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Feature Articles Conservation Priorities for Resplendent Quetzals Based on Analysis of Mitochondrial Dna Control

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Feature Articles Conservation Priorities for Resplendent Quetzals Based on Analysis of Mitochondrial Dna Control FEATURE ARTICLES The Condor 106:449±456 q The Cooper Ornithological Society 2004 CONSERVATION PRIORITIES FOR RESPLENDENT QUETZALS BASED ON ANALYSIS OF MITOCHONDRIAL DNA CONTROL- REGION SEQUENCES SOFIA SOLO RZANO1,3,ALLAN J. BAKER2 AND KEN OYAMA1 1Centro de Investigaciones en Ecosistemas, UNAM, Antigua carretera a Patzcuaro 8701, San Jose de la Huerta, Morelia, 58190, Michoacan, Mexico 2Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen's Park, Toronto, ON M5S 2C6, Canada Abstract. The Resplendent Quetzal (Pharomachrus mocinno) is a threatened bird species classi®ed into two putative subspecies (P. m. mocinno and P. m. costaricensis) and distrib- uted in cloud forests of seven countries in Mesoamerica. Because the birds are rare, tissue samples are dif®cult to obtain, but we analyzed genetic diversity in 25 quetzals from ®ve countries based on 255 bp of domain I of the control region of mitochondrial DNA. Eight haplotypes were detected. Nucleotide diversity for Mexico (P. m. mocinno: 0.0021) and Panama (P. m. costaricensis: 0.0026) were low, and did not differ from the values estimated for other birds species irrespective of whether they were endangered. A haplotype tree rooted with the Pavonine Quetzal (P. pavoninus) recovered two reciprocally monophyletic clades corresponding to each subspecies, so we propose that each subspecies be considered as an evolutionarily signi®cant unit for conservation planning. A minimum spanning network showed the number of genetic differences separating haplotypes within subspecies was small relative to the number of substitutions among them, indicating strong population subdivision (FST 5 0.37). In spite of the limited sampling we propose that in conservation practice Mexico±Guatemala, Nicaragua, El Salvador, and Panama be considered preliminarily as independent conservation management units since they each have unique haplotypes. Ad- ditionally, these countries should construct international agreements to protect the natural vegetation corridors among cloud forests of Mesoamerica and to curtail the illegal trade of quetzals. Key words: evolutionarily signi®cant units, Mesoamerica, mitochondrial DNA, manage- ment units, Pharomachrus mocinno. Prioridades de ConservacioÂn para el Quetzal Basadas en el AnaÂlisis de la RegioÂn Control del ADN Mitocondrial Resumen. El quetzal (Pharomachrus mocinno) es una especie de ave amenazada clasi- ®cada en dos subespecies (P. m. mocinno y P. m. costaricensis) distribuidas en los bosques de niebla de siete paõÂses de MesoameÂrica. Debido a que eÂsta es un ave rara, las muestras de tejido son difõÂciles de obtener, pero pudimos analizar la diversidad geneÂtica en 255 pb del dominio I de la regioÂn control del ADN mitocondrial en 25 quetzales procedentes de cinco paõÂses. Se encontraron ocho haplotipos. La diversidad nucleotõÂdica para MeÂxico (P. m. mocinno: 0.0021) y PanamaÂ(P. m. costaricensis: 0.0026) fue baja, pero no di®ere de la estimada para otras especies de aves amenazadas o no amenazadas. El aÂrbol de haplotipos enraizado con P. pavoninus mostro dos clados recõÂprocamente mono®leÂticos, correspon- Manuscript received 10 September 2003; accepted 15 April 2004. 3 Present address: Apartado Postal 21-041, C.P. 04021, MeÂxico D. F., Mexico. E-mail: slso®[email protected]. unam.mx [449] 450 SOFIA SOLO RZANO ET AL. diendo cada uno a cada subespecie, por lo que proponemos que para planes de conservacioÂn cada subespecie sea considerada como unidad evolutiva signi®cativa independiente. Una red de distancias mõÂnimas mostro que el nuÂmero de diferencias geneÂticas que separa a los haplotipos dentro de las subespecies fue pequenÄo con respecto al nuÂmero de sustituciones que existe entre ellas, indicando una fuerte divisioÂn poblacional (FST 5 0.37). Considerando nuestro muestreo limitado proponemos que para ®nes de conservacioÂn praÂcticos MeÂxico± Guatemala, Nicaragua, El Salvador y Panama sean considerados preliminarmente como unidades de manejo independientes ya que eÂstos presentan haplotipos uÂnicos no compartidos entre localidades. AdemaÂs, estos paõÂses deberõÂan ®rmar acuerdos internacionales para pro- teger los corredores de vegetacioÂn naturales entre los bosques de niebla de MesoameÂrica y tratar de reducir el comercio ilegal de los quetzales. INTRODUCTION reproductive behavior (e.g., courtship, chick The worldwide distribution of the Resplendent rearing), breeding season (dry season), diet, and Quetzal (Pharomachrus mocinno) ranges from vocalizations appear not to differ between sub- southern Mexico across Guatemala, Honduras, species (SS, pers. obs.). El Salvador, Nicaragua, Costa Rica, and Pana- Although the subspecies concept is arti®cial, ma. However, the distribution of quetzals is not it has practical advantages in conservation be- continuous through these countries, but is deter- cause it allows us to identify conservation pri- mined by the patchiness of cloud forests (SoloÂr- orities within species (Ryder 1986). The con- zano et al. 2003). These forests, ranging from cepts of ``evolutionarily signi®cant units'' and 1300 to 3000 m elevation, represent the breeding ``management units'' provide useful tools in ge- habitats for this species (Stotz et al. 1996). netic conservation (Ryder 1986, Moritz 1994a, Presently, the Resplendent Quetzal is classi- 1994b, Frankham et al. 2002). The intent of evo- ®ed under the IUCN Red List in the category of lutionarily signi®cant units is to preserve evo- ``Lower Risk Near Threatened'' (IUCN 2002), lutionary heritage across taxa assuming a histor- but this classi®cation should be revaluated con- ical origin for the genetic differences between sidering that the species is limited to remnant them. This concept emphasizes the phylogeo- patches of evergreen cloud forests, most popu- graphic pattern of genetic variation rather than lations are geographically isolated and small, degree of genetic divergence or the quantity of and breeding habitats are being lost at high an- genetic diversity pooled in a certain population. nual rates (Hanson 1982, SoloÂrzano et al. 2003, Management units represent populations with P. Bubb, unpubl. data). These habitats are them- signi®cant divergence in allele frequencies, but selves conservation priorities because they har- which have not achieved reciprocal monophyly bor high biological and ecological diversity as required for evolutionarily signi®cant units (Hamilton et al. 1995, Nadkarni and Wheel- (Moritz 1994a). The main difference between wright 2000, Bubb 2001). evolutionarily signi®cant units and management Based on morphological characters, two sub- units is that evolutionarily signi®cant units are species of Resplendent Quetzals have been rec- concerned with historical population structure ognized: P. m. mocinno, distributed from south- and serve long-term conservation planning, ern Mexico to northern Nicaragua, and P. m. whereas management units focus on the current costaricensis, found in Costa Rica and western population structure and are useful to establish Panama (Sibley and Monroe 1990). These sub- short-term monitoring programs based on ge- species apparently are isolated geographically netic discontinuity among populations or unique by Lake Nicaragua (8324 km2) and the absence haplotypes harbored in individual populations of the breeding habits in regions adjacent to this (Moritz 1994a, 1994b). The criteria to de®ne lake (Fig. 1). The age of this barrier is not well these concepts have changed from the initial established but probably arose when the Pana- proposals (cf. Ryder 1986, Moritz 1994a, manian Isthmus formed 3 million years ago 1994b), and are still debated (Fraser and Ber- (Keigwin 1982). Although preliminary partial natchez 2001). genetic analysis based on a subunit of ND6, In the present study, our goal is to identify tRNAGlu and control region of mtDNA of 10 in- conservation units for quetzals in Mesoamerica dividuals suggested genetic differentiation of based on mtDNA haplotypes. We discuss our re- subspecies (SoloÂrzano et al., unpubl. data), the sults in the context of genetic conservation rath- QUETZAL CONSERVATION BASED ON MTDNA 451 FIGURE 1. Current distribution (symbols) of Resplendent Quetzals in geographically isolated remnant cloud forests (constructed from Hanson 1981, Sibley and Monroe 1990, SoloÂrzano et al. 2003). The past distribution is indicated by bold lines (modi®ed from Johnsgard 2000). Triangles correspond to P. mocinno mocinno and circles to P. m. costaricensis. Sampled localities: Mexico: NM: Northern Mountains, ET: El Triunfo biosphere reserve, FC: Finca Santa Cruz; Guatemala: BQ: Biotopo Quetzal, SM: Sierra de las Minas biosphere reserve; El Salvador: PM: Parque Montecristo; Nicaragua: PA: Parque Arenal; Panama: BG: Bajo Grande. One sample was not located because its origin is uncertain (ZOOMAT Zoo donation). The outgroup sample PP (P. pavoninus) is from Ecuador (inset). er than a structural analysis of the control region emy of Natural Sciences of Philadelphia, Penn- variation and composition, which will be pub- sylvania. lished elsewhere (SoloÂrzano et al., unpubl. data). DNA ISOLATION, PCR AMPLIFICATION, AND METHODS SEQUENCING We conducted ®eldwork in eight localities (Fig. Total genomic DNA was isolated from blood 1), collecting blood samples during the breeding and tissue samples using standard proteinase-K season to guarantee the origin of the samples. and SDS treatment, followed by extraction with Additionally, the ZOOMAT Zoo in Chiapas, phenol-chloroform and a ®nal ethanol precipita-
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