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Mortality of primates due to roads and power lines in two forest patches in Bangladesh

ABSTRACT

Primates are in imminent risk of extinction due to different types of anthropogenic activities. Mortality due to road accidents and electrocution from power lines are among the major direct anthropogenic threats to the survival of primates. We collected primate mortality data from 2015 to 2017 at Lawachara National Park and Satchari National Park in northeastern Bangladesh. We recorded 27 fatalities in five species of primates caused by road accidents (n = 15) and electrocution (n = 12). Most mortality records were for Trachypithecus phayrei (Blyth, 1847) (n = 8) while the lowest recorded mortality was for Macaca mulatta (Zimmermann, 1780) (n = 3). Ninety percent of primates in Bangladesh are threatened and populations are gradually declining. Our results suggest that roads and power supply lines are major sources of primate mortality that should be managed in these two forests. We strongly suggest avoiding construction of roads and power supply lines inside forests. Furthermore, control of the speed limit of vehicles inside the forests, use of insulated power lines, maintenance of natural canopy bridges and preparation of artificial canopy bridges are strongly recommended.

KEY WORDS:
Bengal slow loris; conservation; electrocution; fragmentation; road accident; Phayre’s langur

Primates are one of the largest groups of seed dispersers in tropical forests (Stevenson 2011Stevenson PR (2011) The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica 43: 512-519. https://doi.org/10.1111/j.1744-7429.2010.00708.x
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). They are vital to the reproductive cycles of many plant species (Beaune et al. 2013Beaune D, Bretagnolle F, Bollache L, Bourson C, Hohmann G, Fruth B (2013) Ecological services performed by the bonobo (Pan paniscus): seed dispersal effectiveness in tropical forest. Journal of Tropical Ecology 29: 367-380. https://doi.org/10.1017/S0266467413000515
https://doi.org/10.1017/S026646741300051...
, Levi and Peres 2013Levi T, Peres CA (2013) Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biological Conservation 163: 99-106. https://doi.org/10.1016/j.biocon.2013.03.016
https://doi.org/10.1016/j.biocon.2013.03...
, Arroyo-Rodríguez et al. 2015Arroyo-Rodríguez V, Andresen E, Bravo SP, Stevenson PR (2015) Seed dispersal by howler monkeys: Current knowledge, conservation implications, and future directions. In: Youlatos D, Kowalewski MM, Garber PA, Cortes-Ortiz L, Urbani B, Youlatos D (Eds) Howler monkeys: Behavior, ecology and conservation. Developments in primatology: Progress and prospects . New York, Springer, 111-139.) and are also central to the livelihood and culture of many societies (Estrada et al. 2017Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, et al. (2017) Impending extinction crisis of the world’s primates: Why primates matter. Science Advances 3: e1600946. https://10.1126/sciadv.1600946
https://10.1126/sciadv.1600946...
). Although primates are recognized as essential components of ecosystems, about 60% of the primates are globally threatened and an astounding 73% of Asian species are threatened (Estrada et al. 2017Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, et al. (2017) Impending extinction crisis of the world’s primates: Why primates matter. Science Advances 3: e1600946. https://10.1126/sciadv.1600946
https://10.1126/sciadv.1600946...
). Habitat loss caused by agriculture, logging, wood harvesting, livestock farming and infrastructure development are some of the primary threats to primates (IUCN 2017IUCN (2017) IUCN red list of threatened species. International Union for Conservation of Nature, v. 2017-3-4. Available online at: Available online at: http:// www.iucnredlist.org . [Accessed: 26/12/2018]
http:// www.iucnredlist.org...
).

Forest fragmentation associated with forest loss can create small and isolated subpopulations, raising extinction probabilities arising from demographic, environmental, and genetic factors (Frankham et al. 2002Frankham R, Briscoe DA, Ballou JD (2002) Introduction to Conservation Genetics. Cambridge, Cambridge University Press, 642 pp., Goosem 2007Goosem M (2007) Fragmentation impacts caused by roads through rainforests. Current Science 93: 1587-1595., Muzaffar et al. 2007Muzaffar SB, Islam MA, Feeroz MM, Kabir M, Begum S, Mahmud S, Chakma S (2007) Habitat characteristics of the endangered Hoolock Gibbons (Hoolock hoolock) of Bangladesh: the role tree species richness. Biotropica 39: 539-545. https://doi.org/10.1111/j.1744-7429.2007.00298.x
https://doi.org/10.1111/j.1744-7429.2007...
). Infrastructure, such as pipelines, roads, railways, and transmission lines have the potential to impact wildlife in many ways, most notably by reducing access to resources and increasing mortality rates (Laurence et al. 2009Laurence WF, Goosem M, Laurance SGW (2009) Impacts of roads and linear clearings on tropical forests. Trends in Ecology & Evolution 24: 659-669. https://doi.org/10.1016/j.tree.2009.06.009
https://doi.org/10.1016/j.tree.2009.06.0...
, Benítez-López et al. 2010Benítez-López A, Alkemade R, Verweij PA (2010) The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biological Conservation 143: 1307-1316. https://doi.org/10.1016/j.biocon.2010.02.009
https://doi.org/10.1016/j.biocon.2010.02...
, Jenkins et al. 2010Jenkins AR, Smallie JJ, Diamond M (2010) Avian collisions with power lines: a global review of causes and mitigation with a South African perspective. Bird Conservation International 20: 263-278. https://doi.org/10.1017/S0959270910000122
https://doi.org/10.1017/S095927091000012...
, Dean et al. 2019Dean WRJ, Seymour CL, Joseph GS, Foord SHA (2019) Review of the Impacts of Roads on Wildlife in Semi-Arid Regions. Diversity 11(81): 1-19. https://doi.org/10.3390/d11050081
https://doi.org/10.3390/d11050081...
). With rapid development in many developing countries, mortality due to road accidents and electrocution from power lines is among the major direct human causes of mortality of terrestrial animals worldwide (Drews 1995Drews C (1995) Road kill of animals by public traffic in Mikumi National Park, Tanzania with notes on baboon mortality. African Journal of Ecology 33: 89-100. https://doi.org/10.1111/j.1365-2028.1995.tb00785.x
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, Fedigan and Zohar 1997Fedigan LM, Zohar S (1997) Sex Differences in Mortality of Japanese Macaques: Twenty-One Years of Data From the Arashiyama West Population. American Journal of Physical Anthropology 102: 161-175. https://doi.org/10.1002/(SICI)10968644(199702)102:2<161::AID-AJPA2>3.0.CO;2-1, Forman and Alexander 1998Forman RTT, Alexander LE (1998) Roads and their major ecological effects. Annual Review of Ecology and Systematics 29: 207-232. https://doi.org/10.1146/annurev.ecolsys.29.1.207
https://doi.org/10.1146/annurev.ecolsys....
, Printes 1999Printes RC (1999) The Lami biological reserve, Rio Grande doSul, Brazil and the danger of power lines to howlers in urban reserves. Neotropical Primates 7: 135-136., Chhangani 2004Chhangani AK (2004) Killing of Hanuman Langur in road accidents in Knumbhalgarh Wildlife Sanctuary, Rajasthan, India. Primate Report 69: 49-57, Lokschin et al. 2007Lokschin LX, Printes RC, Cabral JNH, Buss G (2007) Power lines and howler’s conservation (Alouatta guariba clamitans; Cabrera, 1940) in Porto Alegre, Rio Grande do Sul, Brazil. Netropical Primates 14: 76-80. https://doi.org/10.1896/044.014.0206
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, Parker et al. 2008Parker L, Nijman V, Nekaris KAI (2008) When there is no forest left: fragmentation, local extinction, and small population sizes in the Sri Lankan western purple-faced langur. Endangered Species Research 5: 29-36. https://doi.org/10.3354/esr00107
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, Cáceres et al. 2010Cáceres NC, Hannibal W, Freitas DR, Silva EL, Roman C, Casella J (2010) Mammal occurrence and road kill in two adjacent ecoregions (Atlantic Forest and Cerrado) in south-western Brazil. Zoologia 27: 709-717. https://doi.org/10.1590/S1984-46702010000500007
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, Pragatheesh 2011Pragatheesh A (2011) Effect of human feeding on the road mortality of Rhesus Macaques on National Highway-7 routed along Pench Tiger Reserve, Madhya Pradesh, India. Journal of Threatened Taxa 3: 1656-1662. https://doi.org/10.11609/JoTT.o2669.1656-62
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, Umapathy et al. 2011Umapathy G, Hussain S, Shivaji S (2011) Impact of habitat fragmentation on the demography of lion-tailed macaque (Macaca silenus) populations in the rainforests of Anamalai Hills, Western Ghats, India. International Journal of Primatology 32: 889-900. https://doi.org/10.1007/s10764-011-9508-9
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).

Asia as a continent has undergone development at unprecedented rates during the last 50 years (Muzaffar et al. 2011Muzaffar SB, Islam MA, Kabir DS, Khan MH, Ahmed FU, Chowdhury GW, Aziz MA, Chakma S, Jahan I (2011) The endangered forests of Bangladesh: why the process of implementation of the Convention on Biological Diversity is not working. Biodiversity and Conservation 20: 1587-1601. https://doi.org/10.1007/s10531-011-0048-6
https://doi.org/10.1007/s10531-011-0048-...
, Islam and Sato 2012Islam K, Sato N (2012) Deforestation, Land Conversion and Illegal Logging in Bangladesh: The Case of the Sal (Shorea robusta) Forests. iForest-Biogeosciences and Forestry 5: 171-178. https://doi.org/10.3832/ifor0578-005
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, FAO 2015FAO (2015) Global Forest Resources Assessment 2015. Rome, FAO, Forestry Paper No. 1.). Within Asia, Bangladesh is a small, densely populated country with a total population of over 160 million. Forested lands are heavily fragmented and few forest patches remain scattered in the northeast, southeast and southwest of the country, representing about 9.82% of the total land area (IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.). These patches are surrounded by human habitation, roads and railway lines that often pass through these forests. Thus, primates here are at high risk of mortality from road accidents on highways and from electrocution from electric power supply lines that pass through the remaining forest habitats. In this study the threats of primates arising from road accidents and electrocution were characterized.

We selected two forest patches of northeastern Bangladesh, namely Lawachara National Park (LNP) and Satchari National Park (SNP) for this study. Both national parks consist of mixed evergreen forest types planted in the 1930s and 1940s (Kabir and Muzaffar 2002Kabir DS, Muzaffar SB (2002) The review of the present state of protected areas of Bangladesh. In: Ahmed MF, Tanveer SA, Badruzzaman ABM (Eds) Bangladesh environment 2002. Dhaka, Bangladesh, Bangladesh Poribesh Rokha Andolon, 389-403.). Lawachara National Park is situated in Kamalganj Upazila, Maulvi Bazar District and covers a 1250 ha area (Mollah and Kunda 2004Mollah AR, Kunda DK (2004) Site Level Appraisal for Protected Area Co-Management: Lawachara National Park. Bangladesh, International Resources Group, Nature Conservation Management, 120 pp.). The canopy height of the forested areas in LNP varies from 10 to 30 m (Muzaffar et al. 2007Muzaffar SB, Islam MA, Feeroz MM, Kabir M, Begum S, Mahmud S, Chakma S (2007) Habitat characteristics of the endangered Hoolock Gibbons (Hoolock hoolock) of Bangladesh: the role tree species richness. Biotropica 39: 539-545. https://doi.org/10.1111/j.1744-7429.2007.00298.x
https://doi.org/10.1111/j.1744-7429.2007...
). This forest is fragmented by Sreemangal-Bhanugach highway and Dhaka-Sylhet railway line (Fig. 1). In addition, an electric power supply line also passes through the forest approaching the highway. The second site, Satchari National Park, is within Chunarughat Upazilla, Habiganj District and has an area of 243 ha. The current extent of mixed evergreen forest is about 150 ha (Choudhury et al. 2004Choudhury JK, Biswas SR, Islam M, Rahman SO, Uddin SN (2004) Biodiversity of Shatchari Reserved Forest, Habiganj. Dhaka, Bangladesh, IUCN Bangladesh Country Office, 34 pp.). The canopy height of this forest varies from 15 to 35 m. This forest patch is dissected by the old Dhaka-Sylhet highway and an electric power supply line that passes through the forest approaching the highway (Fig. 1).

Figure 1
Map of two forest patches in Bangladesh, showing the locations of linear infrastructures inside the forest.

We collected primate mortality data from both primary (direct observation) and secondary sources (published articles, interviews, social media uploads and newspaper reports) from 2015 to 2017 at these two national parks. Firstly, we collected primary data by direct observation during field work from July, 2015 to December 2017 during which we spent a total of 37 days in LNP and 68 days in SNP. Secondly, we collected secondary data from published articles. From March 2018 to April 2018 we searched the internet using Google and Google Scholar to find all related articles regarding primate mortality in SNP and LNP. Thirdly, we searched news published by national and local newspapers, online news portals, wildlife conservation groups and social media outlets. Finally, we collected data from interviews with forest staff, local people, as well as data from the record books of the range offices of SNP and LNP (Table 1). We conducted a questionnaire survey over a seven-day period in February 2018 in SNP. In LNP we conducted the questionnaire survey between May 2018 to June 2018. The questionnaire was developed in advance and approved by the Forest Department prior to the study. After data collection we cross-checked all data to avoid duplication of reports. In order to test possible diffe rences between the types of accidents both within and between parks we use the chi-square test (with values of significance determined at α < 0.05).

Table 1
Mortality of primates between 2015 and 2017 in Lawachara National Park (LNP) and Satchari National Park (SNP). (Source of data: I, Interview; SM, Social Media; N, Newspaper; PA, Published Article; DO, Direct Observation).

A total of 27 (Mean = 9 ± SD 4 per year) individual fatali ties of five primate species were recorded, of which 15 were caused by road accidents and 12 were caused by electrocution (Table 1). Most mortality records were for the Phayre’s langur, Trachypithecus phayrei (Blyth, 1847) (n = 8) while the lowest recorded mortality was for the Rhesus Monkey, Macaca mulatta (Zimmermann, 1780) (n = 3). Fourteen individuals of primates died in SNP and 13 individuals in LNP (Table 1). The rate of mortality from road accidents (57.14%) was higher than the rate of mortality from electrocution (42.86%) in LNP, whereas mortality from electrocution (53.85%) was higher than mortality from road accidents (46.15%) in SNP (χ2 = 0.83, p < 0.05). In the case of electrocution, mortality rate of langurs (66.66%) was higher than mortality rates of other primates (16.66%). In contrast, mortality rate of langurs (33.33%) was lower than the mortality rates of other primates (83.33%) due to road accident in both study sites (χ2 = 0.99, p < 0.0001). Between two species of langur, mortality of Capped langur, Trachypithecus pileatus (Blyth, 1843), was higher in SNP (n = 6) than in LNP (n = 1) whereas mortality of Phayre’s langur was higher in LNP (n = 6) than in SNP (n = 2).

Primate mortality rate appeared to be higher in SNP (13 individuals/2.5 km of road = 5.2 deaths per km of road) compared to LNP (2.15 deaths per km of road). The impact of infrastructure is proportional to its length since this affects the area of the effect zone (Forman 2000Forman RTT (2000). Estimate of the area affected ecologically by the road system in the United States. Conservation Biology 14: 31-35. https://doi.org/10.1046/j.1523-1739.2000.99299.x
https://doi.org/10.1046/j.1523-1739.2000...
, Benítez-López et al. 2010Benítez-López A, Alkemade R, Verweij PA (2010) The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biological Conservation 143: 1307-1316. https://doi.org/10.1016/j.biocon.2010.02.009
https://doi.org/10.1016/j.biocon.2010.02...
). Furthermore, primate mortality rate in SNP was particularly high in 2016. In 2016, 12 of 18 natural canopy bridges over the highway were cut down to introduce an electric power supply line in the middle of the forest approaching the highway. We suspect that this was the likely cause of the higher mortality of primates in SNP in 2016. Removal of the natural canopy bridges likely forced the primates to use the road or electric power supply wire to cross the road making them vulnerable to road accidents and electrocution. It may be added that there were no records of electrocution of primates in SNP before 2016. Electrocution of primates were recorded only after the installation of electric power supply lines inside the forest, highlighting that such installations constitute a major threat to primates.

Rhesus and pig-tailed macaques were only recorded to have died from road accidents because these two species frequently use the ground for movement (Southwick et al. 1976Southwick CH, Sidiqi MF, Farooqui MY, Pal BC (1976) Effects of artificial feeding on aggressive behaviour of rhesus monkeys in India. Animal Behavior 24: 11-15., Bernstein 1967Bernstein IS (1967). A field study of the pigtail monkey. Primates 8: 217-228.). Road accidents are considered as one of the major threats for Bengal slow loris as well (Choudhury 1992Choudhury AU (1992) The slow loris (Nycticebus coucang) in northeast India. Primate Report 34: 77−83., Radhakrishna et al. 2006Radhakrishna S, Goswami AB, Sinha A (2006) Distribution and Conservation of Nycticebus bengalensis in Northeastern India. International Journal of Primatology 27: 971−982. https://doi.org/10.1007/s10764-006-9057-9
https://doi.org/10.1007/s10764-006-9057-...
, Kumar and Devi 2010Kumar A, Devi A (2010) Status and conservation of slow loris (Nycticebus bengalensis) in northeast India. Ecotone 2: 18−20. http://www.scribd.com/doc/32168876/Ecotone2-1-2010
http://www.scribd.com/doc/32168876/Ecoto...
, Das et al. 2015Das N, Nekaris KAI, Biswas J, Das J, Bhattacharjee PC (2015) Persistence and protection of the Vulnerable Bengal slow loris Nycticebus bengalensis in Assam and Arunachal Pradesh, north-east India. Oryx 49: 127-132. https://doi.org/10.1017/S0030605312001287
https://doi.org/10.1017/S003060531200128...
). Only Radhakrishna et al. (2010Radhakrishna S, Datta-Roy A, Swapna N, Sinha A (2010). Population survey of the Bengal slow loris, Nycticebus bengalensis, in Meghalaya, northeast India. Primate Conservation 25: 105−110. https://doi.org/10.1896/052.025.0102
https://doi.org/10.1896/052.025.0102...
) reported an incident of mortality from electrocution in this species near Siju Wildlife Sanctuary in Garo Hills, northeastern India. In this study, we recorded two incidents of mortality due to electrocution of Bengal slow loris from LNP. Among the two species of langur, mortality of capped langur occurred only due to electrocution. On the other hand, among eight cases of mortality of Phayre’s langur, five occurred due to electrocution and three were due to road accidents (Fig. 2). From direct observation and interview of forest staff we found that both Capped langurs and Phayre’s langurs frequently use the power supply lines to cross roads. Mortality in langurs occurred primarily due to short-circuiting of two electric parallel power lines connected by overhanging tails. In comparison, the other species have relative short tails (macaques) or almost no tail (e.g. slow loris). This is possibly why the macaques would be less vulnerable to electrocution even if they did use electric lines for movement. However, movement of the slow loris is slow and individuals may move from one wire to the next without releasing their grip on the first wire, causing fatal short-circuiting.

Figure 2
Type of mortality of different primate species in both study sites.

Ten primate species have been recorded from Bangladesh (IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.). Two species are globally Endangered, three are Vulnerable, and one is Near Threatened (Roos et al. 2014Roos C, Boonratana R, Supriatna J, Fellowes JR, Groves CP, Nash SD, Rylands AB, Mittermeier RA (2014) An updated taxonomy and conservation status review of Asian primates. Asian Journal of Primatology 4: 2-38., IUCN 2015). In this study we recorded mortality of one Critically Endangered: Trachypithecus phayrei, and three Vulnerable species: Trachypithecus pileatus, Nycticebus bengalensis (Lacépède, 1800) and Macaca leonina (Blyth, 1863). Ninety percent of primates are threatened and the population of most of the primates are gradually declining in Bangladesh (IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.).

The Phayre’s langur is surviving in few semi-evergreen forests of eastern parts of the country in small fragmented populations (IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.). The total population has declined by more than 80% in the last 20 years making it vulnerable to imminent extinction (Molur et al. 2003Molur S, Brandon-Jones D, Dittus W, Eudey A, Kumar A, Singh M, Feeroz MM, Chalise M, Priya P, Walker S (2003) Status of South Asian Primates: Conservation Assessment and Managment Plan Report. Coimbatore, India, Zoo Outreach Organization/CBSG-South Asia., IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.). Beside habitat destruction, logging, hunting, road accidents and electrocution are major threats of primates in Bangladesh (IUCN 2015IUCN (2015) Red List of Bangladesh. Dhaka, Bangladesh, International Union for Conservation of Nature, vol. 2, 232 pp.). To mitigate the effects of road accidents and electrocution of primates and other wildlife in forest patches in Bangladesh, we strongly suggest avoiding construction of roads and power supply lines inside the last remaining forest patches. However, there is no direct law on the construction of roads and power supply lines inside the forest. As development progresses, roads and electric lines are constructed according to project needs. Stricter control of the speed limit of vehicles inside the forest should be imposed by creating speed breakers. To reduce fatalities from electrocution, we recommend the use of insulated power lines at least in the forested areas. Furthermore, maintenance of natural canopy bridges, and the preparation of artificial canopy bridges over the roads and electric power supply lines could further minimize mortality of primates and other arboreal mammals in forest patches of Bangladesh (Goosem 2004Goosem M (2004) Linear infrastructure in tropical rainforests: mitigating impacts on fauna of roads and powerline clearings. In: Lunney D (Eds) Conservation of Australia’s Forest Fauna. Sydney, Royal Zoological Society of New South Wales, 418-434 pp., Thurber and Ayarza 2005Thurber M, Ayarza P (2005) Canopy bridges along a rainforest pipeline in Ecuador. Kuala Lumpur, Malaysia, Society of Petroleum Engineers Asia Pacific Health, Safety and Environment Conference and Exhibition, 1-4., Dean et al. 2019Dean WRJ, Seymour CL, Joseph GS, Foord SHA (2019) Review of the Impacts of Roads on Wildlife in Semi-Arid Regions. Diversity 11(81): 1-19. https://doi.org/10.3390/d11050081
https://doi.org/10.3390/d11050081...
).

ACKNOWLEDGMENTS

First of all we are thankful the Forest Department of Bangladesh for permission (FD-22.01.0000.004.04.021.15.) to carry out work in forest and to provide information on road kills. The authors are also grateful to Professor Abdul Alim, Chairman, Department of Zoology, Jagannath University, for his support. We are thankful to Md. Anisur Rahman beat officer and Mahbub Hussain range officer of Satchari National Park for their support during the study. We are thankful to Sabit Hasan and Tanvir Ahmad for their support in field work. The field work of 2017 was funded by The Rufford Foundation. We thank David Thomson, Department of Biology, UAE University for reviewing the language of the paper.

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Publication Notes

  • Available online:

    October 1, 2019
  • Zoobank Register:

    http://zoobank.org/FAD55A49-1B0F-4113-A206-C3F4254CE551
  • Publisher:

    © 2019 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Edited by

Editorial responsibility:

Darren Norris

Data availability

Data citations

IUCN (2017) IUCN red list of threatened species. International Union for Conservation of Nature, v. 2017-3-4. Available online at: Available online at: http:// www.iucnredlist.org [Accessed: 26/12/2018]

Publication Dates

  • Publication in this collection
    21 Oct 2019
  • Date of issue
    2019

History

  • Received
    31 Jan 2019
  • Accepted
    06 Aug 2019
  • Published
    01 Oct 2019
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