Phylogenetic relationships, distribution, and conservation of Roosmalens’ dwarf porcupine, Coendou roosmalenorum Voss &amp; da Silva, 2001 (Rodentia, Erethizontidae)

Fernando Heberson Menezes; Thiago Borges Fernandes  Semedo; Juliane Saldanha; Guilherme Siniciato Terra  Garbino; Hugo Fernandes-Ferreira; Pedro Cordeiro-Estrela; Itayguara Ribeiro da Costa

doi:10.3897/zookeys.1179.108766

Abstract

The New World porcupines of the genus Coendou comprise 16 species of arboreal nocturnal rodents. Some of these species are poorly known and have not been included in phylogenetic analyses. Based on recently collected specimens with associated tissue from the Brazilian Amazonia, we investigate the distribution and phylogenetic relationships of Roosmalens’ dwarf porcupine, Coendou roosmalenorum, using an integrative approach using mitochondrial gene sequences and morphological data from new specimens and localities. Our results recovered C. roosmalenorum in the subgenus Caaporamys. However, analyses of our molecular and combined datasets produced different topologies. The new record shows the presence of C. roosmalenorum 480 km to the southeast of the Rio Madeira and 95 km away from Rio Juruena in Mato Grosso state, indicating a wider distribution in southern Amazonia than suspected. All known records of C. roosmalenorum are in the Madeira biogeographical province, to which it might be endemic.

Key words

Amazonia, Brazil, cytochrome b, Madeira Province, Neotropical porcupines

Introduction

New World porcupines of the genus Coendou Lácepède, 1799 are arboreal, herbivorous, nocturnal rodents of the family Erethizontidae which occur in tropical and subtropical regions of the Americas (Eisenberg and Redford 1999). Erethizontids are characterized mainly by having their fur modified into quills, and some species have a bulbous snout and a long dorsally prehensile tail, which is an exclusive trait among prehensile-tailed mammals (Emmons 1997; Voss 2015). Currently the 18 species of erethizontids are classified in three genera, with the genus Coendou comprising 16 species (Menezes et al. 2021).

Since the early 1990s, studies have clarified the taxonomic status and phylogenetic relationships among species of Coendou (Handley and Pine 1992; Voss and Angermann 1997; Voss and da Silva 2001; Voss 2011; Feijó and Langguth 2013; Mendes Pontes et al. 2013; Voss et al. 2013), as well as its subgeneric classification (e.g., Menezes et al. 2021). Additionally, knowledge of the distribution and natural history of Coendou species has advanced (e.g., Freitas et al. 2013; Gregory et al. 2015; Menezes et al. 2020; Ramírez-Chaves et al. 2020a).

Most current knowledge about species of Coendou is restricted to taxa that occur close to urban centers (see Voss 2015). In Amazonia, most records are from the margins of the main rivers. Neotropical porcupines are usually hard to observe because they are not captured by the usual live-trapping sampling methods and have cryptic behavior (Kays and Allison 2001; Gregory et al. 2015; Kaizer et al. 2022). Nevertheless, Coendou species can be locally abundant in some areas, such as Coendou melanurus (Wagner, 1842) in French Guiana (Vié 1999). Hence, information on species distributed in the Amazonian rainforest or along the Andean foothills is scarce. Of the 16 Coendou species that have been assessed by the International Union for the Conservation of Nature (IUCN), Coendou speratus Mendes Pontes et al. 2013 is classified as Endangered (Roach and Mendes Pontes 2020) and six are classified as Data Deficient. Among the latter group is Roosmalens’ dwarf porcupine, C. roosmalenorum Voss & da Silva, 2001 (Delgado 2016a, 2016b; Roach 2016; Roach and Naylor 2016; Weksler et al. 2016a, 2016b).

Coendou roosmalenorum is one of the least known New World species of porcupine. It was originally thought to occur only in the Brazilian Amazon from both banks of the Madeira River, and only anecdotal information is available on its natural history (Voss and da Silva 2001). Since the description of the species, no novel data have been published on its biology, natural history, or distribution. An exception is a Menezes et al.’s (2021) morphological phylogeny which included C. roosmalenorum in the subgenus Caaporamys Menezes, Feijó, Fernandes-Ferreira, da Costa & Cordeiro-Estrela, 2021. Due to the scarcity of information and the lack of fresh tissue samples, the phylogenetic relationships of this species remains uncertain. Herein, we investigate these topics based on a recently collected specimen with associated tissue, from Aripuanã, Mato Grosso, western Brazil.

Materials and methods

Specimens examined

The examined specimens are deposited in two collections (abbreviations in parentheses): Coleção de Mamíferos da Universidade Federal de Mato Grosso (UFMT), Cuiabá and Coleção de Mamíferos da Universidade Federal da Paraíba (UFPB), João Pessoa (Figs 1, 2). The holotype and paratype of Coendou roosmalenorum are deposited in the scientific collection of the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus (Voss and da Silva 2001). The recently collected specimen (UFMT 4930) from which we obtained the tissue sample was accidentally killed by a bulldozer during a forest suppression activity at a mining site in Serra do Expedito, Aripuanã, Mato Grosso (10°40'S, 59°30'W). It is preserved in fluid, and a muscle sample was obtained and preserved in 70% ethanol. The skull is severely damaged but external characters of the pelage and quills allowed us to identify the specimen as C. roosmalenorum.

Figure 1.

Skulls and mandibles of Coendou roosmalenorum specimens deposited in Coleção de Mamíferos da Universidade Federal da Paraíba (UFPB) a UFPB 1188 b UFPB 1189 c UFPB 1238.

Figure 2.

Stuffed skins (a–c) and entire fluid-preserved specimen (d) of Coendou roosmalenorum a UFPB 1188 b UFPB 1189 c UFPB 1238 d UFMT 4930.

The nomenclature of the soft hairs and quills of the porcupines used here follows Menezes et al. (2021). Skull characters follow Menezes et al. (2021) and the descriptions of C. roosmalenorum by Voss and da Silva (2001) and Voss (2015).

DNA purification and sequencing

Genomic DNA of UFMT 4930 was obtained using a saline extraction protocol (Aljanabi and Martinez 1997). We used the primers MVZ05 and MVZ16 (Smith and Patton 1993) to amplify a fragment of the mitochondrial cytochrome b gene (cyt b), following the protocol described by Saldanha et al. (2019). Purification and sequencing were obtained by the Sanger method in both directions with the same amplification primers on an ABI3730xl Genetic Analyzer at the Biotecnologia, Pesquisa e Inovação, São Paulo, Brazil. We obtained a partial cyt b sequence with 821 nucleotide length. This sequence has been deposited in GenBank with accession number OR400787.

Phylogenetic analyses

To investigate the phylogenetic position of Coendou roosmalenorum, we analyzed a molecular dataset and a dataset that combined molecular sequences with morphological character data.

Only cyt b sequences were available for our molecular analysis; these and our new sequence of C. roosmalenorum augmented the molecular dataset previously published by Menezes et al. (2021) (Suppl. material 4). The dataset had a total of 60 sequences, which were aligned using the MUSCLE algorithm in MEGA 11 (Tamura et al. 2021). We did not trim the final alignment and treated the ends of partial sequences as missing data, resulting in an alignment size of 1140 nucleotides. Before the phylogenetic analyses, we tested the best substitution model using the ModelFinder plugin (Kalyaanamoorthy et al. 2017) in the PhyloSuite environment (Zhang et al. 2020). The best-fit model selected according to the Bayesian information criterion (BIC) (see Sullivan and Joyce 2005) was HKY (Hasegawa et al. 1985) with gamma distribution (+G). The HKY+G model was used in all phylogenetic analyses. After model selection, we ran a maximum-likelihood (ML) and Bayesian-inference (BI1) analyses using Chaetomys subspinosus (Olfers, 1818) and Erethizon dorsatum (Linnaeus, 1758) as outgroups. The single available sequence of Coendou pruinosus Thomas, 1905 was not included because its cyt b sequence is short with only 248 nucleotides (KC463880).

An ML consensus tree was inferred using the IQ-TREE (Nguyen et al. 2015) plugin for the PhyloSuite environment under 5000 ultrafast (Minh et al. 2013) bootstraps, as well as the Shimodaira–Hasegawa-like approximate likelihood-ratio test (Guindon et al. 2010), an initial BioNJ tree method (Guindon and Gascuel 2003), and four categories of gamma distribution (gamma = 0.258). Estimated nucleotide frequencies are f(A) = 0.304, f(C) = 0.265 f(G) = 0.124, f(T) = 0.307. BI1 phylogenies were inferred using the MrBayes 3.2.6 (Ronquist et al. 2012) plugin for the PhyloSuite environment with eight chains over 10 million generations sampled every 100, in which the initial 25000 sampled data were discarded as burn-in to estimate consensus trees and evolutionary parameter.

Our combined dataset included the same cyt b sequences described above and the morphological character matrix of Menezes et al. (2021) to produce a nexus file following the procedure described by Maddison et al. (1997). To detect the autapomorphies of C. roosmalenorum, we performed a maximum-parsimony (MP) analysis with 1000 bootstrap replicates in PAUP4 (Swofford 2002; Wilgenbusch and Swofford 2003). The starting tree(s) were obtained via stepwise addition and the tree-bisection-reconnection (TBR) algorithm with a reconnection limit of 8. Branches were collapsed (creating polytomies) if maximum branch lengths were zero. The consensus tree used the 50% majority-rule consensus rule. After the MP analysis, we ran BI2 by using partitioned models in the MrBayes plugin of the PhyloSuite environment. We used the same model and parameters of BI1 for the cyt b partition and the Mk model for discrete characters of Lewis (2001) for the morphological partition.

Genetic distances were calculated for the cyt b dataset in MEGA 11 (Tamura et al. 2021) using Kimura’s 2-parameter (K2P) model (Kimura 1980) considering no gamma distribution or invariant sites following previous studies (e.g., Mendes Pontes et al. 2013; Torres-Martínez et al. 2019). All ambiguous positions were removed for each sequence pair (pairwise deletion option).

Distribution and conservation data

To provide an updated map of the geographic distribution of C. roosmalenorum, we used published records of museum specimens (Voss and da Silva 2001; Voss 2015), together with new records obtained by us (Table 1). Our map includes both geopolitical boundaries (South American countries and Brazilian states) and the biogeographical regions proposed by Morrone et al. (2022).

Table 1.

Download as

CSV

XLSX

List of the known localities of the Brazilian endemic Coendou roosmalenorum. Numbers in the “Locality” column refer to the map (Fig. 5).

	Locality	GPS coordinates	Reference
1	Serra do Expedito, Aripuanã, Mato Grosso	10°40'S, 59°30'W	This study
2	Samuel Hydroelectric Dam, Rio Jamari, Rondônia	8°45'S, 63°27'W	This study
3	BR 364, 49 km E from Porto Velho, Rondônia*	8°45'S, 63°30'W	Voss and da Silva 2001
4	Novo Jerusalém on Lago Matupirizinho, Amazonas	5°33'S, 61°07'W	Voss and da Silva 2001
5	Santa Maria on Lago Matupiri, Amazonas	5°33'S, 61°15'W	Voss and da Silva 2001

We calculated the Extent of Occurrence (EOO), which is the area contained within the smallest continuous boundary that can be drawn to encompass all known, inferred, or projected points of the current presence of a taxon (IUCN 2012). Based on IUCN recommendations, we estimated the EOO using the minimum convex polygon (Burgman and Fox 2003). The Area of Occupancy (AOO) is defined as the area inside the EOO occupied by the species (IUCN 2012). Because C. roosmalenorum is an arboreal mammal, we assumed as the AOO the forest cover currently available based on Projeto Mapbiomas (Souza et al. 2020). This same database was used to estimate the deforestation in the polygon between 1987 and 2020. These analyzes were performed using QGIS v. 3.32.

Results

The specimens we examined all have the diagnostic characters of Coendou roosmalenorum (Fig. 3): brownish dorsal fur covering the quills; bristle-quills with strong yellowish B1, blackish B2, and light yellowish B3 on the dorsal crest; bicolored short quills with long yellowish B1 and very short blackish B2; blackish, unicolored bristles on tail; small body size when compared to other porcupine species; no nasofrontal inflation on the skull; and tail length subequal to body length (Voss and da Silva 2001; Menezes et al. 2020).

Figure 3.

Quills and bristle-quills of select Brazilian porcupine species (Coendou spp.) a Amazonian C. longicaudatus, long tricolored quill b C. baturitensis, long tricolored quill c C. bicolor, long bicolored quill d C. nycthemera, long quills with different distal band colors e C. melanurus, tricolored guard hair and bicolored quill f C. roosmalenorum, tricolored bristle-quill and bicolored quill g C. ichillus, tricolored bristle-quill and bicolored quill. Adapted from Menezes et al. (2020).

Our MP analysis of the combined (molecular + morphological) dataset resulted in the following indices: tree length = 1206 steps, consistency index (CI) = 0.4934, homoplasy index (HI) = 0.5066, CI excluding uninformative characters = 0.4337, HI excluding uninformative characters = 0.5663, retention index (RI) = 0.8231, rescaled consistency index (RC) = 0.4061, f value = 53305, f-ratio = 0.3722.

Both datasets recovered C. roosmalenorum in the subgenus Caaporamys, as expected based on morphological traits. However, the molecular dataset (ML and BI1) and combined dataset (MP and BI2) had two distinct topologies (Fig. 4). The molecular dataset recovered C. roosmalenorum as the sister taxon of C. vestitus, while the combined dataset suggests that C. roosmalenorum is the sister species of C. melanurus. The internal relationships among the four Caaporamys species differ using both datasets. Additionally, the species with smallest genetic distance from C. roosmalenorum is C. vestitus (Table 2).

Table 2.

Download as

CSV

XLSX

Average pairwise K2P sequence distances (scaled as percentages) at the cyt b locus among species of subgenus Caaporamys.

	C. ichillus	C. melanurus	C. roosmalenorum
C. melanurus	8.2%
C. roosmalenorum	5.3%	7.8%
C. vestitus	5.7%	8.4%	5.1%

Figure 4.

Phylogenetic hypotheses of Coendou focused on the species of subgenus Caaporamys based on two distinct datasets. Left: combined morphological and cyt b datasets, the values above the branches represent the posterior probabilities of IB2 and values below represent the bootstrap supports of MP. Right: cyt b; values above the branches represent the posterior probabilities of IB1, and values below represent the bootstrap proportions of ML. Branches of subgenera other than Caaporamys are collapsed.

Our MP analysis of the combined data revealed a single morphological apomorphy in C. roosmalenorum, which is a weakly developed lambdoidal ridge (Char25:1, CI 0.4, Table 3). There is no morphological synapomorphy for the C. melanurus + C. roosmalenorum hypothesis, as the MP analysis resulted in a polytomy for relationships among species of Caaporamys.

Table 3.

Download as

CSV

XLSX

List of morphological apomorphies of Caaporamys species obtained in maximum parsimony of combined data.

Subgenus Caaporamys	Character	Steps	CI	State change	Description
C. ichillus	Char1	1	0.250	1 → 0	Fur not covering quills on the dorsal crest
	Char2	1	0.500	1 → 0	Absence of dorsal fur
	Char11	1	0.500	2 → 0	B3 of bristle-quills is whitish
	Char21	1	0.400	0 → 1	Medial masseter scar oval and wide
	Char24	1	0.667	0 → 1	Temporal crests drawing in dorsal view V-shaped
	Char26	1	0.333	0 → 1	Palatal keel conspicuous
	Char31	1	0.200	1 → 0	Dorsal roof of the external auditory meatus not keeled
	Char33	1	0.500	1 → 0	Orbitotemporal fossa shallow
C. melanurus	Char12	1	0.429	0 → 1	B2 about the same length of B1
C. melanurus	Char13	1	0.500	2 → 1	B3 about the same length of B2
C. vestitus					(No morphological apomorphies)
C. roosmalenorum	Char25	1	0.400	0 → 1	Lambdoidal ridge weakly developed

All the known records of C. roosmalenorum are from the Madeira Province of Amazonia (Fig. 5). The new record (locality 1) is 480 km east of the Samuel Hydroelectric Dam (localities 2 and 3) and 590 km south of the Matupiri lake region (localities 4 and 5). The EOO is estimated to be 108,050 km², and the AOO is 107,764 km².

Figure 5.

Distribution of Caaporamys roosmalenorum in Brazilian Amazonia. Data for the numbered localities are provided in Table 1. The new record (locality 1) is the southeastern most record for the species, from Mato Grosso state, Brazil. The darker gray area represents the Madeira Province sensu Morrone et al. (2022).

Discussion

Phylogenetic relationships of Coendou roosmalenorum

The molecular and combined datasets recovered Coendou roosmalenorum as a member of the subgenus Caaporamys, as expected from its morphological characters. This species has the diagnostic morphological traits of the subgenus, such as the presence of bristle-quills in the dorsal pelage, soft ventral pelage, and unicolored caudal bristles on the tail (Menezes et al. 2021). The new information we obtained agrees with the single previous phylogeny that included the species (Menezes et al. 2021), which reinforces the importance of external characters for the subgeneric classification of Coendou.

However, the two datasets analyzed in this report suggest different topologies, with C. roosmalenorum placed either as the sister species of C. melanurus or C. vestitus. These differing results may be due to the unavailability of morphological data for Caaporamys species. The available morphological dataset for phylogenetic analyses lacks cranial characters for C. melanurus and includes only molecular characters for C. vestitus. In this way, the very homoplasic characters as colors and length of the quills bands appear to have a major contribution to the combined data in the absence of cranial characters.

The color and length of quill bands of Neotropical porcupines have a high level of homoplasy (Table 3; Menezes et al. 2021). Homoplasy is known to have negative effects on phylogenetic inference, such as the reduction of branch supports, artificial grouping (Simpson 2010; Radel et al. 2013), and long-branch attraction (Bergsten 2005). Therefore, we understand the topology of the combined dataset as a case of grouping by homoplasy and consider C. vestitus as the sister species of C. roosmalenorum until new data are obtained.

Distribution and conservation of C. roosmalenorum

Previously, the distribution of C. roosmalenorum was associated with the Rio Madeira, as the species was known from only two localities along that river or its tributary, Rio Jamari (Voss and da Silva 2001). The new record shows the presence of C. roosmalenorum 480 km to the southeast of the Rio Madeira and 95 km away from Rio Juruena in Mato Grosso state, indicating a wider distribution in southern Amazonia, as suspected (Voss 2015). The new record comes from the Amazon rainforest region, which is not subject to seasonal flooding.

All the known records of C. roosmalenorum are in the Madeira Province sensu Morrone et al. (2022). Therefore, we consider the possibility of this porcupine species occurs only in the Madeira Province, or is even more restricted, as are other arboreal mammal species such as the following primates: Callicebus cinerascens, C. ornatus, C. stephennashi, C. brunneus, C. cupreus (see the map in Carneiro et al. 2016), Mico humeralifer, M. humilis, M. chrysoleucos, M. marcai, M. rondoni (Garbino 2014; Garbino and Nascimento 2014), and Chiropotes albinasus (Ferrari et al. 1999). The distribution of C. roosmalenorum may be delimited in the northwest by the Rio Madeira, in the southwest by the Rio Guaporé, and in the east by the Rio Juruena.

Distribution patterns suggest that Coendou species can occur in sympatry with other porcupine subgenera and are only allopatric with species of the same subgenus. Coendou roosmalenorum occurs in sympatry with C. longicaudatus Daudin, 1802, the largest porcupine species of the subgenus Coendou, and it is allopatric with other Caaporamys species. Coendou ichillus Voss & da Silva 2001 is the Caaporamys species that occurs closest to C. roosmalenorum, with records north of the Solimões and Amazonas rivers (Menezes et al. 2020) and west of the Madeira and Guaporé rivers (Gregory et al. 2015). A similar pattern occurs with C. nycthemera (Olfers, 1818), of the subgenus Sphiggurus F. Cuvier, 1823, which is sympatric with the larger C. baturitensis Feijó & Langguth, 2013 throughout most of its distribution and is allopatric with other Sphiggurus species, such as C. bicolor (Tschudi, 1844) and C. speratus Mendes Pontes et al. 2013 (Freitas et al. 2013; Leal et al. 2017; Menezes et al. 2020), which are the closely related to C. nycthemera (Mendes Pontes et al. 2013; Menezes et al. 2021). Also species of the subgenus Coendou are allopatric but sympatric with species of other subgenera; C. prehensilis (Linnaeus 1758) is sympatric with C. speratus (Menezes et al. 2021) and C. rufescens is sympatric with Coendou ichillus (Ramírez-Chaves et al. 2016).

Coendou roosmalenorum is classified as Data Deficient by the IUCN (Roach and Naylor 2016) due the absence of recent information on its status and ecological requirements. The EOO and AOO here documented are certainly underestimated because of the sampling gaps but much larger than threshold for Vulnerable (IUCN 2012). However, this polygon has lost 9.34% of forest cover since 1987, almost completely replaced by pasture (9.13%) (Souza et al. 2020). Considering the Madeira Province, most of its territory is in the Brazilian states of Amazonas and Rondônia, which have lost approximately 15,400 and 15,500 km² of forest cover, respectively, between 2008 and 2022. The municipality of Aripuanã (Mato Grosso state), from where the new record of C. roosmalenorum came, has lost 1,226 km² of forest cover in the same period (INPE 2023). In addition to habitat loss, Coendou species face other threats in South America such as subsistence hunting, predation by domestic dogs, and roadkills (Ramírez-Chaves et al. 2020b, 2021). Moreover, a recent infection by Brazilian porcupine poxvirus has been described (Hora et al. 2021) and recorded in two Coendou species of different subgenera: C. (Sphiggurus) spinosus (F. Cuvier, 1823) (Guerra et al. 2022) and Coendou (Coendou) longicaudatus (Silva et al. 2023).

Therefore, it is necessary to investigate population size and decline to determine the conservation status of C. roosmalenorum more accurately following IUCN criteria. In addition to standard ecological approaches focused on erethizontids, such as visual census, telemetry, and arboreal camera traps (e.g., Giné et al. 2015; Bowler et al. 2017; Melo-Dias et al. 2023), we suggest that alternative sampling methods may yield new records of this poorly known species. Thermal drones, for example, have been efficient to survey and monitor large primates and could be used for other arboreal mammals (de Melo 2021). Citizen-science data, mainly animals photographed by the community, may provide new records, as attested by a recent publication on the genus by Ramírez-Chaves et al. (2020b).

Acknowledgements

We thank Thabata Cavalcante for the geospatial analyses, and we are grateful to Robert S. Voss for his suggestions and contributions that helped improve the quality of our manuscript. We are also grateful to Rogério Rossi, the curator of UFMT, to allow us to collect the sample used for cyt b amplification and sequencing.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

FHM was supported by a scholarship provided by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). GSTG received support from the Latin American Fellowship Committee of the American Society of Mammalogists. TBFS is supported by a fellowship from the Portuguese Foundation for Science and Technology (FCT), under scholarship number 202210212BD. HF-F is supported by the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (Funcap). This study is co-funded by the project NORTE-01-0246-FEDER-000063, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).

Author contributions

Conceptualization: TBFS, FHM, PCE, IRC, HFF. Formal analysis: TBFS, FHM, GSTG. Funding acquisition: TBFS. Investigation: FHM, GSTG, TBFS, HFF. Methodology: TBFS, JS, FHM, GSTG, HFF. Software: FHM. Supervision: PCE, IRC. Validation: GSTG. Writing - original draft: HFF, TBFS, JS, IRC, PCE, FHM, GSTG.

Author ORCIDs

Fernando Heberson Menezes https://orcid.org/0000-0003-4169-0215

Thiago Borges Fernandes Semedo https://orcid.org/0000-0003-4379-5993

Juliane Saldanha https://orcid.org/0000-0003-3983-7169

Guilherme Siniciato Terra Garbino https://orcid.org/0000-0003-1701-5930

Hugo Fernandes-Ferreira https://orcid.org/0000-0001-9064-3736

Pedro Cordeiro-Estrela https://orcid.org/0000-0003-3383-571X

Itayguara Ribeiro da Costa https://orcid.org/0000-0003-0135-6706

Data availability

All of the data that support the findings of this study are available in the main text or Supplementary Information.

References

Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25(22): 4692–4693. https://doi.org/10.1093/nar/25.22.4692

Bergsten J (2005) A review of long-branch attraction. Cladistics 21(2): 163–193. https://doi.org/10.1111/j.1096-0031.2005.00059.x

Bowler MT, Tobler MW, Endress BA, Gilmore MP, Anderson MJ (2017) Estimating mammalian species richness and occupancy in tropical forest canopies with arboreal camera traps. Remote Sensing in Ecology and Conservation 3(3): 146–157. https://doi.org/10.1002/rse2.35

Burgman MA, Fox JC (2003) Bias in species range estimates from minimum convex polygons: Implications for conservation and options for improved planning. Animal Conservation 6(1): 19–28. https://doi.org/10.1017/S1367943003003044

Carneiro J, De Sousa E, Silva J, Sampaio I, Pissinatti A, Hrbek T, Rezende Messias M, Rohe F, Farias I, Boubli J, Schneider H (2016) Phylogeny of the titi monkeys of the Callicebus moloch group (Pitheciidae, Primates). American Journal of Primatology 78(9): 904–913. https://doi.org/10.1002/ajp.22559

de Melo FR (2021) Drones for conservation: New techniques to monitor muriquis. Oryx 55(2): 171–171. https://doi.org/10.1017/S0030605321000028

Delgado C (2016a) Coendou nycthemera. IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T136597A22213629.en [Accessed on: 2023-1-11]

Delgado C (2016b) Coendou quichua. IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T136702A22214415.en [Accessed on: 2023-1-11]

Eisenberg JF, Redford KH (1999) Mammals of the Neotropics (Volume 3): the Central Neotropics: Ecuador, Peru, Bolivia, Brazil. University of Chicago Press, Chicago, 624 pp.

Emmons LH (1997) Neotropical Rainforest Mammals: a Field Guide. University of Chicago Press, Chicago, 396 pp.

Feijó A, Langguth A (2013) Mamíferos de médio e grande porte do nordeste do Brasil: Distribuição e taxonomia, com descrição de novas espécies. Revista Nordestina de Biologia 22: 3–225.

Ferrari SF, Iwanaga S, Coutinho PEG, Messias MR, Neto EH, Ramos EM, Ramos PCS (1999) Zoogeography of Chiropotes albinasus (Platyrrhini, Atelidae) in southwestern Amazonia. International Journal of Primatology 20(6): 995–1004. https://doi.org/10.1023/A:1020838904829

Freitas MA de F, França DPF, Veríssimo D (2013) First record of the Bicoloured-spined Porcupine Coendou bicolor (Tschudi, 1844) for Brazil. Check List 9(1): 94–96. https://doi.org/10.15560/9.1.94

Garbino GST (2014) The Taxonomic Status of Mico marcai (Alperin 1993) and Mico manicorensis (van Roosmalen et al. 2000) (Cebidae, Callitrichinae) from Southwestern Brazilian Amazonia. International Journal of Primatology 35(2): 529–546. https://doi.org/10.1007/s10764-014-9766-4

Garbino GST, Nascimento FO (2014) Mico humeralifer (Primates: Callitrichidae). Mammalian Species 911: 40–47. https://doi.org/10.1644/911.1

Giné GAF, de Barros EH, Duarte JMB, Faria D (2015) Home range and multiscale habitat selection of threatened thin-spined porcupine in the Brazilian Atlantic Forest. Journal of Mammalogy 96(5): 1095–1105. https://doi.org/10.1093/jmammal/gyv117

Gregory T, Lunde D, Zamora-Meza HT, Carrasco-Rueda F (2015) Records of Coendou ichillus (Rodentia, Erethizontidae) from the Lower Urubamba Region of Peru. ZooKeys 509: 109–121. https://doi.org/10.3897/zookeys.509.9821

Guerra JM, Navas-Suárez PE, Ferreira-Machado E, Ervedosa TB, Figueiredo KB, de Carvalho ACSR, Silva ML, Caiaffa MG, da Costa ALM, Teixeira RHF, Buti TEM, Luchs A, Namiyama GM, de Lima LB, Taniwaki NN, Matsumoto PSS, de Azevedo Fernandes NCC (2022) Diagnosis and successful treatment of Brazillian porcupine poxvirus infection in a free-ranging hairy dwarf porcupine (Coendou spinosus). Brazilian Journal of Microbiology 53(4): 2321–2327. https://doi.org/10.1007/s42770-022-00804-3

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52(5): 696–704. https://doi.org/10.1080/10635150390235520

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59(3): 307–321. https://doi.org/10.1093/sysbio/syq010

Handley CO, Pine RH (1992) A new species of prehensile-tailed porcupine, genus Coendou Lacépède, from Brazil. Mammalia 56(2): 237–244. https://doi.org/10.1515/mamm-1992-0207

Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22(2): 160–174. https://doi.org/10.1007/BF02101694

Hora AS, Taniwaki SA, Martins NB, Pinto NNR, Schlemper AE, Santos ALQ, Szabó MPJ, Brandão PE (2021) Genomic analysis of novel poxvirus brazilian porcupinepox virus, Brazil, 2019. Emerging Infectious Diseases 27(4): 1177–1180. https://doi.org/10.3201/eid2704.203818

INPE (2023) Programa de monitoramento da Amazônia e demais biomas. http://terrabrasilis.dpi.inpe.br/downloads/ [Accessed on: 2023-6-27]

IUCN [Ed.] (2012) IUCN Red List Categories and Criteria: Version 3.1. 2^nd edn. IUCN, Gland, Switzerland and Cambridge, UK. https://portals.iucn.org/library/node/10315 [Accessed on: 2023-6-26]

Kaizer MC, Alvim THG, Novaes CL, McDevitt AD, Young RJ (2022) Snapshot of the Atlantic Forest canopy: Surveying arboreal mammals in a biodiversity hotspot. Oryx 56(6): 825–836. https://doi.org/10.1017/S0030605321001563

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589. https://doi.org/10.1038/nmeth.4285

Kays R, Allison A (2001) Arboreal tropical forest vertebrates: current knowledge and research trends. In: Linsenmair KE, Davis AJ, Fiala B, Speight MR (Eds) Tropical Forest Canopies: Ecology and Management. Forestry Sciences. Springer Netherlands, Dordrecht, 109–120. https://doi.org/10.1007/978-94-017-3606-0_9

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16(2): 111–120. https://doi.org/10.1007/BF01731581

Leal ESB, Gomes-Silva FF, de Lyra-Neves RM, Telino-Júnior WR (2017) Range extension and first record of Coendou speratus Mendes Pontes et al., 2013 (Rodentia, Erethizontidae) from a cloud forest enclave in northeastern Brazil. Check List 13(6): 951–957. https://doi.org/10.15560/13.6.951

Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50(6): 913–925. https://doi.org/10.1080/106351501753462876

Maddison DR, Swofford DL, Maddison WP (1997) NEXUS: An extensible file format for systematic information. Systematic Biology 46(4): 590–621. https://doi.org/10.1093/sysbio/46.4.590

Melo-Dias M, Rocha MF, Dalfior ICD, Bissa L, Marcial T, Secco H, Passamani M, Rosa C (2023) Translocation and long-term monitoring of threatened thin-spined porcupines (Chaetomys subspinosus) on the Brazilian coast. Journal for Nature Conservation 74: 126434. https://doi.org/10.1016/j.jnc.2023.126434

Mendes Pontes AR, Gadelha JR, Melo ÉRA, de Sá FB, Loss AC, Caldara V Junior, Costa LP, Leite YLR (2013) A new species of porcupine, genus Coendou (Rodentia: Erethizontidae) from the Atlantic Forest of northeastern Brazil. Zootaxa 3636(3): 421–438. https://doi.org/10.11646/zootaxa.3636.3.2

Menezes FH, Garbino GST, Semedo TBF, Lima M, Feijó A, Cordeiro-Estrela P, da Costa IR (2020) Major range extensions for three species of porcupines (Rodentia: Erethizontidae: Coendou) from the Brazilian Amazon. Biota Neotropica 20(2): e20201030. https://doi.org/10.1590/1676-0611-bn-2020-1030

Menezes FH, Feijó A, Fernandes‐Ferreira H, da Costa IR, Cordeiro‐Estrela P (2021) Integrative systematics of Neotropical porcupines of Coendou prehensilis complex (Rodentia: Erethizontidae). Journal of Zoological Systematics and Evolutionary Research 59(8): 2410–2439. https://doi.org/10.1111/jzs.12529

Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30(5): 1188–1195. https://doi.org/10.1093/molbev/mst024

Morrone JJ, Escalante T, Rodríguez-Tapia G, Carmona A, Arana M, Mercado-Gómez JD (2022) Biogeographic regionalization of the Neotropical region: New map and shapefile. Anais da Academia Brasileira de Ciências 94(1): e20211167. https://doi.org/10.1590/0001-3765202220211167

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–274. https://doi.org/10.1093/molbev/msu300

Radel D, Sand A, Steel M (2013) Hide and seek: Placing and finding an optimal tree for thousands of homoplasy-rich sequences. Molecular Phylogenetics and Evolution 69(3): 1186–1189. https://doi.org/10.1016/j.ympev.2013.08.001

Ramírez-Chaves HE, Suárez-Castro AF, Morales-Martínez DM, Vallejo-Pareja MC (2016) Richness and distribution of porcupines (Erethizontidae: Coendou) from Colombia. Mammalia 80(2): 181–191. https://doi.org/10.1515/mammalia-2014-0158

Ramírez-Chaves HE, Caranton-Ayala D, Morales-Martínez DM, Rosero E (2020a) Filling distribution gaps: First record of the Western Amazonian Dwarf Porcupine, Coendou ichillus Voss & da Silva, 2001 (Mammalia, Rodentia), in the Napo Moist Forests ecoregion of Colombia. Check List 16(6): 1627–1631. https://doi.org/10.15560/16.6.1627

Ramírez-Chaves HE, Romero-Ríos C, Henao-Osorio JJ, Franco-Herrera JP, Ramírez-Padilla BR (2020b) Notes on the natural history of the Stump-tailed Porcupine, Coendou rufescens (Rodentia, Erethizontidae), in Colombia. Neotropical Biology and Conservation 15(4): 471–478. https://doi.org/10.3897/neotropical.15.e56926

Ramírez-Chaves HE, Torres-Martínez MM, Henao-Osorio JJ, Osbahr K, Concha-Osbahr C, Passos FC, Noguera-Urbano E (2021) Distribution update, male genitalia, natural history, and conservation of the stump-tailed porcupine Coendou rufescens in South America. Mammalia 86(2): 160–170. https://doi.org/10.1515/mammalia-2021-0025

Roach N (2016) Coendou baturitensis (Baturite Porcupine). The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T87411473A87411477.en

Roach N, Mendes Pontes AR (2020) Coendou speratus (Dwarf Porcupine). IUCN Red List of Threatened Species: e.T46205559A166610234. https://www.iucnredlist.org/species/46205559/166610234 [Accessed on: 2023-1-11]

Roach N, Naylor L (2016) Coendou roosmalenorum. IUCN Red List of Threatened Species: e.T136518A22214051. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T136518A22214051.en [Accessed on: 2023-1-11]

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029

Saldanha J, Ferreira DC, da Silva VF, Santos-Filho M, Mendes-Oliveira AC, Rossi RV (2019) Genetic diversity of Oecomys (Rodentia, Sigmodontinae) from the Tapajós River basin and the role of rivers as barriers for the genus in the region. Mammalian Biology 97: 41–49. https://doi.org/10.1016/j.mambio.2019.04.009

Silva DJF, Moreira JMAR, Ribeiro M, Maruyama FH, Morgado TO, Nakazato L, Dutra V, Souza MA, Colodel EM (2023) Brazilian porcupinepox virus infection in a free-ranging neotropical porcupine in Mato Grosso, Brazil. Journal of Veterinary Diagnostic Investigation 35(3): 304–306. https://doi.org/10.1177/10406387231161340

Simpson MG (2010) Phylogenetic systematics. In: Simpson MG (Ed.) Plant Systematics, Second Edition. Academic Press, Amsterdam, 17–52. https://doi.org/10.1016/B978-0-12-374380-0.50002-6

Smith MF, Patton JL (1993) The diversification of South American murid rodents: Evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, Linnean Society of London 50(3): 149–177. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x

Souza CM, Shimbo ZJ, Rosa MR, Parente LL, Alencar AA, Rudorff BFT, Hasenack H, Matsumoto M, G. Ferreira L, Souza-Filho PWM, de Oliveira SW, Rocha WF, Fonseca AV, Marques CB, Diniz CG, Costa D, Monteiro D, Rosa ER, Vélez-Martin E, Weber EJ, Lenti FEB, Paternost FF, Pareyn FGC, Siqueira JV, Viera JL, Neto LCF, Saraiva MM, Sales MH, Salgado MPG, Vasconcelos R, Galano S, Mesquita VV, Azevedo T (2020) Reconstructing three decades of land use and land cover changes in Brazilian biomes with Landsat Archive and Earth Engine. Remote Sensing 12: 2735. https://doi.org/10.3390/rs12172735

Sullivan J, Joyce P (2005) Model selection in phylogenetics. Annual Review of Ecology, Evolution, and Systematics 36(1): 445–466. https://doi.org/10.1146/annurev.ecolsys.36.102003.152633

Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38(7): 3022–3027. https://doi.org/10.1093/molbev/msab120

Torres-Martínez MM, Ramírez-Chaves HE, Noguera-Urbano EA, Colmenares-Pinzón JE, Passos FC, García J (2019) On the distribution of the Brazilian porcupine Coendou prehensilis (Erethizontidae) in Colombia. Mammalia 83(3): 290–297. https://doi.org/10.1515/mammalia-2018-0043

Vié J-C (1999) Wildlife rescues—The case of the Petit Saut hydroelectric dam in French Guiana. Oryx 33(2): 115–126. https://doi.org/10.1046/j.1365-3008.1999.00037.x

Voss RS (2011) Revisionary notes on neotropical porcupines (Rodentia: Erethizontidae) 3. An annotated checklist of the species of Coendou Lacépède, 1799. American Museum Novitates 3720(3720): 1–36. https://doi.org/10.1206/3720.2

Voss RS (2015) Superfamily Erethizontoidea Bonaparte, 1845. In: Patton JL, Pardiñas UFJ, D’Elía G (Eds) Mammals of South America, Volume 2: Rodents. University of Chicago Press, Chicago, 786–805.

Voss RS, Angermann R (1997) Revisionary Notes on Neotropical Porcupines (Rodentia: Erethizontidae). 1. Type material described by Olfers (1818) and Kuhl (1820) in the Berlin Zoological Museum. American Museum Novitates, 1–44.

Voss RS, da Silva MNF (2001) Revisionary notes on Neotropical porcupines (Rodentia: Erethizontidae). 2. A review of the Coendou vestitus group with descriptions of two new species from Amazonia. American Museum Novitates 3351: 1–36. https://doi.org/10.1206/0003-0082(2001)351<0001:RNONPR>2.0.CO;2

Voss RS, Hubbard C, Jansa SA (2013) Phylogenetic relationships of New World porcupines (Rodentia, Erethizontidae): Implications for taxonomy, morphological evolution, and biogeography. American Museum Novitates 3769(3769): 1–36. https://doi.org/10.1206/3769.2

Weksler M, Anderson RP, Gómez-Laverde M (2016a) Coendou ichillus. IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T136597A22213629.en [Accessed on: 2023-1-11]

Weksler M, Anderson RP, Gómez-Laverde M (2016b) Coendou vestitus. IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T20633A22213528.en [Accessed on: 2023-1-11]

Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Current Protocols in Bioinformatics 00: 6.4.1–6.4.28. https://doi.org/10.1002/0471250953.bi0604s00

Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20(1): 348–355. https://doi.org/10.1111/1755-0998.13096

Supplementary materials

Supplementary material 1

Dataset 1

Fernando Heberson Menezes, Thiago Borges Fernandes Semedo, Juliane Saldanha, Guilherme Siniciato Terra Garbino, Hugo Fernandes-Ferreira, Pedro Cordeiro-Estrela, Itayguara Ribeiro da Costa

Data type: nex

Explanation note: Nexus file of aligned cytochrome b sequences of Erethizontid used for ML and IB1.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Download file (71.53 kb)

Supplementary material 2

Dataset 2

Fernando Heberson Menezes, Thiago Borges Fernandes Semedo, Juliane Saldanha, Guilherme Siniciato Terra Garbino, Hugo Fernandes-Ferreira, Pedro Cordeiro-Estrela, Itayguara Ribeiro da Costa

Data type: nex

Explanation note: Nexus file of aligned cytochrome b and morphological data of Erethizontid used for MP.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Download file (80.99 kb)

Supplementary material 3

Dataset 3

Fernando Heberson Menezes, Thiago Borges Fernandes Semedo, Juliane Saldanha, Guilherme Siniciato Terra Garbino, Hugo Fernandes-Ferreira, Pedro Cordeiro-Estrela, Itayguara Ribeiro da Costa

Data type: nex

Explanation note: Nexus file of aligned cytochrome b and morphological data of Erethizontid used for IB2.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Download file (77.74 kb)

Supplementary material 4

Erethizontid cytochrome b sequences utilized in phylogenetic analyses

Fernando Heberson Menezes, Thiago Borges Fernandes Semedo, Juliane Saldanha, Guilherme Siniciato Terra Garbino, Hugo Fernandes-Ferreira, Pedro Cordeiro-Estrela, Itayguara Ribeiro da Costa

Data type: docx

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Download file (22.45 kb)

﻿Abstract

Key words

﻿Introduction

﻿Materials and methods

﻿Specimens examined

﻿DNA purification and sequencing

﻿Phylogenetic analyses

﻿Distribution and conservation data

﻿Results

﻿Discussion

﻿Phylogenetic relationships of Coendou roosmalenorum

﻿Distribution and conservation of C. roosmalenorum

﻿Acknowledgements

﻿Additional information

Conflict of interest

Ethical statement

Funding

Author contributions

Author ORCIDs

Data availability

﻿References

Supplementary materials

Abstract

Introduction

Materials and methods

Specimens examined

DNA purification and sequencing

Phylogenetic analyses

Distribution and conservation data

Results

Discussion

Phylogenetic relationships of Coendou roosmalenorum

Distribution and conservation of C. roosmalenorum

Acknowledgements

Additional information

References