IUCN’s red list of threatened species: its importance in the conservation of mammals in Brazil

This paper analyzed representatives of the class Mammalia on the International Union for Conservation of Nature’s (IUCN) Red List of threatened species and evaluated whether the Protected Areas have fulfilled their function of protecting habitats. In the literature review, Protected Areas were found to be part of programs for the protection and recovery of threatened species. However, these areas continue to be insufficient due to the increasing destruction caused by humans, mainly the degradation of habitats upon which these organisms depend. By reviewing twelve IUCN lists containing mammals (from 1964 to 2018), the number of threatened species on each list were found to be increasing, reflecting greater knowledge of mammal species. In Brazil, eight lists were reviewed. Notably, one list contained species that were not included in the subsequent list, which may imply that protections implemented for the conservation of these animals had an effect in mitigating their extinction, and the creation of Protected Areas are chief among the conservation measures that resulted in such successes.


EXTINCTIONS
Since the emergence of life on Earth, 3.5 billion years ago, mass extinctions of species have occurred, whether by natural causes (as in the first five major extinctions) or artificial causes (human in case of the sixth major extinction currently underway) (WAKE; VREDENBURG, 2008;BARNOSKY et al., 2011;KOLBERT, 2015).
Extinctions by natural causes can occur slowly or suddenly. The slow ones, also called background extinctions, occur periodically over millennia. The sudden ones as in the case of the Cretaceous-Paleogene extinction event are responsibles for mass extinctions (involving a large number of organisms) in a short geological time interval and resulting in losses of more than three quarters of the world's species (WAKE;VREDENBURG, 2008;KOLBERT, 2015). The events with a physical cause that led to mass extinctions were: Asteroid impacts, climate change, shifts in plate tectonics, volcanic events, and rising sea levels (PIEVANI, 2014). In the last 540 million years, there have been five major mass extinction events, the so-called Big Five. The best known of these was the one that decimated the dinosaurs, occurring in the Cretaceous, and the largest occurred in the Late Permian, resulting in the loss of 95% of all species (WAKE;VREDENBURG, 2008;BARNOSKY et al., 2011). These were remarkable events that, despite the great magnitude, balanced the loss of some species with the appearance of others, which is not the case today. From a geological point of view, changes are happening too fast and the recovery time of the species has gone unheeded (PIEVANI, 2014).
The artificial cause started with the emergence of humans and the disappearance of other species has been notable, as the transformations that species have undergone nowadays do not compare to anything in terrestrial history (ELDREDGE, 2001;SCHULTZ, 2010;CEBALLOS et al., 2015). Initially, every place that humans set foot, large animals, such as mammals, were decimated, mainly through hunting, then over time the causes and the groups that were impacted also increased (FERNANDEZ; ARAUJO, 2012). These species have not yet been described and many are not even known (PIEVANI, 2014).
Excessive consumption of natural resources, predatory hunting and fishing, pollution, habitat degradation, introduction of invasive species, overexploitation, and population growth are the main causes of biodiversity loss (WILSON, 2010). Animal trafficking is another important source of loss (ROSEN; SMITH, 2010). These events alter ecosystem processes and unleash disorders on continental scales triggering what is called an extinction cascade (DIRZO et al., 2014).
Brazilian Journal of Animal and Environmental Research, Curitiba, v.6, n.2, p. 1802-1831, abr./jun., 2023 Modern extinction rates have risen sharply in the past 200 years, which leads to an association with the ascension of industrial society. Even though scholars cannot say precisely how many species exist and how many have disappeared over the years, it is possible to say that modern rates are exceptionally high, suggesting the existence of the event referred as "Sixth mass extinction" (CEBALLOS et al., 2015). This sixth mass extinction event caused and causes a great impact on biodiversity, also involving the economic and social sector for future generations (WILSON, 2010).

THREATENED SPECIES AND IUCN'S RED LISTS
Even though there is no way to recover all lost biodiversity, it is still possible to reduce this loss through science and technology (WILSON, 2010). In this sense, the International Union for Conservation of Nature's (IUCN) red lists play a major role . The International Union for Conservation of Nature, whose original name was International Union for the Protection of Nature (IUPN), was created on October 5, 1948. It currently has 1,300 member organizations and 15,000 experts organized into six commissions dedicated to species survival, environmental laws, Protected Areas, social and economic policy, ecosystem management, and education and communication. Since its creation, it has become the global authority on the state of nature conservation and the measures necessary to protect it (IUCN, 2019a).
The Red List of Threatened Species was proposed by IUCN in order to identify the threats that lead species to extinction and to monitor the evolution of the biodiversity conservation status.
With these lists published periodically, actions can be taken to recover species threatened with extinction and preserve those that have not yet entered this category .
IUCN published its first list of threatened species in 1964 (SMART; TAYLOR; MITTERMEIER, 2014). In 2016, there were more than 250 lists developed in more than 100 countries, covering all taxonomic classes with information on the conservation status of 82,954 species. The goal for 2020 is to reach 160,000 (COLLEN et al., 2016 (IUCN, 1964).

II) 1964 WWF -The Launching of a New Ark. First Report of the World Wildlife Fund: Sir
Pitter Scott's book (Scott, 1964), published by WWF, which contained 204 species divided into 13 orders. There was no division by families, though it presented a classification system divided into four categories: 1 (37 species) -very rare and believed to be decreasing in numbers; 2 (23 species) -less rare but believed to be threatened -requires surveillance; 3 (18 species) -very rare but believed to be stable or growing; and 4 (126 species) -inadequately known research situation. Of the species on the IUCN's list (1964), nine were not in this book by Scott (1964). were dropped from the list and 31 changed categories, however, the reasons for these changes did not appear (LEE; THORNBACK; BENNETT, 1988). : This list contained 698 species, 16 orders, and 91 families divided into nine categories: Recently Extinct (EX? = 9), Extinct (EX = 34), Endangered (E = 218), Vulnerable (V = 168), Rare (R = 65), Indeterminate (I = 65), Insufficiently Known (K = 138), Threatened (T = 1), and Commercially Threatened (CT = 0). Of the 698, 26 were found in Brazil: (E = 13), (V = 5), (I = 3), and (K = 5). 19 species were dropped from the list and 46 changed categories, however, the reasons for these changes were not mentioned (IUCN, 1990).

VII) 1994 -IUCN's Red List of Threatened Animals:
A significant change is made in this edition. The content has been reorganized and updated. Corrections have been made to nomenclatures and distributions resulting in category changes as appropriate. Also species were added that were recognized as globally threatened since the last edition. Some species listed earlier were removed but, at that time, they were not considered threatened. In this edition, a complete list of species known or considered extinct in nature since approximately 1600 AD was provided for Of the 2,100 species, 109 were found in Brazil: (CR = 5), (EN = 13), (VU = 30), (LR:nt = 49), and (DD = 12). 94 species were removed from the list, but the reasons were not mentioned. 25% of the listed species were threatened with extinction (BAILLIE; GROOMBRIDGE, 1996). However, the threat categories were changed continuously from 1982 to 1994. Until 1994, the species considered threatened were classified in the categories: Endangered (E), Vulnerable (V), Rare (R), Indeterminate (I), and Insufficiently Known (K), even though the latter does not have enough data to state with certainty the conservation status of the species, it was also considered a threat category (GROOMBRIDGE, 1994).
Insufficiently known species (K) are commonly considered to be threatened species, although, there is insufficient data to assert this threat with certainty (GROOMBRIDGE, 1994). As of 1996, there was a revision in the categories and criteria; an update to known species; some were Brazilian Journal of Animal and Environmental Research, Curitiba, v.6, n.2, p. 1802-1831, abr./jun., 2023 re-categorized and others were excluded. Since then, threatened species have been classified into the following categories: Critically Endangered (CR), Endangered (EN) and Vulnerable (VU). And in order to facilitate comparisons, as there was a standardization of the categories, the data found on the IUCN website start from this date (BAILLIE; GROOMBRIDGE, 1996).
The increase in the number of threatened species from year to year should not be directly interpreted as trends of the biodiversity status. The figures presented in Table 2 reflect the growing assessment efforts of IUCN and its partners over time, and not just changes for genuine reasons in the number of threatened species (IUCN, 2018).  Groombridge (1994). Species considered threatened are those that fall into the following IUCN categories: Endangered (E), Vulnerable (V), Rare (R), Indeterminate (I), and Insufficiently Known (K).

SPECIES STATUS CHANGES IN IUCN LISTS FROM 2006 TO 2018
Species status changes can occur for several reasons. IUCN has developed two types for these changes: Genuine Reasons occur when the main threats are no longer present or due to the success of conservation measures in placing them in a lower threat category. They also occur when they change from a less threatened category to a more threatened category as the main threats persist, have increased, or new ones arise. Non-genuine Reasons occur as new information becomes available since the previous assessment, a taxonomic revision, an error in the previous assessment, or a reassessment using the current criteria. Table 3 shows the changes that occurred for genuine reasons or otherwise since the 2006 publication. The previous lists presented changes but did not mention their motivation (IUCN, 2018).  Note that category changes occur on each list due to the fact that information about species is always being updated. It is noteworthy the high number of species (181)  and 17 families, however, there were no categories (IBAMA, 1989(IBAMA, , 1992. Beginning with 2003 list, categories were standardized, and the conservation status of the species could be evaluated in subsequent publications, as seen in Table 4.   Table 5 (DEGUIGNET et al., 2018).

PROTECTED AREAS IN BRAZIL
The hallmark in the history of protected areas in Brazil was the creation of Itatiaia National Park, in 1937, whose objective was to encourage scientific research and recreation for visitors.
Although Itatiaia was the landmark, the idea arose in Brazil much earlier, in 1876, with engineer André Rebouças, who suggested that two parks be created: Sete Quedas and Ilha do Bananal, following the models of Yellowstone (BENSUSAN, 2006) In the SNUC, criteria and rules for the creation, implementation, and management of Conservation Units (CU) were established, presenting the objectives, guidelines, and management categories. The CU were divided into two groups: those of Integral Protection (IP), aiming to preserve nature and allowing only the indirect use of natural resources and, therefore, more restrictive; and those of Sustainable Use (SU), whose purpose was to combine nature conservation with the direct, but sustainable use of part of its natural resources, therefore, less restrictive.   (CNUC, 2018). In 2018 alone, 12 marine CU were created protecting 867,447 km² (ICMBIO, 2019).

PROTECTED AREAS AND RED LISTS OF SPECIES THREATENED WITH GLOBAL AND NATIONAL EXTINCTION
The "Red List of Threatened Species" is one of the most comprehensive sources of information on species conservation as it indicates the state of local and global biodiversity. It aims to identify species, especially those threatened with extinction, and provide information about the state, trends, and threats in order to encourage actions for their conservation. To this end, it monitors the change of species conservation degree and biodiversity indicators, establishes conservation priorities at the local level through the global context. Successful actions include species recovery programs, restoration of ecosystems, control of invasive species, reintroduction, conservation measures, and effective management programs and establishment of Protected Areas (VIÉ et al., 2009;BENNUN et al., 2018). The creation of these areas is useful for the in-situ conservation of species as it is a delimited and regularized space in which the use and occupation of the territory occur according to the socioenvironmental characteristics of each location (MATOS, 2010;PELLIZZARO et al., 2015). International agreements determine the expansion of the protected areas network in the world in an attempt to reverse the continuous extinction of species and ecosystems (PRINGLE, 2017). The highlight was the First World Congress on National Parks held in Seattle, USA, in 1962, which had as one of the main recommendations the creation of protection units for each threatened species (DIEGUES, 1993). Also noteworthy is the Tenth Meeting of the Conference of the Parties to the CBD with the Aichi targets previously mentioned.
The United Nations (UN) has published the global list of protected areas since 1962 ( Figure   1). In the first publication, the number of protected places was minimal, as well as the size of the areas. There was a gradual increase in the following years, reaching exponential growth in 2014. In that same year, the data was crossed demonstrating that more locations were created but with smaller areas. In the past four years, more than 13 million km² have been created by adding almost 30,000 locations to the database (DEGUIGNET et al., 2018).
The increase in the number of mammal species threatened with extinction from the first IUCN list, published in 1964, to the most recent list, published in 2018, is shown in Figure 2.
Notably, each year the number of threatened species increased as well as the number of species that were evaluated for the first time and others reassessed, thus contributing to this increase. Many of these have changed from less threatened to more threatened categories and others have already entered these categories since the first assessment (IUCN, 2018).
There are currently more than 5000 species of mammals that can be found in the terrestrial and aquatic environments of the world. However, on the IUCN's red lists, 25% of these species are found to be endangered (BAILLIE et al., 2010;IUCN, 2018).
According to BAILLIE et al. (2010, p.41), the largest proportions of terrestrial mammals in the world are found in forests. Aquatic mammals are found in inland wetlands. Mammals are threatened due to the exploitation and destruction of these habitats caused by increasing deforestation, logging, agriculture, and coastal destruction. Another threat is hunting (sport, subsistence, or a source of traditional medicines). These threats are related to the growth of human populations.
The best-known species recovery success story is that of the Giant Panda (Ailuropoda melanoleuca David, 1869), a species threatened by poaching, habitat loss, and fragmentation that led the Chinese government to invest in reforestation and increase from four to 67 the number of Protected Areas for the conservation and recovery of the species (WEI et al., 2015). These combined efforts brought the species from Endangered to the Vulnerable on the 2016 list (IUCN, 2016).
However, "research shows that the existing global Protected Areas network -despite more than tripling in size in the last 40 years -is insufficient to prevent the continued depletion of biodiversity" (PRINGLE, 2017, p.91).  Prepared by the authors. Sources: Scott (1964); Thornback e Jenkins (1982); IUCN (1986); Lee, Thornback e Bennett (1988); IUCN (1990); Groombridge (1994); Baillie e Groombridge (1996); Hilton-Taylor (2000); Baillie, Hilton-Taylor e Stuart (2004); Vié et al. (2009);IUCN (2018). Note: In this graph, different threat categories were used according to the year of publication: On the 1964 list, the threat categories were 1, 2 and 4, being 1-very rare and believed to be decreasing in numbers; 2 -less rare, but believed to be threatened -requires vigilance; 3 -very rare, but it is believed to be stable or growing, and 4 -inadequately known research situation; on the 1982 to 1994 lists, the threat categories were: Endangered (E), Vulnerable (V), Rare (R), Indeterminate (I), and Insufficiently Known (K); on the 1996 to 2018 lists, the threat categories were: Critically Endangered (CR), Endangered (EN), and Vulnerable (V).
Brazilian Journal of Animal and Environmental Research, Curitiba, v.6, n.2, p. 1802-1831, abr./jun., 2023 In the 1930s Brazilian Government paid little attention to the creation of Protected Areas because, according to Salvio (2017, p.38), "until the 1970s, Brazil had few and small Protected Areas, predominantly, Parks that protected places of great scenic beauty located on the coast and close to large urban centers. The creation of these areas were still sporadic and slow, resulting in large conservation gaps in the country." However, the decade of the 1980s saw a marked increase in the number and extent of CU (Figure 3). In subsequent decades (1990s and 2000s), the existing network of CU's increased in number faster than it did in total area. Since the 2010s, the number of protected locations decreased compared to the previous decade, but the areas increased, which explains the decrease in the number of locations with the slight increase in the total Protected Area (CNUC, 2018). Up until the 1980s, more areas were created within the categories of Integral Protection, the vast majority of which were composed of National Parks. In the 1990s, the numbers almost tripled, however, unlike previous decades in which many areas of integral protection were created, more Conservation Units in the sustainable use category were created (Figures 4 and 5). The 2000s were the culmination of CU creations, with 832 areas protecting 828,900.40 km², 556,460.42 km² (609) of which are also for Sustainable Use. Similarly, in the 2010s, most of the CU created fell into the "Sustainable Use" category, 43 of which were marine (CNUC, 2018). Brazil is among the richest countries in mammal biodiversity in the world. 732 species were assessed for risk and 110 of these are threatened with extinction due to anthropic actions. It was found that these actions were predatory hunting and fishing, use of wild animals as pets, introduction of exotic species, and habitat loss, fragmentation and degradation (CASSANO et al., 2017;ICMBIO, 2018). The number of threatened species in Brazil also increased during the publication of the lists ( Figure 7). As for the global lists, this increase was due to efforts in research and assessments and also in changing the status of species from one list to another (ICMBIO, 2018).  lists, all species were threatened; on the 1972 list, the threat categories were 1,2 and 4, being 1-Very rare, populations in sharp decline, 2 -Less rare, but threatened, and 4 -Unknown situation in which there was a need for research; on the 2003 to 2018 lists, the threat categories were: Critically Endangered (CR), Endangered (EN), and Vulnerable (V).
The distribution of these species in the CU was done by taxonomic orders (Figure 8). The occurrence of threatened species is higher in the CU of Integral Protection. The orders whose presence of species is greater in the CU of Integral Protection are: Carnivora, Artiodactyla, Perissodactyla, Pilosa, Cingulata, Rodentia and Didelphimorphia. The orders whose presence of species is greater in CU of Sustainable Use area: Primates, Cetartiodactyla, Sirenia, and Chiroptera (ICMBIO, 2018).
The first conservation projects based on the red lists were aimed at the recovery of the golden lion tamarin and muriqui, which are species threatened by illegal exploitation and habitat loss.       & Persson, 1990, Callicebus barbarabrownae Hershkovitz, 1990 and Panthera onca Linnaeus, 1758. The information in the text of the 2018 ICMBio list did not provide significant detail citing only the CU in which they are found, however, there is no discrimination of which CU, thus leaving a gap (ICMBIO, 2018).

CONCLUSIONS
The IUCN Red Lists greatly influence the conservation of mammal species as they provide information about their current status. Through the scientific knowledge generated by these lists, governments, NGO, and civil society can direct their conservation actions.
There are several programs that protect species and their habitats and among them is the creation of Protected Areas. However, even as the number of PA increase, the number of threatened species has also increased. Several factors contribute to such trends including greater efforts to assess an ever greater number of species, overharvest or exploitation to which they are subject, and finally the destruction of the habitats they occupy. In Brazil, the highest incidence of threatened species is in the Protected Areas of Integral Protection. In these locations, human access is limited but even so, success has been limited in reducing threats. Greater involvement is required of all citizens to guarantee success, and especially vigilant government leaders. Conservation of threatened mammals in Brazil will require more streamlined creation and management of Protected Areas, as well as better enforcement of environmental laws. Finally, successful conservation of mammal species requires preservation and restoration of their habitats.