Re-examining the hypothesis of allopatric distribution of Myoprocta acouchy and M. pratti (Mammalia: Dasyproctidae) in South America

Re-examining the hypothesis of allopatric distribution of Myoprocta acouchy and M. pratti (Mammalia: Dasyproctidae) in South America

Héctor E. Ramírez-Chaves^I; Andrés F. Suárez-Castro^II; Bruce D. Patterson^III

^ISchool of Biological Sciences, University of Queensland, Goddard Building 8, St. Lucia 4072, Brisbane, Australia. E-mail: [e-mail] (corresponding author)

^IIGrupo de Investigación en Conservación y Manejo de Vida Silvestre, Instituto de Ciencias Naturales, Universidad Nacional de Colombia

^IIIIntegrative Research Center, Field Museum of Natural History, 1400 S. Lake Shore Dr., Chicago, IL 60605, USA. E-mail: [e-mail]

ABSTRACT

Currently, two allopatric species of acouchies, genus Myoprocta (Rodentia: Dasyproctidae) are recognized. Nevertheless, there is morphological variability in the regions where the species are distributed that suggests either sympatry of two (or more) distinct species or else breakdowns in the characters that have been used to diagnose the species. We reviewed specimens of Myoprocta from Colombia and found that both reddish and greenish forms are sympatric in the Amazon basin of the country, including areas adjoining Ecuador and Peru. These records apparently refute the hypothesis of allopatry for these species in South America. However, the results of a principal components analysis showed little or no morphological separation between these two forms. In addition, a review of skulls throughout the geographic range of M. pratti shows high morphological variation. Although sympatry of reddish and greenish acouchies has been suggested for the Amazon region of Ecuador, our review found no evidence of this. In view of our findings, further revisionary work is needed to clarify the status of these forms.

Key-words: Amazonas; Acouchies; Distribution; Hybridization; Sympatry.

RESUMEN

Actualmente, dos especies alopátricas de acuchís, género Myoprocta (Rodentia: Dasyproctidae) son reconocidas. Sin embargo, existe variabilidad morfológica en las regiones donde las especies se distribuyen que sugiere simpatría entre dos (o más) especies distintas o inconsistencias en los caracteres que han sido usados para diagnosticar las especies. Revisamos ejemplares de Myoprocta de Colombia y encontramos que formas de acuchís rojizos y verduzcos son simpátricos en la cuenca Amazónica del país, incluso en áreas adyacentes a Ecuador y Perú. Estos registros aparentemente refutan la hipótesis de distribución alopátrica para dichas especies en Sudamérica. Sin embargo, los resultados de los análisis de componentes principales mostraron poca o ninguna separación morfológica entre las dos formas. Adicionalmente, la revisión de cráneos a lo largo del área de distribución de M. pratti mostró una alta variación morfológica. Aunque simpatría entre acuchís rojizos y verduzcos ha sido mencionada para la región Amazónica de Ecuador, en nuestra revisión no encontramos evidencia de esto. En vista de nuestros hallazgos, se requiere de una revisión adicional para clarificar el estado de aquellas formas.

Palabras-clave: Amazonas; Acouchís; Distribución; Hibridación; Simpatría.

INTRODUCTION

The acouchies (Myoprocta) are medium-sized caviomorph rodents of the family Dasyproctidae endemic to South America (Voss et al., 2001; Woods & Kilpatrick, 2005). Two species are currently recognized: M. acouchy, distributed in Guyana, French Guiana, Surinam, and Brazil north of the Amazon and east of the Rio Branco, and M. pratti, distributed in southern Venezuela (headwaters of the Orinoco), eastern Colombia and Ecuador, northern Peru, and western Brazil (Woods & Kilpatrick, 2005). Voss et al. (2001) identified a combination of pelage, size, and cranial characters to distinguish Myoprocta species. Myoprocta acouchy (red acouchi) is principally rich reddish-brown dorsally, with saturate long dark hairs along the rump midline and uniformly orange or reddish underparts, whereas M. pratti (green acouchi) is drab yellowish- or grayish-brown dorsally, with less saturate hairs along the rump midline and yellowish underparts. Also, red acouchies are on average larger than green acouchies, and the species were found to have non-overlapping morphometric distributions in multivariate ordinations obtained by principal components analysis. Cranially, the sphenopalatine vacuities, which perforate the bony roof of the mesopterygoid fossa, are very narrow slits (0.1 mm wide) in most specimens of M. acouchy, whereas in M. pratti they are wider (~ 1 mm), with teardrop-shaped openings posteriorly.

Although Voss et al. (2001) substantially clarified the nomenclature of the genus, questions remain concerning the geographic distributions of the referred taxa and whether additional forms exist besides the two recognized species. Voss et al. (2001) considered M. pratti and M. acouchy allopatric, even as they acknowledged implied sympatry of Myoprocta species in records from the Amazonian region of Colombia and Ecuador. They attributed reported instances of sympatry involving Myoprocta species to confusion concerning their technical nomenclature.

Historically, two kinds of acouchies have been recognized in Colombia. Cuervo-Díaz et al. (1986) registered two species of Myoprocta in the Serranía de La Macarena and Amazonas region: M. acouchy and M. exilis. Voss et al. (2001) considered M. exilis a junior synonym of M. acouchy (see also Woods & Kilpatrick, 2005), which simply dismisses evidence for two sympatric species. Alberico et al. (2000) also listed both M. acouchy and M. exilis as elements of Colombia's mammal fauna. These authors recorded M. acouchy in the Colombian departments of Amazonas, Boyacá, Caquetá, and Meta over an elevational range from sea level to 2000 m. Alberico et al. (2000) considered Myoprocta milleri Allen, 1913, from La Murelia in Caquetá, as a junior synonym of M. acouchy, but others regard this name as a synonym of M. pratti (Voss et al., 2001; Woods & Kilpatrick, 2005). Still others regard milleri as a name given to hybrids between red and green acouchies in the headwaters of Río Vaupés (Emmons & Feer, 1997). Recently, following the conclusions of Voss et al. (2001), Solari et al. (2013) recognized only M. pratti in the Amazonas and Orinoco regions of Colombia.

Two species of acouchies have also traditionally been recognized in eastern Ecuador (Albuja, 2011). According to Lönnberg (1925), green acouchies (M. pratti archidonae) inhabit the Napo valley, whereas red acouchies (M. exilis parva) inhabit the Curaray valley; both these taxa were considered green acouchies by Voss et al. (2001). Lönnberg (1921: 41) described parva as a "dark grizzled brownish" acouchi, differing in coloration from both the mostly reddish M. acouchy of the Guianas and the olive or pale yellowish M. pratti from Peru.

In this work, we reviewed specimens housed at four natural history collections in order to clarify the presence and distribution of the species of genus Myoprocta in Colombia and Ecuador, and evaluate the variation in the diagnostic characters used in the most recent revision of the genus (Voss et al., 2001).

MATERIAL AND METHODS

We reviewed specimens housed at the following collections: Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá (ICN); Instituto Alexander von Humboldt, Villa de Leyva (IAvH); Museo de Historia Natural, Universidad del Cauca, Popayán (MHNUC); and Field Museum of Natural History, Chicago (FMNH). Cranial measurements and morphological characters followed Voss et al. (2001), including: Condyle-incisive length (CIL), length of diastema (LD), maxillary toothrow (MTR), length of molars (LM), breadth of M¹ (BM1), breadth of P⁴ (BP4), breadth of palatal bridge (BPB), length of nasals (LN), least interorbital breadth (LIB), breadth of braincase (BB), zygomatic breadth (ZB), and zygomatic length (ZL). In addition, we reviewed photographs of four specimens, including the type specimens of M. pratti archidonae and M. parva, both at the Naturhistoriska riksmuseet, Stockholm (NRM), in order to clarify their assignment to either red or green acouchies.

To evaluate whether there is a morphological gap separating red and green acouchies as discrete groups, we performed a principal component analysis (PCA). We selected variables based on the findings of Voss et al. (2001), who determined that most red acouchies have noticeably larger toothrows, broader interorbits, and longer nasals than green acouchies. In addition, we used the condyle-incisive length (CIL), length of diastema (LD), length of molars (LM), length of nasals (LN), breadth of braincase (BB) and zygomatic breadth (ZB). We included 51 adult specimens (those with complete maxillary tooth eruption) from Colombia, Ecuador, Peru, Brazil, French Guiana, and Surinam, including 35 identified by Voss et al. (2001) and used as reference samples for newly studied specimens from Colombia and Ecuador. The analysis was made with the software PAST v. 2.17 (Hammer et al., 2001).

RESULTS

We reviewed 32 specimens (^{Appendix 1}) from Colombia, 22 of which are attributed to M. pratti and called greenish acouchies based on skin coloration and the shape of the sphenopalatine vacuities. In addition, nine skulls from Colombia exhibited sphenopalatine vacuities appearing as narrow slits in the roof of the mesopterygoid fossa, a qualitative cranial character supposedly diagnostic of M. acouchy (Voss et al., 2001) (Fig. 1). Cranial measurements of specimens of both samples are shown in Table 1.

Although we found some individual variation, skins from Colombia of greenish acouchies are typically drab brownish dorsally with yellowish underparts (Fig. 2). On the other hand, skins of the reddish acouchies are reddish-brown dorsally with uniformly orange or reddish underparts, the diagnostic features of M. acouchy. Some of these reddish individuals tend to be darker, but the color pattern is the same (Fig. 2). Also, they have long and saturate hairs on the rump midline. On the other hand, M. pratti skins vary in this character and those that are darker have a blackish patch on the rump (Fig. 2).

We found no evidence of the presence of red acouchies in Ecuador in the sample we evaluated. Based on external coloration and sphenopalatine vacuities, the NRM specimens are green acouchies. However, the type series of Myoprocta exilis parva (NRM 615574, NRM 585575; Río Curaray, El Oriente, Ecuador) lacks skulls (Daniela Kalthoff, pers. comm.), so that cranial characters could not be assessed.

Results from the PCA analysis showed no clear morphological gap between the red and green acouchies (sensu Voss et al., 2001), either typical forms or their reddish and greenish counterparts in Colombia (Fig. 4). The first three components explain about 88% of the total variability observed. The first principal component (PC 1) explains 69.69% of the variation and the second principal component (PC 2) explains 9.51%. All variables contributed positively to PC 1. Thus, the first principal component reflects variation in overall cranial size. The variables that contributed most strongly to PC 1 were condyleincisive length (0.7346) and length of nasals (0.4541). The other principal components had both positive and negative variable contributions (Table 1), and reflect variation in cranial shape. In the scatter plot, both forms have overlapping morphometric distributions. However, linear measurements of Colombian specimens (Table 2) show that reddish acouchies tend to have longer maxillary tooth rows, longer nasals and broader inter-orbital breadth than greenish acouchies, in parallel with the differences suggested for the red and green species by Voss et al. (2001).

Locality records for reddish acouchies in Colombia are located in the Amazonas region, in the Departments of Amazonas, Leticia, Parque Nacional Natural Amacayacu, San Martin (03º29'S, 70º12'W; 100 m), and Puerto Mogue, cerca de Bocas de la quebrada Cabimas (03º41'S, 70º24'W; 116 m); Department of Meta, Los Micos, La Macarena (03º18'N, 73º54'W; 403 m), Parque Nacional Natural La Macarena, Campamento Izawa, Rio Duda (02º33'N, 74º03'W; 240 m), and Rio Apaporis, without precise locality but probably in the Department of Meta (Fig. 3).

DISCUSSION

Our results confirm the presence of two morphs identified by others as species and living in sympatry in Colombian Amazonia (^{Appendix 1}). The presence of reddish acouchies in Colombia corroborates previous statements that at least two species of the genus occur in sympatry in the eastern part of the country (Emmons & Feer, 1997). Yet it is not possible to state unequivocally that the reddish acouchis of Colombia are identical to M. acouchy, merely that they share morphological characters thought to be diagnostic of that form. Possible hybridization between species must be tested, especially in the headwaters of Apaporis and Vaupés River. If these records represent M. acouchy, then the record the known distribution o west from the nearest confirme Conceicáo, Brazil (see Vos et al., 2001) (Fig. 3).

It is important to highlight that the apparently allopatric ranges of these species is due to inadequate revision of material in national collections of Colombia and the limited information in the check lists of Colombian mammals that have recorded the species. The finding that at least two species are sympatric in Colombia is not surprising, considering that the eastern portion of the country is relatively poorly known in terms of its flora and fauna. In fact, 74 % of the species registered by Lim et al. (2005) from the Guiana Shield have been recorded both in the Amazon Basin and Guyana. Both M. acouchy and M. pratti were listed as occurring in the Orinoco Basin of Colombia and Venezuela, but no information about voucher specimens was provided (Ferrer-Pérez et al., 2009). However, previous assessments (Linares, 1998; Sánchez & Lew, 2012) recorded M. pratti for Venezuela, only from localities south of Orinoco River (Linares, 1998)

Based on the records of reddish acouchies in Department of Amazonas, Leticia, Parque Nacional Natural Amacayacu, locality that is geographically close to the border of the republics of Ecuador and Peru, at least two species of Myoprocta are likely to be present in eastern Ecuador, as previously by Albuja (2011), and in northern Peru, where only M. pratti has been registered (Pacheco et al., 2009). The specimens on which Lonnberg (1921, 1925) based the description of M. e. parva, and M. pratti archidonae are likely green acouchies as previously suggested by Voss et al. (2001). A review of additional specimens in collections from Ecuador and Peru is needed in order to clarify the distribution of red acouchies in South America.

High geographical variation in the external and cranial diagnostic characters of M. pratti and M. acouchy has been observed, and there is an unappreciated variability throughout the geographic range of Myoprocta that suggest breakdowns in the characters used to diagnose taxa. Specimens of M. acouchy from French Guiana and Suriname (FMNH 21785, FMNH 95755) exhibit wider sphenopalatine vacuities (which are slightly teardrop-shaped) and paler coloration that those described by Voss et al. (2001), although the vacuities are not as wide as in M. pratti.

In the other hand, specimens attributed to M. pratti based on the light greenish dorsal coloration, typical of the species from Peru (i.e., FMNH 75196) exhibit sphenopalatine vacuities as narrow slits (~ 0.1 mm wide), as is typical of M. acouchy (neotype illustrated in Voss et al., 2001). Furthermore, although typical red acouchies specimens from Brazil and Surinam tend to be larger than specimens of M. pratti, both greenish and reddish acouchies from Colombia, Ecuador and Peru have overlapping morphometric distributions, contrary to the statement of Voss et al. (2001).

Nevertheless, as previously stated by Voss et al. (2001), red acouchies tend to have longer maxillary tooth rows, longer nasals, and broader inter-orbital breadth, and the difference in coloration between red and green acouchies from Colombia is conspicuous when average specimens of both kinds are compared. Unfortunately, there are too few skins of reddish acouchies from Colombia in collections to evaluate whether coat-color variation could be related with geographic origin (Voss et al., 2001). Further analyses are needed in order to know whether variation in size and cranial shape is related to geographic origin, sexual dimorphism or age variation.

Based on our results, Myoprocta pratti as currently understood probably comprises a complex of species. Two species are apparent in published 12S rRNA gene sequences (Rowe & Honeycutt, 2002), but these samples lack information regarding their provenance and are not vouchered by museum specimens with potentially diagnostic characters. Genetic information could test whether the apparent sympatry of Colombian acouchies involves M. pratti and M. acouchy as suggested by morphological characters or rather whether it involves two divergent morphs that both belong to a complex of species currently identified as M. pratti.

CONCLUSIONS

Two different species of acouchies (reddish and greenish) appear to be present in the Amazonas region of Colombia, apparently refuting the allopatric distribution hypothesis proposed by Voss et al. (2001). However, contrary to earlier beliefs, the species also exhibit overlapping morphometric distributions. The western Amazonian form, M. pratti, is highly variable geographically in purported diagnostic characters; it may well represent a complex of species. Further revision of the genus Myoprocta is needed to clarify the richness and the distribution of the taxa comprised in the genus; information on the genetic distinctions among these forms would be most useful.

ACKNOWLEDGEMENTS

We thank Hugo López-Arévalo (ICN), María del Pilar Rivas Pava (MHNUC) and Fernando Forero (IAvH), for allowing us to review specimens under their care. Daniela Kalthoff kindly provided pictures of the specimens at NRM collections. Hugo Mantilla-Meluk provided assistance with the map. The UQCent and UQI scholarships of University of Queensland provided support to Ramírez-Chaves to develop part of the manuscript.

Aceito em: 05/10/2014

Impresso em: 31/12/2014

APPENDIX 1

Specimens from Colombia, Ecuador and Peru reviewed. Additional specimens from Surinam appear in Voss et al. (2001).

Reddish acouchies, Myoprocta cf. acouchy (9 specimens): COLOMBIA: Amazonas Natural (PNN) Amacayacu, San Martín. (IAvH 5373, skull; IAvH 5374 male, skull Amazonas, Río Amacayacu, Puerto Mogue, cerca de Bocas de la quebrada Cabima skull). Meta, Los Micos (ICN 1493, skull). Meta, PNN La Macarena, Campament 2541, female, skin + skull; IAvH 2542, female, skin + skull). Río Apaporis. ICN (ICN 4717, skull).

Greenish acouchies, Myoprocta cf. pratti: COLOMBIA (22 specimens): Amazonas Natural (PNN) Amacayacu, San Martín (IAvH 5375, female, skull). Guaviare, San la Lindosa (ICN 212, female, skin). Río Apaporis (ICN 775, male, skull; ICN 3665 ICN 4438, female, skull). Caquetá, La Tagua, Tres Troncos (FMNH 71132, female (Trocha del Cable), La Macarena. ICN 1421(female, skin): Meta, left margin of Rive (ICN 285, female, skin). Meta, Villavicencio, Parque Nacional Natural La Macarena 88023, male, skin + skull; FMNH 88024, female, skin + skull; FMNH 88043, female San Antonio, Río Guamués, 400 m (ICN 10048, male, skin + skull). Putumayo (FMNH 71133, female, skin + skull; FMNH 71134, male, skin + skull). Vaupés, skin). Vaupés, between Macuparaná and Caño Castaño, affluent of Par-Wasai (ICN ICN 211, female, skin). Colombia, no locality data (MHNUC 279, skin + skull NUC 281, skin + skull; ICN 3786, skin).

ECUADOR (11 specimens + photographs*): Napo, Río Suno, below Loreto (FMN skull). Napo, Lago Agrio, 12 km NE (FMNH 125085, female, skull; FMNH 125086 Rio Pindo Yaco (FMNH 43186, female, skin + skull; FMNH 43187, female, ski male, skin + skull). Pastaza, Montalvo (FMNH 41485, female, skin + skull; FMNH Pastaza, Río Capahuari (FMNH 43191, male, skin + skull). Pastaza, Río Yana Rum + skull; FMNH 43190, female, skin + skull). Río Curaray, El Oriente (NRM 585577* series of Myoprocta exilis parva, male and female, skins). Archidona (NRM 615574* archidonae, female, skin + skull; NRM 585575*, skin + skull).

PERU (19 specimens): Cuzco, Quispicanchi: Quincemil (FMNH 75195, female, male, skin + skull; FMNH 78667, female, skin + skull). Loreto, Alto Amazonas, aga (FMNH 88907, male, skin + skull; FMNH 88954, female, skin + skull). Loreto Río Yavari Mirim, San Fernando (FMNH 88908 female, skin + skull). Loreto, Marisca Yavari Mirim, Quebrada Esperanza (FMNH 88910, male, skin + skull). Loreto, Marisca Yavari Mirim, boca Río Yaquerana (FMNH 88909, male, skin + skull; FMNH 88911 reto, Maynas, Iquitos (FMNH 24793, female, skin + skull; FMNH 24794, female, skull). Loreto, Maynas, Río Maniti, Santa Cecilia (FMNH 86920, female, skin + Nanay, Santa Luisa (FMNH 86918, female, skin + skull; FMNH 86919, female, female, skin + skull). Loreto, Ucayali, Contamana, Cerro Azul (FMNH 64295, female Dios, Manu, Altamira (FMNH 98072, male, skin + skull). Pasco, Oxapampa, Puerto Victoria (FMNH 24792, male, skin).

APPENDIX 2

Localities of the records in Fig. 3.

Myoprocta acouchy from Voss etal. (2001) and M. cf. acouchy (specimens from Colombia reviewed here): 1. Brazil, Serra do Navio; 2. Boca Rio Piratucu; 3. Lago do Baptista; 4. Lago do Serpa; 5. Lower Solimões; 6. Santo Antonio do Amatari; 7. Pará, Colonia do Veado; 8. Faro; 9. Monte Alegre; 10. Cachoeira Porteira; 11. Roraima, Conceicão; 12. Serra Grande; 13. French Guiana, Paracou; 14. Saut Macaque; 15. St.-Laurent du Maroni; 16. Tamanoir; 17. Kartabo; 18. Guyana, Supinaam River; 19. Potaro; 20. Moraballi; 21. Dadanawa; 22. Surinam, Locksie Hattie; 23. Paloemeu Camp; 24. Kaiserberg Airstrip; 25. Wilhelmina Mountains; 26. Colombia, La Macarena. 27. PNN Amacayacu.

Myoprocta cf. pratti: 1. Colombia, Meta, Río Guejar; 2. Guaviare, Mesas de la Lindosa; 3. Vaupés, Wasai; 4. Vaupés, Laguna de Inaná; 5. Caquetá, La Morelia (Allen, 1913); 6. Putumayo, San Antonio. 7. Ecuador, Lago Agrio, 12 km NE; 8. Napo, Río Suno, below Loreto; 9. Archidona. 10. Pastaza, Rio Pindo Yaco; 11. Río Curaray, El Oriente; 12. Pastaza, Montalvo; 13. Pastaza, Río Capahuari. 14. Peru, Loreto, Maynas, Río Nanay, Santa Luisa; 15. Loreto, Maynas, Iquitos; 16. Loreto, Mariscal Ramon Castilla, Alto Yavari Mirim; 17. Loreto, Alto Amazonas, Río Morona, Quebrada Pushaga; 18. Loreto, Ucayali, Contamana.

Myoprocta pratti: 19. Río Maranón, Pongo de Rentema (Type locality).

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Appendix 1

Publication Dates

• Publication in this collection
  16 Dec 2014
• Date of issue
  2014

History

• Received
  05 Oct 2014