Parides Burchellanus IUCN Redlist Assessment

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Parides burchellanus IUCN Redlist assessment

Technical Report · April 2018

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André Victor Lucci Freitas Augusto Rosa University of Campinas University of Campinas

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Onildo J Marini-Filho Nicolás O. Mega Instituto Chico Mendes de Conservação da Biodiversidade Universidade Federal do Rio Grande do Sul

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Parides burchellanus Amended version Assessment by: Grice, H., Freitas, A.V.L., Rosa, A., Marini-Filho, O., Dias, F.M.S., Mega, N., Mielke, O. & Casagrande, M.

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Citation: Grice, H., Freitas, A.V.L., Rosa, A., Marini-Filho, O., Dias, F.M.S., Mega, N., Mielke, O. & Casagrande, M. 2019. Parides burchellanus (amended version of 2018 assessment). The IUCN Red List of Threatened Species 2019: e.T16240A145165953. http://dx.doi.org/10.2305/IUCN.UK.2019- 1.RLTS.T16240A145165953.en

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THE IUCN RED LIST OF THREATENED SPECIES™ Taxonomy

Kingdom Phylum Class Order Family

Animalia Arthropoda Insecta Lepidoptera Papilionidae

Taxon Name: Parides burchellanus (Westwood, 1872)

Synonym(s): • Papilio jaguarae Foetterle, 1902 • Papilio numa Boisduval, 1836 (preocc. Weber, 1801) • Papilio socama Schaus, 1902 • Parides burchellanus jaguarae (Foetterle, 1902) • Parides panthonus jaguarae Foetterle, 1902

Taxonomic Source(s): Lamas, G. 2004. Atlas of Neotropical Lepidoptera. Checklist: Part 4A (Hesperioidea - Papilionoidea). Association for Tropical Lepidoptera, Gainesville, Florida.

Taxonomic Notes: Previously, some authors recognised two subspecies for this species: the nominate subspecies burchellanus; and subspecies jaguarae (Foetterle, 1902). The latter was previously considered a subspecies of Parides panthonus, but was synonimised with P. burchellanus at the species level by both morphological observations as well as by genetic analysis (Mielke et al. 2004, Silva-Brandão et al. 2008). Assessment Information

Red List Category & Criteria: Endangered B2ab(iii) ver 3.1

Year Published: 2019

Date Assessed: April 25, 2018

Justification: Parides burchellanus has been assessed as Endangered. Although this species has a relatively large extent of occurrence, it is known from no more than four distinct areas, which may in fact represent distinct subpopulations due to the fact that the linear habitat of this species may make dispersal distances too great to ensure genetic exchange. Its area of occupancy is currently estimated to be around 120 km², based on known localities, and even with localities missing is unlikely to extend beyond 500 km². The Cerrado habitat in which the species is found is under immense pressure due to development and transformation of habitat into agriculture; Cerrado habitat has been reduced by around 60% (WWF Brazil) and this is predicted to continue (Ferreira et al. 2013). The species is considered to be in decline, and population monitoring and habitat protection is needed to ensure continued survival of this species.

Previously Published Red List Assessments 2018 – Endangered (EN) http://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T16240A122600436.en

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 1 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en 1996 – Lower Risk/near threatened (LR/nt) http://dx.doi.org/10.2305/IUCN.UK.1996.RLTS.T16240A5586378.en

1994 – Vulnerable (V)

1990 – Vulnerable (V)

1988 – Vulnerable (V)

1986 – Vulnerable (V)

1985 – Vulnerable (V)

Geographic Range

Range Description: This Neotropical species occurs in the Distrito Federal, Minas Gerais and Goiás in eastern Brazil (Tyler et al. 1994). Within the Distrito Federal, this species has been observed in Planaltina (M.M. Casagrande and O.H.H. Mielke pers. comm. 2018). In Minas Gerais, records of this species are available in the municipalities of Brumadinho, Campos Altos, Perdizes, Araxá, Ibiá, São Roque de Minas, Tapiraí, Medeiros, Vargem Bonita and Tapira (Mielke et al. 2004, Beirão et al. 2012, Bedê et al. 2015). Within Goiás and Distrito Federal, this species has been recorded in Anápolis, Formosa, rio Maranhão, rio São Bartolomeu (M.M. Casagrande and O.H.H. Mielke pers. comm. 2018). Historically, this species has been recorded in Fazenda Jaguara and Uberaba within the state of Minas Gerais, and the Maranhão river in the state of Goiás (Tyler et al. 2004, Mielke et al. 2004, Beirão et al. 2012). The locality of Batatais, São Paulo state, is probably invalid. However, it is thought that due to habitat alterations, these populations are now locally extinct as a result of habitat loss and flooding (Bedê et al. 2015). Beirão et al. (2012) recorded populations at high elevations of 930 m above sea level (asl.); these findings are corroborated by following research conducted by Bedê et al. (2015), who observed populations at elevations of 770 m - 1,010 m asl. The estimated extent of occurrence of this species is 89,732 km². From available point data, the estimated area of occupancy is at least 120 km², and likely no larger than 520 km², as estimated from distribution and habitat occupation models (O. Marini-Filho pers. comm. June 2018). This latter value is likely an overestimate as individuals of this species were found in only one out of 36 localities within its potential area of occupancy (O. Marini-Filho pers. comm. June 2018). Occurrences are clustered into four disjunct areas, and with this species occurring along linear habitat, distances between these are too large to be travelled across regularly to ensure genetic exchange. Whether individual subpopulations are viable is difficult to assess; however, three of the four subpopulations have relatively sparse locality records for the species and may be less secure - especially given the evidence of previous local extinctions. The species occupies four locations, reflecting the four disjunct areas into which occurrences are clustered, which are threatened by the rapid conversion of Cerrado into agricultural and urbanised landscapes (Freitas and Marini-Filho 2011).

Country Occurrence: Native: Brazil (Brasília Distrito Federal, Goiás, Minas Gerais)

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 3 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en Population This species was considered to be very local (Tyler et al. 1994). More information regarding the status of specific populations is necessary, however recent studies (e.g. Beirão et al. 2012, Bedê et al. 2015) have allowed insight into the population dynamics of some of the remaining populations of this rare butterfly. In 2002, a population discovered along the Catarina river in Brumadinho, Minas Gerais was described as "vigorous" and consisted of more than 50 adults (Mielke et al. 2004). In 2012, Beirão et al. also identified three resident populations within Brumadinho, as well as three more in Planaltina, Distrito Federal. Despite this seemingly positive discovery, this study identified 63 localities with suitable habitat for Parides burchellanus, of which only six contained populations of the species (Beirão et al. 2012). In 2013, several populations were observed surrounding the São Francisco and Araguari rivers in Minas Gerais, within the municipalities of Campos Altos, Perdizes, Araxá, Ibiá, São Roque de Minas, Tapiraí, Medeiros, Vargem Bonita and Tapira (Bedê et al. 2015).

Additionally, a population was identified in Carmo do Rio Claro (Beirão et al. 2012), however this was later confirmed to be misidentified (Bedê et al. 2015). Historical records of populations exist for Uberlândia, Minas Gerais (Beirão et al. 2012), but have not been observed since 2012 and are thought to have become locally extinct (Bedê et al. 2015). Current Population Trend: Unknown

Habitat and Ecology (see Appendix for additional information) This species occurs primarily in the riparian (gallery) forests of the Cerrado landscape in Brazil, a relatively scarce habitat that is influenced heavily by anthropogenic activity (Collins and Morris 1985, Tyler et al. 1994). This species can be found near river banks, especially in areas where the forest canopy shelters the river, and are often observed flying low to the ground (0.2 - 1.5 m), or just above water (Beirão et al. 2012). When searching for flowers, however, adults can be seen flying to heights of up to 7 m (Beirão et al. 2012). The only reported larval host plant utilised by this species is the sparsely distributed Aristolochia chamissonis (Bedê et al. 2015). Females have also been observed ovipositing on substrates near the host plant (Beirão et al. 2012). Adults employ a generalist feeding strategy and have been observed utilising several different flowers, including the families Balsaminaceae, Rubiaceae, Chrysobalanaceae, Fabaceae, Verbenaceae and Asteraceae (Beirão et al. 2012).

Systems: Terrestrial

Use and Trade This species is traded among collectors, with specimens fetching prices of up to US $1,000 (A. Rosa and A. Freitas pers. comm. June 2018, based on online sources).

Threats (see Appendix for additional information) As with many Lepidoptera, the primary threat to this species is destruction of suitable habitat (New and Collins 1991). This species exhibits high habitat specificity and is monophagous, utilising a sparsely distributed larval host plant. The riparian forest habitat occupied by this species is characterised by its own microclimate and is extremely susceptible to perturbations. It is likely this habitat specialism has

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 4 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en contributed to the rarity of this species, particularly as the Cerrado landscape is increasingly altered for anthropogenic use. Clearing of riparian forests alters microclimate and reduces habitat availability, which has ultimately caused local extinctions in some areas of Minas Gerais and Goiás state (Bedê et al. 2015). Due to the riparian nature of this species, populations are primarily distributed linearly (Bedê et al. 2015); local extinctions may therefore severely affect gene flow between populations/subpopulations, consequently increasing local extinction risk of the remaining colonies.

Although the population size observed by previous studies appear concurrent with other species in the Parides genus, this species exhibits marked population fluctuations, with population size decreasing dramatically towards the dry season, possibly associated with decreased host plant quality (Brown 1992). Population fluctuations may increase susceptibility to local extinctions, particularly in an adverse and changing climate.

In addition to habitat clearing, water pollution has also been acknowledged as a significant threat to this species due to the rapid conversion of Cerrado into agricultural and urbanised landscapes (Freitas and Marini-Filho 2011).

Anthropogenic climate change is likely to be a major determinant of population survival and distribution changes in Lepidoptera due to their sensitivity to environmental fluctuations (Chen et al. 2011, Paaijmans et al. 2013). Additionally, changes in the distribution of co-occurring hostplants could cause spatial mismatches of butterflies and their hostplants (Schweiger et al. 2008). Previous studies have documented range shifts to higher elevations concurrent with increasing temperature in Neotropical butterflies (including those within the Papilionidae family) (Molina-Martínez et al. 2016).

Conservation Actions (see Appendix for additional information) On the IUCN Red List of Threatened Species, this species was previously listed as Vulnerable in 1985 (Collins and Morris 1985) and Near Threatened in 1996 (Gimenez-Dixon 1996), however it is currently considered Critically Endangered by the Brazilian Red List of Threatened Species. Some localities that contain populations of this species border the Parque Nacional da Serra da Canastra (Bedê et al. 2015), however the level of protection afforded by proximity to this national park is likely to be insufficient and warrants investigation. Bedê et al. (2015) suggests that further population assessments be undertaken in this area. The National Action Plan for the Conservation of Lepidoptera Threatened with Extinction stressed that conservation of riparian habitats and waterways is paramount to the survival of this species; additionally, clarification of its geographical distribution is needed (Freitas and Marini-Filho 2011), as the exact locations of extant populations is often disputed. Population monitoring is necessary to ensure any further population changes are picked up and acted on. This is the case of the recently found population around Serra da Canastra, that reflects the increase in research efforts made for the conservation of this butterfly. Credits

Assessor(s): Grice, H., Freitas, A.V.L., Rosa, A., Marini-Filho, O., Dias, F.M.S., Mega, N., Mielke, O. & Casagrande, M.

Reviewer(s): Böhm, M. & Bushell, M.

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 5 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en Bibliography Bedê, L.C., Marini-Filho, O.J., Neto, F.C.C., Ribeiro, F., dos Reis, E.S., do Vale Beirão, M. and Resende, F.O. 2015. Parides burchellanus (Westwood, 1872) (Lepidoptera, Papilionidae): new distribution records from southwestern Minas Gerais state, Brazil. Check List 11(3): 1663.

Beirão, M.V., Campos-Neto, F.C., Pimenta, I.A. and Freitas, A.V. 2012. Population biology and natural history of Parides burchellanus (Papilionidae: Papilioninae: Troidini), an endangered Brazilian butterfly. Annals of the Entomological Society of America 105(1): 36-43.

Brown Jr., K.S. 1992. Borboletas da Serra do Japi: Diversidade, hábitats, recursos alimentares e variação temporal. In: Morellato, L.P.C. (ed.), História natural da Serra do Japi. Ecologia e preservação de uma área florestal no sudeste do Brasil, pp. 142-187. Editora da Unicamp/Fapesp, Campinas.

Chen, I., Hill, J.K., Shiu, H.J., Holloway, J.D., Benedick, S., Chey, V.K., Barlow, H.S. and Thomas, C.D. 2011. Asymmetric boundary shifts of tropical montane Lepidoptera over four decades of climate warming. Global Ecology and Biogeography 20(1): 34-45.

Collins, N.M. and Morris, M.G. 1985. Threatened Swallowtail Butterflies of the World. The IUCN Red Data Book. IUCN, Gland and Cambridge.

Ferreira, M.E., Ferreira Jr, L.G., Miziara, F. and Soares-Filho, B.S. 2013. Modeling landscape dynamics in the central Brazilian savanna biome: future scenarios and perspectives for conservation. Journal of Land Use Science 8(4): 403-421.

Freitas, A.V.L. and Marini-Filho, O.J. 2011. Plano de açao nacional para conservaçao dos lepidópteros ameaçados de extinçao. ICMBio, Brasília: 124.

Gimenez Dixon, M. 1996. Parides burchellanus. The IUCN Red List of Threatened Species 1996.

IUCN. 2018. The IUCN Red List of Threatened Species. Version 2018-2. Available at: www.iucnredlist.org. (Accessed: 15 November 2018).

IUCN. 2019. The IUCN Red List of Threatened Species. Version 2019-1. Available at: www.iucnredlist.org. (Accessed: 21 March 2019).

Mielke, O.H., Mielke, C.G.C. and Casagrande, M.M. 2004. Parides panthonus jaguarae (Foetterle) (Lepidoptera, Papilionidae) rediscovered in Minas Gerais, Brazil: his identity. Revista Brasileira de Zoologia 21(1): 9-12.

Molina‐Martínez, A., León‐Cortés, J.L., Regan, H.M., Lewis, O.T., Navarrete, D., Caballero, U. and Luis‐Martínez, A. 2016. Changes in butterfly distributions and species assemblages on a Neotropical mountain range in response to global warming and anthropogenic land use. Diversity and Distributions 22(11): 1085-1098.

New, T.R. and Collins, N.M. 1991. Swallowtail butterflies: an action plan for their conservation. International Union for Conservation of Nature and Natural Resources/Species Survival Commission Lepidoptera Specialist Group, Gland, Switzerland.

Paaijmans, K.P., Heinig, R.L., Seliga, R.A., Blanford, J.I., Blanford, S., Murdock, C.C. and Thomas, M.B. 2013. Temperature variation makes ectotherms more sensitive to climate change. Global Change Biology 19(8): 2373-2380.

Schweiger, O., Settele, J., Kudrna, O., Klotz, S. and Kühn, I. 2008. Climate change can cause spatial mismatch of trophically interacting species. Ecology 89(12): 3472-3479.

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 6 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en Silva-Brandão, K.L., Azeredo-Espin, A.M.L. and Freitas, A.V.L. 2008. New evidence on the systematic and phylogenetic position of Parides burchellanus (Lepidoptera: Papilionidae). Molecular Ecology Resources 8(3): 502-511.

Tyler, H., Brown Jr., K.S. and Wilson, K. 1994. Swallowtail Butterflies of the Americas. A study in Biological Dynamics, Ecological Diversity, Biosystematics, and Conservation. Scientific Publishers, Gainesville, Florida.

World Wildlife Fund for Nature (WWF) Brazil. 2011. Cerrado: Birthplace of Brazilian waters.

Citation Grice, H., Freitas, A.V.L., Rosa, A., Marini-Filho, O., Dias, F.M.S., Mega, N., Mielke, O. & Casagrande, M. 2019. Parides burchellanus (amended version of 2018 assessment). The IUCN Red List of Threatened Species 2019: e.T16240A145165953. http://dx.doi.org/10.2305/IUCN.UK.2019- 1.RLTS.T16240A145165953.en

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Habitats (http://www.iucnredlist.org/technical-documents/classification-schemes)

Major Season Suitability Habitat Importance? 1. Forest -> 1.5. Forest - Subtropical/Tropical Dry - Suitable -

Threats (http://www.iucnredlist.org/technical-documents/classification-schemes)

Threat Timing Scope Severity Impact Score 1. Residential & commercial development -> 1.1. Ongoing Unknown Unknown Unknown Housing & urban areas Stresses: 1. Ecosystem stresses -> 1.1. Ecosystem conversion 1. Ecosystem stresses -> 1.2. Ecosystem degradation 11. Climate change & severe weather -> 11.1. Habitat Ongoing Unknown Unknown Unknown shifting & alteration Stresses: 1. Ecosystem stresses -> 1.1. Ecosystem conversion 1. Ecosystem stresses -> 1.2. Ecosystem degradation 2. Agriculture & aquaculture -> 2.1. Annual & Ongoing Unknown Unknown Unknown perennial non-timber crops -> 2.1.4. Scale Unknown/Unrecorded Stresses: 1. Ecosystem stresses -> 1.1. Ecosystem conversion 1. Ecosystem stresses -> 1.2. Ecosystem degradation 9. Pollution -> 9.1. Domestic & urban waste water -> Ongoing Unknown Unknown Unknown 9.1.3. Type Unknown/Unrecorded Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation 9. Pollution -> 9.3. Agricultural & forestry effluents -> Ongoing Unknown Unknown Unknown 9.3.4. Type Unknown/Unrecorded Stresses: 1. Ecosystem stresses -> 1.2. Ecosystem degradation

Conservation Actions in Place (http://www.iucnredlist.org/technical-documents/classification-schemes)

Conservation Actions in Place In-Place Land/Water Protection and Management

Occur in at least one PA: Unknown

Conservation Actions Needed (http://www.iucnredlist.org/technical-documents/classification-schemes)

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 8 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en Conservation Actions Needed 1. Land/water protection -> 1.2. Resource & habitat protection

2. Land/water management -> 2.3. Habitat & natural process restoration

Research Needed (http://www.iucnredlist.org/technical-documents/classification-schemes)

Research Needed 1. Research -> 1.2. Population size, distribution & trends

3. Monitoring -> 3.1. Population trends

Additional Data Fields

Distribution Estimated area of occupancy (AOO) (km²): 124-520

Estimated extent of occurrence (EOO) (km²): 89732.542

Number of Locations: 4

Lower elevation limit (m): 770

Upper elevation limit (m): 1010

Amended Correction of one assessor name: previously appeared as "Silva, F." (Fernando Silva), reason: this is now corrected to "Dias, F.M.S." (Fernando Maia Silva Dias).

© The IUCN Red List of Threatened Species: Parides burchellanus – published in 2019. 10 http://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T16240A145165953.en The IUCN Red List of Threatened Species™ ISSN 2307-8235 (online) IUCN 2008: T16240A145165953 Scope: Global Language: English

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The IUCN Red List of Threatened Species™ is produced and managed by the IUCN Global Species Programme, the IUCN Species Survival Commission (SSC) and The IUCN Red List Partnership.

The IUCN Red List Partners are: Arizona State University; BirdLife International; Botanic Gardens Conservation International; Conservation International; NatureServe; Royal Botanic Gardens, Kew; Sapienza University of Rome; Texas A&M University; and Zoological Society of London.

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