertise. reptiles has been completed. Currently, the AZE list only AZE 2.0 should also systematically capture the conser- includes 17 reptiles, but this list will likely increase given vation outcomes (successes & failures), as well as the there are more than 10 000 , , turtles, croco- lessons learned from their efforts. Sharing data in this diles and tuatara worldwide (Bo¨hm et al. 2013). manner will improve the effectiveness of conservation The necessity to update frequently the list of AZEs&s actions. It will also allow the Alliance to measure and follows the need for updates to the Red List, but it also can report on their impact; the information that is increasingly require accounting for habitat/site changes on the ground. demanded by funders. To date, the most thorough investigation of AZEs&s for a region found a considerable need for refinement (Lamor- eux et al. 2015). AZE site delineation is particularly OUTLOOK problematic. For example, Larsen et al. (2012) point out that only limited data exist for all AZE sites regarding The target of reducing extinction risk, T12, is, by defini- boundaries. The Red List itself is also struggling to keep up tion, immediately supported by the conservation of AZE with maintenance and revisions, which then weighs on the species. For the target on PAs, T11, AZE sites’ contribu- accuracy of the AZE list. Rondinini et al. (2014) stressed tions are differentiated according the sub-targets. AZE will the importance of Red List maintenance and proposed steps contribute little to T11a’s 17% area size target and it is by which to achieve this end. We follow this example by difficult to assess, due to data deficiency and lack of laying out the steps by which AZE can become more detailed analysis, how important AZE sites are for eco- effective by tapping the resources of its membership logical representativeness, T11d, and the connection and organizations. integration into the wider landscape, T11f. On the other If we are able to harness and optimize the resources and hand, they will contribute significantly to the other sub- expertise available across all members of the Alliance, we targets. The contribution to sub-target T11c is immediate can advance effective conservation of AZEs&s. The Alli- as it addresses sites of particular importance to biodiver- ance has established an organizational infrastructure, which sity, to which the AZE species belong to as many of them led to the successful identification of AZEs&s. Hitherto, also represent EDGE species, and it safeguards ecosystem this has been done as a volunteer operation. AZE members services provided within and outside the sites. Due to their do not provide managerial or financial support to the small size and the suitability for management as public, Alliance, which means future updates to the data will communal or private PAs, managed AZE sites will help to remain infrequent. The Alliance is exploring the possibility proceed towards achieving the sub-target on the effective of having countries identify and maintain their own and equitable management, T11e. The greatest impact of AZEs&s list, which would feed into a global dataset (M. site protection is as a vehicle for T11. Additionally, the Parr, pers. comm.). However, we think it is time the AZE approach also indirectly supports several other targets member organizations step up by contributing dues to such as T1 (Awareness of biodiversity increased) and T20 AZE. This would ensure regular data updates and allow the (Mobilizing resources).

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 453

Conserving AZE-listed, highly vulnerable and irre- American Bird Conservancy. 2005. Alliance for Zero extinctions. placeable species together with their associated sites will Pinpointing and Preventing Imminent Extinctions. Report. https://abcbirds.org/wp-content/uploads/2015/05/AZE_report. provide significant progress in the achievement of several pdf. Aichi targets and their underpinning goals, if the oppor- AZE. 2010. Sites & Species. Alliance for Zero Extinction. http:// tunities are acted upon. It is not only possible to conserve www.zeroextinction.org/maps/AZE_map_12022010.pdf. AZE sites and to prevent the extinction of many AZE AZE. 2011. Memorandum of Understanding among all parties of the ‘‘Alliance for Zero Extinction.’’ http://www.zeroextinction.org/ species but inexpensive with a high likelihood of success pdf/TermsofUseAZEdata_2011.pdf. (Conde et al. 2015). So far, the conservation potential has AZE. 2013a. Alliance for Zero Extinction. Alliance for Zero only been partially realized (Butchart et al. 2012; Hsu et al. Extinction. http://www.zeroextinction.org/index.html. 2014; SCBD 2014; Butchart et al. 2015). AZE. 2013b. List of sites and species. Alliance for Zero Extinction. http://www.zeroextinction.org/sitesspecies.htm. Conservation is a long-term enterprise, requiring long- Barongi, R., F.A. Fisken, M. Parker, and M. Gusset. 2015. Commit- term monitoring and financing. Because AZE sites tend to ting to conservation: the world zoo and aquarium conservation be relatively small, they will likely be heavily affected by strategy. Gland, Switzerland: WAZA Executive Office. future climate change, hence making planning for climate Bo¨hm, M., B. Collen, J.E.M. Baillie, P. Bowles, J. Chanson, N. Cox, G. Hammerson, M. Hoffmann, et al. 2013. The conservation change adaptation is necessary right from the start. If the status of the world’s reptiles. Biological Conservation 157: AZE approach is to fulfil its potential for achieving targets 372–385. doi:10.1016/j.biocon.2012.07.015. 11 and 12, timely actions must be taken. From an economic Brooks, T.M., R.A. Mittermeier, G.A.B. da Fonseca, J. Gerlach, M. point of view alone, swift action is required wherever Hoffmann, J.F. Lamoreux, C.G. Mittermeier, J.D. Pilgrim, et al. 2006. Global biodiversity conservation priorities. Science 313: possible to minimize the need for ex situ as the main 58–61. conservation approach rather than providing ‘‘only’’ a Brooks, T.M., S.H.M. Butchart, N.A. Cox, M. Heath, C. Hilton- safety net and to avoid the extra costs involved. A joint Taylor, M. Hoffmann, N. Kingston, J.P. Rodrı´guez, et al. 2015. approach to protect and conserve AZEs&s needs to be Harnessing biodiversity and conservation knowledge products to track the Aichi Targets and Sustainable Development Goals. finalized as soon as possible and a suitable organizational Biodiversity 16: 157–174. doi:10.1080/14888386.2015.1075903. setup needs to be established allowing an efficient direction Brooks, T.M., H.R. Akc¸akaya, N.D. Burgess, S.H.M. Butchart, C. and co-ordination of the joint approach. This AZE 2.0 Hilton-Taylor, M. Hoffmann, D. Juffe-Bignoli, N. Kingston, might arise from the current AZE or might be an entirely et al. 2016. Analysing biodiversity and conservation knowledge products to support regional environmental assessments. Scien- new platform, but speed is key. tific Data 3: 160007. doi:10.1038/sdata.2016.7. Butchart, S.H.M., M. Walpole, B. Collen, A. van Strien, J.P.W. Acknowledgements We are indebted to numerous colleagues for Scharlemann, R.E.A. Almond, J.E.M. Baillie, B. Bomhard, et al. engaging with us in discussions and debates around the topic in this 2010. Global biodiversity: Indicators of recent declines. Science paper. In particular, we are thankful to Onnie Byers, Markus Gusset 328: 1164–1168. doi:10.1126/science.1187512. and Nate Flesness for enriching our exploration of this subject. SMF Butchart, S.H.M., J.P.W. Scharlemann, M.I. Evans, S. Quader, S. is thankful to Ricardo Herrera and Rau´l Sanchez for their collegiate Aric, J. Arinaitwe, M. Balman, L.A. Bennun, et al. 2012. support during the preparation of this publication. We are also Protecting important sites for biodiversity contributes to meeting grateful to two anonymous reviewers for their comments and global conservation targets. PLoS ONE 7: e32529. doi:10.1371/ suggestions. journal.pone.0032529. Butchart, S.H.M., M. Clarke, R.J. Smith, R.E. Sykes, J.P.W. Open Access This article is distributed under the terms of the Scharlemann, M. Harfoot, G.M. Buchanan, A. Angulo, et al. Creative Commons Attribution 4.0 International License (http:// 2015. Shortfalls and Solutions for meeting national and global creativecommons.org/licenses/by/4.0/), which permits unrestricted conservation area targets: Meeting conservation area targets. use, distribution, and reproduction in any medium, provided you give Conservation Letters 8: 329–337. doi:10.1111/conl.12158/full. appropriate credit to the original author(s) and the source, provide a Butler, W.F., and T.G. Acott. 2007. An inquiry concerning the link to the Creative Commons license, and indicate if changes were acceptance of intrinsic value theories of Nature. Environmental made. Values 1: 149–168. Byers, O., C. Lees, J. Wilcken, and C. Schwitzer. 2013. The One Plan Approach: The philosophy and implementation of CBSG’s approach to integrated species conservation planning. WAZA REFERENCES Magazine 14: 2–5. Ceballos, G., P.R. Ehrlich, A.D. Barnosky, A. Garcia, R.M. Pringle, Abella´n, P., and D. Sa´nchez-Ferna´ndez. 2015. A gap analysis and T.M. Palmer. 2015. Accelerated modern human-induced comparing the effectiveness of Natura 2000 and national species losses: Entering the sixth mass extinction. Science protected area networks in representing European amphibians Advances 1: e1400253–e1400253. doi:10.1126/sciadv.1400253. and reptiles. Biodiversity and Conservation 24: 1377–1390. Conde, D.A., F. Colchero, M. Gusset, P. Pearce-Kelly, O. Byers, N. doi:10.1007/s10531-015-0862-3. Flesness, R.K. Browne, and O.R. Jones. 2013. Zoos through the Adenle, A.A., C. Stevens, and P. Bridgewater. 2015. Global Lens of the IUCN Red List: A global metapopulation approach conservation and management of biodiversity in developing to support conservation breeding programs. PLoS ONE 8: countries: An opportunity for a new approach. Environmental e80311. Science & Policy 45: 104–108. doi:10.1016/j.envsci.2014.10. Conde, D.A., F. Colchero, B. Gu¨neralp, M. Gusset, B. Skolnik, M. 002. Parr, O. Byers, K. Johnson, et al. 2015. Opportunities and costs

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 454 Ambio 2017, 46:443–455

for preventing vertebrate extinctions. Current Biology 25: R219– Oaxaca. International Union for Conservation of Nature xxiv: R221. 320 Crutzen, P.J. 2002. Geology of mankind. Nature 415: 23–23. Larsen, F.W., W.R. Turner, and T.M. Brooks. 2012. Conserving Emerson, J., D.C. Esty, M.A. Levy, C.H. Kim, V. Mara, A. de critical sites for biodiversity provides disproportionate benefits to Sherbinin, and T. Srebotnjak. 2010. 2010 Environmental people. PLoS ONE 7: e36971. doi:10.1371/journal.pone. Performance Index (EPI). New Haven: Yale Center for Envi- 0036971. ronmental Law & Policy, Yale University. Leme´nager, T., D. King, J. Elliott, H. Gibbons, and A. King. 2014. Fa, J.E., S.M. Funk, and D. O’Connell. 2011. Zoo conservation Greater than the sum of their parts: Exploring the environmental biology. Cambridge: Cambridge University Press. complementarity of state, private and community protected Fa, J.E., M. Gusset, N. Flesness, and D.A. Conde. 2014. Zoos have areas. Global Ecology and Conservation 2: 238–247. doi:10. yet to unveil their full conservation potential. Animal Conser- 1016/j.gecco.2014.09.009. vation 17: 97–100. Martin, T.G., S. Nally, A.A. Burbidge, S. Arnall, S.T. Garnett, M.W. Funk, S.M., and J.E. Fa. 2010. Ecoregion prioritization suggests an Hayward, L.F. Lumsden, P. Menkhorst, et al. 2012. Acting fast armoury not a silver bullet for conservation planning. PLoS ONE helps avoid extinction: Acting fast avoids extinctions. Conser- 5: e8923. doi:10.1371/journal.pone.0008923. vation Letters 5: 274–280. doi:10.1111/j.1755-263X.2012. Gascon, C., J.P. Collins, R.D. Moore, D.R. Church, J.E. McKay, and 00239.x. J.R.I. Mendelson. 2007. Amphibian Conservation Action Plan. Mascia, M.B., S. Pailler, R. Krithivasan, V. Roshchanka, D. Burns, Gland, Switzerland Cambridge, UK: IUCN/SSC Amphibian M.J. Mlotha, D.R. Murray, and N. Peng. 2014. Protected area Specialist Group. downgrading, downsizing, and degazettement (PADDD) in Gascon, C., T.M. Brooks, T. Contreras-MacBeath, N. Heard, W. Africa, Asia, and Latin America and the Caribbean, Konstant, J. Lamoreux, F. Launay, M. Maunder, et al. 2015. The 1900–2010. Biological Conservation 169: 355–361. doi:10. importance and benefits of species. Current Biology 25: R431– 1016/j.biocon.2013.11.021. R438. doi:10.1016/j.cub.2015.03.041. McCarthy, D.P., P.F. Donald, J.P.W. Scharlemann, G.M. Buchanan, Gusset, M., and G. Dick. 2010. ‘‘Building a Future for Wildlife’’? A. Balmford, J.M.H. Green, L.A. Bennun, N.D. Burgess, et al. Evaluating the contribution of the world zoo and aquarium 2012. Financial costs of meeting global biodiversity conserva- community to in situ conservation. International Zoo Yearbook tion targets: Current spending and unmet needs. Science 338: 44: 183–191. 946–949. doi:10.1126/science.1229803. Gusset, M., and G. Dick. 2011. The global reach of zoos and Moss, A., E. Jensen, and M. Gusset. 2015. Evaluating the contribution aquariums in visitor numbers and conservation expenditures. Zoo of zoos and aquariums to Aichi Biodiversity Target 1: Educa- Biology 30: 566–569. tional Impacts of Zoo Visits. Conservation Biology 29: 537–544. Gusset, M., J.E. Fa, and W.J. Sutherland. 2014. A horizon scan for doi:10.1111/cobi.12383. species conservation by Zoos and Aquariums. Zoo Biology 33: Myers, N., R.A. Mittermeier, C.G. Mittermeier, G.A.B. da Fonseca, 375–380. doi:10.1002/zoo.21153. and J. Kent. 2000. Biodiversity hotspots for conservation Hoffmann, M., C. Hilton-Taylor, A. Angulo, M. Bo¨hm, T.M. Brooks, priorities. Nature 403: 853–858. S.H. Butchart, K.E. Carpenter, J. Chanson, et al. 2010. The Newbold, T., L.N. Hudson, A.P. Arnell, S. Contu, A. De Palma, S. impact of conservation on the status of the world’s vertebrates. Ferrier, S.L.L. Hill, A.J. Hoskins, et al. 2016. Has land use Science 330: 1503–1509. pushed terrestrial biodiversity beyond the planetary boundary? A Holmes, G. 2014. What is a land grab? Exploring green grabs, global assessment. Science 353: 288–291. doi:10.1126/science. conservation, and private protected areas in southern Chile. The aaf2201. Journal of Peasant Studies 41: 547–567. doi:10.1080/03066150. OECD. 2016. Gross domestic product (GDP) (indicator). doi: 10. 2014.919266. 1787/dc2f7aec-en. Holmes, G. 2015. Markets, nature, neoliberalism, and conservation Pritchard, D.J., J.E. Fa, S. Oldfield, and S.R. Harrop. 2012. Bring the through private protected areas in southern Chile. Environment captive closer to the wild: Redefining the role of ex situ and Planning A 47: 850–866. doi:10.1068/a140194p. conservation. Oryx 46: 18–23. doi:10.1017/S0030605310001766. Howes, B., R. Pither, and K. Prior. 2009. Conservation implications Redford, K.H., P. Coppolillo, E.W. Sanderson, G.A.B. Da Fonseca, E. should guide the application of conservation genetics research. Dinerstein, C. Groves, G. Mace, S. Maginnis, et al. 2003. Endangered Species Research 8: 193–199. doi:10.3354/ Mapping the conservation landscape. Conservation Biology 17: esr00207. 116–131. Hsu, A., J. Emerson, M. Levy, A. de Sherbinin, L. Johnson, O. Malik, Ricketts, T.H., E. Dinerstein, T. Boucher, T.M. Brooks, S.H.M. and M. Jaiteh. 2014. Environmental Performance Index. Yale Butchart, M. Hoffmann, J.F. Lamoreux, J. Morrison, et al. 2005. Center for Environmental Law and Policy. Pinpointing and preventing imminent extinctions. Proceedings Isaac, N.J.B., S.T. Turvey, B. Collen, C. Waterman, and J.E.M. of the National Academy of Sciences of the United States of Baillie. 2007. Mammals on the EDGE: conservation priorities America 102: 18497–18501. doi:10.1073/pnas.0509060102. based on threat and phylogeny. PLoS ONE 2: e296. Rockstro¨m, J., W. L. Steffen, K. Noone, A˚ Asa Persson, F. S. Chapin IUCN. 2016. The IUCN Red List of threatened species. Version III, E. Lambin, T. M. Lenton, M. Scheffer, et al. 2009. Planetary 2016-1. boundaries: exploring the safe operating space for humanity. Jenkins, C.N., and L. Joppa. 2009. Expansion of the global terrestrial Rodrigues, A.S.L., S.J. Andelman, M.I. Bakarr, L. Boitani, T.M. protected area system. Biological Conservation 142: 2166–2174. Brooks, R.M. Cowling, L.D.C. Fishpool, G.A.B. da Fonseca, Juffe-Bignoli, D., T.M. Brooks, S.H.M. Butchart, R.B. Jenkins, K. et al. 2004. Effectiveness of the global protected area network in Boe, M. Hoffmann, A. Angulo, S. Bachman, et al. 2016. representing species diversity. Nature 428: 640–643. doi:10. Assessing the cost of global biodiversity and conservation 1038/nature02422. knowledge. PLoS ONE 11: e0160640. doi:10.1371/journal.pone. Rondinini, C., M. Di Marco, P. Visconti, S.H.M. Butchart, and L. 0160640. Boitani. 2014. Update or outdate: Long-term viability of the Lamoreux, J. F., M. W. McKnight, and R. Cabrera Hernandez. 2015. IUCN Red List. Conservation Letters 7: 126–130. doi:10.1111/ Amphibian Alliance for Zero Extinction Sites in Chiapas and conl.12040.

Ó The Author(s) 2017. This article is published with open access at Springerlink.com 123 www.kva.se/en Ambio 2017, 46:443–455 455

SCBD. 2010. Decision adopted by the Conference of the Parties to Wilson, K.A., N.A. Auerbach, K. Sam, A.G. Magini, A.S.L. Moss, the Convention on Biological Diversity at its tenth meeting. X/2. S.D. Langhans, S. Budiharta, D. Terzano, et al. 2016. Conser- The Strategic Plan for Biodiversity 2011–2020 and the Aichi vation research is not happening where it is most needed. PLoS Biodiversity Targets. https://www.cbd.int/doc/decisions/cop-10/ Biology 14: e1002413. doi:10.1371/journal.pbio.1002413. cop-10-dec-02-en.pdf. Young, R.P., M.A. Hudson, A.M.R. Terry, C.G. Jones, R.E. Lewis, V. SCBD. 2014. Progress towards the Aichi biodiversity targets: an Tatayah, N. Zue¨l, and S.H.M. Butchart. 2014. Accounting for assessment of biodiversity trends, policy scenarios and key conservation: Using the IUCN Red List Index to evaluate the actions: Global biodiversity outlook 4 (GBO-4) technical report. impact of a conservation organization. Biological Conservation Montreal, , Canada: Secretariat of the Convention on 180: 84–96. doi:10.1016/j.biocon.2014.09.039. Biological Diversity (CBD). Zoological Society of London, ZSL. 2016. EDGE of Existence SCBD. 2016. Convention on Biological Diversity. List of Parties. programme Convention on Biological Diversity. https://www.cbd.int/ information/parties.shtml AUTHOR BIOGRAPHIES Seto, K.C., B. Gu¨neralp, and L.R. Hutyra. 2012. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and Stephan M. Funk is a lecturer at the Universidad de La Frontera in carbon pools. Proceedings of the National Academy of Sciences Chile. His research area is conservation biology, species ecology, 109: 16083–16088. molecular genetics, and human and wildlife population genetics. He is Steffen, W., P.J. Crutzen, and J.R. McNeill. 2007. The Anthropocene: Director of Science at the not-for-profit consultancy NatureHeritage Are humans now overwhelming the great forces of nature. dedicated to biodiversity conservation. Ambio 36: 614–621. Address: Centro de Excelencia en Medicina Traslacional, Universi- Stern, N.H., and H.M. Treasury. 2006. Stern review: The economics dad de La Frontera, Piso 4, Av Alemania 0458, Temuco, Chile. of climate change, vol. 30. London: HM Treasury. Address: Nature Heritage, St. Lawrence, Jersey. Tapley, B., K.S. Bradfield, C. Michaels, and M. Bungard. 2015. e-mail: [email protected] Amphibians and conservation breeding programmes: Do all threatened amphibians belong on the ark? Biodiversity and Dalia Conde is the Director of Science at Species 360 and Associate Conservation 24: 2625–2646. doi:10.1007/s10531-015-0966-9. Professor at the Department of Biology at the Max-Planck Odense Thornton, D. H., and R. J. Fletcher. 2013. Body size and spatial scales Center on the Biodemography of Aging, in Denmark. Her research in avian response to landscapes: a -analysis. Ecography. ranges from species ecology to the role of zoos in conservation. doi:10.1111/j.1600-0587.2013.00540.x. Address: Department of Biology, Max Planck Odense Center, UNEP-WCMC. 2016. Protected Planet 2014-2015- World Database University of Southern Denmark, Campusvej 55, 5230 Odense M, on Protected Areas dataset. Protected Planet. Denmark. Waldron, A., A.O. Mooers, D.C. Miller, N. Nibbelink, D. Redding, Address: Species 360, 7900 International DriveSuite 1040, Bloom- T.S. Kuhn, J.T. Roberts, and J.L. Gittleman. 2013. Targeting ington, MN 55425, USA. global conservation funding to limit immediate biodiversity e-mail: [email protected] declines. Proceedings of the National Academy of Sciences 110: 12144–12148. doi:10.1073/pnas.1221370110. John Lamoreux is a conservation scientist who focuses on strategies Watson, J.E.M., N. Dudley, D.B. Segan, and M. Hockings. 2014. The to improve the conservation status of threatened species. He con- performance and potential of protected areas. Nature 515: tributed to this article as an independent researcher. 67–73. doi:10.1038/nature13947. Address: 11013 Ring Rd, Reston, VA 20190, USA. Watson, J.E.M., E.S. Darling, O. Venter, M. Maron, J. Walston, H.P. e-mail: [email protected] Possingham, N. Dudley, M. Hockings, et al. 2015. Bolder science needed now for protected areas. Conservation Biology. John E. Fa (&) is a Professor of Biodiversity and Human Devel- doi:10.1111/cobi.12645. opment in the School of Science & The Environment at the Manch- Watson, J.E.M., D.F. Shanahan, M. Di Marco, J. Allan, W.F. ester Metropolitan University. His research area is conservation Laurance, E.W. Sanderson, B. Mackey, and O. Venter. 2016. science with particular emphasis on endangered species, biodiversity, Catastrophic declines in wilderness areas undermine global and use of wildlife by humans in tropical ecosystems. environment targets. Current Biology online. doi:10.1016/j.cub. Address: Division of Biology and Conservation Ecology, School of 2016.08.049. Science & The Environment, Manchester Metropolitan University, Wilson, K.A., M.C. Evans, M. Di Marco, D.C. Green, L. Boitani, H.P. All Saints Building, All Saints, Manchester M15 6BH, UK. Possingham, F. Chiozza, and C. Rondinini. 2011. Prioritizing e-mail: [email protected] conservation investments for mammal species globally. - sophical Transactions of the Royal Society B: Biological Sciences 366: 2670–2680. doi:10.1098/rstb.2011.0108.

Ó The Author(s) 2017. This article is published with open access at Springerlink.com www.kva.se/en 123 www.nature.com/scientificreports

OPEN Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos received: 10 June 2016 accepted: 30 September 2016 across mammals Published: 07 November 2016 Morgane Tidière1, Jean-Michel Gaillard1, Vérane Berger1,. Dennis W H. Müller2, Laurie Bingaman Lackey3, Olivier Gimenez4, Marcus Clauss5 & Jean-François Lemaître1

While it is commonly believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared four survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of free-ranging and zoo populations of more than 50 mammal species. We found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The effect was most notable in species with a faster pace of life (i.e. a short life span, high reproductive rate and high mortality in the wild) because zoos evidently offer protection against a number of relevant conditions like predation, intraspecific competition and diseases. Species with a slower pace of life (i.e. a long life span, low reproduction rate and low mortality in the wild) benefit less from captivity in terms of longevity; in such species, there is probably less potential for a reduction in mortality. These findings provide a first general explanation about the different magnitude of zoo environment benefits among mammalian species, and thereby the effort that is needed to improve captive conditions for slow-living species that are particularly susceptible to extinction in the wild.

Zoological gardens represent artificial environments in which animals are maintained, bred and displayed. By doing so, zoos achieve a diversity of goals beyond their visitors’ recreation: basic zoological and conservation education reaches 700 million visitors per year all over the world1. Continuing research and expertise building by many thousands of zoo staff worldwide continuously improves knowledge of animal, population and ecosystem management. Zoos also aim to maintain viable ex situ insurance populations of endangered species that can be used for re-introduction to the wild2,3. Zoo staff manages and generates funding for in situ conservation projects1,4. Finally, zoos facilitate opportunities for researchers to increase expertise in a large variety of areas, from basic zoology to applied husbandry and molecular biology. When assessing the justification of holding nondomestic species in zoos, the welfare of the individual animals housed in captivity is a critical ethical issue that has to be weighed against these aims5. There is no single proxy to measure the welfare of animals. Indicators typically employed include measures of survival (such as longevity, annual survival, or ageing rate), reproduction (such as fertility or litter size), physiology (such as stress hormones or the occurrence of specific diseases) and behavior (such as stereotypies)5,6. It is typically believed that zoo ani- mals live longer than their free-ranging conspecifics due to the consistent provision of food, water, and shelter from harsh climates, the absence of predation and management to minimize violent intraspecific encounters and accidents, as well as veterinary prophylactic and therapeutic intervention. However, zoo animals may be subject to behavioral deficits6. While an increasing number of comparative studies have demonstrated species-specific dif- ferences in the response to zoo-conditions7–9, and a few species-specific comparisons of survival metrics between free-ranging and captive specimens have been published10,11, large-scale inter-specific comparisons of captive and

1Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622, Villeurbanne, France. 2Zoologischer Garten Halle GmbH, Fasanenstr. 5a, 06114 Halle (Saale), Germany. 3World Association of Zoos and Aquariums (WAZA), Gland, Switzerland. 4UMR 5175, Centre d’Ecologie Fonctionnelle et Evolutive, campus CNRS, 1919 route de Mende, 34293, Montpellier Cedex 5, France. 5Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland. Correspondence and requests for materials should be addressed to M.T. (email: [email protected])

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 1 www.nature.com/scientificreports/

Figure 1. Graphical displays of the metrics of survival and actuarial senescence analyzed in this study. Data from female (Panthera leo) in zoo (in brown) and free-ranging (in green) conditions are used for illustrative purposes. Female lions in the zoo population live longer (age in years) and have a lower baseline annual mortality (in log%), a later onset of senescence (in years) and a lower rate of actuarial senescence (measured as the exponential rate of mortality increase per year).

free-ranging populations have not yet been performed. Indeed, it is probably difficult to gather accurate demo- graphic estimates in these two contrasted environments for a large range of species. In mammals, comparisons between wild and zoo populations published so far were based on a small number of species (consistently less than 25) and did not control for confounding effects of phylogeny12,13 or were restricted to a narrow taxonomic range (e.g. the mammalian order Artiodactyla14). In addition, these studies have led to conflicting results because they both failed12,13 and succeeded14 to detect the expected lower actuarial senescence rate (i.e. the rate of decrease in annual survival with increasing age) in zoos. Lastly, none of these studies included survival metrics other than senescence rate, such as longevity or age at the onset of senescence. Therefore, whether the common belief that mammals in zoos outlive their wild counterparts holds true remains unknown. To address this question, we compared a set of survival metrics derived from life tables available from the literature for males and females of free-ranging populations of 59 mammalian species (including eight different orders, see Supplementary Figure S1) to those derived from the data on captive specimens of the same species from the Species360 database13,15 (formerly named International Species Information System database, ISIS). Based on these sex-specific life tables, four metrics describing the survival pattern of each species were calculated: longevity, baseline annual mortality, age at the onset of senescence and rate of senescence (Fig. 1). We compared these metrics between free-ranging and captive populations using linear models and controlled for phylogenetic relatedness among species using a mammal super-tree16. An expected higher longevity in zoos can originate from a lower baseline mortality, a later onset of senescence, a lower rate of senescence, or any combination of these measures (Fig. 1). Results In 84% of species we analyzed (85% for males and 83% for females, including all carnivores), longevity was higher in zoos than in the wild for both sexes (Figs 2 and 3A). The positive relationship between longevity in the zoo and in the wild had a slope less than 1 (Table 1), indicating that short-lived species benefited from living in zoos to a higher extent than long-lived ones (Fig. 3A). In about 69% of the species (76% for males and 63% for females), the age at the onset of senescence was identical or delayed in zoos compared to the wild (Fig. 3B). The positive rela- tionship between zoo and wild data of onset of senescence also had a slope less than 1 (Table 1), again indicating that species with an early onset of actuarial senescence delayed this onset in captivity to a larger extent than spe- cies with a late onset of actuarial senescence. For these latter species, often no difference in response to captivity occurred, and some species even displayed an earlier onset of senescence in zoos (Supplementary Figure S2). The slopes of the relationship between the baseline mortality (Fig. 3C) or the rates of actuarial senescence (Fig. 3D) at the zoo and in the wild were close to zero (Table 1), indicating that these metrics did not strongly covary between zoo and wild populations. While the baseline mortality was lower in zoos for about 62% of the species (61% for males and 64% for females) and the rate of senescence was lower in zoos for about 73% of the species (76% for males and 71% for females), the nearly horizontal slopes underline the importance of the species’ pace of life for these two metrics: species with a high baseline mortality and high rate of senescence in the wild (i.e. species with a faster pace of life) typically had lower values at the zoo. In contrast, species with a low baseline mortality and

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 2 www.nature.com/scientificreports/

Figure 2. Longevity in free-ranging and zoo conditions for males (triangles) and females (circles) of each species of Artiodactyla, Carnivora, Primates and other orders (Diprotodontia, Lagomorpha, Perissodactyla, Rodentia and Scandentia). Species living longer in zoos are indicated with solid lines and species living shorter in zoos are indicated with dotted lines. Full species names are given in Supplementary Table S1. Animal pictures: nebojsa78©123RF.com.

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 3 www.nature.com/scientificreports/

Figure 3. Comparison of (A) longevity, (B) age at the onset of senescence, (C) baseline annual mortality, and (D) rate of senescence (for males and females, respectively) between zoo and wild populations of 59 mammalian species. Points represent raw data, full lines represent the relationship between captive and wild estimates (on a log scale with 95% confidence interval of the model in grey) and the grey dashed line represents the equation y =​ x. For females, African (Loxodonta africana) and Asian (Elephas maximus) elephants and (Hippopotamus amphibius) were added for illustrative purposes, but were not included in the analysis.

Longevity Baseline mortality Onset of senescence Rate of senescence slope intercept slope intercept slope intercept slope intercept Males 53 species 51 species 51 species 45 species 0.330 (0.191; 0.469) 6.432 (4.461; 8.403) −0.010 (−0.053; 0.033) 0.143 (0.113; 0.174) 0.538 (0.330; 0.746) 2.200 (1.122; 3.279) 0.186 (0.001; 0.372) 0.113 (0.092; 0.135) Females 58 species 56 species 56 species 48 species 0.351 (0.246; 0.456) 6.621 (4.410; 8.833) −0.010 (−0.080; 0.061) 0.115 (0.102; 0.128) 0.327 (0.123; 0.532) 2.413 (0.878; 3.947) 0.005 (−0.178; 0.188) 0.073 (0.055; 0.091)

Table 1. Parameter estimates (with 95% confidence interval) of linear regressions (on the log-scale) linking the species-specific metrics obtained in zoo and free-ranging populations. Estimates were obtained from Linear Models when the phylogenetic signal λ​ was statistically not different from zero (i.e. for longevity, age at the onset of senescence and rate of senescence) and from Phylogenetic Generalized Least-Squares models when λ​ statistically differed from zero (for baseline mortality).

a low rate of senescence in the wild (i.e. species with a slower pace of life) typically had higher values at the zoo. Notably, mammals in zoos displayed less variation in both baseline mortality and rate of senescence than in the wild (Fig. 3), indicating more standardized conditions in zoos. All these patterns were remarkably similar for both sexes (Fig. 3). Discussion Our findings indicate that, in general, a life in zoos allows mammals to live longer. However, our data suggest that the species-specific pace of life influences the extent to which a given species may benefit from captivity. Species with a faster pace of life typically suffer from high levels of environmentally-driven mortality in the wild including predation17, and zoos offer good protection against such causes of mortality. Mammals with a slower pace of life, however, are typically characterized by a later age at first reproduction, a longer gestation period, lower reproduc- tive rates and lower annual mortality18. They do not benefit as much from living in zoos in terms of survivorship, or even have a slightly reduced longevity and higher senescence rates, which might be attributable to an earlier onset of breeding in these species in a zoo setting19,20. Thus, our broad-scale study supports previous work report- ing that both Asian and African elephant females live longer in the wild than in zoos10 (Fig. 3) and provides a first general explanation why different species may benefit with different magnitudes from captivity. Data for the common hippopotamus21, included in Fig. 3 for a visual comparison alongside the elephant species, corroborate this interpretation. These findings emphasize that husbandry efforts to optimize the longevity of species with a slower pace of life should be intensified.

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 4 www.nature.com/scientificreports/

To what extent improvement of captive conditions has already occurred in zoos cannot be evaluated with our data. For long-lived species, we cannot include animals born in recent years because of the need to include only extinct cohorts to avoid overestimating age-specific mortality rates (i.e. only dead individuals can be included in life tables). If we assume that age-specific mortality decreases over time in zoos thanks to improved husbandry conditions, especially in recent years and independently of a species’ pace of life, then the absence of recent cohorts for long-lived species in our analyses might account at least partly for our finding that the survival benefit of living in zoos was less pronounced in long- than in short-lived species. We might expect improved living condi- tions in zoos to have delayed positive effects in long-lived species. For example, there has been tremendous effort in building new elephant enclosures in a great number of zoos in the last decade (DWHM and MC, pers. obs.) and large-scale studies have been performed on the potential to increase captive elephant welfare22. However, the benefits of such efforts on survival measures will not be detectable before many years from now. In this respect, it should be kept in mind that our findings, especially concerning the longer-lived species, mostly reflect past husbandry practices that are not necessarily representative any longer. Our study refutes previous conclusions that the rate of actuarial senescence of vertebrates is not influenced by captivity13. When accounting for differences in the pace of life among species, we clearly demonstrate that faster-living species senesce at a lower rate in zoos than in the wild. In addition, we show that both males and females respond similarly to captive conditions. Such a discovery provides indirect evidence that the genuine sex differences in survival patterns in mammalian species subjected to high sexual selection23 involve physiological mechanisms and cannot only be explained by higher susceptibility of males to environmental conditions. Carnivores show enhanced survival in zoos in our study, but are more susceptible to behavioral abnormalities7, highlighting the need for husbandry techniques to reduce these abnormalities while simultaneously maintaining the survival benefits. Although zoos offer simplified environments, social interactions might be as complex and challenging as in the wild, considering the high frequency of non-antagonistic contacts with humans and other species. Do animals, even when born and raised in zoos, perceive their enclosures as a spatial constraint in terms of compressed home ranges, or as an actual restriction of freedom in terms of a limitation of their own choices? Alternatively, do animals perceive zoos as a safe habitat where potential predators, food scarcity, or extreme cli- matic conditions are absent, allowing them to drastically reduce vigilance24? Our mere comparison of survival metrics between wild and captive populations should not be interpreted as a conclusive ethical judgment. Our findings should rather be considered as evidence that zoos generally enhance the longevity of mammals, except in species where there is little potential for such an enhancement because of their slower pace of life, which is already linked to both a low mortality and a high longevity in the wild. Because species with a slow pace of life are particularly threatened by extinction25, maintaining ex situ insurance populations of such threatened species remains a crucial conservation strategy. Methods Life tables. Zoo and wild population life tables were compiled from the Species360 database and literature, respectively (see Lemaître et al.14 for more details). Concerning free-ranging populations, publications contain- ing life-tables from semi-captive populations were excluded to allow a strict comparison between captive and free-ranging populations. For 25 species, we collected several life tables from the same or different populations. When available, we gave preference to life tables obtained from longitudinal data. When several life tables of a given quality were available, we averaged them. When life tables were given in months or not with an integer of years, a standardization was made to obtain the survival at each integer age. For 9 species, the total number of individuals followed or considered was not given in the focal study. In such cases, we arbitrarily assumed that 100 individuals were considered per sex (close to the median value of the number of individuals alive at 1 year of age in the life tables we used). For wild life tables with a known total number of individuals (N =​ 50 species), the lowest was found for females of Mustela vison for which the life table only included 30 individuals, and the highest is observed for males of Oryctolagus cuniculus with a total of 9,020 individuals (Supplementary Table S1). For captive populations, we only used extinct cohorts of animals for which the sex and both birth and death dates were known, implying that animals were born in captivity. Extinct cohorts were defined as all cohorts born before a given year, which is determined as 2013 minus three quarters of the maximum longevity recorded for the species (Supplementary Table S1). As in captivity the sex ratio could be biased due to the culling of some young males during the first year for management issues (mostly in ruminants), we only computed parameters when at least 25 individuals for each sex of each species were alive at 1 year of age to get accurate estimates of age-specific survival. We finally obtained a dataset of 52 species for which data for both females and males were available, with one additional species with male-only data (leading to 53 species in males) and 6 additional species with female- only data (leading to 58 species in females) (Supplementary Table S1). For both captive and wild populations, we made the same calculations to obtain exactly comparable life tables. For visual comparison only, we included data from females of the two elephant species26,27 and sex-combined data from the common hippopotamus21 in the resulting data plots but did not include them in the analyses, as their data did not correspond to the data selection criteria stated above.

Metrics of survival. To measure species- and sex-specific patterns of survival and actuarial senescence in captive and free-ranging populations, we used four distinct but complementary metrics: the longevity, the base- line annual mortality, the age at the onset of actuarial senescence and the rate of actuarial senescence (see Fig. 1. for a graphical display of these metrics). The longevity was extracted from species-specific life tables for both males and females and for both captive and wild populations (Supplementary Table S1). We defined longevity as the age at which 90% of individuals from the initial cohort (alive at 1 year of age) had died (Fig. 1). This allows avoiding spurious estimates due to the exceptionally long life of a few individuals15. However, this trait (called ‘longevity’ hereafter) is not a direct measure of senescence because it does not include any explicit information

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 5 www.nature.com/scientificreports/

about age-dependent decline in survival. For other metrics, we first measured the logit-transformed age-specific mortality from a given life table. We thus constrained survival of 1 to be equal to 0.99, and we fitted a Generalized Additive Model to obtain the age-specific mortality curve. Since both theoretical and empirical evidence reveal that actuarial senescence does not start prior to the age of sexual maturity28,29, the onset of actuarial senescence was defined as the age at which the annual mortality rate was the lowest between the age at sexual maturity and the age at which 90% of individuals from the initial cohort have died (Fig. 1, Supplementary Table S1). The age at sexual maturity (in years) was collected for each sex and each species from a specific literature sur- vey (Supplementary Table S2). The baseline mortality for each sex of each species and for both captive and free-ranging conditions was defined as the annual mortality observed at the age corresponding to the onset of senescence (Fig. 1, Supplementary Table S1). The baseline mortality at the onset of actuarial senescence corre- sponds to the lowest mortality observed for a given sex, species, and environment (i.e. wild or captive) between the age at sexual maturity and the age at which 90% of individuals from the initial cohort have died. The rate of senescence was measured as the slope of the linear regression of survival (on a log scale) on age computed between the age at the onset of senescence and the age at which 90% of individuals from the initial cohort have died (i.e. our measure of longevity)30 (Fig. 1, Supplementary Table S1). For short-lived species and life tables with a small sample size, we used the age at which at least 5 individuals of a given sex were still alive instead of the age at which 90% of the initial cohort was dead, both to achieve unbiased estimates due to the too few years lived by short-lived species, and to avoid estimating survival from less than 5 individuals. All estimates are reported in Supplementary Table S1 and displayed on Fig. 2 and Supplementary Figures S2–S4.

Comparative analysis. To avoid biased assessment of the variation in survival patterns between captive and free-ranging populations, we controlled all the analyses for the non-independence between species due to shared ancestry using ‘Phylogenetic Generalized Least-Squares’ (PGLS) models31. A phylogeny was built for the 59 spe- cies (Supplementary Figure S1) using the phylogenetic super-tree of mammals published by Bininda-Emonds et al.16,32. Survival and senescence metrics were compared between free-ranging and captive males and females using linear models. Longevity and the onset and rate of actuarial senescence metrics were log-transformed, while baseline annual mortality was logit-transformed prior to any analysis. In a first part, the results of which are dis- played in the main text, we analyzed the relationship between the metric measured in zoos (dependent variable) and the corresponding metric measured in wild populations (independent variable). A higher (for longevity and onset of senescence) or a lower (for baseline mortality and rate of senescence) value in captivity indicates that the focal species performs better in zoos. In a second part, we tested whether the quality of demographic estimates in the wild (i.e. measured from longitudinal or transversal studies) and species body mass (log-transformed) influenced the relationships between captive and wild metrics. Survival and senescence patterns are strongly asso- ciated with body mass33. Typically, larger species live longer18 and show a lower rate of senescence34 compared to small species, and have a slower pace of life35. To assess whether the patterns we report held when accounting for size differences among species, we included log-transformed body mass as a covariate in our models in a second- ary analysis. We collected information about sex-specific mean adult body mass from the literature for each spe- cies analyzed (Supplementary Table S2). Therefore, for each of the four survival or senescence metrics in zoos and for a given sex, the full model included the corresponding wild metric and mean adult body mass as covariates, and the two-way interaction between the wild metric and data quality (as a fixed factor using longitudinal data as the reference). We then reduced the model by testing nested models by likelihood-ratio tests (LRT) so that the final model only included variables with statistically significant effects. A total of 3 nested models were tested for each of the metrics analyzed (Supplementary Table S3). A G-test was performed in each case. Models including the interaction between data quality and the wild estimates were never selected, whatever the survival or actuarial senescence metric considered (Supplementary Table S3). This suggests that quality of the wild demographic esti- mates did not influence the relationship between zoo and wild metrics. Moreover, we observed that body mass influenced zoo metrics in the same direction as the pace of life (Supplementary Table S4), leaving the patterns unchanged, whether including body mass in the models or not. All of these results are provided in Supplementary data (Supplementary Tables S3 and S4). For ruminant species, it has been shown that grazer species (whose natu- ral diet consists mainly of grass) perform better than browser species (whose natural diet consists mainly of leaves or twigs) in captivity, in terms of survival and actuarial senescence9,14. In a complementary analysis, we therefore took this pattern into account and corrected the four survival and senescence metrics by including the percentage of grass in the natural diet of each ruminant species in the model. For all ruminant species, survival and senes- cence metrics were then adjusted for 60% (median, N = ​27) of grass in the natural diet. However, results remained remarkably similar with or without this correction (Supplementary Table S5). All analyses were performed with R version 2.14.036 and parameter estimates are given with the 95% confidence interval. References 1. Gusset, M. & Dick, G. The global reach of zoos and aquariums in visitor numbers and conservation expenditures. Zoo Biol. 30, 566–569 (2011). 2. Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509 (2010). 3. Conde, D. A., Flesness, N., Colchero, F., Jones, O. R. & Scheuerlein, A. An emerging role of zoos to conserve biodiversity. Science 331, 1390–1391 (2011). 4. Tribe, A. & Booth, R. Assessing the role of zoos in wildlife conservation. Hum. Dimens. Wildlfe 8, 65–74 (2003). 5. Hosey, G., Melfi, V. & Pankhurst, S. Zoo Animals: Behaviour, Management, and Welfare. (OUP Oxford, 2013). 6. Mason, G. J. Species differences in responses to captivity: stress, welfare and the comparative method. Trends Ecol. Evol. 25, 713–721 (2010). 7. Clubb, R. & Mason, G. Animal welfare: captivity effects on wide-ranging carnivores. Nature 425, 473–474 (2003). 8. Mason, G., Clubb, R., Latham, N. & Vickery, S. Why and how should we use environmental enrichment to tackle stereotypic behaviour? Appl. Anim. Behav. Sci. 102, 163–188 (2007).

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 6 www.nature.com/scientificreports/

9. Müller, D. W. H. et al. Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants. Proc. R. Soc. B Biol. Sci. 278, 2076–2080 (2011). 10. Clubb, R. et al. Compromised survivorship in zoo elephants. Science 322, 1649 (2008). 11. Larson, S. M., Colchero, F., Jones, O. R., Williams, L. & Fernandez-Duque, E. Age and sex-specific mortality of wild and captive populations of a monogamous pair-bonded primate (Aotus azarae). Am. J. Primatol. 78, 315–325 (2016). 12. Ricklefs, R. E. & Scheuerlein, A. Comparison of aging-related mortality among birds and mammals. Exp. Gerontol. 36, 845–857 (2001). 13. Ricklefs, R. E. Life-history connections to rates of aging in terrestrial vertebrates. Proc. Natl. Acad. Sci. 107, 10314–10319 (2010). 14. Lemaître, J.-F., Gaillard, J.-M., Bingaman Lackey, L., Clauss, M. & Müller, D. W. H. Comparing free-ranging and captive populations reveals intra-specific variation in aging rates in large herbivores. Exp. Gerontol. 48, 162–167 (2013). 15. Moorad, J. A., Promislow, D. E. L., Flesness, N. & Miller, R. A. A comparative assessment of univariate longevity measures using zoological animal records. Aging Cell 11, 940–948 (2012). 16. Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007). 17. Promislow, D. E. L. & Harvey, P. H. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. 220, 417–437 (1990). 18. Gaillard, J.-M., Loison, A., Festa-Bianchet, M., Yoccoz, N. G. & Solberg, E. In Life Span: Evolutionary, Ecological, and Demographic Perspectives 29, 39–56 (Carey, J. R. & Tuljapurkar, S., 2003). 19. Taylor, V. J. & Poole, T. B. Captive breeding and infant mortality in Asian elephants: a comparison between twenty western zoos and three eastern elephant centers. Zoo Biol. 17, 311–332 (1998). 20. Littleton, J. Fifty years of chimpanzee demography at Taronga Park Zoo. Am. J. Primatol. 67, 281–298 (2005). 21. Laws, R. M. Dentition and ageing of the hippopotamus. Afr. J. Ecol. 6, 19–52 (1968). 22. Meehan, C. L., Mench, J. A., Carlstead, K. & Hogan, J. N. Determining connections between the daily lives of zoo elephants and their welfare: an epidemiological approach. PLOS ONE 11, e0158124 (2016). 23. Tidière, M. et al. Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants. Evolution 69, 3123–3140 (2015). 24. van Schaik, C. P. et al. The reluctant innovator: and the phylogeny of creativity. Phil Trans R Soc B 371, 20150183 (2016). 25. Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. Predicting extinction risk in declining species. Proc. R. Soc. Lond. B Biol. Sci. 267, 1947–1952 (2000). 26. Moss, C. J. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J. Zool. 255, 145–156 (2001). 27. Mar, K. U. In Giants on our Hands: Proceedings of the International Workshop on the Domesticated Asian Elephant 195–211 (Baker, I. & Kashio, M., 2002). 28. Péron, G., Gimenez, O., Charmantier, A., Gaillard, J.-M. & Crochet, P.-A. Age at the onset of senescence in birds and mammals is predicted by early-life performance. Proc. R. Soc. B Biol. Sci. 277, 2849–2856 (2010). 29. Gamelon, M. et al. Do age-specific survival patterns of fit current evolutionary theories of senescence? Evolution 68, 3636–3643 (2014). 30. Lemaître, J.-F. & Gaillard, J.-M. Polyandry has no detectable mortality cost in female mammals. PLOS ONE 8, e66670 (2013). 31. Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002). 32. Bininda-Emonds, O. R. P. The delayed rise of present-day mammals. Nature 456, 274 (2008). 33. Brunet-Rossini, A. K. & Austad, S. N. In Handbook of the Biology of Aging. 243–266 (Edward J. Masoro and Steven N. Austad, 2006). 34. Jones, O. R. et al. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol. Lett. 11, 664–673 (2008). 35. Gaillard, J.‐M. et al. Generation time: a reliable metric to measure life‐history variation among mammalian populations. Am. Nat. 166, 119–123 (2005). 36. R Development Core Team. R: A language and environment for statistical computing. (2011). Acknowledgements Data reported in this paper originate from Species360 for captive life tables and from literature for free-ranging life tables, and are available in the Supplementary Materials (Tables S1 and S2). M.T. is funded by the French Ministry of Education and Research. We thank Jeanne Peter Zocher of the Vetsuisse Faculty (Zurich) for the permission to use her images of hippopotamus, elephants and lion. We also thank Jean-Michel Hatt, Sandra Wenger and Stamos Tahas for comments on the manuscript. Author Contributions J.M.G., D.W.H.M., M.C. and J.F.L. designed the study; M.T., J.M.G., V.B., D.W.H.M., L.B.L., M.C. and J.F.L. collated the data; M.T., J.M.G., V.B., O.G., M.C. and J.F.L. analyzed the data; M.T. and M.C. wrote the first draft of the manuscript that then received input from all other authors. Additional Information Supplementary information accompanies this paper at http://www.nature.com/srep Competing financial interests: The authors declare no competing financial interests. How to cite this article: Tidière, M. et al. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Sci. Rep. 6, 36361; doi: 10.1038/srep36361 (2016). Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

© The Author(s) 2016

Scientific Reports | 6:36361 | DOI: 10.1038/srep36361 7